Spike the PCHA! Overuse injury of the Posterior Circumflex Humeral Artery in elite volleyball van de Pol, D.

Transcription

1 UvA-DARE (Digital Academic Repository) Spike the PCHA! Overuse injury of the Posterior Circumflex Humeral Artery in elite volleyball van de Pol, D. Link to publication Citation for published version (APA): van de Pol, D. (2016). Spike the PCHA! Overuse injury of the Posterior Circumflex Humeral Artery in elite volleyball. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam ( Download date: 04 Apr 2019

2 SPIKE the PCHA! Overuse injury of the Posterior Circumflex Humeral Artery in elite volleyball Daan van de Pol

3

4

5 This thesis was prepared at the Department of Radiology, Academic Medical Center, University of Amsterdam, The Netherlands The printing of this thesis was financially supported by: University of Amsterdam, Amsterdam, The Netherlands Dynamic Medical & Veterinary Products BV. ISBN/EAN Cover Ipskamp Drukkers BV, Enschede Lay-out Ipskamp Drukkers BV, Enschede Printed by Ipskamp Printing BV, Enschede Copyright 2016 Daan van de Pol, Amsterdam, The Netherlands All rights reserved. No part of this thesis may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, without prior written permission of the author, or when appropriate, of the publishers of the publication included in this thesis.

6 Spike the PCHA! Overuse injury of the Posterior Circumflex Humeral Artery in elite volleyball ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Universiteit van Amsterdam op gezag van de Rector Magnificus prof. dr. D.C. van den Boom ten overstaan van een door het College voor Promoties ingestelde commissie, in het openbaar te verdedigen in de Agnietenkapel op vrijdag 1 april 2016, te uur door Daan van de Pol geboren te Amsterdam

7 PROMOTIECOMMISSIE Promotor: Prof. dr. M. Maas Universiteit van Amsterdam Co-promotores: Dr. P.P.F.M. Kuijer Universiteit van Amsterdam Dr. R.N. Planken Universiteit van Amsterdam Overige leden: Prof. dr. C.M.A.M. van der Horst Universiteit van Amsterdam Prof. dr. G.M.M.J. Kerkhoffs Universiteit van Amsterdam Prof. dr. J.A. Reekers Universiteit van Amsterdam Prof. dr. J. Gielen Universiteit Antwerpen Prof. dr. W. van Mechelen Vrije Universiteit Amsterdam Dr. J.L. Tol Universiteit van Amsterdam Faculteit der Geneeskunde

8 Voor Joanne, Nel en Paul

9 TABLE OF CONTENTS Chapter General introduction 1.2 Research questions 1.3 Outline of the thesis PART I Symptomatology and associated risk factors Chapter 2 High prevalence of self-reported symptoms of digital ischemia in elite male volleyball players in the Netherlands: a cross-sectional national survey Chapter 3 Risk factors associated with self-reported symptoms of digital ischemia in elite male volleyball players in the Netherlands Chapter 4 Test-retest reliability of the SPI-Questionnaire to detect symptoms of digital ischemia in elite volleyball players Chapter 5 Self-reported symptoms and risk factors for digital ischemia among international world-class beach volleyball players PART II Imaging Chapter 6 B-mode ultrasound assessment of the posterior circumflex humeral artery The SPI-US protocol: a technical procedure in 4-steps Chapter 7 Reproducibility of the SPI-US protocol for ultrasound diameter measurements of the posterior circumflex humeral artery and deep brachial artery: an inter-rater reliability study Chapter 8 Ultrasound assessment of the posterior circumflex humeral artery in elite volleyball players: aneurysm prevalence, anatomy, branching pattern and vessel characteristics

10 PART III Clinical management Chapter 9 The international SPIKE study on posterior circumflex humeral artery pathology among elite volleyball players: four profiles for clinical management (4P4M) Chapter 10 Conservative management of a vascular shoulder overuse injury in a professional volleyball player: use of novel MR Angiography in diagnosis and follow-up PART IV Summary, references and appendices Chapter Summary 11.2 Conclusions 11.3 Clinical implications 11.4 Future research Chapter Samenvatting 12.2 Conclusies References Appendices List of abbreviations List of publications PhD portfolio Dankwoord Curriculum vitae

11

12 CHAPTER 1 General introduction Research questions Outline of the thesis

13

14 1.1 - GENERAL INTRODUCTION Volleyball was introduced more than 100 years ago by the American physical educator William Morgan 1, and today enjoys one of the highest participation rates of any sport in the world. With the great success of the world competitions organised by the Fédération Internationale de Volleyball (FIVB), the number of active players in the world has grown exponentially recent decades (Figure 1). 110 By most estimates, volleyball ranks second only to football (soccer) in terms of global popularity. 100 One of the most appealing aspects of the sport is that it can be played indoors and outdoors, by the young and the old, by males and females, and by both the able-bodied and those with physical impairments. 100 Volleyball is furthermore unique among team sports in that it has evolved into two distinct Olympic disciplines: a two-person per side outdoor game typically played on sand (beach volleyball), and an indoor version featuring six players on each team (indoor volleyball). 1 As with all sports, those who enjoy either of the two volleyball disciplines assume a certain risk of injury the moment they step on to the court. 100 Volleyball, whether played indoors or on the beach, is a relatively safe sport in terms of overall injury rate 8,9,122, Figure Players (in millions) active in the world after volleyball introduction (1885). (a) In 1916 the Spalding Volleyball Guide, written by Robert C. Cubbon, estimated 200,000 players in the United States alone. (b) In 1990 a figure of 150 million players was estimated (170 countries). (c) In 1994 FIBV claimed 200 million players. 1 (d) In 2004 volleyball had more than 500 million registered players worldwide (data FIBV, 2004). (e) Today there are 800 million players worldwide who play volleyball at least once a week (46 million of them in the United States). 110 General introduction I 11

15 particularly compared to contact sports such as football (soccer) and field hockey. 51 For instance, research conducted during the Athens 2004 Olympics confirms that volleyball enjoyed the lowest injury rate of any contested team sport. 51 Published data suggest that the injury pattern is similar for men and women, and that volleyball athletes appear to be at greatest risk of acute injuries of the ankle (inversion sprains) and overuse injuries of the knee (predominantly patellar tendinopathy) and the shoulder (Figure 2). 8,100,122,134 The most common overuse-related injuries of the shoulder girdle in volleyball players involve impingement, subscapular neuropathy, and functional instability. 49,110 Vascular injuries of the shoulder girdle in volleyball Vascular injuries of the shoulder girdle in volleyball are rare and infrequently addressed in the sports medicine literature. 2 Volleyball players are at risk of vascular overuse injuries in the dominant shoulder due to repetitive abduction and external rotation of the arm 2,27,73,97 Position-dependent compression of the subclavian and axillary vessels may result in functional limitation and a decline in overhead athletic performance as a result of heaviness, fatigue, paresthesias, and effort-related pain. 97 When these symptoms are associated with pulse deficits, pallor, or differences in temperature in the dominant or spiking arm and hand, aneurysm formation with thromboembolism might be present. 27,49 In volleyball, emboli in the spiking hand have been reported to originate from aneurysms in the hypothenar 65, forearm 57 and more proximal in the ipsilateral shoulder. Figure A comparison of the acute injury patterns observed in two prospective epidemiological studies. 8,122 The presented data represent the number of acute time-loss injuries in one season sustained by both male and female volleyball players during both training and competition (combined) while participating in a European national adult competitive amateur league I Chapter 1

16 Posterior Circumflex Humeral Artery (PCHA) Pathology In 1993, Reekers 95 was the first to suggest a causal relationship between traumatic aneurysm of the PCHA and volleyball. Fifteen years later, between November 2008 and November 2010, six volleyball players with ischemic digits of the dominant hand presented themselves in the Academic Medical Center (AMC) in Amsterdam. Following angiography of the hand and forearm, some of these players showed small microemboli in the digital arteries and were given thrombolytic therapy (Figure 3). Within weeks of returning to play, these players returned with identical complaints. Further evaluation, including angiography of the shoulder, showed an aneurysmatic dilatation of the PCHA with thrombus formation and emboli in the digital arteries of the ipsilateral limb (Figures 3 and 4). These players were treated by ligation of the PCHA to prevent further embolization and after rehabilitation returned to play at the highest level of competition within 3-4 months after surgery. All were elite male volleyball players active in the national top league and between 21 and 31 years of age. 1 This sudden increase in volleyball players with digital ischemia due to PCHA pathology was noted in 2010 by the physiotherapist of the Dutch national beach volleyball team and the former physician of the Dutch national indoor volleyball team. At that time, just five case reports had been published worldwide on volleyball players with finger ischemia due to arterial emboli originating from a thrombosed aneurysm in the PCHA in the dominant shoulder. 68,95,96,115,126 Knowledge about this injury needs to be extended on an international scale considering the potential amputation of a finger as the devastating end result in a population of young, healthy and fit elite volleyball players. Therefore, from 2010 on, we set out to elucidate the unexplored entity of PCHA pathology among volleyball players. Figure 3 89 Digital Subtraction Angiography of the right hand of a 27-year-old volleyball player with ischemic symptoms of multiple digits. The arrows point to multiple abrupt stops in digital arteries, caused by microemboli General introduction I 13

17 Figure 4 89 Digital Subtraction Angiography of the right arm of a 27-year-old volleyball player with ischemic symptoms of multiple digits (the same player as in Figure 1). The arrow points to the abrupt stop of contrast in the posterior circumflex humeral artery caused by thrombosis. Pathogenesis Several studies suggest that repetitive powerful overhead movements in volleyball, like spiking and serving, cause chronic vessel wall injury as a result of positional traction and compression of the proximal PCHA. 3,17,95 This cumulative PCHA trauma can cause a continuum of pathology ranging from local intimal hyperplasia to vessel widening of <150% (dilatation) and >150% (aneurysm), and occlusion. 27 Although small in size, turbulent flow in these aneurysms readily produces mural thrombus, which has a high propensity to embolize to the distal extremity, particularly during repetitive overhead movements. 27 It is assumed that during the spiking and serving motion in volleyball, when the humeral head acts to compress the aneurysmal PCHA and the intraluminal thrombus like a tube of toothpaste, thrombi can be extruded from the aneurysmal artery branch into the axillary artery and embolize to the circulation of the forearm, hand, and digits. 49,95,126 Symptoms In an early stage of disease, symptoms might only manifest after overhead movements in volleyball as a result of embolization into the digital circulation. This can lead to a wide range of symptoms in the spiking hand during or directly after volleyball. Similar symptoms will often be caused by, and attributed to, musculoskeletal injuries 3, and might therefore initially be perceived as minor, and thus ignored by the athlete. As a 14 I Chapter 1

18 result, athletes generally present themselves in an advanced stage of the disease with debilitating symptoms of ischemia in the spiking hand in daily life, like coldness, discoloration and paresthesia. 68,95,96,115,126 These symptoms result in an inability to play volleyball and reduced daily quality of life, and may ultimately lead to necrosis and finger loss when trivialized. Therefore, awareness of these symptoms, with a timely detection is warranted. Which exact symptoms are associated with arterial emboli in the spiking hand originating from an aneurysmal and thrombosed PCHA in the dominant shoulder in volleyball players is unclear. Even so, the prevalence of these symptoms, related to digital ischemia and possibly due to vascular pathology in the shoulder, among elite indoor and beach volleyball players is unknown. These topics are addressed in Chapters 2, 4 and 5. 1 Diagnostics and imaging Diagnosis of PCHA pathology is established based on history-taking, physical examination and diagnostic imaging, both non-invasive and invasive. Non-invasive testing, like digital photoplethysmography and vascular ultrasound (US), are used in the work-up towards invasive testing, i.e. digital subtraction angiography (DSA), the standard of reference or less invasive computed tomographic angiography (CTA) and magnetic resonance angiography (MRA). All three are associated with ionizing radiation or the use of potentially nephrotoxic contrast media. However, these modalities are currently required for diagnosis and treatment planning. An attractive modality for low threshold vascular imaging is US, which is readily available, applicable on-site, inexpensive, and patient friendly. In general, US is the first-line imaging modality for peripheral aneurysm assessment. 42 It enables non-invasive measurement of vessel diameters and detection of intravascular thrombus. 42 Currently there is no standardized vascular US protocol available for imaging of the PCHA. 17 International standardization of PCHA imaging with US would assist in accurate assessment in both a clinical and screening setting, and for research purposes. Imaging of the PCHA with US is discussed in Chapters 6, 7 and 8. Imaging of the PCHA with MRA is described in Chapter 10. Treatment and rehabilitation Potential invasive treatment options include surgical ligation and endovascular coiling. 3 Coil embolization is an option if the proximal PCHA is relatively long, unaffected, and contains no thrombi. 3 Possible complications of coiling include the potential for further embolism and dislocation of coils or plugs. 3 Ligation of the PCHA can be performed if an endovascular approach is not possible or when it is preferred by either the patient or surgeon. Endovascular treatment can result in an earlier return to the previous level of competition compared to surgical ligation. 3 The rehabilitation programme might be supervised by a physiotherapist and consist of early mobilization without making the overhead motion, followed by a full active range of motion exercises approximately 6 weeks after surgery. A full return to the level of previous activity is realized within 3-4 months after surgery 120, with continuation of anti-thrombotic medication (aspirin 100 mg General introduction I 15

19 daily) for an arbitrary total of 6 months. 3 Since the effect of conservative management for PCHA pathology with symptomatic emboli in the spiking arm in volleyball players is unknown, it is elaborated on in Chapter 10. Prevention Knowledge about this vascular injury will raise awareness and enable recognition, which is an important factor in preventing serious ischemic complications. 3 As stated above, invasive treatment options for PCHA aneurysms result in several months of revalidation and absence from sports activities. However, if PCHA pathology can be detected at an early stage, serious ischemic complications, irreversible tissue damage, and surgical ligation of the PCHA might be prevented. 89 Since volleyball players are considered potentially at risk for developing critical digital ischemia, analysis of the presence of PCHA pathology, and associated risk factors, is warranted for prevention. Ultimately, as shown in Chapter 9, establishing risk profiles of individual athletes could support clinical management and optimize care. Moreover, since volleyball players become at risk for PCHA pathology when symptoms of digital ischemia arise, analysis of the presence of risk factors associated with these symptoms could serve as a first step in prevention. Therefore, Chapters 3 and 5 discuss risk factors associated with symptoms of digital ischemia in elite volleyball players. In summary then, elite volleyball players are at risk of ischemic digits due to arterial emboli originating from an aneurysmal and thrombosed PCHA in the dominant shoulder. Knowledge about this injury needs to be extended on an international scale considering the potential amputation of a finger as the devastating end result in a population of young, healthy and fit elite volleyball players. 16 I Chapter 1

20 1.2 RESEARCH QUESTIONS Based on the preceding arguments, the thesis is divided into three parts: I) symptomatology and associated risk factors; II) imaging; and III) clinical management, and involves the following research questions: 1 PART I - Symptomatology and associated risk factors 1. Which symptoms are most likely to be associated with PCHA pathology with distal embolization in the spiking hand in volleyball players? (Chapter 2) 2. Can the newly developed Shoulder PCHA pathology and digital Ischemia Questionnaire (SPI-Q) be used for the reliable detection of these symptoms in elite volleyball players? (Chapter 4) 3. What is the prevalence of these symptoms in the spiking hand among elite indoor and beach volleyball players? (Chapters 2 and 5) 4. Which risk factors are associated with these symptoms among elite indoor and beach volleyball players? (Chapters 3 and 5) PART II - Imaging 1. How can the proximal PCHA be assessed in a standardized way using vascular US, and can this be formulated in a protocol? (Chapter 6) 2. Can the newly developed Shoulder PCHA pathology and digital Ischemia UltraSound (SPI-US) protocol be used for reliable diameter assessment of the proximal PCHA and DBA? (Chapter 7) 3. What is the prevalence of PCHA aneurysms in the dominant shoulder among international elite indoor and beach volleyball players? (Chapter 8) 4. Which characteristics, such as anatomy, branching pattern, course and diameter, distinguish the PCHA from the DBA? (Chapter 8) PART III Clinical management 1. What is the association between PCHA pathology in the dominant shoulder and selfreported symptoms of digital ischemia in the spiking hand in elite volleyball players? (Chapter 9) 2. Which risk factors are associated with PCHA pathology in the dominant shoulder in elite volleyball players, and is a dose-response relationship present? (Chapter 9) 3. Can risk profiles of individual athletes be recognized based on the combination of the presence of PCHA pathology and symptoms of digital ischemia, and can clinical management guidelines be formulated per profile? (Chapter 9) 4. Can conservative management for a PCHA aneurysm with symptomatic embolization in the spiking arm in volleyball players be considered as an alternative to invasive treatment modalities? (Chapter 10) Research questions I 17

21

22 1.3 - OUTLINE OF THE THESIS In volleyball, spiking is the act of scoring a point by slamming the ball over the net into the opposing court effectively. 130 In this thesis, the first steps of elucidating the unexplored entity of Shoulder PCHA pathology and digital Ischemia in Known Elite volleyball players are made in order to provide an effective contribution to knowledge. Hence the title: SPIKE the PCHA. The thesis is divided into three parts: the first part covers symptomatology and associated risk factors, the second part focuses on imaging, and the third part concerns clinical management. 1 PART I Symptomatology and associated risk factors Chapter 2 describes which symptoms are most likely to be associated with PCHA pathology with distal embolization in volleyball players, and assesses the prevalence of these symptoms in the dominant limb among elite male indoor volleyball players in the Netherlands. In Chapter 3 we assess which risk factors are associated with self-reported symptoms of digital ischemia among elite male indoor volleyball players in the Netherlands. The test-retest reliability of the Shoulder PCHA pathology and digital Ischemia Questionnaire (SPI-Q), which can be used for the detection of self-reported symptoms of digital ischemia in elite volleyball players, is determined in Chapter 4. In Chapter 5 we assess the prevalence of self-reported symptoms of digital ischemia in the spiking hand, and associated risk factors, among international world-class beach volleyball players. PART II Imaging In Chapter 6, we present a 4-step standardized vascular ultrasound (US) protocol for the assessment of the proximal PCHA: the SPI-US protocol (Shoulder PCHA pathology and digital Ischemia UltraSound protocol). The inter-observer reliability of the SPI-US protocol for the diameter assessment of proximal PCHA and DBA is assessed in Chapter 7. In Chapter 8 the prevalence of PCHA aneurysms in the dominant shoulder of elite volleyball players is determined, and PCHA and DBA characteristics are described that can be used to accurately identify and assess the PCHA using the SPI-US protocol. Outline of the thesis I 19

23 PART III Clinical management In Chapter 9 four risk profiles among elite volleyball players are presented based on the presence of US-detected PCHA pathology in the dominant shoulder, reporting of symptoms of digital ischemia in the spiking hand, and identified risk factors. Per profile, guidelines for clinical management are proposed to optimize care. Chapter 10 describes the effect of conservative management for a PCHA aneurysm with symptomatic embolization in the spiking arm in a professional volleyball player with the use of novel Magnetic Resonance Angiography. 20 I Chapter 1

24

25

26 PART I Symptomatology and associated risk factors

27

28 CHAPTER 2 High prevalence of self-reported symptoms of digital ischemia in elite male volleyball players in the Netherlands: a cross-sectional national survey Daan van de Pol P. Paul F.M. Kuijer Ton Langenhorst Mario Maas American Journal of Sports Medicine. 2012;40(10): doi: /

29

30 ABSTRACT Background In the last three years six volleyball players with ischemic digits and small micro-emboli in the digital arteries of the dominant hand presented themselves in our hospital. These complaints were caused by an aneurysmatic dilatation of the posterior circumflex humeral artery (PCHA) with distal occlusion and digital emboli in the isolateral limb. All were elite male volleyball players active in the national top league. Little is known about the exact symptoms associated with PCHA pathology with digital emboli (PCHAP with DE) and its prevalence in elite volleyball players. If vascular injury can be identified at an early stage, thromboembolic complications and irreversible damage to the digits might be prevented. 2 Purpose To assess the prevalence of symptoms which are consistent with digital ischemia and may be due to PCHAP with DE in elite male volleyball players in the Netherlands. Study design Cross-sectional study. Methods A questionnaire survey was performed among elite volleyball players in the Dutch national top league and the Dutch beach volleyball team. The questionnaire was constructed using literature-based data on symptoms associated with PCHAP with DE, together with data retrieved from medical files. Results A total of 99 of the 107 athletes participated: a response rate of 93%. Most reported symptoms associated with PCHAP with DE were cold, blue or pale digits in the dominant hand during or immediately after practice or competition. The prevalence of these symptoms ranged from 11% to 27%. The prevalence of cold digits during practice and competition was 27%. The prevalence of cold, blue and pale digits during or immediately after practice and competition was 12%. Conclusion An unexpectedly high percentage of elite volleyball players reported symptoms that are associated with PCHAP with DE in the dominant hand. Since these athletes are considered potentially at risk for developing critical digital ischemia, further analysis of the presence of digital ischemia and PCHA pathology is warranted. Digital ischemia in elite volleyball players in the Netherlands I 27

31 INTRODUCTION In the last three years we have seen increased numbers of volleyball players with ischemic digits of the dominant hand. Following angiography of the hand and forearm, some of these players showed small microemboli in the digital arteries and were given thrombolytic therapy (Figure 1). Within weeks after return to play these players returned with identical complaints. Further evaluation, including angiography of the shoulder, showed an aneurysmatic dilatation of the posterior circumflex humeral artery (PCHA) with thrombus formation and emboli in the digital arteries of the isolateral limb (Figure 1 and 2). These players were treated by ligation of the PCHA to prevent further embolization and after rehabilitation returned to play at the highest level of competition after several weeks. All were elite male volleyball players playing in the national top league and between 21 and 31 years of age. In the Netherlands, with a total population of about 17 million, volleyball is one of the top three team sports and is played by more than 125,000 athletes on different levels. Of these athletes, some 110 elite volleyball players are active in the Dutch national top league. The presence of an aneurysm of the PCHA is a rare entity found in elite volleyball players 68,95,96,115,126, and often occurs at the origin of the PCHA but can also involve the axillary artery. 49 Besides for volleyball players, PCHAP with DE has also been described in the literature in baseball pitchers. 2,26,55,66,79,108,120 During the spiking or serving motion in volleyball, when the humeral head acts to compress the aneurysmal PCHA and the intraluminal thrombus like a tube of toothpaste, thrombi can be extruded from the aneurysmal artery branch into the axillary artery and embolize to the circulation of the forearm, hand, and digits. 26,49,66 The embolic complications of the affected extremity, in combination with pain and ischemia, can lead to the manifestation of this entity. 95,96,126 The aneurysm is occult as long as the player is free of symptoms 126, and collateral flow is so abundant that symptoms may not occur except at highest levels of exercise. 49 It is therefore recommended that these athletes be kept under periodic surveillance to detect arterial injury or abnormality to prevent irreversible damage. 68,108 However, little is known about the exact symptoms associated with PCHA pathology with digital emboli (PCHAP with DE) in elite volleyball players or the exact prevalence of these symptoms in these players. Many players would presumably have some degree of compression of the PCHA in an abducted and externally rotated position but will never develop any clinical abnormality requiring treatment. 68,108 Therefore, active surveillance of elite volleyball players with these symptoms could clarify the prevalence of these symptoms associated with PCHAP with DE. This type of surveillance has not been performed to date. Also, no screening or surveillance is currently available for this diagnosis. If vascular injury can be identified at an early stage in these volleyball players who experience apparently innocuous symptoms, thromboembolic complications and irreversible 28 I Chapter 2

32 damage to the digits might be prevented. 68,108 The aim of the present study is: 1) to assess which symptoms are most likely associated with PCHAP with DE; and 2) to assess the prevalence of these symptoms in the dominant limb among elite male volleyball players in the Dutch national top league and in the Dutch beach volleyball team 2 Figure 1 Digital Subtraction Angiography of the right hand of a 27-year-old volleyball player with ischemic symptoms of multiple digits. The arrows point to multiple abrupt stops in digital arteries, compatible with microemboli Figure 2 Digital Subtraction Angiography of the right arm of a 27-year-old volleyball player with ischemic symptoms of multiple digits (the same player as in Figure 1). The arrow points to the abrupt stop of contrast in the posterior circumflex humeral artery caused by thrombosis. Digital ischemia in elite volleyball players in the Netherlands I 29

33 MATERIALS AND METHODS Study Design A cross-sectional questionnaire survey was performed among elite volleyball players in the Dutch national top league and the Dutch beach volleyball team. Participants In cooperation with the Dutch Volleyball Association (Nevobo), all team managers of the Dutch national top league teams and the Dutch beach volleyball team were contacted and asked to participate in the study. After permission had been granted by the coaches, a researcher (DvdP) visited the team, explained the aim of the study and the pathology that they were potentially exposed to, and requested that the questionnaire be filled in right after a practice session during the competitive season. Participation was voluntary and anonymous. Questionnaires and return envelopes were left behind for players absent at the time of the visit. This survey was administered once during the season After one and three weeks respectively, a polite reminder was sent by , requesting that the questionnaire be returned within one month after the initial group session. No official approval of the Medical Ethics Review Committee at our academic hospital was needed for this questionnaire survey to be conducted. Questionnaire Content After a literature review, a questionnaire was developed to detect ischemic symptoms using reports of the same patients with confirmed abnormalities of the PCHA. The focus of the study was to detect ischemic symptoms known to be associated with DE from an abnormal PCHA and to determine the frequency of these symptoms. The symptoms are usually temporary and resolve after volleyball participation. This preliminary survey was evaluated by four members of the Dutch beach volleyball team to improve its readability. The questionnaire comprised two general domains: those regarding the individual player and those regarding specific symptoms associated with digital ischemia. The questions used in this study are shown in Table 1. Symptoms from medical literature A search in Pubmed and SPORTdiscus was performed to identify studies that reported on cases of PCHAP with DE. The search was carried out from the earliest date possible to July 7, 2011 using a combination of the following key words (MeSH and/or text words): aneurysm AND posterior circumflex humeral artery AND volleyball. This resulted in four references in Pubmed and one reference in SPORTdiscus. Studies were included if they reported on at least one case of PCHAP with DE in elite volleyball players and if symptoms of the disease were reported. After checking for duplicates, this resulted in the inclusion of three studies. Furthermore, checking the reference list of the included 30 I Chapter 2

34 studies resulted in one additional study. Finally, an expert in our academic hospital suggested one more study, resulting in five studies being included: five case reports on a total of nine elite volleyball players with PCHAP with DE. 68,95,96,115,126 Symptoms from medical files An expert on sports radiology (MM) provided a list of elite volleyball players who visited our academic hospital with complaints suspected of being a vascular injury. These medical files were analysed and patient reports were included if they involved volleyball players at a national or regional level diagnosed with PCHAP with DE without other comorbidity, and if they received treatment at our hospital for the injury. Six patients were included, all between 21 and 31 years of age, treated in the period between November 2008 and November Table 2 shows that in the medical literature, 89% of the patients reported cold digits in general and 56% reported this complaint during or immediately after practice or competition. For the sake of clarity, in 44% of the patients the presence or absence of these complaints was not reported. Furthermore, 89% reported discoloured digits (blue or pale) and 67% reported pain in the digits in general (Table 2). In the medical files, 100% of the patients reported cold digits in general, as well as 100% during or immediately after practice or competition. Moreover, 50% reported discoloured digits and 50% reported pain in the digits in general (Table 2). All the above-mentioned symptoms were reported in the dominant hand. Selection of symptoms associated with PCHA pathology with digital emboli In order to specify which symptoms are most likely associated with PCHAP with DE, the symptoms mentioned in the medical literature and medical files were reviewed (Table 2). We decided that symptoms suggesting an association should be reported as present in at least 50% of the patients from the medical literature and/or medical files and should not be reported as absent in these patients. As shown in Table 2, only complaints of cold digits in general, cold digits during or immediately after practice or competition and discoloured digits (all in the dominant hand) met this criterion. General pain was excluded due to the fact that one patient reported the absence of this symptom. In addition, it is hard to distinguish ischemic pain from pain resulting from trauma and as a result, a positive answer on this question could potentially lead to high false-positive rates due to this symptom. Finally, this decision was supported by Jackson 49, who stated that the signs of ischemia that typically distinguish arterial injuries from musculoskeletal injury are those of changes in temperature and colour. Additionally, these symptoms had to occur during or immediately after practice or competition because symptoms are most likely to occur at high levels of exercise 49, when Digital ischemia in elite volleyball players in the Netherlands I 31

35 during the spiking motion in volleyball, thrombi can be extruded from the aneurysmal PCHA into the axillary artery and embolize to the circulation of the forearm, hand and digits. 26,49,66 This is supported by the high percentage of patients that reported cold digits specifically during or after practice or competition (Table 2). Table 1 shows the formulated questions based on these symptoms labelled as associated with PCHAP with DE, as asked in the questionnaire. Table 1 Questions regarding the individual player and specific symptoms associated with digital ischemia, as asked in the questionnaire 1 What is your age? 2 What is your body height? 3 What is your body weight? 4 How many years in total do you play volleyball? 5 How many years do you play professional volleyball? 6 How many hours in total do you play volleyball in a week (training and competition)? 7 Does cardiovascular disease occur in your family? 8 Do you smoke or have you smoked in the past? 9 Do you suffer from one or more cold fingers in your dominant hand a. during practice or competition? b. immediately after practice or competition? 10 Do you suffer from one or more blue fingers in your dominant hand a. during practice or competition? b. immediately after practice or competition? 11 Do you suffer from one or more pale fingers in your dominant hand a. during practice or competition? b. immediately after practice or competition? 32 I Chapter 2

36 Table 2 Symptoms associated with PCHA pathology with digital emboli in the dominant arm in elite volleyball players Symptoms Medical literature 5 studies, 9 patients Yes/No/Not Reported Medical files 6 files, 6 patients Yes/No/Not Reported 2 Cold digits in general 8/0/1 6/0/0 during or immediately after practice or competition 5/0/4 6/0/0 provoked by cold circumstances 2/0/7 3/0/3 Discoloured/blue/pale digits 8/0/1 3/0/3 Pain in digits in general 6/1/2 3/0/3 provoked by cold circumstances 0/1/8 1/0/5 Pain in forearm 2/0/7 0/0/6 Pain in shoulder 0/1/8 2/0/4 Pressure pain of the hand palm 0/0/9 1/0/5 Cramping of the hand palm 1/0/8 0/0/6 Sensibility dysesthesias or paresthesias in digits 3/4/2 2/0/4 decreased sensibility or numbness in digits 1/3/5 1/2/3 Early arm fatigue or less endurance 0/1/8 1/0/5 Decrease in arm strength 0/1/8 1/0/5 Splinter haemorrhages under nails 2/0/7 0/0/6 Swelling of the digits 1/0/8 0/0/6 Digital ischemia in elite volleyball players in the Netherlands I 33

37 Data analyses The data from the returned questionnaires were entered in SPSS (version 16.0, 2007, SPSS Inc.). The questionnaires were randomly checked for correct data entry by a second researcher (PK). Mean, standard deviation, minimum and maximum of age, body height, body weight, total years playing volleyball, years playing professional volleyball and weekly hours playing volleyball in practice or competition were reported for the group as a whole. Also, the percentages of volleyball players who reported a family history of cardiovascular disease and (had) smoked were reported. The prevalence of symptoms associated with PCHAP with DE was calculated in the following manner: the percentage of all volleyball players who sometimes or more often reported having cold or blue or pale digits in the dominant hand during or directly after practice or competition. The prevalence of a combination of these symptoms associated with PCHAP with DE was calculated in the following manner: the percentage of all volleyball players who sometimes or more often reported having cold and blue and pale digits in the dominant hand during or directly after practice or competition. RESULTS Participants Ten of the 11 included volleyball teams participated in our study. Ninety-nine of the 107 included volleyball players completed and returned the questionnaire: a response rate of 93%. On average, participants were 24 years old, had a body height of 196 centimeters and had been playing professional volleyball for four years and 17 hours a week (Table 3). Fifty-one percent of the participants reported that there was no presence of cardiovascular disease in their family, 29% gave an affirmative answer and 20% reported they did not know (n=98). Seventy-eight percent of the participants reported that they did not smoke and never had smoked in the past, and 22% smoked or had smoked in the past. Prevalence of symptoms associated with digital ischemia in the dominant hand The prevalence of complaints of cold digits during practice or competition in the participants was 27% (Table 4). In this group of participants (n=27), 41% reported that there was no presence of cardiovascular disease in their family (n=11), 41% gave an affirmative answer (n=11) and 18% reported they did not know (n=5). Also, in this group of participants, 70% reported that they did not smoke and never had smoked in the past (n=19), and 30% smoked or had smoked in the past (n=8). The prevalence of complaints of cold digits immediately after practice or competition in the participants was 17%. The prevalence of complaints of blue digits during and immediately after practice or compe- 34 I Chapter 2

38 tition was respectively 18% and 11%. The prevalence of complaints of pale digits during and immediately after practice or competition was respectively 20% and 12% (Table 4). The prevalence of participants who sometimes or more often reported complaints of a combination of both cold and pale and blue digits, during or immediately after practice or competition was 12%. The reported prevalence of a combination of cold and blue digits was 17%, the reported combination of both cold and pale digits was 19% and the reported combination of blue and pale digits was 12% (Table 5). 2 Table 3 Individual characteristics of the participants N Mean SD Minimum Maximum Age (years) Body height (centimeters) Body weight (kilograms) Years volleyball Years professional volleyball Hours volleyball per week Table 4 Prevalence of symptoms associated with digital ischemia during or immediately after practice or competition in the dominant hand in elite male volleyball players (n=99) During practice or competition Immediately after practice or competition Total Sometimes Often Always Total Sometimes Often Always Cold digits 27%* 18%* 8%* 1%* 17% 13% 4% 0% Blue digits 18% 13% 4% 1% 11% 9% 2% 0% Pale digits 20% 15% 4% 1% 12% 11% 1% 0% * n=98 Digital ischemia in elite volleyball players in the Netherlands I 35

39 Table 5 Prevalence of a combination of symptoms associated with digital ischemia during or imme-diately after practice or competition in the dominant hand in elite male volleyball players (n=99) During or immediately after practice or competition Cold AND blue AND pale digits 12% Cold AND blue digits 17% Cold AND pale digits 19% Blue AND pale digits 12% DISCUSSION The main finding of this questionnaire survey among 99 elite volleyball players is that 27% of respondents reported that they sometimes or more often suffered from cold digits in the dominant hand during practice or competition, with 17% reporting this complaint immediately after practice or competition. Moreover, 12% suffered from a combination of cold and pale and blue digits in the dominant hand during or immediately practice or competition. One would not expect such high rates of complaints, highly related to digital ischemia and potentially due to vascular disease, among young, healthy and fit elite athletes with a mean age of 24 years. Strengths and weaknesses of the study A total of about 110 elite volleyball players across ten teams are active in the Dutch national top league. Nine of these teams participated in the study and 91 of the 99 players from these teams completed the questionnaire, as well as eight out of eight elite volleyball players from the Dutch beach volleyball team. As a result, 99 of 107 players completed the survey: a response rate of 93%. Due to this high percentage, the obtained results are representative of the actual prevalence of reported complaints associated digital ischemia and potentially due to PCHAP with DE among male elite volleyball players in the Netherlands in the season Since the surveyed symptoms were derived from data derived from medical literature, together with data retrieved from medical files, these symptoms are related to digital ischemia and potentially due to vascular disease. This contributes to the content validity of our questionnaire. Moreover, the symptoms were surveyed in clear and understandable language and are easily recognized by the players, ensuring the reliability of the answers. The sensitivity and specificity of the surveyed symptoms for digital ischemia and PCHAP with DE in our study population has yet to be determined. 36 I Chapter 2

40 The presence of these symptoms in elite volleyball players can also be explained by a wide variety of vascular pathologies including cardiac embolism, atherosclerosis, vasculitides, arterial thoracic outlet syndrome (TOS), hypothenar hammer syndrome (HHS), quadrilateral space syndrome (QSS), and vasomotor disorders such as Raynaud s phenomenon. Given the young age of these athletes, and their high levels of fitness, the presence of cardiac embolism, atherosclerosis and vasculitides seems unlikely to be the cause of the complaints. Of the other disorders, Raynaud phenomenon is the most common with a prevalence of 8% in US white men 117 and 1-10% in Dutch men depending on the definition used. 10 In contrast, the median age at onset of primary Raynaud s phenomenon is 14 years 129, while secondary Raynaud s phenomenon often arises after the age of 40 years with the underlying disease frequently evident at the time of disease onset. 14 Furthermore, Raynaud s phenomenon spreads symmetrical to all fingers of both hands. 129 The other disorders are even less common in this demographic. Therefore, other potential etiologies are considered less likely. Since the symptoms of the abovementioned pathologies overlap that of digital ischemia and PCHAP with DE, sports medicine specialists should remain alert to the possibility of vascular pathology in elite athletes using repetitive overhead arm motions and complaining of ischemia-related symptoms. 2,49,68,75,108 When an athlete presents himself with these symptoms, further investigation should demonstrate which exact condition is the cause. It is important to realize that all these diseases should be taken seriously and, if not diagnosed in time, can lead to significant functional impairment and a worsened prognosis. 2 To verify whether the symptoms described in the study population are actually associated with digital ischemia and PCHAP with DE, additional research is required. Contrast arteriography is the gold standard for visualizing the upper limb arterial system 44, with computed tomography angiogram (CTA) 44, and magnetic resonance angiography (MRA) 21 as alternatives. However these methods are time-consuming, expensive and invasive. An alternative might be non-invasive vascular laboratory testing like measurement of finger pressures and waveforms. Although these studies can confirm or rule out digital ischemia, they cannot identify the source of injury in the face of an abnormal test. 49 Additional imaging like ultrasound with Doppler is an easy, quick and reliable way to assess the axillary artery and its branches, like the PCHA, and thus identify any incipient compression, thrombosis or aneurysm. 55, These methods provide a non-invasive and quick way to assess the sensitivity and specificity of our questionnaire, regarding the prediction of digital ischemia and PCHAP with DE. Implications for practice The high prevalence of suspicious complaints among healthy volleyball players suggests that the numbers of volleyball players that present themselves in hospital with symptoms of digital ischemia potentially as a result of PCHAP with DE represents only a fraction of the number of volleyball players who suffer from less innocuous symptoms of ischemic Digital ischemia in elite volleyball players in the Netherlands I 37

41 digits. This may be the result of an early stage of this disease, stressing the importance of active surveillance and a better insight into modifiable risk factors to achieve effective prevention. Active surveillance should make it possible to identify vascular injury at an early stage in those volleyball players who experience apparently innocuous symptoms. In this way, thromboembolic complications and irreversible damage to the digits might be prevented 68,108, thereby possibly making surgical ligation of the PCHA unnecessary. This type of surveillance among elite volleyball players to identify those with PCHA compression, thrombosis, or aneurysm has not been performed to date since this type of screening could potentially lead to many false-positive results. 68,108 However, the team physician could offer a short screening questionnaire, for example twice a year, to his team in order to identify those players with inducing or exacerbating complaints of cold or discoloured digits. Because symptoms mostly occur during practice or competition, surveillance might be most relevant after periods with increased physical activity, such as a few weeks after the start of the training season and a few weeks after the winter recess. Players might be more vulnerable in these periods. In this way, players with suspicious symptoms can be selected and after history and a physical examination, a referral for the appropriate vascular tests can be made. Moreover, by completing the questionnaire, the volleyball player himself hopefully becomes more aware that the apparently innocuous symptoms can ultimately lead to a serious injury. The characteristics of this condition meet most of the criteria of Wilson and Jungner 131, and would therefore be suitable for surveillance. Furthermore, given the high prevalence of complaints suspicious to digital ischemia in this young population of healthy athletes, modifiable risk factors should be identified to achieve effective prevention. Potential risk factors include both personal-, sports- and work-related risk factors. An example of a personal risk factor is an anatomical variance of the origin of the arteria circumflex humeri 120, possibly resulting in a predisposition for vascular pathology. 97 This anatomical variation has not been described in our included medical files and case reports. Examples of sports-related risk factors are the number of hours playing volleyball in a week, the number of spikes in a practice session, position in the field, and number of hours performing strength training above shoulder height. McIntosh et al. 68 suggested that guidelines need to be developed for practice time and/ or number of hits per day. Finally, the influence of physical strain during daily working activities could be a contributing factor. Examples might be working with vibrating tools and performing repetitive work with the arms above shoulder height. 24,70,113,135 In conclusion, symptoms of cold, blue or pale digits in the dominant hand during or immediately after practice or competition are related to digital ischemia and seem associated with PCHAP with DE. An unexpectedly high percentage of interviewed 38 I Chapter 2

42 elite male volleyball players in the Netherlands reported these symptoms: depending on these symptoms (or a combination of them), the prevalence varied between 27% and 11%. Since these athletes are considered potentially at risk for developing critical digital ischemia, further analysis of the presence of digital ischemia and pathology of the posterior circumflex humeral artery is warranted. In addition, more attention should be given to periodic surveillance and prevention. 2 Digital ischemia in elite volleyball players in the Netherlands I 39

43

44 CHAPTER 3 Risk factors associated with self-reported symptoms of digital ischemia in elite male volleyball players in the Netherlands Daan van de Pol P. Paul F.M. Kuijer Ton Langenhorst Mario Maas Scandinavian Journal of Medicine & Science in Sports. 2014;24(4):e230-e237. doi: /sms.12145

45

46 ABSTRACT One in every four elite male volleyball players in the Netherlands reported blue or pale digits in the dominant hand. Little is known about risk factors. To assess whether personal-, sports- and work-related risk factors are associated with these symptoms in these volleyball players, a survey was performed among elite male volleyball players in the Dutch national top league and the Dutch beach volleyball team. The questionnaire assessed the presence of symptoms and risk factors. Binary logistic regression was performed to calculate Odds Ratios (OR). A total of 99 of the 107 athletes participated a response rate of 93%. Two sports-related risk factors were associated with symptoms of blue or pale digits: 18 to 30 years playing volleyball (OR=6.70; 95%CI ) and often/always performing weight training to increase dominant limb strength (OR=2.70; 95%CI ). No significant other sports-, personal- or work-related risk factors were found. Playing volleyball for more than 17 years and often/always performing weight training to increase dominant limb strength were independently associated with an increased risk on ischemia-related complaints of the dominant hand in elite male volleyball players. 3 Risk factors for digital ischemia in elite volleyball players in the Netherlands I 43

47 INTRODUCTION Symptoms of cold, blue and pale digits in the dominant hand during or immediately after practice or competition are associated with digital ischemia. A striking percentage of 31% of elite male volleyball players with a mean age of 24 years reported at least one of these symptoms in the dominant hand. 89 This high prevalence of potential vascular pathology, detected using a literature-based questionnaire, has led to some concerned publicity in the international media. 40 High rates of complaints, strongly related to digital ischemia, are not expected in these young, healthy elite athletes. The presence of unilateral ischemia-related symptoms in the upper extremity in elite male volleyball players can be explained by a wide variety of vascular pathologies, including arterial thoracic outlet syndrome 97, aneurysms of the axillary artery or its branches 3,49,89, quadrilateral space syndrome 97, forearm vessel aneurysms like the antebrachial-palmar hammer syndrome 57, hypothenar hammer syndrome 65, digital arterial pathology 19,46,48,116, and vasomotor disorders such as Raynaud s phenomenon 14,129, and Raynaud-like vasospasm of the digital arteries. 66 Given the high prevalence raising the suspicion of digital ischemia in these elite male volleyball players, risk factors should be identified as a first step in prevention. Potential risk factors include both personal-, sports-related and work-related risk factors. No epidemiological studies on this subject have been found in the medical literature. Therefore, the aim of the present study is to assess which risk factors are associated with self-reported symptoms of digital ischemia among elite male volleyball players in the Dutch national top league and in the Dutch beach volleyball team. MATERIALS AND METHODS Study design A cross-sectional questionnaire survey was performed among elite volleyball players in the Dutch national top league and the Dutch beach volleyball team to assess risk factors associated with self-reported symptoms of digital ischemia. The results of the prevalence of self-reported symptoms of digital ischemia in elite male volleyball players in the Netherlands have previously been reported. 89 The Medical Ethics Review Committee of our academic hospital has informed us that the Medical Research Involving Human Subjects Act (WMO) did not apply to this questionnaire survey and that no official approval of this study was required. 44 I Chapter 3

48 Participants In cooperation with the Dutch Volleyball Association (Nevobo), all team managers of the Dutch national top league teams and the Dutch beach volleyball team were invited to participate in the study. After permission had been granted by the coaches, a researcher (DvdP) visited the team, explained the aim of the study and the pathology that they were potentially at risk of, and requested that the questionnaire be filled in immediately after a practice session during the competitive season. Participation was voluntary and anonymous. Questionnaires and return envelopes were left behind to be picked up and completed by players absent at the time of the visit. This survey was administered once during the season. After one and three weeks respectively, a polite reminder was sent by , requesting that the questionnaire be returned within one month of the initial group session. 3 Questionnaire content A literature-based questionnaire was developed to detect ischemic symptoms using reports of volleyball players with confirmed digital ischemia. 89 In this study, symptoms of cold, blue and pale digits in the dominant hand during or immediately after practice or competition were considered to be associated with digital ischemia based on the following arguments: these symptoms were the only symptoms that were reported as present, in at least 50% of the medical files of volleyball players with confirmed digital ischemia at our hospital; 2. pain was excluded because it is hard to distinguish between ischemic pain and pain resulting from trauma; 3. Jackson 49 stated that the signs of ischemia that typically distinguish arterial injury from musculoskeletal injury are those of changes in temperature and colour. In the questionnaire survey, additional questions were formulated to detect and assess potential risk factors possibly associated with digital ischemia. The questionnaire comprised four general domains: those regarding demographics, like age; those regarding personal risk factors, like smoking; those regarding sports-related risk factors like years spent playing volleyball, and those regarding work-related risk factors like working with vibrating tools (Appendix A). Data analyses The data from the returned questionnaires were entered in SPSS (version 16.0, 2007, SPSS Inc.). The questionnaires were randomly checked for correct data entry by a second researcher (PK). Participants Two groups were formed, with one group consisting of volleyball players with symptoms of blue or pale digits in the dominant hand during or immediately after practice or Risk factors for digital ischemia in elite volleyball players in the Netherlands I 45

49 competition, and the other group consisting of players without these symptoms. Additionally, volleyball players who reported only cold digits in the dominant hand during or immediately after competition without reporting blue or pale digits (n=5) were excluded from the analysis, because this symptom was considered less specific for digital ischemia. Mean, standard deviation, minimum and maximum of age, body height, body weight and number of working hours per week were reported for both groups. Also, the percentage of volleyball players who reported shoulder injury history, the use of medicine, and paid or unpaid work were reported for both groups. Risk factors First, to assess differences between the symptomatic and asymptomatic group, personal-, sports-related and work-related risk factors were tested using an independent T-test or a Chi-Square test. Where a frequency in a cell of the 2x2 table was smaller than 5, a Fisher s Exact test was used instead of a Chi-Square test to calculate the p-value. In all tests, a p-value 0.10 was considered significant given the relatively small group size and to overcome missing potential clinically relevant differences. Next, the Odds Ratio (OR) and 95%-confidence interval (95%CI) were calculated for all personal, sports-related and work-related risk factors using a univariate binary logistic regression. The personal, sports-related and work-related risk factors are listed in Appendix A. Finally, for the risk factors with a p-value 0.10, an OR and 95% CI were calculated using a multivariate binary logistic regression. RESULTS Ten of the 11 included volleyball teams participated in our study. Ninety-nine of the 107 included volleyball players completed and returned the questionnaire a response rate of 93%. Participants Two groups were formed based on the case definition: 1. Players who reported blue or pale digits in the dominant hand during or directly after practice or competition sometimes or more often (n=26) (Symptomatic group) 2. Players who did not report cold or blue or pale digits in the dominant hand during or directly after practice or competition sometimes or more often (n=68) (Reference group) 46 I Chapter 3

50 Volleyball players in the symptomatic group were on average 25 years old and in the reference group 24 years old, weighed 86.0 and 87.4 kg and had a body height of cm and cm, respectively (Table 1). The participants in both groups did not differ significantly (Table 1). Table 1 Characteristics of the participants Symptomatic group (n=26) Reference group (n=68) Significance 3 Age (years) Mean: 25.0 SD: 5.3 Range: Mean: 24.0 SD: 4.3 Range: t = 0.98 p = 0.33 Body height (centimeters) Mean: SD: 6.6 Range: Mean: SD: 7.6 Range: t = 0.49 p = 0.62 Body weight (kilograms) Mean: 86.0 SD: 7.1 Range: Mean: 87.4 SD: 7.4 Range: t = p = 0.40 Shoulder injury history (Yes: +, No: -) +: 13/26 (50%) -: 13/26 (50%) +: 23/67 (34%) -: 44/67 (66%) χ 2 = 1.94 p = 0.16 Use of medicine (Yes: +, No: -) +: 2/26 (8%) -: 24/26 (92%) +: 1/67 (2%) -: 66/67 (98%) χ 2 = 2.31 p = 0.19 Paid or unpaid work (Yes: +, No: -) +: 14/26 (54%) -: 12/26 (46%) +: 36/68 (53%) -: 32/68 (47%) χ 2 = 0.01 p = 0.94 Number of working hours per week (hours) Mean: 15.3 SD: 18.3 Range: 0-50 Mean: 12.0 SD: 15.5 Range: 0-50 t = 0.88 p = 0.38 Risk factors Personal risk factors The Chi-Square test revealed no significant differences between both groups for personal risk factors like smoking and family on cardiovascular disease (Appendix A). An overview of all personal risk factors is shown in Appendix A. Also, no significant associations were found in the results of the univariate binary logistic regression analyses (Table 2). Sports-related risk factors On average, volleyball players in the symptomatic group had played volleyball for 16 years and in the reference group for 13 years. This difference was significant (t=1.85, p=0.07). A significant difference was also found for the frequency of performing weight training to increase dominant limb strength (65% versus 41%) (χ 2 = 4.42, p=0.04) (Appendix A). For Risk factors for digital ischemia in elite volleyball players in the Netherlands I 47

51 the other sports-related risk factors both groups did not differ significantly. An overview of these risk factors is shown in Appendix A. The univariate binary logistic regression revealed significant associations for the following two sports-related risk factors: total years playing volleyball (OR=1.01; 95%CI ), and the frequency of performing weight training to increase dominant limb strength (OR=2.70; 95%CI ) (Table 2). For the other sports-related risk factors the univariate binary logistic regression revealed no significant associations like years playing professional volleyball (OR=1.03; 95%CI ) or total practice and competition hours in a week (OR=1.00; 95%CI ) (Table 2). Work-related risk factors The Chi-Square test and independent t-test revealed no significant differences between both groups regarding the work-related risk factors. An overview of these risk factors is shown in Appendix A. Also, no significant associations were revealed in the univariate binary logistic regression analyses (Table 2). Table 2 Univariate binary logistic regression outcomes (odds ratio and 95% confidence interval) of potential risk factors associated with self-reported symptoms of digital ischemia in elite male volleyball players Personal risk factors Symptomatic group versus reference group Smoking (Yes) OR 1.53 (95% CI ) Use of alcohol (Yes) OR 0.36 (95% CI ) Family history on cardiovascular disease (Yes) OR 2.26 (95% CI ) Sports-related risk factors Total years playing volleyball OR 1.01 (95% CI ) * Years playing professional volleyball OR 1.03 (95% CI ) Total practice and competition hours in a week OR 1.00 (95% CI ) Position in the field (Attacker) OR 0.67 (95% CI ) Smashing away from the shoulder (Often/Always) OR 2.05 (95% CI ) Type of service (Jump service) OR 1.03 (95% CI ) Performing dominant limb weight training in general (Yes) OR 2.42 (95% CI ) Frequency of performing dominant limb weight training during warming-up before practice (Often/Always) OR 0.84 (95% CI ) 48 I Chapter 3

52 Symptomatic group versus reference group Number of minutes per week performing dominant limb weight training during warming-up before practice Frequency of performing dominant limb weight training during warming-up before competition (Often/Always) Number of minutes per week performing dominant limb weight training during warming-up before competition Frequency of performing weight training to increase dominant limb strength (Often/Always) Number of hours per week performing weight training to increase dominant limb strength Frequency of performing weight training to maintain dominant limb strength (Often/Always) Number of hours per week performing weight training to maintain dominant limb strength Work-related risk factors OR 1.00 (95% CI ) OR 0.63 (95% CI ) OR 1.00 (95% CI ) OR 2.70 (95% CI ) * OR 1.53 (95% CI ) OR 1.45 (95% CI ) OR 1.75 (95% CI ) 3 Perceived heaviness of work (Scale 0-10) OR 0.89 (95% CI ) Working with vibrating tools more than 1 hour per day (Often/Always) Working in a cold environment more than 1 hour per day (Often/Always) Performing repetitive work with the arms more than 2 times per minute (Often/Always) Working above shoulder height more than 1 hour per day (Often/Always) OR 0.00 (95% CI ) ** OR 0.00 (95% CI ) ** OR 0.76 (95% CI ) OR 0.00 (95% CI ) ** Performing work with tools heavier than 1 kg (Often/Always) OR 1.81 (95% CI ) Performing work with a computer or mouse more than 4 hours per day (Often/Always) OR 0.90 (95% CI ) Lifting over 15 kg per day (Often/Always) OR 2.09 (95% CI ) Performing powerful work with the hands (like screwing or kneading) more than 1 hour per day (Often/Always) OR 0.90 (95% CI ) * = significant (p 0.10) ** = no odds ratio (OR) could be calculated because no volleyball players reported being exposed to this risk factor Risk factors for digital ischemia in elite volleyball players in the Netherlands I 49

53 Multivariate regression outcomes The multivariate binary logistic regression revealed significant associations for two sports-related risk factors: total years playing volleyball with OR 1.11 (95%CI ) and the frequency of performing weight training to increase dominant limb strength with OR 3.56 (95%CI ) (Table 3). After categorizing the total years playing volleyball in four categories (0-10 years, years, years, and years) as well as the frequency of performing weight training to increase dominant limb strength (never, sometimes, often, always), the multivariate binary logistic regression revealed a significant association for the subcategory years playing volleyball with OR 6.70 (95%CI ). A non-significant result was found for often/always performing weight training to increase dominant limb strength with an OR 3.41 (95% CI ) and OR 3.96 (95%CI ), respectively. For the other subcategories, the multivariate binary logistic regression also revealed no significant differences. Table 3 Multivariate binary logistic regression outcomes (odds ratio and 95% confidence interval) of two sports-related risk factors: total years playing volleyball and frequency of performing weight training to increase dominant limb strength Symptomatic group versus reference group Total years playing volleyball OR 1.11 (95% CI ) 0-10 years (n=25) Reference years (n=22) OR 1.88 (95% CI ) years (n=23) OR 1.63 (95% CI ) years (n=22) OR 6.70 (95% CI ) Frequency of performing weight training to increase dominant limb strength never (n=16) OR 3.56 (95% CI ) Reference sometimes (n=33) OR 0.85 (95% CI ) often (n=27) OR 3.41 (95% CI ) always (n=18) OR 3.96 (95% CI ) 50 I Chapter 3

54 DISCUSSION The main finding of this questionnaire survey among 99 elite male volleyball players is that the total years playing volleyball, and the frequency of performing weight training to increase dominant limb strength were identified as risk factors associated with selfreported symptoms of digital ischemia. Regardless of the cause of these apparently innocuous complaints, the identification of these risk factors could serve as a first step in prevention. 3 Risk factors and etiology These two sports-related risk factors might be related to 1) repetitive blunt trauma to the forearms and hands, and 2) repetitive rotary movements of the shoulder girdle, both possibly resulting in an overload and deterioration of vascular structures. It has been suggested that vascular trauma is likely to be sustained during extreme hours of practice 68, and that reduction in training duration and intensity should result in less overload of the dominant limb, thereby providing a greater opportunity for tissue recovery. 100 Studies among athletes exposed to repetitive blunt trauma to the forearms and hands have reported ischemia-related symptoms of the hand as a result of forearm vessel aneurysms 57, hypothenar hammer syndrome 65, digital arterial pathology 19,46,48,116, and Raynaud-like vasospasm of the digital arteries. 66 Studies among athletes who practice repetitive rotary movements of the shoulder girdle have reported ischemia-related symptoms of the hand as a result of arterial thoracic outlet syndrome 97, quadrilateral space syndrome 97, and aneurysms of the axillary artery 49 or its branches, like the posterior circumflex humeral artery (PCHA). Aneurysms of the PCHA have been reported in elite volleyball players 3,68,89,95,96,115,126, and baseball pitchers. 2,26,55,66,79,108,120 During a volleyball player s career, the exposure to blunt trauma to the forearms and hands increases gradually due to the numerous spikes, serves, passes, and other movements required in elite volleyball. 100 This cumulative effect might explain why a volleyball career of more than 17 years is associated with a significant 6.7-fold increased risk on ischemia-related complaints in the dominant hand. Furthermore, as a result of often/ always performing weight training to increase dominant limb strength, the volleyball player might acquire more power in his strokes. This could lead to more vigorous spikes and serves resulting in an increased moment of impact of the ball on the dominant hand and thus more blunt trauma to local vascular structures. In addition, also the type of weight training might be stressful for vascular structures. However, we have no data about the type of kinetics performed. Again, there seems to be a cumulative effect since often/always performing this type of weight training is associated with a significant 2.7- fold higher risk of ischemia-related complaints in the dominant hand compared to never Risk factors for digital ischemia in elite volleyball players in the Netherlands I 51

55 and sometimes performing this training. Our results suggest that especially strengthincreasing weight training, and not weight training itself, results in an increased risk. Other potential risk factors assessed in this study did not lead to a significant result. For instance, the number of practice and competition hours per week could have been a contributing factor. Some studies have suggested a reduction in training intensity 100, and guidelines for number of smashes, practice and competition hours per day 68, in order to prevent dominant limb overload. Although a relation between reported symptoms and the number of practice and competition hours per week seemed plausible, our study did not reveal this relation. The same was true for position in the field as suggested by Rosi et al. 105 and McIntosh et al. 68. Regarding work-related risk factors, working with vibrating tools was thought to be a potential risk factor. Studies have demonstrated that these activities could lead to digital artery occlusion 23, and to acute reductions in finger blood flow. 135 Van der Worp et al. 134 concluded that volleyball players with physically demanding jobs have an increased risk of developing patellar tendinopathy. A similar increased work-related risk might have been present for hand injuries in volleyball players working with vibrating tools and performing repetitive work with the arms above shoulder height. 23,24,70,113,135 However, our results did not provide evidence for this relation in Dutch elite male volleyball players with blue and pale digits. Relevance for clinical sport practice At the moment, the existing literature on the prevention of volleyball injuries and it s risk factors is relatively sparse. 100 However, a number of studies have addressed this topic in the past. 4,8,125,133 Given the high prevalence of complaints raising the suspicion of digital ischemia in young, healthy athletes, the identification of the sports-related risk factors playing volleyball for more than 17 years and often/always performing weight training to increase dominant limb strength might be a first step in prevention. The overview of the other potential risk factors should also make it possible to monitor or modify these factors at an early stage in those volleyball players experiencing apparently innocuous symptoms. In this way, the onset or worsening of thromboembolic complications and irreversible damage to the digits might be understood and prevented. 68,108 With regard to the years playing volleyball, it is clear that this is a non-modifiable risk factor. However, this result implies that in surveillance, for instance by using a screening questionnaire 89, extra attention should be given to players who have played volleyball for more than 17 years. A weakness of the present study is that, although an association between performing weight training to increase dominant limb strength and reported ischemia-related symptoms in the dominant hand was found, the specifics of this strength training were not defined. Therefore, before recommendations regarding potentially more suitable exercises can be made, a better insight into a player s strength exercise routines should 52 I Chapter 3

56 be obtained. Biomechanical factors, like the exact type of movements and range of motion, and training characteristics like intensity, frequency and duration might be relevant. Another weakness is the lack of proof of actual digital ischemia in elite male volleyball players, although the reported symptoms are very suggestive. However, we believe that, regardless of the cause of these symptoms, we have identified significant risk factors for these symptoms, making prevention possible. In conclusion, playing volleyball for more than 17 years and often/always performing weight training to increase dominant limb strength were significantly associated with self-reported blue or pale digits in the dominant hand during or immediately after practice or competition in elite male volleyball players. No significant other sports-, personal- or work-related risk factors were found. 3 Perspectives The identification of the sports-related risk factors playing volleyball for more than 17 years and often/always performing weight training to increase dominant limb strength are a first step in signalling and preventing apparently innocuous symptoms of digital ischemia. A better insight into the dominant limb weight training among elite male volleyball players might result in more safe strength training without an association with symptoms of digital ischemia. Elite male volleyball players, playing volleyball for more than 17 years, warrant regular surveillance for symptoms of digital ischemia possibly due to thromboembolic complications. This way, sports medicine specialists can be more proactive in helping prevent possibly irreversible damage to the digits among elite male volleyball players. Risk factors for digital ischemia in elite volleyball players in the Netherlands I 53

57 APPENDIX A Overview of demographics, personal, sports-related and work-related risk factors for the symptomatic and reference group of elite male volleyball players Answering category Symptomatic Group (n=26) Reference Group (n=68) Significance Demographics Age Years Mean: 25.0 SD: 5.3 Range: Body height Centimeters Mean: SD: 6.6 Range: Body weight Kilograms Mean: 86.0 SD: 7.1 Range: Mean: 24.0 SD: 4.3 Range: Mean: SD: 7.6 Range: Mean: 87.4 SD: 7.4 Range: t = 0.98 p = 0.33 t = 0.49 p = 0.62 t = p = 0.40 Shoulder injury history Yes: + No: - +: 13/26 (50%) -: 13/26 (50%) +: 23/67 (34%) -: 44/67 (66%) χ 2 = 1.94 p = 0.16 Use of medicine Yes: + No: - +: 2/26 (8%) -: 24/26 (92%) +: 1/67 (2%) -: 66/67 (98%) χ 2 = 2.31 p = 0.19 Paid or unpaid work Yes: + No: - +: 14/26 (54%) -: 12/26 (46%) +: 36/68 (53%) -: 32/68 (47%) χ 2 = 0.01 p = 0.94 Number of working hours per week Hours Mean: 15.3 SD: 18.3 Range: 0-50 Mean: 12.0 SD: 15.5 Range: 0-50 t = 0.88 p = 0.38 Personal risk factors Smoking (currently or in the past) Yes: + No: - +: 7/26 (27%) -: 19/26 (73%) +: 13/67 (19%) -: 54/67 (81%) χ 2 = 0.63 p = 0.43 Use of alcohol (currently) Yes: + No: - +: 23/26 (89%) -: 3/26 (11%) +:64/67 (96%) -: 3/67 (4%) χ 2 = 1.55 p = 0.34 Family history on cardiovascular disease Yes: + No: - +: 11/23 (48%) -: 12/23 (52%) +: 15/52 (29%) -: 37/52 (71%) χ 2 = 2.54 p = I Chapter 3

58 Answering category Symptomatic Group (n=26) Reference Group (n=68) Significance Sports-related risk factors Total years playing volleyball Years playing professional volleyball Years Mean: 15.8 SD: 5.6 Range:7-30 Years Mean: 4.8 SD: 4.8 Range: 1-18 Mean: 13.4 SD: 5.4 Range: 4-28 Mean: 4.2 SD: 4.1 Range: 1-18 t = 1.85 p = 0.07 t = 0.61 p = Number of practice and competition hours per week Hours Mean: 17.1 SD: 5.9 Range: 7-25 Mean: 17.2 SD: 6.1 Range: 5-30 t = p = 0.92 Position in the field Attacker: + Defender: - +: 9/16 (56%) -: 7/16 (44%) +: 27/41 (66%) -: 14/41 (34%) χ 2 = 0.46 p = 0.50 Smashing away from the shoulder Often/always: + Never/sometimes: - +: 13/26 (50%) -: 13/26 (50%) +: 22/67 (33%) -: 45/67 (67%) χ 2 = 2.35 p = 0.13 Type of service Jump service: + Float service: - +: 9/21 (43%) -: 12/21 (57%) +: 27/64 (42%) -: 37/64 (58%) χ 2 = 0.00 p = 0.96 Performing dominant limb weight training in general Yes: + No: - +: 25/26 (96%) -: 1/26 (4%) +: 62/68 (91%) -: 6/68 (9%) χ 2 = 0.68 p = 0.67 Frequency of performing dominant limb weight training during warming-up before practice Often/always: + Never/sometimes: - +: 5/26 (19%) -: 21/26 (81%) +: 15/68 (22%) -: 53/68 (78%) χ 2 = 0.09 p = 0.76 Number of minutes per week performing dominant limb weight training during warming-up before practice Minutes Mean: 14.0 SD: 22.8 Range: Mean: 13.0 SD: 30.8 Range: t = 0.16 p = 0.87 Frequency of performing dominant limb weight training during warming-up before competition Often/always: + Never/sometimes: - +: 2/26 (8%) -: 24/26 (92%) +: 8/68 (12%) -: 60/68 (88%) χ 2 = 0.33 p = 0.72 Risk factors for digital ischemia in elite volleyball players in the Netherlands I 55

59 Answering category Symptomatic Group (n=26) Reference Group (n=68) Significance Number of minutes per week performing dominant limb weight training during warming-up before competition Minutes Mean: 3.4 SD: 9.6 Range: 0-40 Mean: 3.3 SD: 7.6 Range: 0-40 t = 0.03 p = 0.98 Frequency of performing weight training to increase dominant limb strength Often/always: + Never/sometimes: - +: 17/26 (65%) -: 9/26 (34%) +: 28/68 (41%) -: 40/68 (59%) χ 2 = 4.42 p = 0.04 Number of hours per week performing weight training to increase dominant limb strength Hours Mean: 0.8 SD: 0.9 Range: 0-4 Mean: 0.6 SD: 0.6 Range:0-3 t = 1.4 p = 0.16 Frequency of performing weight training to maintain dominant limb strength Often/always: + Never/sometimes: - +: 15/26(58%) -: 11/26 (42%) +: 32/66 (48%) -: 34/66 (52%) χ 2 = 0.63 p = 0.49 Number of hours per week performing weight training to maintain dominant limb strength Hours Mean: 0.6 SD: 0.6 Range: 0-2 Mean: 0.4 SD: 0.5 Range: 0-2 t = 1.2 p = 0.21 Work-related risk factors Perceived heaviness of work Scale = not heavy at all 10 = as heavy as conceivable Mean: 1.9 SD: 2.0 Range: 0-5 Mean: 2.5 SD: 2.2 Range: 0-8 t = p = 0.43 Working with vibrating tools more than 1 hour per day Often/always: + Never/sometimes: - +: 0/26 (0%) -: 26/26 (100%) +: 1/68 (2%) -: 67/68 (98%) χ 2 = 0.39 p = 1.00 Working in a cold environment more than 1 hour per day Often/always: + Never/sometimes: - +: 0/26 (0%) -: 26/26 (100%) +: 1/68 (2%) -: 67/68 (98%) χ 2 = 0.39 p = I Chapter 3

60 Answering category Symptomatic Group (n=26) Reference Group (n=68) Significance Performing repetitive work with the arms more than 2 times per minute Often/always: + Never/sometimes: - +: 3/26 (11%) -: 23/26 (89%) +: 10/68 (15%) -: 58/68 (85%) χ 2 = 0.16 p = 1.00 Working above shoulder height more than 1 hour per day Often/always: + Never/sometimes: - +: 0/26 (0%) -: 26/26 (100%) +: 1/68 (2%) -: 67/68 (98%) χ 2 = 0.39 p = Performing work with tools heavier than 1 kg Often/always: + Never/sometimes: - +: 2/26 (8%) -: 24/26 (92%) +: 3/68 (4%) -: 65/68 (96%) χ 2 = 0.40 p = 0.61 Performing work with a computer or mouse more than 4 hours per day Often/always: + Never/sometimes: - +: 6/26 (23%) -: 20/26 (77%) +: 17/68 (25%) -: 51/68 (75%) χ 2 = 0.04 p = 0.84 Heavy lifting over 15 kg per day Often/always: + Never/sometimes: - +: 3/26 (11%) -: 23/26 (89%) +: 4/68 (6%) -: 64/68 (94%) χ 2 = 0.87 p = 0.39 Performing powerful work with the hands (like screwing or kneading) more than 1 hour per day Often/always: + Never/sometimes: - +: 1/25 (4%) -: 24/25 (96%) +: 3/68 (4%) -: 65/68 (95%) χ 2 = 0.01 p = 1.00 Risk factors for digital ischemia in elite volleyball players in the Netherlands I 57

61

62 CHAPTER 4 Test-retest reliability of the SPI-Questionnaire to detect symptoms of digital ischemia in elite volleyball players Daan van de Pol Tigran Zacharian Mario Maas P. Paul F.M. Kuijer Submitted

63

64 ABSTRACT The Shoulder PCHA pathology and digital Ischemia Questionnaire (SPI-Q) has been developed to enable periodic surveillance of elite volleyball players, who are at risk for digital ischemia. Prior to implementation, assessing reliability is mandatory. Therefore, the test-retest reliability of the SPI-Q was assessed among the population at risk. A questionnaire survey was performed with a two-week interval among 65 elite male volleyball players assessing symptoms of cold, pale and blue digits in the dominant hand during or after practice or competition using a 4-point Likert scale (never, sometimes, often, always). Kappa (κ), percentage of agreement (POA), and Intra-class Correlation Coefficient (ICC) were calculated for individual symptoms, severity of symptoms, and to distinguish symptomatic and asymptomatic players. 4 For the individual symptoms, κ ranged from poor (0.25) to good (0.63), and POA ranged from moderate (78%) to good (97%). To classify symptomatic players, the SPI-Q showed good reliability (κ=0.83; 95%CI ) and the same was true for the severity of symptoms (ICC=0.82; 95%CI ). Since the SPI-Q is reliable, it can be used for periodic surveillance to detect and monitor elite volleyball players with symptoms of digital ischemia in time. Test-retest reliability of the SPI-Questionnaire I 61

65 INTRODUCTION Elite volleyball players are at risk for digital ischemia, which may be due to arterial emboli originating from an aneurysmal and thrombosed posterior circumflex humeral artery (PCHA) in the dominant shoulder 89, among other causes. 46,49,57,65,96,97,129 Irrespective of the cause, creating awareness and monitoring these seemingly innocuous symptoms to detect onset and worsening is important since these athletes are at risk of emboli in the dominant hand, possibly resulting in irreversible tissue damage, and ultimately necrosis and finger loss if trivialized. For this purpose, the Shoulder PCHA pathology and digital Ischemia Questionnaire (SPI-Q) was developed using reports of volleyball players with confirmed digital ischemia combined with medical literature on symptoms associated with digital ischemia. 89 Currently, the most commonly used instruments in patients with peripheral arterial disease, such as chronic critical lower limb ischemia, include generic quality of life (QoL) questionnaires, such as the Short Form-36 (SF-36) and disease-specific QoL questionnaires, such as the Vascular Quality of Life questionnaire (VascuQol). 74,78,128 However, to our knowledge, no disease-specific questionnaires exist for symptoms of digital ischemia in the upper limb. Before the SPI-Q can be used for periodic surveillance, its measurement properties should be tested. Therefore, the purpose of this study is to assess the test-retest reliability of the SPI-Q for detection of symptoms of digital ischemia in the population at risk: elite male volleyball players. METHODS Study design A prospective cohort study was performed among elite male volleyball players in the Netherlands. Official approval of this study was waived by the Institutional Review Board (IRB) of our academic hospital. Participant selection A power analysis in nquery advisor 7.0 (Statistical Solutions Ltd, 2007) showed that 62 participants were needed with kappa=0.7, precision=0.15 and a one-sided confidence level of α=0.05. The inclusion criteria were: (1) being an elite male indoor volleyball player active in the Dutch national top or second league in the seasons ; and (2) written informed consent. To secure sufficient variety in players with and without symptoms of digital ischemia, 84 volleyball players who reported at least one symptom of cold, blue or pale digits in the dominant hand during or directly after practice or 62 I Chapter 4

66 competition were selected from a previous study, and supplemented with volleyball players who reported no symptoms (n=22). 91 Study protocol An electronic questionnaire was sent through a digital link with a two-week interval between test (t=1) and retest (t=2). This time interval was chosen to prevent both recall bias and change in health condition/symptoms. 118 To assure no bias was caused by a change in the prevalence of symptoms between t=1 and t=2, for each of the six symptoms the following question and answer categories were formulated in the retest questionnaire: Does this symptom occur less often, equally often or more often than 14 days ago when you filled in the first questionnaire? If a participant answered one of these six questions with less often or more often, the participant was excluded from the analysis. 4 Questionnaire content The SPI-Q was developed using reports of volleyball players with confirmed digital ischemia, based on evidence from the medical literature 89, and comprises two general domains: A) characteristics of the individual player, such as age and total years playing volleyball; and B) those concerning symptoms of digital ischemia in the dominant hand, like cold, blue or pale digits, occurring both during and directly after practice as well as in competition (Table 1). A 4-point Likert scale was used for the answer categories of the questions on symptoms: never, sometimes, often, always. The complete questionnaire used in the study is included in Appendix A. Data analyses The data from the questionnaires were entered in SPSS (version 21.0, 2012, SPSS Inc.) and randomly checked for correct entry. The mean, standard deviation, maximum and minimum of age, body weight, body height, total years playing volleyball, and total hours volleyball played in the last 14 days were reported for the group as a whole. Test-retest reliability was calculated and expressed in three ways: 1. Linear weighted kappa (κ) was calculated for each of the individual symptoms of digital ischemia, i.e. cold, blue or pale digits during and after practice and competition. κ is the recommended parameter for the estimation of reliability for categorical data 58,72, and was calculated using a website 54. The linear weights for the weighting matrix were calculated using the following formula: 1 ((i j) / (k-1)), where i is the category rated in test 1, j the category rated in test 2 and k the total number of categories. 112,121 To reflect sampling error, the confidence interval (CI) of the linear weighted κ was also calculated. The following decision criterion was formulated for the interpretation of the values of κ: >0.60 = good, = moderate, and <=0.40 = poor. 31,36,37,60 To assess the dependence of κ from the Test-retest reliability of the SPI-Questionnaire I 63

67 Table 1 Questions regarding specific symptoms of digital ischemia, as asked in the SPI-Q questionnaire 1 Do you suffer from one or more cold fingers in your dominant hand a during practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always b directly after practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always 2 Do you suffer from one or more blue fingers in your dominant hand a during practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always b directly after practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always 3 Do you suffer from one or more pale fingers in your dominant hand a during practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always b directly after practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always distribution of data, the percentage of agreement (POA) of the measurements classified in the same categories in the test and retest questionnaires was calculated for each of the individual symptoms of digital ischemia, i.e. cold, blue or pale digits during and after practice and competition. 15 The following criterion was formulated for the interpretation of the values of POA: >90% = good, 70-90% = moderate, and <70% = poor. 31,36,37 2. Unweighted κ was calculated for the reliability of the combined question: is a volleyball player symptomatic? To do so, the answers to the individual symptoms of digital ischemia, i.e. cold, blue or pale digits during and after practice and competition were combined in order to label a volleyball player as symptomatic or asymptomatic. The case definition of symptomatic was: a volleyball player who reported one or more of the symptoms cold or blue or pale digits during or after volleyball. Volleyball players without these symptoms were defined as asymptomatic. The values of the κ were interpreted in the same manner as described above for the linear weighted κ. 3. Intra-class correlation coefficient (ICC), model single measure, two-way random, and absolute agreement 111, was calculated to express the reliability of the sumscore to determine the severity of symptoms of digital ischemia, i.e. cold, blue 64 I Chapter 4

68 or pale digits during and after practice and competition. Points were given to all four answer categories: never (0 points), sometimes (1 point), often (2 points) and always (3 points), resulting in a maximum score of 18 points. The following decision criteria were formulated for the interpretation of the values of ICC: >0.75 = good, = moderate, and < 0.50 = poor. 28,31,36,37 To put the ICC in the context of the data from which it was derived, the standard error of measurement (SEM), the smallest detectable change (SDC), and the limits of agreement (Loa) were also calculated, with smaller SEMs and SDCs or Loas indicating less measurement error. 18 The following two formulas were used: SD difference = 2 x SEM consistency, and Loa = SDC = mean difference ± 1,96 x SD difference RESULTS Participants From March to May 2015, a total of 106 volleyball players were invited to participate, of whom 73 agreed to participate and 71 of these 73 completed the questionnaire both times, a response rate of 97%. Six volleyball players were excluded because they reported a change in the frequency of symptoms in the two weeks between completing both questionnaires: five volleyball players reported symptoms less often, and one reported symptoms more often. These participants were advised about follow-up. As a result, 65 volleyball players, completing both questionnaires in 15±4 days (range 7-31 days), were included (Figure 1). On average, volleyball players were 27±5 years old (range: Figure 1 Flow chart of participant inclusion Test-retest reliability of the SPI-Questionnaire I 65

69 years), had a body height of 195±7 centimetres (cm) (range: cm), and had been playing volleyball for 17±6 years in total (range 6-33 years) and 15±8 hours in the last 14 days (range 0-30 hours). Prevalence of symptoms of digital ischemia Cold and pale digits during practice or competition were most prevalent with percentages ranging from 20% to 26%. Blue digits directly after playing volleyball were rarely reported (3%) and none of the volleyball players reported a symptom as always being present (Table 2). During test (t=1) and retest (t=2), respectively 37% (n=24) and 35% (n=23) of surveyed volleyball players reported at least one of the symptoms of cold or blue or pale during or after volleyball. Test-retest reliability Individual symptoms of digital ischemia Linear weighted κ for the individual symptoms of digital ischemia ranged from poor (0.25) for pale digits after practice or competition to good for cold digits during practice or competition (0.63). The POA for these individual symptoms ranged from moderate (78%) for pale digits during competition to good (97%) for blue digits after competition (Table 3). Table 2 Prevalence of symptoms (% and number) of digital ischemia during or directly after practice or competition in the dominant hand in elite male volleyball players during test (t=1) and retest (t=2) (n=65) During practice or competition Directly after practice or competition Never % (n) Sometimes % (n) Often % (n) Always % (n) Symptomatic % (n) Never % (n) Sometimes % (n) Often % (n) Always % (n) Symptomatic % (n) Cold t= 1 80 (52) 15 (10) 5 (3) 0 20 (13) 90.8 (59) 9 (6) (6) Cold t= 2 74 (48) 20 (13) 6 (4) 0 26 (17) 86.2 (56) 12 (8) 2 (1) 0 14 (9) Blue t= 1 92 (60) 6 (4) 2 (1) 0 8 (5) 97 (63) 3 (2) (2) Blue t= 2 90 (59) 8 (5) 2 (1) 0 10 (6) 97 (63) 3 (2) (2) Pale t= 1 75 (49) 22 (14) 3 (2) 0 25 (16) 89.3 (58) 9 (6) 2 (1) 0 11 (7) Pale t= 2 78 (51) 19 (12) 3 (2) 0 22 (14) 86 (56) 12 (8) 2 (1) 0 14 (9) 66 I Chapter 4

70 Symptomatic for digital ischemia The unweighted κ calculated for the combined question to determine whether a volleyball player is symptomatic based on one or more symptoms of digital ischemia was good (0.83) (Table 4). Severity of symptoms of digital ischemia The ICC calculated for the sum-score to determine the severity of symptoms of digital ischemia showed good agreement (0.82; 95%CI ). The SEM was 0.72, the MDC was 2.00, and the Loas were ± 2.00 ( ) (Table 5). 4 Table 3 Prevalence in test (t=1) and retest (t=2), percentage of agreement (POA), linear weighted kappa (κ), and 95%CI of symptoms of digital ischemia during and after practice and competition among elite male indoor volleyball players N Prevalence t=1 (%) Prevalence t=2 (%) POA (%) Linear weighted κ 95%CI Cold digits during Cold digits after Blue digits during Blue digits after Pale digits during Pale digits after Table 4 Prevalence in test (t=1) and retest (t=2), percentage of agreement (POA), unweighted kappa (κ) and 95%CI of the combined question: is a volleyball player symptomatic? n Prevalence t=1 (%) Prevalence t=2 (%) POA (%) Unweighted κ 95% CI Combined question: is a volleyball player symptomatic? (yes/no) Test-retest reliability of the SPI-Questionnaire I 67

71 Table 5 Intra-class correlation coefficient (ICC), standard error of measurement (SEM), minimal detectable change (MDC) and limits of agreement (Loa) of the sum-score (0-18) for the severity of symptoms of digital ischemia n ICC 95% CI SEM MDC Loa Sum-score of symptoms (minimum 0 - maximum 18) DISCUSSION This study shows that the SPI-Q is a reliable questionnaire for detecting cold and blue digits, to distinguish symptomatic volleyball players from asymptomatic ones based on one or more symptoms, and for grading the severity of symptoms. Only assessing pale digits showed poor to moderate results. This is the first study to provide a reliable tool that can assess symptoms of digital ischemia in elite volleyball players: the population at risk. To our knowledge, no comparable questionnaires have been developed, nor tested, for upper limb ischemia in this or any other population of elite overhead athletes at risk, such as baseball pitchers. 27 For lower limb ischemia, questionnaires like the VascuQol have been developed and extensively tested for their measurement properties. 22,30 However, these questionnaires are mostly used for QoL outcomes of patients diagnosed with or treated for chronic critical lower limb ischemia 74, while the SPI-Q has been developed for targeted detection and monitoring of symptoms of digital ischemia in healthy elite overhead athletes. To classify symptomatic players based on one or more symptoms, the SPI-Q showed good reliability. This indicates that the SPI-Q is a reliable instrument for detecting symptomatic volleyball players. Furthermore, good reliability was found for the sumscore to determine the severity of symptoms of digital ischemia reported in the SPI-Q. For the SPI-Q sum-score, the MDC and Loa were calculated to assess which changes can be detected outside the measurement error. An MDC of 2.00 (rounded) suggests that a change of 2 points or more can be detected by the SPI-Q questionnaire as real change on a scale from 0-18, suggesting acceptable measurement error. However, what the exact magnitude of the real change should be to be considered as a clinically important change or minimally important change (MIC) is to be determined in future research regarding responsiveness and validity. 123 In addition, the outcomes for the individual symptoms of digital ischemia were diverse: the linear weighted κ ranged from 0.25 to 0.63 ( poor to good reliability), and the POA values ranged from 78% to 97% ( moderate to good ), making these questions seem less suited for detecting elite male volleyball players with symptoms when used individually. This seems especially true for detecting pale digits. 68 I Chapter 4

72 However, the big difference between the linear weighted κ values and POA implies high agreement by chance and might have resulted from the homogeneity of symptoms across the different answer categories. 112,124 Strengths and weaknesses A strength of this study was the power analysis via nquery advisor 7.0 and the inclusion of 65 volleyball players, since a sample size of at least 62 was considered adequate. Another strength is that all symptomatic players from a previous study were selected to secure sufficient variety in the main outcome presence and absence of symptoms. Little variety would have caused a poor level of reliability, as found in other studies. 35 A weakness of the SPI-Q is that none of the participants reported experiencing one of the symptoms as always. Therefore, one might consider modifying the answer categories often and always to regularly and often, respectively. Of course, the effects of these changes on reliability of reporting of individual symptoms should be assessed in future studies. 4 Clinical implications The self-reported prevalence of cold or blue or pale digits in the dominant hand during or immediately after practice or competition is 38% among international world-class male and female beach volleyball players, and 31% among elite male indoor volleyball players. 88,89 These symptoms are associated with digital ischemia, which can be caused by a wide variety of vascular and non-vascular pathologies 90, including arterial emboli originating from an aneurysmal and thrombosed PCHA in the dominant shoulder. 89 Volleyball players with confirmed digital ischemia present themselves late in disease with severely disabling coldness, discolouration, pain and paresthesia in the dominant hand. 93 Active surveillance enables identification of apparently innocuous symptoms, like coldness and discolouration, at an early stage, and might prevent thromboembolic complications, irreversible tissue damage, and possibly surgical ligation of the PCHA. 89 The responsiveness of the SPI-Q needs to be determined in future studies. The current study has proven the SPI-Q to be reliable for detecting elite male indoor volleyball players with symptoms of digital ischemia, and for grading the severity of these symptoms. Therefore, we can recommend using the SPI-Q for periodic surveillance to detect and monitor elite volleyball players with symptoms of digital ischemia in time. Test-retest reliability of the SPI-Questionnaire I 69

73 APPENDIX A SPI-Q QUESTIONNAIRE Domain A: personal and sports characteristics of the participants 1. What is your age? 2. What is your body height? 3. What is your body weight? 4. How many years in total have you played volleyball? 5. How many hours in total have you played volleyball in the last 14 days? (training and competition) Domain B: symptoms associated with digital ischemia 6. How often do you suffer from one or more cold fingers in your dominant hand during practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always 7. How often do you suffer from one or more cold fingers in your dominant hand directly after practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always 8. How often you suffer from one or more blue fingers in your dominant hand during practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always 9. How often do you suffer from one or more blue fingers in your dominant hand directly after practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always 10. How often do you suffer from one or more pale fingers in your dominant hand during practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always 11. How often do you suffer from one or more pale fingers in your dominant hand directly after practice or competition? q No, never q Yes, sometimes q Yes, often q Yes, always 70 I Chapter 4

74

75

76 CHAPTER 5 Self-reported symptoms and risk factors for digital ischaemia among international worldclass beach volleyball players Daan van de Pol Sena Alaeikhanehshir Mario Maas P. Paul F.M. Kuijer Journal of Sports Sciences. 2015;5:1-7. doi: /

77

78 ABSTRACT The prevalence of ischemia-related symptoms is remarkably high among elite indoor volleyball players. Since the exposure to sport-specific demands may be higher in beach volleyball compared to indoor volleyball, the aim of this study was to assess the prevalence of ischemia-related symptoms and associated risk factors among worldclass beach volleyball players. Therefore, a questionnaire survey was performed among beach volleyball players active during the 2013 Grand Slam Beach Volleyball in the Netherlands. In total, 60 of the 128 beach volleyball players (47%) participated: 26 males and 34 females from 17 countries. The self-reported prevalence of cold or blue or pale digits in the dominant hand during or immediately after practice or competition was 38% (n=23). Two risk factors were independently associated with symptoms of blue or pale digits: more than 14 years playing volleyball (odds ratio (OR) % confidence interval (90% CI) ) and sex (female) (OR %CI ). In conclusion, the prevalence of symptoms associated with digital ischemia is high among international world-class beach volleyball players. Female sex and the length of the volleyball career were independently associated with an increased risk of ischemia-related symptoms. The high prevalence of these seemingly innocuous symptoms and possible associated risk factors warrant regular monitoring since early detection can potentially prevent thromboembolic complications and irreversible tissue damage. 5 Symptoms and risk factors for digital ischemia in world-class beach volleyball I 75

79 INTRODUCTION In the medical literature, cold and discoloured digits were reported by 89% of volleyball players with confirmed digital ischemia caused by emboli due to pathological changes of the posterior circumflex humeral artery (PCHA) in the ipsilateral shoulder (Figure 1&2). 89 These data, although self-reported, strongly suggest underlying PCHA pathology; however, this exact association has yet to be confirmed. Distal embolization from an aneurysmal and thrombosed PCHA can disable the athlete and threaten the athlete s career and viability of the involved parts. Invasive treatment possibilities involve surgical ligation and endovascular coiling 3, while conservative treatment consists of cessation of sports activities. Active surveillance might make it possible to identify vascular injury at an early stage in those volleyball players who experience apparently innocuous symptoms. This way, thromboembolic complications and irreversible tissue damage can potentially be prevented. Volleyball is unique among team sports in that it has evolved into two distinct Olympic disciplines: a two-person per side outdoor game typically played on sand (beach volleyball) and an indoor version featuring six players on each team (indoor volleyball). The Fédération Internationale de Volleyball (FIVB) estimates that 500 million people play volleyball worldwide, with the greatest area of growth in beach volleyball. 98 Although the essential skills of the two disciplines are identical, beach volleyball distinguishes itself from indoor volleyball through several characteristics, the most obvious being the composition of the playing surface. Game-specific characteristics might lead to different demands placed on the upper extremity. For instance, higher rates of overuse injuries of the shoulder have been reported in beach volleyball compared to indoor volleyball. 1 In this regard, among elite male indoor volleyball players in the Netherlands, one-third reported symptoms of cold, blue and/or pale digits in the dominant hand during volleyball, with the length of the volleyball career and the intensity of performing strength-increasing weight training identified as associated risk factors. 90 These high rates of symptoms related to digital ischemia among young and fit elite male indoor volleyball players stress the need for an inventory of these numbers in elite beach volleyball players. Therefore, the aim of this study was to assess the prevalence of known ischemia-related symptoms and associated risk factors among international world-class beach volleyball players. 76 I Chapter 5

80 5 Figure 1 89 Digital Subtraction Angiography of the right hand of a 27-year-old volleyball player with ischemic symptoms of multiple digits. The arrows point to multiple abrupt stops in digital arteries, compatible with microemboli. Figure 2 89 Digital Subtraction Angiography of the right arm of a 27-year-old volleyball player with ischemic symptoms of multiple digits (the same player as in Figure 1). The arrow points to the abrupt stop of contrast in the posterior circumflex humeral artery caused by thrombosis. Symptoms and risk factors for digital ischemia in world-class beach volleyball I 77

81 MATERIALS AND METHODS Study design A cross-sectional questionnaire survey was performed among international world-class beach volleyball players during the 2013 Beach Volleyball Grand Slam Tournament in The Hague, the Netherlands. Official approval for the study was granted by the Medical Ethics Review Committee, and permission was obtained from the medical commission at the Fédération Internationale de Volleyball (FIVB). Participants After permission was granted by the FIVB and the Dutch Volleyball Association (Nevobo), all players, coaches and medical staff were informed about the study via and during the technical meeting that all teams were required to attend. Athletes were invited to participate at any time during the tournament and were actively asked during the tournament by the main researcher and volunteers. During the four-day main tournament, the athletes were surveyed on-site in the medical treatment area. The main tournament of the Beach Volleyball Grand Slam Tournament consisted of 32 male teams and 32 female teams, which resulted in 128 potential participants. To obtain a large study sample, both male and female athletes were invited. Written informed consent was obtained. The inclusion criteria were (1) full competitive activity during the main tournament and (2) written informed consent. Exclusion criteria included a history of vascular injury or surgery of the dominant shoulder, confirmed Raynaud s Phenomenon, use of cardiovascular medication and age below 18 years. Questionnaire content A specifically developed questionnaire to detect ischemic symptoms and to identify known risk factors associated with digital ischemia in volleyball was used. This questionnaire was developed by Van de Pol et al. using reports of volleyball players with confirmed digital ischemia and based on evidence from the medical literature, and was also used among professional indoor volleyball players (Appendix A). 89,90 The questionnaire comprised four general domains: (1) those regarding demographics, such as age; (2) those regarding personal risk factors and medical conditions, such as family history of cardiovascular disease; (3) those regarding known sports-related risk factors, such as years spent playing volleyball; and (4) those regarding specific symptoms associated with digital ischemia, such as cold digits during practice or competition. Data analyses Data were entered in SPSS (version 20.0, SPSS Inc., Chicago, IL, USA) and correct data entry was checked for by a second researcher. 78 I Chapter 5

82 Characteristics of the participants The mean, standard deviation, minimum and maximum of respectively age, body height, body weight, total years playing volleyball, total years playing beach volleyball, total years playing professional volleyball and weekly hours playing volleyball in practice or competition were reported for the total group of beach volleyball players, and for males and female separately. Additionally, the percentage of beach volleyball players that reported a family history of cardiovascular disease and smoking were reported. Prevalence of symptoms The prevalence of symptoms associated with digital ischemia was calculated in the following manner: the percentage of all beach volleyball players who sometimes or more often reported having cold or blue or pale digits in the dominant hand during or directly after practice or competition. These prevalences were reported for the total group of beach volleyball players, and for males and females separately. 5 Then, participants were stratified according to a positive history of the two more severe ischemia-related symptoms reported in the questionnaire namely blue or pale. The case definition of the symptomatic group was reporting symptoms of blue or pale digits in the dominant hand during or immediately after practice or competition. The reference group was defined as players without these two symptoms. Risk factors First, to assess differences between the symptomatic and reference group, demographical parameters, and personal and sports-related risk factors were tested using an independent t-test or a χ 2 test (Appendix B). In all tests, a p-value 0.10 was considered significant. This cut-off value was deliberately chosen since this is the first study on these symptoms among international beach volleyball players and, given the relatively small group size, a p-value of 0.10 is warranted to overcome missing potential clinically relevant differences. Next, the odds ratio (OR) and 90% confidence interval (90% CI) were calculated for all demographical, personal and sports-related risk factors using a univariate binary logistic regression. Subsequently, the collinearity between the univariately analysed variables with a p-value 0.10 was calculated. For all non-collinear variables with a p-value <0.10, an OR including 90% CI was calculated using a multivariate binary logistic regression, and subcategory analyses will be performed in line with Van de Pol et al. 90 Symptoms and risk factors for digital ischemia in world-class beach volleyball I 79

83 RESULTS Participants In total, 63 of the 128 eligible beach volleyball players (64 males and 64 females) voluntarily participated in the study (49%). Three players (two males and one female) were excluded from the study due to confirmed Raynaud s Phenomenon. As a result, 60 beach volleyball players from 17 countries, 26 males and 34 females, were included in our study, an inclusion rate of 47%. On average, participants were 26 years old, had a body height of 186 cm and had been playing beach volleyball for 13 years and 19 hours a week (Table 1). Twenty-three percent of the participants reported the presence of cardiovascular disease in their family. Eighteen percent smoked or had smoked in the past. Male beach volleyball players were on average 27 years old, had a body height of 1.95 m, and had a volleyball career length of 14 years (Table 1). Female beach volleyball players were on average 26 years old, had a body height of 1.79 m, and had a volleyball career length of 13 years (Table 1). Among the male participants 27% (n=7) reported that they smoked or had smoked in the past, while among the female participants this figure was 12% (n=4). Prevalence of symptoms associated with digital ischemia in the dominant hand The prevalence of symptoms of pale digits during practice or competition in the participants was 18% (Table 2). Ten percent reported pale digits after practice or competition. The prevalence of participants that reported the combination of blue or pale digits in the dominant hand during or immediately after practice or competition was 22%. 80 I Chapter 5

84 Table 1 Characteristics of the participants Total Male Female N Mean SD Min Max N Mean SD Min Max N Mean SD Min Max Age (years) Body height (cm) Body weight (kg) Total years volleyball Years beach volleyball Years professional volleyball Hours volleyball per week Symptoms and risk factors for digital ischemia in world-class beach volleyball I 81

85 Table 2 Prevalence of self-reported symptoms (or combinations thereof) associated with digital ischemia during or immediately after practice or competition in the dominant hand in international world-class beach volleyball players Total group n=60 Male n=26 Female n=34 Cold digits during 15 25% 5 19% 10 29% Cold digits after 10 17% 3 12% 7 21% Blue digits during 2 3% 1 3% 1 3% Blue digits after 2 3% 0 0% 2 6% Pale digits during 11 18% 2 8% 9 27% Pale digits after 6 10% 0 0% 6 18% Blue OR pale digits, during OR after Cold OR blue OR pale digits, during OR after 13 22% 2 8% 11 32% 23 38% 6 23% 17 50% Factors associated with complaints of ischemic symptoms The symptomatic group of players who reported blue or pale digits in the dominant hand during or directly after practice or competition sometimes or more often consisted of 13 beach volleyball players. The reference group consisted of 47 beach volleyball players. Demographical parameters The symptomatic group consisted of two males and 11 females and the reference group of 24 males and 23 females a significant difference (χ 2 = 5.30, p = 0.02) (Appendix B). The independent t-test revealed no significant differences between the groups for other demographical parameters like age and body height (Appendix B). The univariate binary logistic regression also revealed a significant association for the demographical parameter sex (OR 5.75, 90% CI ) (Table 3). Personal risk factors Thirty-nine percent of the beach volleyball players in the symptomatic group reported the presence of cardiovascular disease in their family, while in the reference group this was 19%. Eight percent of the beach volleyball players in the symptomatic group reported that they smoked or had smoked in the past. For the male players, 0% (0/2) of the symptomatic group smoked and 29% (7/24) of the reference group. For the females, these data were 9% (1/11) and 13% (3/23), respectively. The χ 2 test revealed no significant differences between the groups for all personal risk factors (Appendix B). 82 I Chapter 5

86 Additionally, no significant associations were found in the results of the univariate binary logistic regression analyses (Table 3). Sports-related risk factors On average, beach volleyball players in the symptomatic group had a volleyball career length of 15 years and in the reference group 13 years a significant difference (t = -1.71, p = 0.09). For the other sports-related risk factors, neither group differed significantly (Appendix B). The univariate binary logistic regression also revealed a significant association for total years playing volleyball (OR 1.12, 90% CI ). For the other sports-related factors, the univariate binary logistic regression revealed no significant associations like total practice and competition hours in a week (OR = 1.00, 90% CI ) or the frequency of performing weight training to increase dominant limb strength (OR 0.75, 90% CI ) (Table 3). 5 Multivariate regression outcomes No collinearity between sex and total years playing volleyball was found (variance inflation factor = 1.004, tolerance = 0.996). The multivariate binary logistic regression revealed a significant association for sex (female) with an OR 4.62 (90% CI ) (Table 4). Total years playing volleyball categorized in two categories (0-13 years and years) showed a significant association for the subcategory years playing volleyball with OR 4.42 (90% CI ) (Table 4). Symptoms and risk factors for digital ischemia in world-class beach volleyball I 83

87 Table 3 Univariate binary logistic regression outcomes (odds ratio and 90% confidence interval) of demographics and potential risk factors associated with self-reported symptoms of digital ischemia in international world-class beach volleyball players Domain A: demographics Symptomatic group versus reference group Age OR 1.09 (90% CI ) Sex (Female) OR 5.75 (90% CI ) * Height OR 0.98 (90% CI ) Weight OR 0.96 (90% CI ) Domain B: personal risk factors Raynaud in family (Yes) OR 0.00 (90% CI 0.00 ) ** Family history on cardiovascular disease (Yes) OR 2.64 (90% CI ) Smoking (Yes) OR 0.31 (90% CI ) Domain C: sports-related risk factors Total years playing volleyball OR 1.12 (90% CI ) * Years playing beach volleyball OR 0.97 (90% CI ) Years playing professional volleyball OR 1.01 (90% CI ) Total practice and competition hours in a week OR 1.00 (90% CI ) Smashing/spiking frequency OR 4.41 (90% CI ) Smashing/spiking away from the shoulder (Often/Always) OR 1.06 (90% CI ) Performing dominant limb weight training in general (Yes) OR 2.79 (90% CI ) Frequency of performing weight training to increase dominant limb strength (Often/Always) Number of hours per week performing weight training to increase dominant limb strength Frequency of performing weight training to maintain dominant limb strength (Often/Always) Number of hours per week performing weight training to maintain dominant limb strength OR 0.75 (90% CI ) OR 1.08 (90% CI ) OR 3.24 (90% CI ) OR (90% CI E) * Significant (p 0.10) ** No odds ratio (OR) could be calculated as no volleyball players reported being exposed to this risk factor. 84 I Chapter 5

88 Table 4 Multivariate binary logistic regression outcomes (odds ratio and 90% confidence interval) of sex and total years playing volleyball Symptomatic group versus reference group Sex (female) OR 4.62 (90% CI ) Total years playing volleyball OR 1.11 (90% CI ) 0-13 years (n=31) years (n=28) DISCUSSION Reference OR 4.42 (90% CI ) 5 The two main findings are (1) the prevalence of participants reporting blue or pale digits in the dominant hand during or immediately practice or competition was 22% (n=13) and (2) volleyball career length and sex were independently associated with an increased risk on ischemia-related symptoms of the dominant hand. Prevalence: difference between elite male beach volleyball players and elite male indoor volleyball players This is the first study that reports the prevalence of symptoms associated with digital ischemia in international world-class beach volleyball players. The reported prevalence of blue or pale digits during practice or competition in the dominant hand among the participating elite male beach volleyball players (n=24) was lower than the reported prevalence among elite male indoor volleyball players in the Netherlands (n=99) (8% vs. 26%, respectively). 89 This difference was significant (OR 0.23, 90% CI , p =0.06) This result seems to invalidate the hypothesis that beach volleyball players are more prone to ischemia-related symptoms of the dominant hand, and possibly putative sport-specific vascular injuries of the dominant limb, than indoor volleyball players. This lower prevalence might be related to game-specific differences between beach and indoor volleyball. First, beach volleyball players are shorter in height and weigh less compared to indoor volleyball players. 81 This might be related to different biomechanical, physiological, and tactical and technical demands. Biomechanical differences in beach volleyball compared to indoor volleyball are those related to the adaptation for instance the kinematics of the approach phase, or the movement of the centre of mass due to playing in the sand. However, recently no differences have been reported for upper limb amplitude of motion or angular velocity. 119 An example of a physiological difference is the greater area that beach volleyball players have to cover: two players covering an 8 8m field compared to a 9 9m with six players in indoor volleyball. Lastly, and closely related to the preceding, tactical and technical strategies are that off-speed placement Symptoms and risk factors for digital ischemia in world-class beach volleyball I 85

89 shots to catch the opponent off guard, like tips and roll shots, are a more effective gamewinning strategy than the hard smashes or spikes as in indoor volleyball. This may result in less blunt trauma to the hand and digits, and less fierce repetitive rotary movements in the shoulder of beach volleyball players. Other possible preventive elements in beach compared to indoor volleyball are the reduced air pressure in the beach volleyball ( kg cm 2 vs kg cm 2 ), and the considerably lower average duration of a beach volleyball match (50 min with 90 rallies vs. 95 min with 165 rallies). 82 In addition, Raynaud-like symptoms, like pale digits, are known to be aggravated by cold circumstances 14,129 and might therefore be less provoked in the warm seasons and environmental temperatures in which beach volleyball is generally played. Sports-related risk factor for symptoms associated with digital ischemia This is the first study to identify a sports-related risk factor for symptoms associated with digital ischemia among beach volleyball players. A significant fourfold increased risk was found for a volleyball career length of more than 14 years volleyball and the increased risk per played volleyball year was The influence of the volleyball career length on symptoms of digital ischemia in elite volleyball was also established in elite male indoor volleyball players in the Netherlands with a similar significant 1.1-fold (95% CI ) increased risk per played volleyball year. A possible explanation for the risk factor volleyball career length might be that the exposure to blunt trauma to the forearms and hands, and repetitive rotary movements of the shoulder, increase gradually during a volleyball player s career, resulting in a deterioration of vascular structures. 90 For example, a highly skilled indoor volleyball attacker with hours weekly practice time performs about 40,000 smashes/spikes in a single season. 59 Despite the fact that no comparable numbers were found for beach volleyball, this figure might well be indicative for high-level beach volleyball players. This cumulative sport-specific exposure might well have contributed to proven cases of ischemia-related symptoms of the hand in volleyball players as a result of local vascular trauma in the forearm and (hypo)thenar 57,65, or an overload of vascular structures in the shoulder like the PCHA. 3,68,89,95,96,115,126. Sex as a risk factor for symptoms associated with digital ischemia Prevalence of sex differences in health-related outcomes in beach volleyball has been reported. For example, female beach volleyball players have more injuries to the hands and fingers, and fewer injuries to the ankle/foot. 4,114 Female beach volleyball players in the present study reported a higher prevalence for all symptoms (or combinations thereof) associated with digital ischemia than their male colleagues (Table 2). These differences might be explained by sex-specific game characteristics and general sex differences. Examples of sex-specific differences in game characteristics are fewer terminal actions and more continuous actions in defence and attack in women s games 56, which is likely 86 I Chapter 5

90 to contribute to a longer playing time per point in women s games, thereby increasing cumulative exposure for the upper extremity. Apart from technical and tactical differences among sex, other variables might explain the differences observed in our female population. Firstly, women are more likely to perceive cold in hands and digits due to differences in peripheral vascularisation, fat distribution, hormonal regulation, nerve distribution and sensitivity to temperature alterations. 11 Secondly, women are known to have an increased risk of vasoconstriction in the hand leading to cold and pale digits, as is seen in Raynaud s Phenomenon. 14 Thirdly, women indicate and cope with physical discomfort differently, which might explain the increased female-to-male ratio in clinical settings. 39 Interestingly, in their study on volleyball-related shoulder pain, Reeser et al. 99 stated that even if there were no significant sex differences in the prevalence of shoulder problems female volleyball players reported lower overall shoulder function and sought medical care more frequently than male volleyball players. 5 Relevance for clinical sports practice Consensus among studies in volleyball players exists about the added value of identifying symptoms and risk factors in an early stage to decrease time lost from sports participation and to develop effective preventive measurements. 6,7,16,100 Prospective assessment of the prevalence of symptoms at regular intervals seems most suitable to identify overuse injuries. 6 These types of injuries are characterized by discomfort, do not necessarily cause a player to stop playing and lead to postponed detection and medical treatment. 110,122 Symptoms of digital ischemia are suited for surveillance because they meet these criteria, including the Wilson and Jungner criteria for surveillance, like the presence of an early symptomatic stage, a suitable test and available treatment. 131 The short screening questionnaire (Appendix A) might be of use for this purpose. We recommend the frequency to be higher for beach volleyball players with a career length of more than 14 years. In the case of inducing or exacerbating of the symptoms, low threshold additional imaging, for instance with Colour Doppler Ultrasound of the whole dominant upper limb, should be applied to exclude structural vascular pathology. Strengths and limitations The inclusion rate of 47% in this study is both a strong and a weak point. Considering that all 60 participants are young, fit and healthy athletes at the top of their sports career, the included population seems a valid cohort of world-class beach volleyball players. However, 47% merely represents half of the tournament s competitors, and selection bias might be present. It is possible that certain volleyball players, for instance symptomatic or female athletes, were more inclined to participate. No group matching for sex was performed, simply because the goal was to include as many world-class beach volleyball players as possible. Had the other half of the volleyball players not reported any symptoms, the prevalence would still be about 19% (half of 38%, Table 2) for cold, Symptoms and risk factors for digital ischemia in world-class beach volleyball I 87

91 blue or pale digits. Even in that case, regular monitoring of these seemingly innocuous symptoms seems warranted in these young, fit and healthy males and females. Although the content validity of our questionnaire is established based on reports of volleyball players with confirmed digital ischemia from the literature and from medical files 89, upcoming studies should reveal the sensitivity and specificity of the reported ischemic complaints for pathological changes of the PCHA in the shoulder of both elite beach and indoor volleyball players. In conclusion, the prevalence of symptoms associated with digital ischemia is high among international world-class beach volleyball players. Female sex and the length of the volleyball career were independently associated with an increased risk of ischemiarelated symptoms. The high prevalence of these seemingly innocuous symptoms and possible associated risk factors warrant regular monitoring since early detection can potentially prevent thromboembolic complications and irreversible tissue damage. 88 I Chapter 5

92 APPENDIX A QUESTIONNAIRE SURVEY Domain A: demographics 1. What is your name? (optional) 2. What is your nationality? 3. What club or team do you play for? 4. What is your age? years 5. What is your sex? q Male q Female 6. What is your body height? centimeters 5 7. What is your body weight? kilograms 8. What is your dominant/hitting arm? q Right q Left Domain B: personal risk factors and medical conditions 9. Have you ever had an injury to or had surgery on the blood vessels in your dominant shoulder? q Yes (continue with question 10) q No (continue with question 11) 10. If so, what kind of injury/injuries? 11. Do you suffer from Raynaud s Phenomenon? 12. Does Raynaud s Phenomenon occur in your family? 13. If so, in which family member(s)? 14. Does cardiovascular disease occur in your family? 15. If so, in which family member(s)? 16. Do you smoke/have you ever smoked cigarettes or other tobacco products? 17. Are you on medication for your blood pressure, heart or blood vessels? 18. If so, what medication and for what reason? q Yes q No q Yes (continue with question 13) q No (continue with question 14) q Yes (continue with question 15) q No (continue with question 16) q Yes q No q Yes (continue with question 18) q No (continue with question 19) Symptoms and risk factors for digital ischemia in world-class beach volleyball I 89

93 Domain C: sports-related risk factors 19. How long have you been playing volleyball? 20. How long have you been playing beach volleyball? 21. How long have you been playing professional beach volleyball? 22. How many hours a week do you play beach volleyball? (practice and matches together) years years years hours in a week 23. How many times during practice or a match do you smash/spike? 24. How many times do you smash/spike the ball away from the shoulder? (smashing/spiking sideways when facing forward) 25. Do you perform weight training for your dominant arm/shoulder? 26. a. Do you perform weight training to increase the strength in your dominant arm/shoulder? q Seldom q Sometimes q Seldom q Sometimes q Regularly q Often q Regularly q Often q Yes (continue with question 26) q No (continue with question 28) q Seldom q Sometimes b. If so, how many minutes per week? minutes 27. a. Do you perform weight training to maintain the strength in your dominant arm/shoulder? q Seldom q Sometimes a. If so, how many minutes per week? minutes q Regularly q Often q Regularly q Often 90 I Chapter 5

94 Domain D: symptoms associated with digital ischaemia 28. Do you suffer from cold fingers in your dominant hand? a. during practice or matches? q No, never q Yes, sometimes q Yes, often q Yes, always b. directly after practice or matches? q No, never q Yes, sometimes q Yes, often q Yes, always Do you suffer from blue fingers in your dominant hand? a. during practice or matches? q No, never q Yes, sometimes q Yes, often q Yes, always b. directly after practice or matches? q No, never q Yes, sometimes q Yes, often q Yes, always 30. Do you suffer from pale fingers in your dominant hand? a. during practice or matches? q No, never q Yes, sometimes q Yes, often q Yes, always b. directly after practice or matches? q No, never q Yes, sometimes q Yes, often q Yes, always Symptoms and risk factors for digital ischemia in world-class beach volleyball I 91

95 APPENDIX B Overview of demographics, personal, and sports-related risk factors for the symptomatic and reference group of international world-class volleyball players Answering category Symptomatic Group (n=13) Reference Group (n=47) Significance Domain A: Demographics Age Years Mean: 27.0 SD: 2.9 Range: Mean: 26.0 SD: 3.7 Range: t = p = 0.34 Sex Male: Female: : 2 /13 (15%) : 11/13 (85%) : 24/47 (51%) : 23/47 (49%) χ 2 = 5.30 p = 0.02 Body height Centimetres Mean: SD: 11.9 Range: Body weight Kilograms Mean: SD: 12.0 Range: Domain B: Personal risk factors Mean: SD: 9.72 Range: Mean: 78.9 SD: 12.3 Range: t = 0.50 p = 0.63 t = 1.51 p = 0.14 Family history on Raynaud s Phenomenon Yes: + No: - +: 0/13 (0%) -: 13/13 (100%) +: 0/47 (0%) -: 47/47 (100%) χ 2 = 0.00 p = 0.00 * Family history on cardiovascular disease Yes: + No: - +: 5/13 (38%) -: 8/13 (62%) +: 9/47 (19%) -: 38/47 (81%) χ 2 = 2.12 p = 0.15 Smoking Yes: + No: - +: 1/13 (8%) -: 12/13 (92%) +: 10/47 (21%) 37/47 (79%) χ 2 = 1.30 p = 0.30 Domain C: Sports-related risk factors Total years playing volleyball Years Mean: 15.2 SD: 4.3 Range: 9-21 Mean: 12.7 SD: 4.7 Range: 4-29 t = p = 0.09 Years playing beach volleyball Years Mean: 8.7 SD: 3.2 Range: 4-13 Mean: 9.1 SD: 3.6 Range: 2-18 t = 0.32 p = 0.75 Years playing professional beach volleyball Years Mean: 6.1 SD: 2.6 Range: 2-10 Mean: 6.0 SD: 2.9 Range: 0-13 t = p = I Chapter 5

96 Answering category Symptomatic Group (n=13) Reference Group (n=47) Significance Number of practice and competition hours per week Hours Mean: 19.5 SD: 5.4 Range: Mean: 19.4 SD: 6.7 Range: 4-40 t = p = 0.97 Smashing/spiking frequency Smashing/spiking away from the shoulder Regularly/ often: + Seldom/ sometimes: - Regularly/ often: + Seldom/ sometimes: - +: 13/13 (100%) -: 0/13 (0%) +: 9/13 (69%) -: 4/13 (31%) +: 46/47 (98%) -: 1/47 (2%) +: 32/47 (68%) -: 15/47 (32%) t = 0.30 p = 0.60 χ 2 = p = Performing dominant limb weight training in general Yes: + No: - +: 13/13 (100%) -: 0/13 (0%) +: 42/47 (89%) -: 5/47 (11%) χ 2 = 1.51 p = 0.22 Frequency of performing weight training to increase dominant limb strength Regularly/ often: + Seldom/ sometimes: - +: 8/13 (62%) -: 5/13 (38%) +: 32/47 (68%) -: 15/47 (32%) χ 2 = 0.20 p = 0.70 Number of hours per week performing weight training to increase dominant limb strength Hours Mean: 1.12 SD: 0.71 Range: Mean: 1.10 SD: 0.93 Range: t = p = 0.90 Frequency of performing weight training to maintain dominant limb strength Regularly/ often: + Seldom/ sometimes: - +: 12/13 (92%) -: 1/13 (8%) +: 37/47 (79%) -: 10/47 (21%) χ 2 = 0.30 p = 1.30 Number of hours per week performing weight training to maintain dominant limb strength Hours Mean: 0.41 SD: 0.01 Range: Mean: 0.41 SD: 0.11 Range: t = p = 0.90 * = no Chi-Square or p-value could be calculated because no volleyball players reported being exposed to this risk factor. Symptoms and risk factors for digital ischemia in world-class beach volleyball I 93

97

98 PART II Imaging

99

100 CHAPTER 6 B-mode ultrasound assessment of the Posterior Circumflex Humeral Artery - The SPI-US protocol: a technical procedure in 4-steps Daan van de Pol Mario Maas Aart Terpstra Marja J.C. Pannekoek-Hekman P. Paul F.M. Kuijer R. Nils Planken Journal of Ultrasound in Medicine. Accepted for publication Sept doi: /ultra

101

102 ABSTRACT Elite overhead athletes are at risk of vascular injury due repetitive abduction and external rotation of the dominant arm. The posterior circumflex humeral artery (PCHA) is prone to degeneration, aneurysm formation and thrombosis in elite volleyball players and baseball pitchers. PCHA related thromboembolic complications prevalence is unknown in this population. However, the prevalence of symptoms associated with digital ischemia is 31% in elite volleyball players. A standardized non-invasive imaging tool will aid in early detection of PCHA pathology, prevention of thromboembolic complications, and measurement reproducibility. A standardized vascular US protocol for assessment of the proximal PCHA (SPI-US protocol) is presented. 6 Ultrasound of the PCHA - The SPI-US protocol I 99

103 INTRODUCTION Elite volleyball players frequently suffer from cold, discoloured, and painful fingers in the dominant hand which might be the result of emboli derived from the posterior circumflex humeral artery (PCHA) in the ipsilateral shoulder. 89 The PCHA is a side branch of the third part of the axillary artery and is prone to degeneration in elite overhead athletes, such as volleyball players and baseball pitchers, as a result of vascular injury due to repetitive abduction and external rotation of the arm. This repetitive injury of the proximal PCHA can lead to degeneration, aneurysm formation, thrombosis, and distal embolization. The prevalence of elite overhead athletes with PCHA related thromboembolic complications is still unknown. However, the prevalence of digital ischemic symptoms is up to 31% in elite volleyball players. 89 A late diagnosis can disable the overhead athlete and threaten the athletes career. 17 Correct and timely recognition of signs and symptoms of embolization are key in diagnosis. An attractive imaging modality is vascular ultrasound (US), that is readily available, applicable on-site, inexpensive, and patient friendly. In general US is the firstline imaging modality for aneurysm assessment. It enables non-invasive and patient friendly measurement of vessel diameters and detection of intravascular thrombus. 42 Early detection of PCHA degeneration, aneurysm formation and intravascular thrombus can potentially prevent thromboembolic complications and irreversible tissue damage. Currently there is no standardized vascular US PCHA protocol available. 17 A standardized US PCHA protocol is important because worldwide standardization and implementation will aid in targeted and accurate PCHA imaging. The PCHA is a relatively small branch arising from the axillary artery. The axillary artery (AA) is a continuation of subclavian artery distal to the first rib and gives rise to six branches, according to most descriptions. 43,80 The superior thoracic artery arises from the first part of AA. The thoracoacromial artery (TAA) and lateral thoracic artery (LTA) arise from the second part. Three branches arise from the third part; the subscapular artery (SAA), anterior circumflex humeral artery (ACHA), and PCHA (Figure 1). 43,80 The PCHA frequently is the last branch arising from the AA. However, the deep brachial artery (DBA) arising from the proximal brachial artery frequently has an aberrant origin, and may arise from the dorsal AA, nearby and closely resembling the PCHA. 5,20,76 The PCHA is prone to degeneration in overhead athletes where the DBA has not been reported to be at risk in overhead athletes in the medical literature. Therefore it is important to discriminate the PCHA from the DBA. The prevalence of PCHA origin variations is up to 33-42%. Common PCHA anatomical variants include a common trunk of SSA and PCHA (12-34%) (Figure 2), or a common trunk of the PCHA and DBA (8%) (Figure 3). 43, I Chapter 6

104 The proximal PCHA is characterized by its dorsal origin, slight obtuse angle, and curved course running along the dorsal surgical neck of the humeral bone, deflecting from the AA. The proximal DBA is also characterized by a dorsal origin, but with a sharp angle, and a straight course running almost parallel to the AA towards the triceps brachii muscle. This anatomical knowledge is important for correct PCHA identification. Aneurysm can be defined as a segmental vessel dilatation of more than 50% compared to the closest normal appearing vessel segment proximal or distal to the aneurysmatic segment. 50 An example of an aneurysmatic PCHA in an elite volleyball player is shown in Figure 4. A known limitation of US is that it is observer dependent which may limit the diagnostic accuracy of this imaging modality. Both cross-sectional and longitudinal views are important to identify vessels, their course and to localize abnormalities. Furthermore, the reproducibility of vascular diameter measurements can be improved by using both cross-sectional and longitudinal views for the assessment of vascular diameters. The cross-sectional diameter measurement should be performed perpendicular to the vessel centerline whereas in the longitudinal view the diameter measurement should be performed along the centerline. Standardization of vascular US protocols is important to improve inter- and intra-observer reproducibility. 84,85 However, a standardized PCHA US protocol is currently not available to enable accurate diagnosis of PCHA pathology. Therefore, we present a 4-step standardized vascular US protocol for assessment of the proximal PCHA: the SPI-US protocol (Shoulder PCHA pathology and digital Ischemia UltraSound protocol). 6 Ultrasound of the PCHA - The SPI-US protocol I 101

105 Figure 1 Classic PCHA origin from the axillary artery I, first part of axillary artery; II, second part of axillary artery; III, third part of axillary artery; B, brachial artery; STA, superior thoracic artery; TAA, thoracoacromial artery; LTA, lateral thoracic artery; ACHA, anterior circumflex humeral artery; SSA, subscapular artery; PCHA, posterior circumflex humeral artery; DBA, deep brachial artery Figure 2 Common trunk of the PCHA and SSA I, first part of axillary artery; II, second part of axillary artery; III, third part of axillary artery; B, brachial artery; STA, superior thoracic artery; TAA, thoracoacromial artery; LTA, lateral thoracic artery; ACHA, anterior circumflex humeral artery; SSA, subscapular artery; PCHA, posterior circumflex humeral artery; DBA, deep brachial artery 102 I Chapter 6

106 6 Figure 3 Common trunk of the PCHA and DBA I, first part of axillary artery; II, second part of axillary artery; III, third part of axillary artery; B, brachial artery; STA, superior thoracic artery; TAA, thoracoacromial artery; LTA, lateral thoracic artery; ACHA, anterior circumflex humeral artery; SSA, subscapular artery; PCHA, posterior circumflex humeral artery; DBA, deep brachial artery Figure 4 Longitudinal B-mode ultrasound image of the aneurysmatic proximal PCHA in a professional volleyball player. AA, axillary artery; PCHA, posterior circumflex humeral artery Ultrasound of the PCHA - The SPI-US protocol I 103

107 ULTRASOUND PROTOCOL Step 1. The patient is seated next to the operator with the target arm in 60 abduction with the hand resting on the iliac crest (Figure 5). A high frequency broadband linear array transducer is positioned sagittal oblique in the axillary pit, directed towards the gleno-humeral joint. The axillary artery (AA) and the axillary vein (AV) are identified by a cross-sectional sweep and longitudinal view. Both views are important to identify the course and calibre of the vessels and localization of abnormalities. In general, the AV is larger than the AA and the AV is compressible, whereas the AA is not. An important landmark is the large calibre TAA, arising from the dorsal side of the AA (Figure 6). Step 2. A cross-sectional sweep is performed from the axillary pit down to the origin of the brachial artery for general anatomical evaluation, localization of side braches and for specific assessment of the PCHA and DBA. Step 3. The PCHA and DBA are identified. The PCHA origin is located proximal to the DBA origin. The proximal PCHA is characterized by its dorsal origin and curved course running along the dorsal surgical neck of the humeral bone, deflecting from the AA (Figures 7 and 8). The proximal DBA is also characterized by a dorsal origin and has a straight course running almost parallel to the AA towards the Triceps Brachii muscle. The DBA is the last dorsal branch of the AA in the axillary pit (Figure 9). Step 4. The PCHA and DBA diameters are measured at approximately 1 cm distance from the origin. In the event of PCHA dilatation, the maximum diameter of the PCHA is measured. In addition the diameter of the closest normal appearing PCHA vessel segment proximal, or otherwise distal, to the dilated vessel segment is measured. Additionally, the presence of intravascular thrombus and/or vessel occlusion is identified and recorded. Waveform characteristics are obtained to visualize a triphasic or blunted signal. A blunted signal is correlated with a more distal occlusion. 104 I Chapter 6

108 6 Figure 5 Participants position during the examination Figure 6 Cross-sectional view at the proximal axillary pit AA, axillary artery; TAA, thoracoacromial artery Ultrasound of the PCHA - The SPI-US protocol I 105

109 Figure 7 Cross-sectional view of the PCHA; 1. At PCHA origin; 2. Half way to surgical neck of the humerus; 3. Along surgical neck of the humerus AA, axillary artery; PCHA, posterior circumflex humeral artery; HH, humeral head 106 I Chapter 6

110 Figure 8 Longitudinal view of the PCHA AA, axillary artery; PCHA, posterior circumflex humeral artery 6 Figure 9 A. Cross-sectional view of the DBA; B. Longitudinal view of the DBA AA, axillary artery; AV, axillary vein; DBA, deep brachial artery; HH, humeral head Ultrasound of the PCHA - The SPI-US protocol I 107

111 IMPLEMENTATION Volleyball is among the most widely played sports in the world and is played by around 260 million people regularly. Elite volleyball players worldwide are potentially at risk of PCHA aneurysm and thrombosis with distal embolization. 89 Diagnosis is established based on history-taking, physical examination and diagnostic imaging, both non-invasive and invasive. Non-invasive testing, like digital photoplethysmography and vascular ultrasound, are used in the work-up towards invasive testing, i.e. digital subtraction angiography (DSA), the standard of reference or less invasive computed tomographic angiography (CTA). Both are associated with ionizing radiation and the use of contrast media. However these modalities are currently required for diagnosis and treatment planning. Athletes present themselves late in disease with symptoms of digital ischemia in daily live. Symptoms include coldness, discoloration, pain and paresthesia. These symptoms may cause severe discomfort, reduced daily quality of life, and may ultimately lead to necrosis and finger loss when trivialized. In an early stage of disease, the aneurysm is occult as long as the player is free of symptoms. Symptoms might only manifest after overhead movements in volleyball, when emboli are squeezed out of the aneurysmatic and thrombosed PCHA into the axillary artery and embolize into the digital circulation. This can lead to transient local coldness and discoloration during or directly after volleyball. 89 A screening questionnaire can be used to triage these athletes who experience vague symptoms during volleyball, possibly related to distal embolization 89. These athletes might benefit from non-invasive screening diagnostic imaging in an early stage to objectify local PCHA pathology. A convenient imaging modality is vascular ultrasound (US), which is readily available, inexpensive, patient friendly and enables on-site application. Vascular ultrasound has been reported previously to visualize and measure blood flow in the distal PCHA in healthy volunteers through a posterolateral approach on the upper arm. 103 However, the majority of PCHA pathology in volleyball players has been reported in the proximal part of the PCHA, near the take-off from the axillary artery. 17,115,126 This is consistent with the location of pathology seen in volleyball players who were diagnosed and treated in our academic hospital. 3,89,95,96 The presented standardized vascular (SPI-US) protocol is quick and easy and enables on-site application which can aid in early detection of PCHA pathology. Furthermore, this protocol can be used in a clinical setting in the diagnostic work-up towards diagnosis and treatment planning. Standardization of US PCHA imaging will contribute to the reproducibility of the acquired measurements, intercollegial exchange of reference values, and more knowledge on this overhead-sport-specific injury. The protocol instructions and corresponding images provide clear guidance for identification and 108 I Chapter 6

112 assessment of the PCHA. International dissemination of this protocol should make it possible to identify PCHA injury at an early stage. A first step to do so has been taken during a large international beach volleyball tournament in the summer of In conclusion, a standardized 5 to 10 minute vascular US (SPI-US) protocol is presented for PCHA assessment in order to detect aneurysm related embolization. The results of a subsequent study to determine the reproducibility and accuracy of the presented protocol are expected. 6 Ultrasound of the PCHA - The SPI-US protocol I 109

113

114 CHAPTER 7 Reproducibility of the SPI-US protocol for ultrasound diameter measurements of the Posterior Circumflex Humeral Artery and Deep Brachial Artery: an inter-rater reliability study Daan van de Pol Sena Alaeikhanehshir P. Paul F.M. Kuijer Aart Terpstra Marja J.C. Pannekoek-Hekman R. Nils Planken* Mario Maas* * RP and MM equally contributed to this study European Radiology 2015 Dec 10. [Epub ahead of print] doi:0.1007/s

115

116 ABSTRACT Objectives Elite overhead athletes are at risk of posterior circumflex humeral artery (PCHA) degeneration, aneurysm formation and thrombosis. Identification of the proximal PCHA and the nearby originating deep brachial artery (DBA) can be a challenge, even among experienced sonographers. The aim of this study was to assess the accuracy and precision of a newly designed standardized ultrasound (US) protocol (SPI-US) for assessment of the PCHA and DBA. Methods Two experienced sonographers determined diameters of the PCHA and DBA using the SPI-US protocol. Inter-observer agreement was evaluated using intra-class correlation coefficient (ICC), Standard Error of Measurement (SEM), Minimal Detectable Change (MDC), Bland-Altman (BA) analysis and Variance Component analysis (VARCOMP). Results Thirty-three healthy volunteers participated. The ICC for diameter measurement of the PCHA and DBA were 0.70 (95%CI ) and 0.60 (95%CI ), respectively. The SEM for the PCHA and DBA was 0.32 mm and 0.29 mm and MDC was 0.90 mm and 0.80 mm, respectively. The BA and VARCOMP analysis showed no systematic and only marginal sonographer bias. 7 Conclusions The SPI-US protocol is accurate and precise for PCHA and DBA diameter assessment in cases where they originate from the axillary artery. PCHA and DBA diameter measurements are sonographer-independent using the SPI-US protocol. Reproducibility of the SPI-US protocol I 113

117 INTRODUCTION Elite overhead athletes are at risk of vascular injury in the dominant shoulder due to repetitive abduction and external rotation of the arm. The posterior circumflex humeral artery (PCHA) is a side branch of the third part of the axillary artery (AA) and is prone to degeneration, aneurysm formation and thrombosis in elite overhead athletes such as professional volleyball players and baseball pitchers. 2,3,17,89,95,115,126 Digital ischemia due to embolic occlusion ensues from extrusion of intraluminal thrombus squeezed from the aneurysmatic PCHA into the AA during sports-specific overhead activity. 49,115,126 The embolic complications of the affected extremity, in combination with pain and ischemia, can lead to the manifestation of this entity. In volleyball players, the vast majority of PCHA aneurysm formation and thrombosis has been reported in the proximal part of the PCHA, in the trajectory from the take-off from the AA up to the passage through the quadrilateral space (QS) (Figure 1). 3,17,89,95,115,126 The QS is bounded by the long head of the triceps medially, the surgical neck of the humerus laterally, the tendon of the teres major and latissimus dorsi muscles inferiorly, and the teres minor muscle or the scapulohumeral capsule superiorly. 67,77 Although the PCHA is frequently the last branch arising from the AA, with a prevalence of origin variations reported to be 33-42% 43,80, the deep brachial artery (DBA), which normally arises from the proximal brachial artery, may have an aberrant origin and also arise from the dorsal AA, nearby and closely resembling the PCHA (Figure 2 & 3). 5,20,76 The PCHA is prone to degeneration in overhead athletes where the DBA has not been reported to be at risk in overhead athletes in the medical literature. Therefore it is important to discriminate the PCHA from the DBA. Ultrasound (US) is preferred for initial vascular assessment since this technique is patient friendly, easily available, cheap, fast, non-invasive and not associated with radiation exposure. 93 US has been reported previously for assessment of the distal PCHA through a posterolateral approach on the upper arm. 102,103 However, identification and assessment of the proximal PCHA and DBA with US can be a challenge, even among experienced sonographers. 93 Also, a known limitation of US is that it is observer dependent which may limit the diagnostic accuracy of this imaging modality. Since peripheral artery aneurysms are defined as a focal vessel segment dilatation of more than 50% compared to the closest normal appearing vessel segment proximal or distal to the aneurysmal segment 50, accurate and precise wall-to-wall diameter measurement are essential. It is evident that standardization of vascular US protocols is important to improve inter- and intra-observer reproducibility. 84,85 Recently, a standardized US protocol to measure proximal PCHA and DBA diameters and detect aneurysm related embolization has been developed - the SPI-US protocol I Chapter 7

118 However the clinimetric characteristics of this protocol, such as inter-observer reliability and reproducibility of measured diameters, has not yet been determined. Therefore, the aim of this study was to assess the accuracy and precision of the newly designed standardized SPI-US protocol for diameter assessment of proximal PCHA and DBA in cases where they originate from the axillary artery. 7 Figure 1 Diagrammatic representation of the quadrilateral space from posterior Key: QS, quadrilateral space (drawing by K.F. de Geus) Reproducibility of the SPI-US protocol I 115

119 Figure 2 Classic PCHA origin from the axillary artery (drawing by K.F. de Geus) Key: AA. axillary artery; I, first part of axillary artery; II, second part of axillary artery; III, third part of axillary artery; B, brachial artery; STA, superior thoracic artery; TAA, thoracoacromial artery; LTA, lateral thoracic artery; ACHA, anterior circumflex humeral artery; SSA, subscapular artery; PCHA, posterior circumflex humeral artery; DBA, deep brachial artery Figure 3 Common trunk of the PCHA and DBA (drawing by K.F. de Geus) Key: AA. axillary artery; I, first part of axillary artery; II, second part of axillary artery; III, third part of axillary artery; B, brachial artery; STA, superior thoracic artery; TAA, thoracoacromial artery; LTA, lateral thoracic artery; ACHA, anterior circumflex humeral artery; SSA, subscapular artery; PCHA, posterior circumflex humeral artery; DBA, deep brachial artery 116 I Chapter 7

120 MATERIALS AND METHODS Study Design To determine inter-observer reliability of the newly designed standardized SPI-US protocol for diameter measurements of the PCHA and DBA when performed by experienced sonographers, a cross-sectional within subject study with two sonographers was performed among healthy volunteers. Participant Selection nquery advisor 7.0 (Statistical Solutions Ltd, 2007) was used to determine the requirements for a reliability test with two registered sonographers. To assess an intraclass correlation coefficient of 0.8, 24 normal anatomical variants of the PCHA and 24 normal anatomical variants of the DBA were needed with a two-sided test with a P-value of 0.05 and a distance from correlation to limit of Participants were recruited from the medical faculty at the Academic Medical Center in Amsterdam. The inclusion criteria were (1) healthy males and females aged between 18 and 35 years, and (2) written informed consent. 7 Volunteers with a history for vascular surgery of the dominant shoulder or lack of written informed consent were not considered eligible for inclusion. The Medical Ethics Review Committee of our academic hospital stated that the Medical Research Involving Human Subjects Act (WMO) did not apply to this study and that no official approval of this study was required. Study protocol Prior to the ultrasound examination each participant completed a short questionnaire with questions regarding age, gender, body height, body weight, and total hours of overall sports activity per week. Subsequently, measurements of proximal PCHA and DBA diameters were performed in the dominant and non-dominant shoulder by two sonographers individually. Each shoulder was regarded as a distinctive entity, since anatomical variations of the PCHA have been reported to be bilateral in 0% to 88% of cases. 80. Diameters were measured once in millimeters (mm). In case of an origin variation with the PCHA or DBA arising from a common trunk, the diameter was not measured and the vessel was not included in the analysis. These cases were excluded because accurate identification and correct assessment of PCHAs and DBAs originating from a common trunk using US is cumbersome due to large variation in branching patterns. The two sonographers were independent and blinded for each other s results. Reproducibility of the SPI-US protocol I 117

121 Sonographers Both sonographers in this study were registered vascular technicians (RVT) with more than 20 years of experience with vascular US, who studied the anatomy of the branching pattern of the AA and its anatomical variations intensively from the start of this study, and had extensive experience in conducting the standardized SPI-US protocol among more than 300 volleyball players. Ultrasound assessment Ultrasound assessment was performed using a Philips iu22 (Philips 2004 & Philips 2007, version NZE 239) with high frequency broadband linear array transducers (8-4 MHz and 9-3 MHz). The standardized SPI-US protocol as designed by van de Pol et al was used for all PCHA and DBA diameter measurements. 93 Sonographer insight knowledge on PCHA and DBA anatomy, branching pattern and vessel characteristics, as reported by van de Pol et al. 92, facilitated accurate identification of the PCHA and DBA and provided clear guidance for correct assessment. Data analysis Data were entered in SPSS (version 21.0, 2012, SPSS Inc.) and correct data entry was checked. Demographic data of the participants are shown as means, standard deviations, and ranges. Inter-rater reliability intra-class correlation coefficients (ICC) for diameters of the PCHA and DBA were calculated using a two-way random effects model. Both ICC s were single measure ICC s. The classification used for the interpretation of the obtained ICC s was according to Fleiss 29 (<0.40, poor reliability; , good reliability; >0.75, excellent reliability). Standard error of measurement (SEM) was acquired using the earlier obtained ICCs with the SEM formula SEM = SD (1 ICC). 124 Unlike the ICC, which is a relative measure of reliability, the SEM provides an absolute index of reliability. The SEM has the same unit as the measurement of interest, in this case millimeters (mm). In context of absolute reliability, also the minimal detectable change (MDC) was determined with the MDC formula, MDC 95 = SEM * 1.96 * 2. The MDC represents the magnitude of change necessary to exceed the measurement error of two repeated measures at a 95% confidence interval (CI). Bland-Altman plots were used to assess systematical differences and biases between the two sonographers for PCHA and DBA. Finally, a variance components analysis (VARCOMP) was performed to determine sonographer and participant contribution to the variance. In summary, the ICC, SEM, Bland-Altman analysis and VARCOMP analysis are all parameters used to express the value of reliability. 118 I Chapter 7

122 RESULTS Participants Thirty-three healthy participants with a mean age of 25 years were included, 26 males (79%) and 7 females (21%). On average participants were 25 years old (range years), had a body height of 184 centimeters (range centimeters), and a body weight of 78 kilograms (range kilograms). The inclusion of 33 participants resulted in 66 included shoulders and as many PCHA s and DBA s. The PCHA originated from a common trunk in 45% of cases (n=30), and the DBA originated from a common trunk in 58% of cases (n=38). This resulted in the inclusion of 36 PCHA s and 28 DBA s that originated directly from the AA (Figure 4). The mean measured PCHA diameter by sonographer 1 was 3.7 mm (95% CI ) and 3.7 mm (95% CI ) by sonographer 2. The mean measured DBA diameter by sonographer 1 was 2.3 mm (95% CI ) and 2.4 mm (95% CI ) by sonographer 2 (Table 1). 7 Figure 4 Flow chart of the inclusion of the participant Reproducibility of the SPI-US protocol I 119

123 Table 1 Mean, standard deviation, and range of PCHA and DBA diameters by sonographer 1 and 2 with level of reliability n Sonographer 1 Sonographer 2 Mean (95%CI) ICC (95%CI) SEM (mm) MDC (mm) Mean (mm) SD Range (mm) Mean SD Range Mean SD Range PCHA ( ) ( ) DBA ( ) ( ) Key: PCHA, posterior circumflex humeral artery; DBA, deep brachial artery; mm; millimeters; SD, standard deviation; ICC, intra-class correlation coefficient; CI confidence interval; SEM, standard error of measurement; MDC, minimal detectable change 120 I Chapter 7

124 Reliability ICC & SEM & MDC The ICC for the diameter measurement between sonographer 1 and 2 was 0.7 (95% CI ) for the PCHA, and 0.6 (95% CI ) for the DBA, which corresponds with good reliability according to Fleiss. 29 The obtained SEM was 0.3 mm for the PCHA and 0.3 mm for the DBA. The MDC was 0.9 mm for the PCHA and 0.8 mm for the DBA (Table 1). Bland-Altman analyses The Bland-Altman for measured PCHA diameters shows no proportional bias. Most data points are plotted below the mean difference line, which results in a sufficient level of agreement between the two sonographers. The Bland-Altman plot for measured DBA diameters shows an even better level of agreement. The mean of the differences among the two sonographers is almost nil for PCHA and DBA diameter measurements, which reflects good inter-rater concordance. Only two data points are plotted outside the limits of agreement (±1.96 SD), which is supportive for sufficient level of agreement between the two sonographers (Figure 5). Variance Component (VARCOMP) analysis The VARCOMP analysis revealed that the variation in measured PCHA diameters was mostly participant-dependent: 67%. The sonographers-dependent variation was 1%, the side-dependent variation (left or right shoulder) was 3% and the remaining was random error. The variation in measured DBA diameters was also mostly participant-dependent: 52%. The sonographers-dependent variation was 1%, the side-dependent variation (left or right shoulder) was 5%, and the remaining was random error. 7 Figure 5 Bland-Altman analyses of difference in PCHA and DBA diameters between sonographers 1 and 2 (X-axis), against the means of diameter measurements obtained by both sonographers (Y-axis) Key: O1, sonographer 1; O2, sonographer 2; DM, diameter (millimeters); PCHA, posterior circumflex humeral artery; DBA, deep brachial artery Reproducibility of the SPI-US protocol I 121

125 DISCUSSION Main findings The main finding of this study is that the newly designed standardized SPI-US protocol is accurate and precise for diameter assessment of the PCHA and DBA in cases where they originate from the axillary artery, with an ICC of 0.70 and 0.60 and a MDC of 0.90 mm and 0.80 mm, respectively. PCHA and DBA diameter measurements are sonographerindependent using the SPI-US protocol. Elite volleyball players worldwide are potentially at risk of PCHA aneurysm and thrombosis with distal embolization. 89 Vascular ultrasound is an appropriate diagnostic imaging modality in this population since it is readily available, inexpensive, patient friendly, and enables on-site application. Standardization of US measurements by sonographers is important to improve reproducibility and inter-rater reliability, which has been the subject of several studies in other medical fields. 84,85 Although these studies involve veins and not arteries, they also report on reproducibility using (different combinations of) parameters such as ICC, SEM, Bland-Altman and VARCOMP to express the value of reliability, in order to assess US protocols for diagnostic purposes. Since the clinimetric characteristics of the SPI-US protocol are sufficient, the question remains if it can be used for diagnostic purposes i.e. to detect PCHA aneurysms. In the medical literature, a peripheral artery aneurysms is defined as a focal vessel segment dilatation of more than 50% compared to the closest normal appearing vessel segment proximal or distal to the aneurysmatic segment. 50 Data regarding normal vessel diameters are sparse, and for the PCHA to our knowledge unavailable. In the 36 measured PCHA diameters in this study, the mean measured diameter was 3.70 mm (95% CI ). This would mean an increase in PCHA diameter in our study population with 50% of 3.70mm = 1.85mm, resulting in a total diameter of 5.55mm ( mm) or more. With a calculated MDC of 0.90mm it is safe to say that this type of dilatation of the PCHA would have been detected. Therefore, it can be concluded that the SPI-US protocol performed by our experienced sonographers seems clinically valid for aneurysm detection in this population. Strengths & Weaknesses A strength of this study is that five statistic outcome measures are used to calculate the inter-rater reliability of the standardized US protocol for measuring PCHA and DBA diameters, since most studies only use one or two statistic tests. 34,38,52,63,86 Also, the VARCOMP analysis revealed that PCHA diameter measurements are sonographerindependent which is in line with the findings of Planken et al 84, who also calculated the SEM and MDC in their vascular ultrasound reproducibility study. A second strength is the use of the determined ICC s to calculate the SEM, since most other studies do 122 I Chapter 7

126 not perform an inter-rater study prior of determining the SEM, and tend to use an ICC value from another study. 124 A clinical strength of this study is the standardized PCHA diameter measurement at cm from the origin, since the vast majority of PCHA aneurysms has been reported in the proximal part of the PCHA, near the take-off from the AA. 3,17,89,95,115,126 A limitation of this study is the lack of a reference modality to confirm whether the sonographically examined and measured arteries were indeed the PCHA and DBA, and to confirm if examined PCHAs and DBAs truly originated from a common trunk or not. However, ultrasound assessment was performed by two sonographers, blinded to each other s results. Both sonographers in this study were experienced and familiar with the standardized SPI-US protocol. Moreover, they had extensive experience in conducting the SPI-US protocol among more than 300 volleyball players. 91,92 This knowledge on PCHA and DBA anatomy, branching pattern and vessel characteristics facilitated accurate identification of the both arteries and provided clear guidance for correct assessment, which contributed to a high reliability. However, the lack of a reference modality remains a limitation of the current study. Another limitation is the exclusion of cases with PCHAs and DBAs originating from a common trunk. However, a recent study shows that PCHA aneurysms occur only in PCHAs that originate directly from the axillary artery. 92 Therefore, diameter measurements of PCHAs originating from a common trunk instead of the AA seems to be clinically less relevant. 7 Clinical implications Volleyball is among the most widely played sports in the world and is played by around 260 million people regularly. Elite volleyball players worldwide are potentially at risk of PCHA aneurysm and thrombosis with distal embolization. 89 PCHA diameters can be accurately and precisely measured using the SPI-US protocol. Also, the calculated MDC enables application of this protocol for detection of PCHA aneurysms. The reproducibility of the acquired diameters can aid in intercollegial exchange of reference values for PCHA diameters. International dissemination of this protocol can make it possible to identify PCHA injury, both for an on-site periodic surveillance, and in a clinical setting. We recommend this protocol to be performed by sonographers with good anatomical knowledge of AA branching patterns and its anatomic variations. Future studies should address the trainability of this protocol, the reproducibility of acquired measurements, and the interpretation of its results in a population of experienced vascular sonographers. Also, standardized diameter measurements of the PCHA should be performed in a large population of elite overhead athletes to obtain data Reproducibility of the SPI-US protocol I 123

127 regarding normal PCHA diameters and vessel characteristics. These PCHA characteristics and diameters can be used as reference values (normal versus aneurysmal) for clinical assessment and research. Finally, future studies should assess the use of the SPI-US protocol for aneurysm detection in a large group of elite overhead athletes at risk. In summary, the standardized SPI-US protocol is accurate and precise for diameter assessment of the PCHA and DBA in cases where they originate from the axillary artery. PCHA diameter measurements are sonographer-independent using the standardized US protocol. In this population, the SPI-US protocol seems clinically valid for aneurysm detection when performed by two experienced sonographers. International dissemination of this protocol should make it possible to identify PCHA injury, both for on-site periodic surveillance, and in a clinical setting. 124 I Chapter 7

128

129

130 CHAPTER 8 Ultrasound assessment of the Posterior Circumflex Humeral Artery in elite volleyball players: aneurysm prevalence, anatomy, branching pattern and vessel characteristics Daan van de Pol Mario Maas Aart Terpstra Marja J.C. Pannekoek-Hekman Sena Alaeikhanehshir P. Paul F.M. Kuijer R. Nils Planken European Radiology. Conditionally accepted for publication Feb 2016.

131

132 ABSTRACT Objectives To determine the prevalence of Posterior Circumflex Humeral Artery (PCHA) aneurysms and vessel characteristics of the PCHA and Deep Brachial Artery (DBA) in elite volleyball players. Methods Two-hundred-eighty players underwent standardized ultrasound assessment of the dominant arm by a vascular technologist. Assessment included determination of PCHA aneurysms (defined as segmental vessel dilatation 150%), PCHA and DBA anatomy, branching pattern, vessel course, and diameter. Results The PCHA and DBA were identified in 100% and 93% (260/280) of cases, respectively. The prevalence of PCHA aneurysms was 4.6% (13/280). All aneurysms were detected in proximal PCHA originating from the axillary artery (AA). The PCHA originated from the AA in 81% of cases (228/280), and showed a curved course dorsally towards the humeral head in 93% (211/228). The DBA originated from the AA in 73% of cases (190/260), and showed a straight course parallel to the AA in 93% (177/190). 8 Conclusions PCHA aneurysm prevalence in elite volleyball players is high and associated with a specific branching type: a PCHA that originates from the axillary artery. Radiologists should have a high index of suspicion for this vascular overuse injury. For the first time vessel characteristics and reference values are described to facilitate ultrasound assessment. Aneurysm prevalence and vessel characteristics of the PCHA I 129

133 INTRODUCTION Elite overhead athletes, like volleyball players, are at risk of ischemic digits due to arterial emboli originating from an aneurysmal and thrombosed proximal posterior circumflex humeral artery (PCHA) in the dominant shoulder, although the exact prevalence among these athletes is unknown. 89 Although ultrasound (US) is the first-line imaging modality for assessment of the PCHA, identifying and assessing the PCHA is a cumbersome process in the hands of radiologists and vascular technologists. The PCHA is a relatively small branch originating from the third part of the axillary artery (AA). Although it is frequently the last branch originating from the AA, with a prevalence of origin variations reported to be 33-42% 43,80, the deep brachial artery (DBA), which normally originates from the proximal brachial artery, may have an aberrant origin and also arise from the dorsal AA, near to and closely resembling the PCHA (Figures 1 & 2). 5,20,76 Since the PCHA is prone to injury in overhead athletes where the DBA has not been reported to be at risk in overhead athletes in the medical literature, it is important to distinguish between the PCHA and the DBA. The SPI-US protocol 93 enables accurate US assessment of the PCHA and DBA with excellent inter-observer agreement. 87 This US protocol can therefore be used to assess PCHA and DBA anatomy, branching pattern, diameter measurement and detection of aneurysms. However, reference values for arterial diameters should be considered when reporting aneurysms in accordance with the suggested standards for reporting on aneurysms by Johnson et al. 50 The data regarding normal PCHA diameters are not yet published in the medical literature. Data on normal and aneurysmal PCHA diameters and arterial characteristics would facilitate the accurate identification and assessment of the PCHA, and could be used as reference values for aneurysmal and normal vessels in clinical assessment and for research purposes. For other peripheral aneurysms, such as the common femoral artery and the popliteal artery, similar data is commonly used for diagnostic and therapeutic purposes. 42,132 The purpose of this study, therefore, is (1) to determine the prevalence of PCHA aneurysms in elite volleyball players; and (2) to describe PCHA and DBA characteristics that can be used to accurately identify and assess the PCHA. 130 I Chapter 8

134 Figure 1 87 Classic PCHA origin from the axillary artery (drawing by K.F. de Geus) Key: AA. axillary artery; I, first part of axillary artery; II, second part of axillary artery; III, third part of axillary artery; B, brachial artery; STA, superior thoracic artery; TAA, thoracoacromial artery; LTA, lateral thoracic artery; ACHA, anterior circumflex humeral artery; SSA, subscapular artery; PCHA, posterior circumflex humeral artery; DBA, deep brachial artery 8 Figure 2 87 Common trunk of the PCHA and DBA (drawing by K.F. de Geus) Key: AA. axillary artery; I, first part of axillary artery; II, second part of axillary artery; III, third part of axillary artery; B, brachial artery; STA, superior thoracic artery; TAA, thoracoacromial artery; LTA, lateral thoracic artery; ACHA, anterior circumflex humeral artery; SSA, subscapular artery; PCHA, posterior circumflex humeral artery; DBA, deep brachial artery Aneurysm prevalence and vessel characteristics of the PCHA I 131

135 MATERIALS AND METHODS Study Design A cross-sectional ultrasound study was performed among elite volleyball players active at national and international top level from January to July Official approval was granted by the Institutional Review Board (IRB) at our academic hospital and permission was obtained from the Institutional Review Board at the Fédération Internationale de Volleyball (FIVB). Participants Participants were recruited in cooperation with the FIVB and the Dutch Volleyball Association (Nevobo). Those eligible for inclusion were all elite male indoor volleyball players active in the Dutch national top league, second league or Dutch national volleyball team in the season , and all elite male and female beach volleyball players active during the main tournament of the 2014 Beach Volleyball Grand Slam Tournament in The Hague. Volleyball players were not considered eligible for inclusion in the case of a positive history for vascular surgery of the dominant shoulder, use of cardiovascular medication, or lack of written informed consent. Ultrasound assessment All US examinations were performed by one of two registered vascular technologists (RVTs) using a Dynamic LOGIQ e (General Electric Company 2006) scanner equipped with a 12L-RS linear array transducer probe (5-13 MHz), following the standardized SPI- US protocol 93, which enables reliable and sonographer-independent PCHA diameter measurements. 87 Both RVTs had more than 20 years experience with vascular US, had studied the anatomy of the branching pattern of the AA and its anatomical variations intensively, and were experienced in conducting the US protocol that was used. US examination included assessment of branching pattern (origin variations), local anatomy (artery course at the origin), and determination of PCHA and DBA diameters (measured at one centimetre (cm) distance from the origin). Arterial diameters were measured on cross-sectional grayscale B-mode images. In addition, participants were screened for the presence of PCHA aneurysms. Aneurysms were defined as a segmental vessel diameter increase 1.5, and segmental vessel diameter increase between 1 and 1.5 was defined as dilatation. 50 In the event of intravascular thrombus, colour Doppler was used to confirm the presence of thrombus by no flow regions. In a later phase, the obtained US data were independently reviewed by both RVTs and classified as normal, doubtful or pathologic. In the case of divergent conclusions, both RVTs discussed these data in order to reach consensus. Finally, US images of all 132 I Chapter 8

136 pathologic and doubtful cases were reviewed, discussed and definitely classified as normal or pathologic during consensus meetings in which both RVTs and a vascular radiologist participated. Data analysis The mean, standard deviation, minimum and maximum of age, body height, and body surface area (BSA) were reported for men and women separately. Body surface area was calculated according to Du Bois formula (BSA cm 2 = weight kg * height cm * 71.84). 25 The proximal course (defined as parallel or curved), and the prevalence and type of PCHA and DBA origin variations were reported for the group as a whole. The mean, standard deviation, minimum and maximum of normal and aneurysmal PCHA and DBA diameters were reported in millimetres (mm) and corrected for BSA in mm per square metre (m 2 ). The intra-participant PCHA-DBA diameter ratio was calculated to objectify the interdependence, and the intra-participant PCHA diameter ratio was calculated to objectify increase in segmental vessel diameter. RESULTS Participants From January to July 2014, a total of 281 elite volleyball players were assessed using the standardized SPI-US protocol. One player was excluded from the study due to a history of PCHA surgery in the dominant shoulder. As a result, 280 elite volleyball players were included: 245 men and 35 women. Male participants were on average 25±5 years old (range: years), had a body height of 194±7 cm (range: cm), and a BSA of 2.16±0.1 m 2 (range: m 2 ). Female participants were on average 26±4 years old (range: years), had a body height of 180±6 cm (range: cm), and a BSA of 1.87±0.1 m 2 (range: m 2 ). 8 Aneurysm prevalence and diameters of aneurysmal and normal PCHA and DBA In total, 17 PCHA abnormalities were detected 13 aneurysms (11 in men and 2 in women), three dilatations, and one occlusion, resulting in a 4.6% (13/280) prevalence of PCHA aneurysms. All participants were informed and advised about follow-up. All aneurysms were detected in a PCHA that originated directly from the axillary artery. Ten aneurysms (77%) were found in the most proximal PCHA vessel segment within 1 cm from the origin out of the axillary artery (Figure 3). All aneurysms were fusiform-shaped and showed arterial wall irregularities. In four cases the PCHA demonstrated a tortuous course. Intravascular thrombus was visualised in three cases (Figure 4). Characteristics of the PCHA aneurysm are listed per volleyball player in Table 1. Aneurysm prevalence and vessel characteristics of the PCHA I 133

137 Table 1 Characteristics of the PCHA aneurysm per volleyball player Sex Age (years) BSA 1 (m 2 ) 2 Aneurysmal PCHA diameter (mm) 3 Aneurysmal PCHA diameter corrected for BSA 1 (mm/m 2 ) 4 Normal PCHA diameter (mm) 3 Normal PCHA diameter corrected for BSA (mm/m 2 ) 4 Intraparticipant PCHA diameter ratio Aneurysm - distance to origin (mm) 2 Aneurysm - shape Aneurysm - arterial wall compli-cations Aneurysm presence of intravascular thrombus M Tortuous, fusiform Irregular No M Fusiform Irregular, thickened Yes M Fusiform Irregular No M Tortuous, fusiform Irregular No M Fusiform Irregular No M Fusiform Irregular, thickened Yes M Tortuous, fusiform Irregular, thickened Yes M Fusiform Irregular, thickened No M Fusiform Irregular No F Fusiform Irregular No M Tortuous, fusiform Irregular No F Fusiform Irregular No M Fusiform Irregular No 1 BSA = Body Surface Area; 2 m 2 = square meter; 3 mm = millimetres; 4 mm/m 2 = millimetres per square meter 134 I Chapter 8

138 Figure 3 Longitudinal B-mode ultrasound image of the aneurysmatic proximal PCHA in a 31-yearold professional volleyball player Key: AA, axillary artery; PCHA, posterior circumflex humeral artery 8 Figure 4 Upper panel: longitudinal B-mode ultrasound image of the aneurysmatic proximal PCHA with intravascular thrombus in a 29-year-old professional volleyball player. Lower panel: colour Doppler ultrasound image of the aneurysmatic proximal PCHA, note there is no colour flow in the thrombus region (arrowhead) Key: PCHA, posterior circumflex humeral artery Aneurysm prevalence and vessel characteristics of the PCHA I 135

139 The mean aneurysm PCHA diameter in men was 5.9mm±1.7 (95%CI ), and 5.2mm±0.2 (95%CI ) in women. Corrected for BSA, the diameter for men and women was 2.8 mm/m 2 ±0.8 and 2.9 mm/m 2 ±0.1, respectively (Table 2). These diameters were significantly greater compared to non-dilated PCHA vessel segments (p<0.01) (Figures 5 & 6). All DBAs showed a smooth calibre over the proximal course without any dilatations or aneurysmal segments. Figure 5 Scatter plot of absolute PCHA diameters in millimetres Figure 6 Scatter plot of PCHA diameters corrected for Body Surface Area in millimetres per square meter 136 I Chapter 8

140 In total, the diameters of 280 normal PCHA vessel segments were measured, with a mean diameter of 3.8 mm±0.6 (95%CI ) in 245 men, and 3.5 mm±0.6 (95%CI ) in 35 women. Corrected for BSA, the diameter for men and women was 1.8 mm/ m 2 ±0.3 and 1.8 mm/m 2 ±0.4, respectively (Table 2). The diameters of 260 normal DBA vessel segments were measured with a mean diameter of 2.3mm ±0.5 (95%CI ) in 225 men, and 2.0mm±0.5 (95%CI ) in 35 women. Corrected for BSA, the diameter for both men and women was 1.1±0.2 (Table 2). The intra-participant PCHA-DBA diameter ratio was >1 in all these participants. Diameters of 20 DBAs were unable to be determined due to absence in the axillary pit or as a result of origin variation leading to insufficient imaging quality. Anatomy, branching pattern and course of PCHA and DBA The PCHA was identified in 100% of cases and the DBA in 93% (n=260). For the 7% of cases (n=20) in which the DBA was not identified in the axillary pit, the cause might be due to a more distal origin from the brachial artery, an anatomical variant with an absent DBA, or because it was being overlooked by the vascular technologist. An anatomical variation of the PCHA was found in 52 of 280 cases (19%), and included a common trunk with the DBA (n=16), a common trunk with a different artery from the DBA (n=18), a common trunk with two other arteries (n=10), and a trunk with a proximal origin that was not visualised (n=8). The DBA was found to arise from a common trunk in 70 of 260 cases (27%). 8 Table 2 Normal and aneurysmal PCHA and DBA diameters Normal diameter Aneurysmal diameter Men Women Men Women N mean n mean n mean n mean PCHA in millimetres corrected for Body Surface Area in millimetres per square meter ± ± ± ± ± ± ± ±0.1 DBA in millimetres corrected for Body Surface Area in millimetres per square meter ± ± ± ±0.2 n.a. 1 n.a. 1 1 n.a. = not applicable Aneurysm prevalence and vessel characteristics of the PCHA I 137

141 The PCHA showed a curved course dorsally towards the humeral head in 93% of the normal anatomical variants (211/228) (Figure 7), and 7% could not be determined due to insufficient imaging (n=17). The DBA showed a straight course parallel to the axillary artery in 93% of the normal anatomical variants (177/190) (Figure 8), and 7% could not be determined due to insufficient imaging (n=13). The proximity of the PCHA origin seemed to determine the degree and level of curvature. A proximal PCHA origin from the axillary artery led to a more distal curve towards the humeral head (e.g. after 2 to 3 cm), whereas a more distal origin led to an instant and more sharp curve. The DBA course did not seem to be influenced by the proximity of the origin. Figure 7 Longitudinal B-mode ultrasound image of the view of the PCHA with a curved course dorsally towards the humeral head Key: AA, axillary artery; PCHA, posterior circumflex humeral artery Figure 8 Longitudinal B-mode ultrasound image of the view of the DBA with a straight course parallel to the axillary artery Key: AA, axillary artery; DBA, deep brachial artery 138 I Chapter 8

142 In the case of an origin variation, the PCHA and DBA course proved more difficult to determine. In 52 PCHA origin variants, 73% showed a curved course towards the humeral head (n=38), and 27% could not be determined due to insufficient imaging (n=14). In 70 DBA origin variants, 69% showed a straight course parallel to the axillary artery (n=48), and 31% could not be determined due to insufficient imaging (n=22). An overview of PCHA and DBA characteristics is shown in Table 3. Table 3 Overview of PCHA and DBA vessel characteristics and diameters Origin Course PCHA Dorsal of the axillary artery, proximal of the DBA Curved towards the dorsal side of the humerus DBA Dorsal of the axillary artery, distal of the PCHA Straight and parallel to the axillary artery Presence in axillary pit Always present Commonly present (absent in 7% of cases) Intra-individual ratio >1.0 (PCHA dm* / DBA dm*) Average diameter (in millimetres) 3.8 (men) 3.5 (women) <1.0 (DBA dm* / PCHA dm*) 2.3 (men) 2.0 (women) 8 Average diameter (corrected for Body Surface Area in millimetres per square meter) 1.8 (men) 1.8 (women) 1.1 (men) 1.1 (women) Originating directly from the axillary artery 81% of cases 75% of cases *dm = diameter DISCUSSION The prevalence of proximal PCHA aneurysms in elite volleyball players is high and associated with a specific branching type, namely a PCHA that originates directly from the axillary artery. In contrast, no PCHA aneurysms were detected in anatomical variants such as a common trunk of the PCHA and DBA. The DBA was normal in all athletes and no DBA aneurysms were detected. The described vessel characteristics enable a distinction to be made between the PCHA and DBA, where the PCHA is larger and has a curved course dorsally towards the humeral head. The PCHA was present in the axillary pit in 100% of cases, arose from a common trunk in 19%, and showed a curved course dorsally towards the humeral head in 93% of Aneurysm prevalence and vessel characteristics of the PCHA I 139

143 cases. The average normal PCHA diameter was 3.8 mm for men, 3.5 mm for women and, corrected for BSA, 1.8 mm/m 2 for both. For the aneurysmal PCHA, these diameters were 5.9 mm for men and 5.1 for women. All aneurysms were detected in a PCHA that originated directly from the axillary artery. All DBAs showed a smooth calibre over the proximal course without any aneurysmal segments. The DBA was present in the axillary pit in 93% of cases, arose from a common trunk in 25%, and showed a straight course parallel to the axillary artery in 93% of cases. The average normal DBA diameter was 2.3 for men, 2.0 for women, and 1.1 mm/m 2 for both. The intra-individual PCHA-DBA diameter ratio was 1.0 in all participants. Worldwide elite overhead athletes, like volleyball players, are potentially at risk of ischemic digits due to arterial emboli originating from an aneurysmal and thrombosed PCHA in the dominant shoulder. Several studies report PCHA-specific injuries. 2,3,17,68,71,89,95,96,109,115,126 The incidence of PCHA aneurysms in this specific population is high, as shown by the current study. Identification of PCHA aneurysms at an early stage might prevent thromboembolic complications and irreversible tissue damage. 89 Potential therapeutic options include surgical ligation and endovascular coiling 3, while conservative treatment consists of cessation of sports activities. 88 However, identification and assessment of the PCHA is cumbersome in the hands of radiologists and vascular technologists due to anatomical variations and the very similar DBA originating nearby. The reported PCHA and DBA vessel characteristics enable easy and reliable PCHA and DBA identification and discrimination using US. This information facilitates accurate US assessment of the PCHA and DBA in both a clinical and screening setting. We expect the accuracy of the SPI-US protocol to improve when the diameters and arterial course are considered by radiologists and vascular technologists. Furthermore, we provide reference values for normal and aneurysmal PCHA diameters for male and female elite volleyball players. When corrected for BSA, the values for male and female volleyball players are comparable. Normal and aneurysmal PCHA and DBA diameters Normal values for arteries prone to aneurysm formation are commonly determined using US, and are currently used for diagnostic and therapeutic purposes. 83,132 Diameters of normal PCHA vessel segments were homogenous with a small standard deviation. However, the normal PCHA vessel segment diameter differed for males and females. When corrected for BSA, these diameters were comparable for male and female volleyball players. This implies that unisex PCHA reference values can be used when absolute diameters are corrected for BSA. Aneurysm characteristics Aneurysm characteristics such as the site (anatomic segment), morphologic features (e.g. shape and arterial wall complications) and clinicopathologic manifestation (e.g. 140 I Chapter 8

144 thrombotic occlusion and embolization) should be reported according to the suggested standards for reporting on aneurysms by Johnson et al. 50 Classification by anatomic segment is important since aneurysms located in different sites may be associated with variations in their natural history. 50 Ten aneurysms originated within 8 mm from the origin, while the remaining three were detected between 12 and 15 mm of the origin. We hypothesized these aneurysms to have a similar etiology, since the slightly more distal site of injury is presumably due to a more proximal PCHA origin in the axillary pit. A different etiology, for instance entrapment of the vessel in the quadrilateral space, is unlikely since the midsection of the PCHA is traversing the quadrilateral space, while the lesions were seen in the proximal part of the vessel. In this case, the axillary nerve accompanies the PCHA in the neurovascular bundle several cm distal to the origin and was not visualised. 95 Morphological features of all thirteen aneurysms comprised vessel wall irregularities and a fusiform shape. Also, four aneurysmal PCHAs showed a tortuous course, which might be correlated to increased symptoms as is seen in aneurysms of the popliteal artery. 32 Lastly, intravascular thrombus was detected in three aneurysms, a source of distal embolization, and thrombotic digital occlusion. 50,89 Larger aneurysms are more likely to contain thrombus 32, although this was not supported by our results. However, it is possible that intravascular thrombus was not visualised due to recent embolization during overhead movements 3,95, possibly resulting in false negatives during the US examination. 8 Anatomy, branching pattern and course of PCHA and DBA Thorough knowledge of the possible anatomical variations of the axillary artery and its tributaries is vital when assessing the PCHA and DBA. The prevalence of PCHA origin variations is up to 33-42% in the medical literature 43,80, and 19% in our study. Interestingly, in the current study all thirteen aneurysms were detected in PCHAs that originated directly from the axillary artery. This is consistent with the location of pathology seen in volleyball players who were diagnosed and treated in our academic hospital 3,89,95,96, as well as in other reports on PCHA aneurysms in the medical literature. 2,17,68,71,109,115,126 This implies that a PCHA originating directly from the axillary artery is a risk factor for the development of a PCHA aneurysms and thrombosis and that variant anatomy might be protective against aneurysm and thrombus formation. Among almost 350 examined PCHAs of healthy subjects no PCHA pathology was detected. 43,102,103 Since the PCHA curves towards the humeral head and the DBA proceeds straight and parallel to the axillary artery in most cases of both the normal branching types and anatomical variants, it is vital to objectify the PCHA curve in both the longitudinal and the transversal plane for positive PCHA identification. 93 Strengths, weaknesses and future studies A strength of the current study is that normal PCHA diameters were determined in a large group of elite volleyball players, the population at risk. 50 Another strength is the thorough Aneurysm prevalence and vessel characteristics of the PCHA I 141

145 process of data reviewing by multiple experts, since this process had contributed to an optimal classification of the collected data. A weakness of the current study is that in 7% of cases (n=20), the DBA was not identified in the axillary pit, which might be due to a more distal origin from the brachial artery, an anatomical variant with an absent DBA, or because it was overlooked by the vascular technologists. Therefore, the prevalence of DBA pathology remains uncertain in these athletes, although DBA abnormalities do not seem likely considering the available data in the current study. Future studies need to assess the clinical value of PCHA screening by US in this specific population to determine the relation between symptoms and PCHA aneurysms as detected by US, since most peripheral aneurysms are known to be asymptomatic. 42 In conclusion, the prevalence of PCHA aneurysms in elite volleyball players is high and associated with a specific branching type, namely a PCHA that originates directly from the axillary artery. Radiologists should have high index of suspicion for this vascular overuse injury among elite volleyball players. The described PCHA and DBA vessel characteristics provide clear guidance to identify and assess the PCHA and DBA. Only the PCHA needs to be screened for aneurysms, which can be easily detected using ultrasound. The high prevalence of detected PCHA aneurysms demands an active policy on prevention and periodic surveillance that is easily performed using the provided PCHA and DBA characteristics. This study is the first to provide radiologists and vascular technologists with insights into how ultrasonography can be used for surveillance of a vascular overuse injury which is prevalent in elite overhead athletes, like volleyball players. 142 I Chapter 8

146

147

148 PART III Clinical management

149

150 CHAPTER 9 The international SPIKE study on Posterior Circumflex Humeral Artery pathology among elite volleyball players: four profiles for clinical management (4P4M) Daan van de Pol P. Paul F.M. Kuijer Aart Terpstra Marja J.C. Pannekoek-Hekman Sena Alaeikhanehshir Olivier Bouwmeester R. Nils Planken Mario Maas Submitted

151

152 ABSTRACT Background: Elite volleyball players are at risk of ischemic digits due to arterial emboli originating from an aneurysmal and thrombosed posterior circumflex humeral artery (PCHA) in the dominant shoulder. The prevalence of PCHA pathology (PCHAP), and associated symptoms and risk factors, is unknown. This hampers clinical management. Purpose: To provide individual risk profiles for clinical management of PCHAP based on prevalence, symptoms and associated risk factors in elite volleyball players. Study Design: Cross-sectional study Methods: From January through July 2014, ultrasound (US) assessment of the PCHA in the dominant shoulder was performed, and evaluated by two experienced vascular technologists and a vascular radiologist. PCHAP was defined as local vessel dilatation, aneurysm, and occlusion. A questionnaire (Q) survey assessed the presence of symptoms of digital ischemia (DI) in the dominant hand and possible risk factors. Binary logistic regression was performed to calculate Odds Ratios (OR) including 90% confidence intervals (90%CI). Results: Two-hundred-seventy-eight elite indoor and beach volleyball players participated. PCHAP was detected in 17 participants (6.1%): three dilatations (1.1%), 13 aneurysms (4.7%), of which three contained intravascular thrombus, and one occlusion (0.4%). Three participants with PCHAP (two aneurysms and one occlusion) were symptomatic (18%) and 14 were not (82%). In total, 96 of 278 participants (35%) reported symptoms, of whom 93 had no PCHAP (OR=0.39; 95%CI ). A total volleyball career duration of 17 years or more and an age of 27 years or more were associated with a 9-fold (90%CI ) and 14-fold (90%CI ) increased risk of PCHAP, respectively. A dose-response relationship seemed present for both risk factors. The distribution across the four risk profiles, based on the presence of PCHAP (US+ or US ) and symptoms of DI (Q+ or Q ), was: I) 1.1% US+Q+ (n=3); II) 5.0% US+Q (n=14); III) 33.5% US Q+ (n=93); and IV) 60.4% US Q (n=168). 9 Conclusion: Four risk profiles (US+Q+, US+Q, US Q+, US Q ) were recognized among elite volleyball players based on the combination of presence of US-detected PCHAP, with a 6.1% prevalence, and reporting of symptoms of DI. For each profile, recommendations for clinical management are proposed to optimize care for this potentially limbthreatening injury. Four profiles for clinical management of PCHA pathology I 149

153 INTRODUCTION Elite overhead athletes are at risk of vascular overuse injuries in the dominant shoulder due to repetitive abduction and external rotation of the arm. 2,27,73,97 Aneurysmal degeneration, thrombosis and distal occlusion of the proximal posterior circumflex humeral artery (PCHA) is a rare sport-related overuse injury mostly found among elite volleyball players 2,3,17,33,47,64,68,89,95,96,115,126,127, and elite baseball pitchers. 2,12,27,53,55,66,79,108 Thrombosis might lead to distal embolization to the circulation of the forearm, hand, and digits in the ipsilateral limb during the spiking or serving motion in volleyball, when the humeral head acts to compress the aneurysmal PCHA and the intraluminal thrombus like a tube of toothpaste, causing retrograde embolism into the nearby axillary artery. 3,49,89 However, the prevalence of PCHA pathology and related thromboembolic complications is unknown. Cold and discoloured digits were reported by 89% percent of volleyball players with confirmed digital ischemia (DI) caused by emboli due to pathological changes of the PCHA in the ipsilateral shoulder. 89 Among surveyed elite indoor and beach volleyball players, these symptoms were prevalent in respectively 31% and 38%, with the duration of the volleyball career, the intensity of performing strength-increasing weight training, and female sex identified as associated risk factors These data, although self-reported and cross-sectionally collected, are indicative of underlying PCHA pathology. Since these volleyball players are considered potentially at risk for developing critical DI, further analysis of the presence of PCHA pathology, and associated risk factors, is warranted for prevention. Ultimately, establishing risk profiles of individual athletes based on the results would support clinical management. For this purpose, the Shoulder PCHA pathology and digital Ischemia in Known Elite volleyball players (SPIKE) study was conducted. The aim of this study was: (1) to assess the prevalence of PCHA pathology in the dominant shoulder among elite volleyball players; (2) to determine its association with self-reported symptoms of DI; and (3) to assess possible personal- and sports-related risk factors, including dose-response relationship, in order to establish risk profiles of individual athletes and to provide clinical management recommendations. MATERIALS AND METHODS Study design A cross-sectional ultrasound (US) and questionnaire (Q) survey study was performed among elite male and female indoor and beach volleyball players active at national and international top level from January through July Official approval was granted by 150 I Chapter 9

154 the Institutional Review Board at our academic hospital and permission was obtained from the Institutional Review Board at the Fédération Internationale de Volleyball (FIVB). Participants Volleyball players were recruited in cooperation with the FIVB and the Dutch Volleyball Association (Nevobo). Those eligible for inclusion were all elite male indoor volleyball players active in the Dutch national top league, second league or Dutch national volleyball team in the season, and all elite beach volleyball players active at the 2014 The Hague Beach Volleyball Grand Slam Tournament. Volleyball players were not considered eligible for inclusion in the case of a positive history for vascular surgery of the dominant shoulder, use of cardiovascular medication, or lack of written informed consent. Study protocol All volleyball players, coaches, and medical staff were informed about the study via and via Indoor volleyball players teams were visited and examined on-site during a practice session, and beach volleyball players were visited and examined on-site during the main tournament. Prior to the US examination of the proximal PCHA, participants gave written informed consent and completed a questionnaire. Ultrasound assessment The prevalence of PCHA pathology was assessed using US, the preferred initial imaging modality since it is easily available, cheap, non-invasive, fast and not associated with radiation exposure. All US examinations were performed by one of two registered vascular technologists (RVTs), using a Dynamic LOGIQ e (General Electric Company 2006) scanner equipped with a 12L-RS linear array transducer probe (5-13 MHz), following the standardized SPI-US protocol. 87,93 Both RVTs had more than 20 years experience with vascular US, had studied the anatomy of the branching pattern of the AA and its anatomical variations intensively, and were experienced in conducting the US protocol that was used. 9 Volleyball players were screened for the presence of PCHA pathology, namely aneurysms, dilatations, and occlusions. Aneurysms were defined as a segmental vessel diameter increase 1.5. Segmental vessel diameter increase between 1 and 1.5 was defined as dilatation. Arterial diameters were measured on cross-sectional grayscale B-mode images perpendicular to the vessel centerline. In the event of PCHA dilatation, the maximum diameter of the PCHA was measured. In addition, the diameter of the closest normally appearing PCHA vessel segment proximal, or otherwise distal, to the dilated vessel segment was measured. The presence of intravascular thrombus and/or vessel occlusion was identified and recorded. In the event of intravascular thrombus, colour Doppler was used to confirm the presence of thrombus in no flow regions. Waveform characteristics were obtained to visualize a triphasic or blunted signal. Four profiles for clinical management of PCHA pathology I 151

155 In a later phase, the obtained US data were independently reviewed by both RVTs and classified as normal, doubtful or pathological. In the case of divergent conclusions, both RVTs discussed these data in order to reach consensus. Finally, US images of all pathological and doubtful cases were reviewed, discussed and definitively classified as normal or pathological during consensus meetings in which both RVTs and a vascular radiologist participated. Symptoms and risk factors The SPI-Q (Shoulder PCHA pathology and digital Ischemia Questionnaire) was used; a standardized questionnaire which enables targeted detection of symptoms of DI in elite male volleyball players with good intrarater agreement. 94 The SPI-Q questionnaire was developed using reports of volleyball players with confirmed DI, based on evidence from the medical literature, and comprises four general domains: A) those regarding specific symptoms of DI, such as cold, blue or pale digits during practice or competition; B) those regarding demographics and personal risk factors, such as age, sex, and cardiovascular disease in first-degree family members; and C) those regarding sports-related risk factors, such as the total duration of the volleyball career, position in the field, and the intensity of performing strength-increasing weight training. Data analyses For discrete variables, the mean, standard deviation, minimum, and maximum were reported. Percentages were reported for categorical variables. The prevalence of symptoms was calculated in the following manner: the percentage of all volleyball players who sometimes or more often reported having cold or blue or pale digits in the dominant hand during or directly after practice or competition. The presence of aneurysms, intravascular thrombus, dilatations, and occlusions were reported for the group as a whole. Subsequently, two groups were formed: 1. Volleyball players who showed PCHA pathology on US examination (US+ group) were divided into three subgroups: a. PCHA aneurysm, with and without intravascular thrombus b. PCHA occlusion c. PCHA dilatation (a pre-pathological stage and therefore classified as pathology) 2. Volleyball players who did not show PCHA pathology on US examination (US group) The association between detected PCHA pathology and reported symptoms and risk factors was expressed as an odds ratio (OR) including 90% confidence intervals (90%CI) using a univariate binary logistic regression. This was done for the following: A) symptoms of DI; B) personal risk factors; and C) sports-related risk factors. In all tests, a p-value 0.10 was considered significant to overcome missing potential clinically relevant differences. Subsequently, the collinearity between the univariate variables with a p-value 0.10 was 152 I Chapter 9

156 calculated. Next, for all non-collinear variables with a p-value <0.10, an OR including 90%CI was calculated using a multivariate binary logistic regression. In addition, to assess a potential dose-response relationship between PCHA pathology and symptoms and risk factors with a p-value <0.10, three groups of almost equal size were formed, and the association was expressed as an OR including 90%CI, again using a univariate binary logistic regression subcategory analysis. Finally, risk profiles were formed based on the combination of the presence of pathology, symptoms and risk factors. RESULTS Participants From January 2014 through July 2014, a total of 281 elite volleyball players were assessed. Three players were excluded from the study: two due to clinically confirmed Raynaud s phenomenon and one due to a history of PCHA surgery in the dominant shoulder. As a result, 278 elite volleyball players were included: 243 men and 35 women. This group consisted of 217 male elite indoor volleyball players from two countries (78%), and 61 elite beach volleyball players from 19 countries (22%): 35 women (57%) and 26 men (43%). On average, volleyball players were 25±5 years old (range: years), had a body height of 193±8 centimeters (cm) (range: cm), and had been playing volleyball for 15±5 years (range 4-31 years) and 12±6 hours a week (range 3-30 hours). For a complete overview of the characteristics of the participants we refer to Appendix A. PCHA pathology PCHA pathology was detected in 17 volleyball players (6.1%) (US+ group). No PCHA pathology was found in the remaining 261 volleyball players (US group). On average, volleyball players in the US+ group were 29±4 years old, and played volleyball for 18±4 years, while volleyball players in the US group were on average 25±5 years old, and played volleyball for 14±5 years. In the US+ group, 12% (n=2) reported the presence of cardiovascular disease in first-degree family and 30% (n=5) reported that they smoked or had smoked in the past, while in the US group these numbers were respectively 12% (n=30) and 23% (n=60) (Appendix A). 9 In total, 13 PCHA aneurysms were found (Figure 1), of which three contained intravascular thrombus. Ten of these aneurysms, including the three with intravascular thrombus, involved male indoor volleyball players (77%), two were found in female beach volleyball players (15%), and one in a male beach volleyball player (8%). As a result, the prevalence of PCHA aneurysms in females was 5.7% (2/35), and in males 4.5% (11/243). In one case, which involved a male beach volleyball player, the PCHA could not be visualized more than one centimeter from the origin and a blunted waveform was found, which is correlated with a more distal occlusion. Lastly, three PCHA dilatations were detected in Four profiles for clinical management of PCHA pathology I 153

157 Figure 1 Longitudinal B-mode ultrasound image of the aneurysmal proximal PCHA in a 31-year old professional volleyball player Key: AA, axillary artery; PCHA, posterior circumflex humeral artery three male indoor volleyball players, none of which contained intravascular thrombus (Table 1). All volleyball players were informed and advised about follow-up. Symptoms associated with PCHA pathology In total, 96 volleyball players (35%) reported symptoms of cold or blue or pale digits in the dominant hand during or directly after practice or competition sometimes or more often in the questionnaire (Q+ group), whereas 182 volleyball players did not (Q group) (65%). Three of 17 US+ volleyball players (two aneurysms and one occlusion) reported symptoms of DI, a prevalence of 18% in the US+ group (3/17), and a prevalence of 2% in the Q+ group (3/96). Fourteen US+ volleyball players did not report symptoms, a prevalence of 82% in the US+ group (14/17), and a prevalence of 8% in the Q group (14/182). No significant association between PCHA pathology and symptoms of DI between the two groups was revealed (OR=0.39; 90%CI ) (Table 2). Risk factors associated with PCHA pathology Personal risk factors The univariate binary logistic regression revealed a significant association for the personal risk factor age (OR=1.17; 90%CI ). For the other personal risk factors, the univariate binary logistic regression revealed no significant associations like cardiovascular disease in first-degree family (OR=1.00; 90%CI ) or smoking (OR=1.37; 90%CI ) (Table 2). Sports-related risk factors The univariate binary logistic regression revealed significant associations for the sportsrelated risk factor: total years playing volleyball (OR=1.14; 90%CI ). For the 154 I Chapter 9

158 Table 1 Type and prevalence of PCHA pathology (US+) in elite male and female beach and indoor volleyball players Percentage in US+ group (n=17) Percentage in total group (n=278) Total (n=17) 100% 6.1% Dilatation (n=3) 17.7% 1.1% Aneurysm (n=13) without intravascular thrombus (n=10) with intravascular thrombus (n=3) 76.5% 58.8% 17.6% 4.6% 3.5% 1.1% Occlusion (n=1) 5.8% 0.4% Key: US+, volleyball players with PCHA pathology on ultrasound examination Table 2 Univariate binary logistic regression outcomes (odds ratio and 90% confidence interval) of symptoms of digital ischemia and risk factors for PCHA pathology in elite male and female beach and indoor volleyball players Domain A: Symptoms of digital ischemia US+ versus US group Cold digits during volleyball (sometimes/often/always) OR 0.55 (90% CI ) Cold digits after volleyball (sometimes/often/always) OR 0.95 (90% CI ) Blue digits during volleyball (sometimes/often/always) OR 1.45 (90% CI ) 9 Blue digits after volleyball (sometimes/often/always) OR 1.19 (90% CI ) Pale digits during volleyball (sometimes/often/always) OR 1.03 (90% CI ) Pale digits after volleyball (sometimes/often/always) OR 0.39 (90% CI ) Symptomatic (one of the symptoms cold or blue or pale during or after volleyball) OR 0.39 (90% CI ) Domain B: Personal risk factors Age OR 1.17 (90% CI ) Height OR 0.96 (90% CI ) Weight OR 0.98 (90% CI ) Sex (male) OR 1.09 (90% CI ) Raynaud s Phenomenon in first-degree family (yes) OR 0.00 (90% CI 0.00 ) * Cardiovascular disease in first-degree family (yes) OR 1.00 (90% CI ) Smoking (yes) OR 1.37 (90% CI ) Four profiles for clinical management of PCHA pathology I 155

159 US+ versus US group Domain C: Sports-related risk factors Type of volleyball (beach volleyball) OR 1.10 (90% CI ) Total years playing volleyball OR 1.14 (90% CI ) Total years playing professional volleyball OR 1.03 (90% CI ) Total practice and competition hours in a week OR 0.95 (90% CI ) Position in the field (indoor attacker i.e. opposites & outside hitters) OR 0.98 (90% CI ) Position in the field (indoor blocker i.e. middle blockers) OR 1.74 (90% CI ) Smashing/spiking frequency (regularly/often) OR 2.00 (90% CI ) Smashing/spiking away from the shoulder (often/always) OR 1.94 (90% CI ) Performing dominant limb weight training in general (yes) OR 0.57 (90% CI ) Frequency of performing weight training to increase dominant limb strength (often/always) Number of minutes per week performing weight training to increase dominant limb strength Frequency of performing weight training to maintain dominant limb strength (often/always) Number of minutes per week performing weight training to maintain dominant limb strength OR 0.69 (90% CI ) OR 0.76 (90% CI ) OR 1.48 (90% CI ) OR 1.11 (90% CI ) * = no odds ratio (OR) could be calculated as none of the US+ group reported being exposed to this risk factor. Key: US+, volleyball players with PCHA pathology on ultrasound examination; US, volleyball players without PCHA pathology on ultrasound examination other sports-related risk factors, the univariate binary logistic regression revealed no significant associations like position in the field (attacker) (OR=0.98; 90%CI ) or smashing/spiking frequency (OR=2.00; 90%CI ) (Table 2). Dose-response relationship Although no collinearity between age and total years playing volleyball was found (VIF = 2.396, tolerance = 0.417), no multivariate regression analysis was performed due to a strong correlation between both (0.74). For both risk factors, a dose-response relationship seemed present. For age, the OR increased by 3.07 (23-26 years) to (27-41 years) 156 I Chapter 9

160 compared with the reference group of years. For total years volleyball, the OR increased from 5.65 (12-16 years) to 9.21 (17-31 years) compared with the reference group of 4-11 years (Table 3). Risk profiles for clinical management Volleyball players were categorized into four risk profiles based on the combination of the presence of PCHA pathology (US+ or US ) and symptoms of DI (Q+ or Q ). The distribution across the four risk profiles was: I) 1.1% US+Q+ (n=3); II) 5.0% US+Q (n=14); III) 33.5% US Q+ (n=93); and IV) 60.4% US Q (n=168) (Table 4). Table 3 Categorical univariate binary logistic regression outcomes (odds ratio and 90% confidence interval) of age and total years playing volleyball US+ versus US group Age OR 1.17 (90% CI ) years (n=90) Reference years (n=90) OR 3.07 (90% CI ) years (n=98) OR (90% CI ) Total years playing volleyball OR 1.14 (90% CI ) 4-11 years (n=82) Reference years (n=92) OR 5.65 (90% CI ) years (n=98) OR 9.21 (90% CI ) Key: US+, volleyball players with PCHA pathology on ultrasound examination; US, volleyball players without PCHA pathology on ultrasound examination Table 4 Four risk profiles for elite volleyball players based on the combination of the presence of PCHA pathology (US+ or US ) and symptoms of digital ischemia (Q+ or Q ): symptomatic PCHA pathology (US+Q+), asymptomatic PCHA pathology (US+Q ), symptomatic without PCHA pathology (US Q+), and asymptomatic without PCHA pathology (US Q ) US + US Total Q+ 1.1% (n=3) 33.5% (n=93) 34.6% (n=96) Q 5.0% (n=14) 60.4% (n=168) 65.4% (n=182) Total 6.1% (n=17) 93.9% (n=261) 100% (n=278) Four profiles for clinical management of PCHA pathology I 157

161 DISCUSSION Among 278 elite indoor and beach volleyball players, 6.1% showed PCHA pathology in the dominant shoulder on US examination. The high rate of this sports-related vascular overuse injury among healthy elite athletes in the prime of their career is alarming since it implies that worldwide elite volleyball players are at risk of PCHA pathology. Volleyball players with confirmed DI caused by emboli due to pathological changes of PCHA in the ipsilateral shoulder are known to present themselves at a later stage of the condition. Therefore, active surveillance to detect and monitor PCHA pathology at an early stage seems warranted as this might prevent thromboembolic complications, irreversible tissue damage, and surgical ligation of the PCHA. 89 We describe four risk profiles among elite volleyball players based on the combination of the presence of US-detected PCHA pathology (US+ or US ) and reporting of symptoms of DI (Q+ or Q ): I) symptomatic PCHA pathology (US+Q+); II) asymptomatic PCHA pathology (US+Q ); III) symptomatic without PCHA pathology (US Q+); and IV) asymptomatic without PCHA pathology (US Q ). This continuum of risk profiles likely progresses from IV to I, with the total duration of the volleyball career as the main sports-related risk factor. For each profile, clinical management recommendations are proposed for this potentially limb-threatening injury. Symptomatic PCHA pathology (US+Q+) This group of volleyball players is at risk of irreversible tissue damage as a result of prolonged DI, which may ultimately lead to necrosis and finger loss. Therefore, these athletes should be referred to a vascular surgeon for comprehensive assessment of the entire upper extremity vascular tree to detect symptomatic emboli, and to discuss treatment options. Asymptomatic PCHA pathology (US+Q ) Annual SPI-US monitoring seems appropriate in this group of volleyball players given the risk of aneurysm expansion and thrombosis. 42,50 Thrombosis might lead to distal embolization to the circulation of the forearm, hand, and digits after overhead movements in volleyball, resulting in transient cold and discoloured digits. 93 Since these symptoms might initially seem innocuous to the athlete, it is advisable to use the SPI-Q twice a year to create awareness and to detect the onset of symptoms of DI, in which case pulse deficits, pallor, or differences in temperature should be assessed 27, and the team physician should consult with a vascular surgeon about follow-up. Because symptoms of DI might mostly occur during practice or competition, surveillance might be most relevant after periods with increased physical activity, such as a few weeks after the start of the training season and a few weeks after the winter recess. Athletes might be more vulnerable in these periods I Chapter 9

162 Symptomatic without PCHA pathology (US Q+) The unilateral ischemia-related symptoms in these volleyball players might be caused by repeated microtrauma of the hand by vigorous ball contact, as occurs during volleyball 96, or a wide variety of vascular pathologies including arterial thoracic outlet syndrome 97, aneurysms of the axillary artery or its branches 49, quadrilateral space syndrome 97, forearm vessel aneurysms 57, hypothenar hammer syndrome 65, digital arterial pathology 19,46, and vasomotor disorders such as Raynaud s phenomenon 14,129, and traumatic vasospasm of the digital arteries. 57 Nevertheless, it is advisable to remain vigilant for PCHA pathology in these volleyball players, given the increased risk as the volleyball career progresses. Embolization from an injured PCHA to the end arteries in the hand and digits typically presents with coldness and discoloration, 89 and may also include disabling numbness, pain, and occasional fingertip ulcerations. 27,89 Cold temperature hypersensitivity is also a common symptom and can be misinterpreted as vasospasm in the presence of normal radial and ulnar pulses. 27 To grade the severity, and to increase awareness for subtle aggravation, yearly monitoring of symptoms of DI using the SPI-Q seems appropriate, and might be most relevant in periods with increased physical activity. Team physicians need to have a high index of suspicion when symptoms arise acutely or when they are associated with pulse deficits, pallor, or differences in temperature. 27 If so, a vascular surgeon should be consulted about follow-up, which could include brachial and finger pressure measurement, digital photoplethysmography, a chest X-ray, and vascular US of the PCHA using the SPI-US protocol. 3,27,93 Asymptomatic without PCHA pathology (US Q ) Since these volleyball players become at risk for PCHA pathology when symptoms of DI arise, using the SPI-Q every two years to detect the onset of these symptoms seems appropriate, with the added benefit that volleyball players might become more aware of these seemingly innocuous symptoms. 89 We suggest implementing this surveillance in routine yearly medical examinations, or otherwise performing this 2-minute questionnaire survey yearly at the start of the season. 9 Prevalence of PCHA pathology and risk factors in sports This study objectifies the prevalence of PCHA pathology, and is the first to identify dose-response related risk factors in the population at risk: a large cohort of elite volleyball players active at national and international top level. In 1993, Reekers et al. 95 was the first to report three cases of elite volleyball players with ischemic digits due to arterial emboli originating from a thrombosed aneurysm in the PCHA in the dominant shoulder, and to suggest a causal relationship with volleyball. Since then, the majority of cases of PCHA pathology with distal emboli have been reported in elite volleyball players 2,3,17,33,47,64,68,89,95,96,115,126,127. Also, multiple cases have been reported in elite baseball pitchers 2,12,27,53,55,66,79,108, tennis players 47,61,64, swimmers 26, kayakers 109, yoga practitioners 101, trapeze flying artists 96, and American football players. 61 The Four profiles for clinical management of PCHA pathology I 159

163 assumption is that the common denominator in these sports repetitive vigorous overhead movements such as spiking and serving in volleyball causes chronic vessel wall injury as a result of positional traction and compression of the proximal PCHA. 3,17,95 This cumulative trauma can lead to a continuum of PCHA pathology ranging from intimal lesions to vessel dilatation of <150% (found in three cases), aneurysmal degeneration with vessel dilatation >150% (found in 13 cases), intra-aneurysmal thrombus formation (found in three cases), and occlusion (found in one case). 3,27,95,126 No PCHA pathology was detected in some 350 examined PCHAs of healthy subjects. 43,102,103 Cumulative PCHA trauma is illustrated by the two identified dose-response related risk factors from this study; age and total volleyball career duration. Age is known to be a risk factor for overuse injuries of the shoulder in male and female volleyball players. 99,110 Interestingly, total volleyball career duration was also associated with self-reported symptoms of DI in the dominant hand in two separate studies among elite indoor and beach volleyball players. 88,90 The fact that this risk factor is a common denominator in these two studies and the current study indicates a causal relation between DI and PCHA aneurysms. Strengths and weaknesses A strength of the current study is that PCHA pathology was determined in a large group of elite volleyball players, the population at risk, with the use of standardized diagnostic modalities. Therefore, the found prevalence of PCHA pathology seems a reliable first estimate for elite volleyball players. However, since the current study has shown the prevalence of PCHA pathology to be higher among asymptomatic volleyball players, the actual prevalence among beach volleyball players might have been even higher had the other half of the tournament s competitors participated. Another strength is the thorough process of data reviewing by multiple experts, since this process contributed to an optimal classification of the collected data. A possible weakness of the current study is that only the PCHA in the dominant shoulder has been assessed for pathology, while unilateral ischemia-related symptoms in the upper extremity can be explained by a wide variety of vascular pathologies, which was not assessed for. We deliberately chose targeted PCHA assessment since volleyball players are known to be at risk specifically for PCHA pathology. Future studies should assess the added value of suggested clinical management recommendations in order to prevent onset and worsening of PCHA pathology. In addition, although symptoms do not seem to be related to PCHA pathology in this crosssectional study, future studies should prospectively assess the reporting of symptoms of DI at regular intervals 6,122 to reveal a possible association with PCHA pathology. Moreover, 160 I Chapter 9

164 since no cause was found for the ischemia-related symptoms in the majority of volleyball players in this study, future studies should assess other possible (vascular) pathologies, as well as elaborate on clinical management. In conclusion, the prevalence of PCHA pathology in the dominant shoulder is high (6.1%) among indoor and beach volleyball players active at national and international top level. We describe four risk profiles among elite volleyball players based on the combination of the presence of US-detected PCHA pathology and reporting of symptoms of DI. For each profile, recommendations for clinical management are proposed to optimize care for this potentially limb-threatening injury. 9 Four profiles for clinical management of PCHA pathology I 161

165 APPENDIX A - CHARACTERISTICS OF THE PARTICIPANTS Domain A: Symptoms of digital ischemia PCHA pathology (US+ group) (n=17) No PCHA pathology (US group) (n=261) Total (n=278) Cold digits during volleyball (sometimes/often/always: +, never: -) +: 3/17 (18%) -: 14/17 (82%) +: 73/261 (28%) -: 188/261 (72%) +: 76/278 (27%) -: 202/278 (73%) Cold digits after volleyball (sometimes/often/always: +, never: -) +: 2/17 (12%) -: 15/17 (88%) +: 32/261 (12%) -: 229/261 (88%) +: 34/278 (12%) -: 244/278 (88%) Blue digits during volleyball (sometimes/often/always: +, never: -) +: 2/17 (12%) -: 15/17 (88%) +: 22/261 (8%) -: 239/261 (92%) +: 24/278 (9%) -: 254/278 (91%) Blue digits after volleyball (sometimes/often/always: +, never: -) +: 1/17 (6%) -: 16/17 (94%) +: 13/261 (5%) -: 248/261 (95%) +: 14/278 (5%) -: 264/278 (95%) Pale digits during volleyball (sometimes/often/always: +, never: -) +: 1/17 (6%) -: 16/17 (94%) +: 15/261 (94%) -: 246/261 (6%) +: 16/278 (6%) -: 262/278 (94%) Pale digits after volleyball (sometimes/often/always: +, never: -) +: 1/17 (6%) -: 16/17 (94%) +: 36/261 (14%) -: 225/261 (86%) +: 37/278 (13%) -: 241/278 (87%) Symptomatic (one of the symptoms cold or blue or pale during or after volleyball: +, none: -) +: 3/17 (18%) -: 14/17 (82%) +: 93/261 (36%) -: 168/261 (64%) +: 96/278 (35%) -: 182/278 (65%) Domain B: Personal risk factors Age (years) Mean: 29 SD: 4 Range: Mean: 25 SD: 5 Range: Mean: 25 SD: 5 Range: Body height (centimeters) Mean: 190 SD: 10 Range: Mean: 193 SD: 8 Range: Mean: 193 SD: 8 Range: Body weight (kilograms) Mean: 83 SD: 10 Range: Mean: 85 SD: 10 Range: Mean: 85 SD: 10 Range: I Chapter 9

166 PCHA pathology (US+ group) (n=17) No PCHA pathology (US group) (n=261) Total (n=278) Sex (male:, female: ) : 15/17 (88%) : 2/17 (12%) : 228/261 (87%) : 33/261 (13%) : 243/278 (87%) : 35/278 (13%) Raynaud s Phenomenon in firstdegree family (yes: +, no: -) +: 0/17 (0%) -: 17/17 (100%) +: 6/257 (2%) -: 251/257 (98%) +: 6/274 (2%) -: 268/274 (98%) Cardiovascular disease in firstdegree family members (yes: +, no: -) +: 2/17 (12%) -: 15/17 (88%) +: 30/255 (12%) -: 225/255 (88%) +: 32/272 (12%) -: 240/272 (88%) Smoking (currently or in the past) (yes: +, no: -) +: 5/17 (30%) -: 12/17 (80%) +: 60/257 (23%) -: 197/257 (77%) +: 65/274 (24%) -: 209/274 (76%) Domain C: Sports-related risk factors Type of volleyball (beach volleyball: +, indoor volleyball: -) +: 4/17 (77%) -: 13/17 (23%) +: 57/261 (%) -: 204/261 (%) +: 61/278 (22%) -: 217/278 (78%) Total years playing volleyball (years) Mean: 18 SD: 4 Range: Mean: 14 SD: 5 Range: 4-31 Mean: 15 SD: 5 Range: Total years playing professional volleyball (years) Mean: 3 SD: 4 Range: 0-12 Mean: 3 SD: 4 Range: 0-20 Mean: 3 SD: 4 Range: 0-20 Total practice and competition hours in a week (hours) Mean: 11 SD: 7 Range: 3-30 Mean: 12 SD: 6 Range: 3-30 Mean: 12 SD: 6 Range: 3-30 Position in the field (indoor volleyball) (attacker i.e. opposites & outside hitters: +, other: -) +: 6/13 (46%) -: 7/13 (54%) +: 95/204 (53%) -: 109/204 (47%) +: 101/217 (46%) -: 116/217 (54%) Position in the field (indoor volleyball) (blocker i.e. middle blockers: +, other: -) +: 5/13 (38%) -: 8/13 (62%) +: 54/204 (26%) -: 150/204 (74%) +: 59/217 (27%) -: 158/217 (73%) Smashing/spiking frequency (regularly/often: +, never/ sometimes: -) +: 15/17 (88%) -: 2/17 (12%) +: 202/256 (79%) -: 54/256 (21%) +: 217/273 (80%) -: 56/273 (20%) Four profiles for clinical management of PCHA pathology I 163

167 PCHA pathology (US+ group) (n=17) No PCHA pathology (US group) (n=261) Total (n=278) Smashing/spiking away from the shoulder (often/always: +, never/ sometimes: -) +: 11/17 (65%) -: 6/17 (35%) +: 124/255 (49%) -: 131/255 (51%) +: 135/272 (50%) -: 137/272 (50%) Performing dominant limb weight training in general (yes: +, no: -) +: 12/17 (71%) -: 5/17 (29%) +: 207/256 (81%) -: 49/256 (19%) +: 219/273 (80%) -: 54/273 (20%) Frequency of performing weight training to increase dominant limb strength (often/always: +, never/ sometimes: -) +: 6/17 (35%) -: 11/17 (65%) +: 113/256 (44%) -: 143/256 (56%) +: 119/273 (44%) -: 154/273 (56%) Number of minutes per week performing weight training to increase dominant limb strength Mean: 32 SD: 39 Range: Mean: 40 SD: 49 Range: Mean: SD: 48 Range: 40 Frequency of performing weight training to maintain dominant limb strength (often/always: +, never/ sometimes: -) +: 11/17 (65%) -: 6/17 (35%) +: 141/255 (55%) -: 114/255 (44%) +: 152/272 (56%) -: 120/272 (44%) Number of minutes per week performing weight training to maintain dominant limb strength Mean: 44 SD: 46 Range: Mean: 40 SD: 44 Range: Mean: 40 SD: 44 Range: Key: US+, volleyball players with PCHA pathology on ultrasound examination; US, volleyball players without PCHA pathology on ultrasound examination 164 I Chapter 9

168

169

170 CHAPTER 10 Conservative management of a vascular shoulder overuse injury in a professional volleyball player: use of novel MR Angiography in diagnosis and treatment follow-up Daan van de Pol* R. Nils Planken* P. Paul F.M. Kuijer Aart Terpstra Marja J.C. Pannekoek-Hekman Mario Maas * DP and RP equally contributed to this study Submitted

171

172 ABSTRACT We report on a 34-year-old elite male elite volleyball player with symptomatic emboli in the spiking hand from a partially thrombosed aneurysm of the posterior circumflex humeral artery (PCHA) in his dominant shoulder. At initial diagnosis and follow-up, a combination of time-resolved and high-resolution steady state Contrast-Enhanced Magnetic Resonance Angiography (CE-MRA) enabled detailed visualization of: (1) emboli that were not detectable by vascular ultrasound; and (2) the PCHA aneurysm, including compression during abduction and external rotation (ABER provocation). At 15-month follow-up, including forced cessation of volleyball activities over the preceding nine months, the PCHA aneurysm remained unchanged. Central filling defects in the palmar arch and digital arteries resolved over time and affected arterial vessel segments showed post-thrombotic changes. Digital blood pressure values improved substantially and almost normalized during follow-up. In conclusion, this case report is the first to show promising results of conservative management for a vascular shoulder overuse injury in a professional volleyball player as an alternative to more invasive clinical modalities. 10 Conservative management for a PCHA aneurysm I 169

173 INTRODUCTION We present a case of a 34-year-old elite volleyball player with symptomatic emboli in the spiking hand and a partially thrombosed aneurysm of the posterior circumflex humeral artery (PCHA) in his dominant shoulder, who was selected in the context of an on-site ultrasound surveillance study. 91 He was advised about follow-up and referred to our tertiary medical center for state-of-the-art non-invasive and invasive vascular imaging. Fifteen months later, he was re-evaluated. CASE REPORT Initial presentation At the end of the national volleyball play-offs, the 34-year-old right-hand-dominant male volleyball player was referred to a vascular surgeon at our medical center. He reported a two-year history of ischemic symptoms of his spiking hand, e.g. cold, pale and painful digits, which initiated in the second and third digits and had recently expanded to the fourth and fifth digits. Since the start of the play-off season, with increased match frequency (up to three a week), he continuously experienced cold, discoloration and numbness. The athlete is a middle blocker, has played volleyball for 28 years at semiprofessional level, and for 10 hours a week. He has a part-time office job, is a nonsmoker with no medical history and no medication use, and reports no cardiovascular disease in first-degree family. Physical examination confirmed cold and discoloured digits and abnormal capillary refill (digit II, III, IV, and V). Subungual petechiae were present in the fourth digit. The Allen s test was positive, and radial artery and ulnar artery pulsations were normal. No clinical abnormalities were present in the left hand. Stateof-the-art vascular ultrasound examination using the standardized and accurate SPI- US protocol 87,93 revealed a partially thrombosed proximal PCHA aneurysm in his right/ spiking shoulder (Figure 1). The palmar arch and digital arteries could not be depicted during ultrasound assessment, and therefore neither the presence nor the absence of digital emboli could be demonstrated. Non-invasive digital arterial blood pressure evaluation revealed abnormal pressure values at the level of the proximal phalanx (digit I-V: 159, 144, 149, 159, 0 mmhg) and middle phalanx (digits II-IV: 85, 97, 81 mmhg), and photoplethysmographic curves were non-triphasic in digits II-V of the right hand, both indicative of inadequate perfusion of digits II to V (Figure 2 left panel). To assess the presence of digital emboli, a combined MR protocol consisting of time-resolved and high-resolution steady state Contrast-Enhanced Magnetic Resonance Angiography (CE-MRA) was performed. Filling defects and multiple emboli were detected in the distal radial artery, palmar arch, common palmar artery, and digital arteries (Figure 3), which corresponded to the abnormal non-invasive digital arterial pressure values. Moreover, the PCHA aneurysm was assessed and depicted in two positions: (1) supine anatomic 170 I Chapter 10

174 position (diameter 8mm, length 25mm, at 8 mm from the PCHA origin); and (2) during abduction and external rotation (ABER provocation), to simulate spiking and serving during volleyball, which showed compression of the distal part of the aneurysm (Figure 4). The remaining arterial run-off down to the hand showed no abnormalities. After careful consideration in a shared decision, it was decided not to perform surgery nor undergo drug therapy. The athlete was discharged without oral anti-thrombotic medication. 15-month follow-up After 15 months, follow-up was performed. Complete cessation of volleyball activities over the preceding nine months caused us to wonder what anamnestic and imaging changes had occurred: the discoloration, numbness and pain in the spiking hand had disappeared, and he only reported cold not warm digits in the right hand while playing outdoor tennis in the winter time, which disappeared instantly in warm circumstances. Physical examination revealed no clinical abnormalities in the right hand, and the subungual petechiae were resolved. Radial artery and ulnar artery pulsations were normal. Vascular ultrasound examination revealed a PCHA aneurysm in his right/ spiking shoulder without intravascular thrombus. Non-invasive digital arterial blood pressure evaluation revealed normal pressure values at the level of the middle phalanx (digits II-V: 151, 151, 141, 154 mmhg). Photoplethysmographic curves were triphasic in all digits of the right hand, but remained flattened in digits II and III (Figure 2 right panel). CE-MRA showed improved vascular patency in the right hand and resolution of central filling defects in the distal radial artery, palmar arch, and digital arteries (Figure 3). Affected digital artery vessel segments showed post-thrombotic changes with decreased diameters and occlusion of some affected segments (Figure 3). The PCHA aneurysm remained unchanged compared to baseline (Figure 4). 10 Conservative management for a PCHA aneurysm I 171

175 Figure 1 Upper panel: longitudinal B-mode ultrasound image of the aneurysmatic proximal PCHA with intravascular thrombus in a 29-year-old professional volleyball player. Lower panel: colour Doppler ultrasound image of the aneurysmatic proximal PCHA, note there is no colour flow in the thrombus region (arrowhead). Key: PCHA, posterior circumflex humeral artery 172 I Chapter 10

176 Figure 2 Left panel (initial presentation): abnormal digital arterial blood pressure values at the level of the proximal phalanx (digits I-V: 159, 144, 149, 159, 0 mmhg) and middle phalanx (digits II-IV: 85, 97, 81 mmhg). Photoplethysmographic waveform patterns were non-triphasic in all digits of the right hand. The left hand shows no abnormalities. Right panel (follow-up): Normal digital arterial blood pressures and photoplethysmographic waveform patterns in both hands on follow-up 10 Conservative management for a PCHA aneurysm I 173

177 D C Figure 3 Contrast-Enhanced MR Angiography using a 1.5T MR system (Siemens MAGNETOM Avanto, Siemens Healthcare 2009) after infusion of a blood pool contrast agent (Ablavar, Lantheus Medical Imaging 2009). Resolution 0.3x0.3x0.3 mm using a 15-element knee coil. A) initial diagnosis scan: maximum intensity projection of time-resolved CE-MRA at initial diagnosis shows filling defects in the distal radial artery, palmar arch, common palmar arteries, and digital arteries (arrowheads); B) initial diagnosis scan: cross-sectional multi-planar reconstruction of digital arteries with a central filling defect in digits IV and V (arrowheads); C) initial diagnosis scan: longitudinal multi-planer reconstruction of the hand with a central filling defect in the common palmar artery (arrowhead); D) follow-up scan: resolution of thrombus and decreased artery diameters in digits IV and V (arrowheads); E) follow-up scan: resolution of thrombus in the common palmar artery (arrowhead). 174 I Chapter 10

178 Figure 4 Contrast-Enhanced MR Angiography using a 1.5T MR system (Siemens MAGNETOM Avanto, Siemens Healthcare 2009) after infusion of a blood pool contrast agent (Ablavar, Lantheus Medical Imaging 2009). Resolution 0.6x0.6x0.6 mm using a 6-element body matrix coil. Volume-rendered images of the axillary artery, branching of the PCHA and proximal PCHA aneurysm (arrowhead) in ABER position (A) and anatomic position during diagnosis (B), and follow-up (C). The proximal PCHA aneurysm (arrowhead) is largely compressed in the ABER position. Thick slab maximum intensity projections (9 mm) of the PCHA aneurysm (arrowheads) at initial diagnosis (D), and follow-up (E). 10 Conservative management for a PCHA aneurysm I 175

179 DISCUSSION Although conservative treatment has been suggested for PCHA pathology 88,127, to our knowledge, this patient (n=1) study is the first to report on successful conservative management for this severe vascular shoulder overuse injury with digital emboli in an elite volleyball player. After 15 months without anti-thrombotic medication, and with cessation of volleyball activities over the previous nine months, the PCHA aneurysm did not show changes compared to baseline. However, distal radial artery, palmar arch, and digital artery intravascular thrombus dissolved. Digital arteries showed post-thrombotic changes including narrowing of luminal diameters and some distal occlusions. However, symptoms dissolved and physical examination measurements as well as brachial artery and finger pressure measurements almost normalized. The residual symptoms cold digits during outdoor tennis in the winter might be the result of demand-ischemia as a result of inadequate vasodilation during outdoor leisure activities in cold circumstances due to post-thrombotic vessel changes. Moreover, this case report is the first to show that a novel combined MR protocol consisting of time-resolved and high-resolution steady state CE-MRA enables detailed visualization of symptomatic emboli in the spiking arm and hand, which are not detectable by vascular ultrasound, and that are in agreement with symptoms and noninvasive hemodynamic measurements. Additionally, this protocol enables visualization of the PCHA aneurysm during ABER provocation, which is of added value to simulate the positional traction and compression of the proximal PCHA during the spiking and serving motion in volleyball. The assumption is that these repetitive powerful overhead movements cause chronic PCHA vessel wall injury 3,17,95, which can be assessed by the CE-MRA protocol. Aneurysmal degeneration, thrombosis and distal occlusion of the PCHA is a rare sportrelated overuse injury mostly found among elite volleyball players 89, with a prevalence of 4.6%. 92 PCHA thrombosis might lead to distal embolization to the circulation of the forearm, hand, and digits in the ipsilateral limb during the spiking or serving motion in volleyball, when the humeral head acts to compress the aneurysmal PCHA and the intraluminal thrombus, causing retrograde embolism into the axillary artery. 3,49,89 Invasive treatment options for thrombosed PCHA aneurysms include surgical ligation and endovascular coiling 3, and are likely to completely reduce the recurrence emboli. However, this type of therapy does not affect the symptomatic emboli and associated symptoms. It seems that conservative management can be considered a valuable alternative for invasive therapeutic options for partially thrombosed PCHA aneurysms. 176 I Chapter 10

180 However, the cessation of the provoking factor, repetitive powerful overhead movements such as spiking and serving in volleyball, might be key for success and for the feasibility of conservative management. In conclusion, for a vascular shoulder overuse injury with symptomatic embolization in the spiking arm in a professional volleyball player, this case report is the first to show promising results of conservative management as an alternative to more invasive clinical modalities such as surgery or percutaneous interventional techniques. 10 Conservative management for a PCHA aneurysm I 177

181

182 PART IV Summary, references and appendices

183

184 CHAPTER 11 Summary Conclusions Clinical implications Future research

185

186 11.1 SUMMARY In 1993, Reekers 95 was the first to describe a traumatic aneurysm of the PCHA in a volleyball player, suggesting a causal relationship. Fifteen years later, between 2008 and 2010, several elite male volleyball players presented themselves in the Academic Medical Center (AMC) in Amsterdam with ischemic digits in the spiking hand due to arterial emboli originating from an aneurysmal and thrombosed posterior circumflex humeral artery (PCHA) in the dominant shoulder. At that time, just five case reports had been published worldwide on volleyball players with this injury. 68,95,96,115,126 Knowledge about this sports-related overuse injury needs to be extended on an international scale considering the potential amputation of a finger as the devastating end result in a population of young, healthy and fit elite volleyball players. This is exemplified by the story of a 45-year-old retired Dutch volleyball player who contacted us after reading our first publication. When he was active at national top level in the 90s, he experienced severe complaints of coldness, discoloration, paresthesia and pain in several digits in his spiking hand for which no cause was found. Ultimately, the third digit in his spiking hand became necrotic and had to be amputated. In this thesis, the first steps of elucidating the unexplored entity of Shoulder PCHA pathology and digital Ischemia in Known Elite volleyball players are made in order to provide an effective contribution to knowledge about this vascular overuse injury. In volleyball, spiking is the act of scoring a point by slamming the ball over the net into the opposing court effectively. 130 Hence the title SPIKE the PCHA. The first part of the thesis (PART I) covered our research on clinical characteristics like symptomatology and associated risk factors. PART II focused on research on optimal imaging strategies for detection and prevention. Combining new findings with conclu-sions from Part I and II generates suggestions for clinical management, discussed in PART III. 11 PART I Symptomatology and associated risk factors Athletes generally present themselves in an advanced stage of the disease with debilitating symptoms of digital ischemia in the spiking hand, like coldness, discoloration and paresthesia. 68,95,96,115,126 These symptoms result in an inability to play volleyball and reduced daily quality of life. In an early stage of the disease, symptoms might only manifest after overhead movements in volleyball as a result of embolization into the digital circulation of the spiking hand. This can lead to a wide range of symptoms during or directly after volleyball. Similar symptoms will often be caused by, and attributed to, musculoskeletal injuries 1, and might therefore initially be perceived as minor, and thus ignored by the athlete. However, since there is a risk of necrosis and amputation, awareness of these symptoms, with a timely detection, is warranted. Summary I 183

187 The objectives of chapter 2 were twofold. The first objective was to determine which symptoms are most likely to be associated with PCHA pathology (PCHAP) with distal embolization (DE) in the spiking hand in volleyball players. Using literature-based data on symptoms reported by volleyball players with confirmed digital ischemia as a result of PCHAP with DE, together with data retrieved from medical files of volleyball players treated for this injury, complaints of cold, blue and pale digits during or immediately after practice as well as competition were most strongly associated with DE as a result of PCHAP. Questions were formulated based on these symptoms of digital ischemia and included in the Shoulder PCHA pathology and digital Ischemia - Questionnaire (SPI-Q). The second objective was to assess the prevalence of these symptoms in the spiking hand among elite male volleyball players in the Netherlands. Ninety-nine of 107 elite male volleyball players in the Netherlands completed the SPI-Q in a national survey in 2011: 91 indoor- and 8 beach volleyball players, a participation rate of 93%. An unexpectedly high percentage of 31% of these volleyball players reported symptoms of digital ischemia that are associated with PCHAP with DE in the spiking hand. These athletes are considered potentially at risk for developing critical digital ischemia since these symptoms might be the result of an early stage of the disease. Therefore further analysis of the presence of PCHAP and DE, and a better insight into modifiable risk factors to achieve effective prevention, is warranted. In chapter 3, we assessed whether personal-, sports- and work-related risk factors are associated with self-reported symptoms of digital ischemia in the spiking hand. A national questionnaire survey in 2011 assessed the presence of symptoms and risk factors in 99 elite male volleyball players in the Netherlands: 91 indoor- and 8 beach volleyball players. Two sports-related risk factors were independently associated with symptoms of blue or pale digits in the spiking hand: a total volleyball career duration of 18 years or more (OR=6.70; 95%CI ) and often or always performing weight training to increase dominant limb strength (OR=2.70; 95%CI ). The identification of these sports-related risk factors is a first step in signalling and preventing apparently innocuous symptoms of digital ischemia. The next step of implementation of the SPI-Q for periodic surveillance of elite volleyball players at risk for digital ischemia was to test its measurement properties. In chapter 4, the test-retest reliability of the SPI-Q was assessed with a two-week interval among 65 elite male indoor volleyball players, assessing symptoms of cold, pale and blue digits in the spiking hand during or after practice or competition. The results showed that the SPI-Q is a reliable questionnaire for: 1) detecting elite male indoor volleyball players with symptoms of digital ischemia in the spiking hand (kappa=0.83; 95%CI ); and 2) for grading the severity of these symptoms (ICC=0.82; 95%CI ). These findings indicate that the SPI-Q can be used for periodic surveillance of elite volleyball players. 184 I Chapter 11

188 Since the exposure to sport-specific demands is different in beach volleyball compared to indoor volleyball, the aim of chapter 5 was to assess the prevalence of ischemiarelated symptoms in the spiking hand, and associated risk factors, among international world-class beach volleyball players. A questionnaire survey was performed during an international beach volleyball tournament in which 60 beach volleyball players participated: 26 males and 34 females from 17 countries, a participation rate of 49%. Thirty-eight percent of these volleyball players reported symptoms of digital ischemia that are associated with PCHAP with DE in the spiking hand. A total volleyball career duration of 14 years or more (OR=4.42; 90%CI ), and sex (female) (OR=4.62; 90%CI ) were independently associated with an increased risk of ischemiarelated symptoms. Compared to elite indoor volleyball players assessed in chapters 2 and 3, the prevalence of symptoms of digital ischemia in the spiking hand was higher among elite beach volleyball players (38% versus 31%), and total volleyball career duration was a joint risk factor. PART II Imaging In general, ultrasound (US) is the first-line imaging modality for peripheral aneurysm assessment. 42 It is readily available, applicable on-site, inexpensive, patient friendly and enables non-invasive measurement of vessel diameters and detection of intravascular thrombus. 42 Currently there is no standardized vascular US protocol available for imaging the PCHA. 17 Such a protocol would enable worldwide uniform assessment of PCHA pathology. Moreover, given the complex local anatomy, including the frequently nearby originating and closely resembling deep brachial artery (DBA), evidence based recommendations and instructions for imaging would enable targeted PCHA identification and assessment. In chapter 6, we present a 4-step standardized vascular US protocol for assessing the proximal PCHA: the Shoulder PCHA pathology and digital Ischemia UltraSound (SPI- US) protocol. International standardization of PCHA imaging will help in accurate identification and assessment. 11 The next step in the development of the SPI-US protocol was to assess its measurement properties. In chapter 7, the inter-rater reliability of the SPI-US protocol for diameter assessment of the PCHA and DBA was assessed. Two vascular technologists independently determined diameters of the PCHA and DBA in 32 healthy volunteers using the SPI-US protocol. The results showed that the SPI-US protocol is accurate and precise for diameter assessment of the PCHA (ICC=0.70; 95%CI ) and DBA (ICC=0.60; 95%CI ), with sonographer-independent PCHA diameter measurements. Moreover, with a calculated Minimal Detectable Change (MDC) of 0.90 mm, the SPI-US seemed clinically valid for aneurysm detection when performed by experienced vascular technologists. Summary I 185

189 International dissemination of this protocol might make it possible to identify PCHA injury, both in an on-site screening setting, and in a clinical setting. The objectives of chapter 8 were twofold. The first objective was to determine the prevalence of PCHA aneurysms in the dominant shoulder in elite volleyball players. The second objective was to describe PCHA and DBA anatomy, branching pattern, course and diameters. The SPI-US protocol was used to assess the PCHA and DBA in the dominant shoulder in 280 elite indoor and beach volleyball players, 245 men and 35 women. The PCHA was identified in 100% of the cases. Aneurysms were detected in the proximal PCHA in 4.6% (13/280) of elite volleyball players and associated with a specific branching type, namely a PCHA that originates directly from the axillary artery. The PCHA originated from the axillary artery (AA) in 81% of cases (228/280), and showed a curved course dorsally towards the humeral head in 93% of these cases (211/228), with a mean diameter of 3.8 mm (95%CI ) in men, and 3.5 mm (95%CI ) in women. The DBA was identified in 93% of cases (260/280), all without aneurysms. The DBA originated from the AA in 73% of cases (190/260), and showed a straight course parallel to the AA in 93% of these cases (177/190), with a mean diameter of 2.3 mm (95%CI ) in men, and 2.0 mm (95%CI ) in women. The described vessel characteristics and diameters provide clear guidance to identify and assess the PCHA and DBA using US. The high prevalence of detected PCHA aneurysms among elite volleyball players demands an active policy on prevention and periodic surveillance. PART III Clinical management Increasing awareness among medical professionals through the dissemination of knowledge about this vascular injury will enable recognition, which is important to prevent the development of an advanced stage of the disease with serious ischemic complications. Invasive treatment options for PCHA aneurysms result in several months of rehabilitation and absence from volleyball activities. However, if PCHA pathology can be detected at an early stage, serious ischemic complications, irreversible tissue damage, and surgical ligation of the PCHA might be prevented. 89 Since volleyball players are considered potentially at risk for developing critical digital ischemia in the spiking hand, analysis of the presence of PCHA pathology, and associated risk factors is warranted for prevention. Ultimately, establishing risk profiles of individual athletes would support clinical management. The objectives of chapter 9 were fourfold: (1) to assess the prevalence of PCHA pathology in the dominant shoulder among elite volleyball players; (2) to determine its association with self-reported symptoms of digital ischemia in the spiking hand; (3) to assess possible personal- and sports-related risk factors, including dose-response relationship; and (4) to provide individual risk profiles for the clinical management of PCHA pathology based on prevalence, symptoms and associated risk factors. Two-hundred-seventy-eight 186 I Chapter 11

190 elite indoor- and beach volleyball players completed the SPI-Q assessing symptoms of digital ischemia and associated risk factors, prior to SPI-US screening for the presence of PCHA pathology, namely aneurysms, dilatations, and occlusions. PCHA pathology was detected in 17 participants (6.1%). In total, 96 of 278 participants reported symptoms associated with ischemic digits (35%) which were not associated with PCHA pathology (OR=0.39; 95%CI ). A total volleyball career duration of 17 years or more and an age of 27 years or more were associated with a 9-fold (OR 9.21; 90%CI ) and 14-fold (OR 13.61; 90%CI ) increased risk of PCHA pathology, respectively. Four risk profiles for elite volleyball players were formulated based on the combination of: (1) the presence of US-detected PCHA pathology (US+ or US ); and (2) symptoms of digital ischemia (Q+ or Q ); I) 1.1% US+Q+ (n=3), II) 5.0% US+Q (n=14), III) 33.5% US Q+ (n=93), and IV) 60.4% US Q (n=168). For each risk, profile recommendations for clinical management are proposed to optimize care for this potentially limb-threatening vascular overuse injury. Chapter 10 describes a case of a 34-year-old elite male volleyball player with symptomatic emboli in the spiking hand from a partially thrombosed aneurysm of the PCHA in his dominant shoulder. At 15-month follow-up after cessation of volleyball activities, digital blood pressure values almost normalized and a novel Magnetic Resonance Angiography (MRA) protocol showed an unchanged PCHA aneurysm and resolution of central filling defects in the digital arteries with post-thrombotic changes. This case report is the first to show promising results of conservative management as an alternative to more invasive treatment modalities for this vascular shoulder overuse injury. 11 Summary I 187

191

192 11.2 CONCLUSIONS PART I Symptomatology and associated risk factors (Chapters 2-5) Among surveyed elite indoor- and beach volleyball players, symptoms of cold and discoloured digits in the spiking hand during or directly after practice or competition were prevalent in respectively 31% and 38% of the players. The duration of the volleyball career, the intensity of performing strength-increasing weight training, and the female sex were identified as associated risk factors (Table 1). These symptoms and risk factors for digital ischemia, which are associated with PCHA pathology, can be assessed adequately in an international arena using the Shoulder PCHA pathology and digital Ischemia Questionnaire (SPI-Q): a reliable instrument for identifying elite volleyball players with symptoms of digital ischemia, and for grading the severity of these symptoms. Table 1 Overview of the main outcomes of Chapters 2, 3, 5 (PART I), and 9 (PART III) Prevalence Associated risk factors Overall Indoor Beach Beach Increased risk Symptoms of digital ischemia 35% 31% 23% 50% Indoor volleyball: volleyball career of 18 years* frequency of strengthincreasing exercises* Beach volleyball: volleyball career of 14 years* female sex 7-fold 3-fold 4-fold 5-fold PCHA pathology 6.1% 6.0% 7.7% 5.7% volleyball career of 17 years* age of 27 years* * dose-response relation present 9-fold 14-fold 11 PART II Imaging (Chapters 6-8) The standardization of PCHA examination using the Shoulder PCHA pathology and digital Ischemia UltraSound (SPI-US) protocol, combined with detailed knowledge on PCHA and DBA vessel characteristics and diameters, enabled targeted, accurate and precise diameter measurements, as well as PCHA aneurysm detection (Table 2). Among the examined elite volleyball players, proximal PCHA aneurysms were prevalent in 4.6% and associated with a specific branching type, namely a PCHA that originates directly from the axillary artery. Conclusions I 189

193 Table 2 Overview of the main outcomes of Chapters 7 and 8 (PART II) PCHA DBA ICC for diameter measurement 0.70 (95%CI ) 0.60 (95%CI ) SEM 0.32 mm 0.29 mm MDC 0.90 mm 0.80 mm Presence of aneurysms Yes (4.6% prevalence) No Presence of aneurysms in anatomical variants Location of aneurysms No Proximal (within 1.5 cm of origin) No n.a. Presence in axillary pit Always present Commonly present (absent in 7% of cases) Originating directly from the AA 81% of cases 75% of cases Location of origin Course at origin Dorsal of the AA, proximal of the DBA Curved towards the dorsal side of the humerus Dorsal of the AA, distal of the PCHA Straight and parallel to the AA Intra-individual ratio >1.0 (PCHA dm / DBA dm) <1.0 (DBA dm / PCHA dm) Average diameter (in mm) 3.8 ( ) 3.5 ( ) 2.3 ( ) 2.0 ( ) Average diameter (corrected for BSA) 1.8 ( ) 1.8 ( ) 1.1 ( ) 1.1 ( ) Key: ICC, intra-class correlation coefficient; SEM, standard error of measurement; MDC, minimal detectable change; AA, axillary artery; mm, millimeter; cm, centimeter; dm, diameter;, men;, women; BSA, body surface area; n.a., not applicable PART III Clinical management (Chapters 9 and 10) To optimize care for this potentially limb-threatening vascular overuse injury, and to prevent serious ischemic complications in the spiking hand, clinical management recommendations for individual athletes have been formulated based on the combination of the presence or absence of PCHA pathology, associated risk factors, and reporting of symptoms of digital ischemia (Tables 1 and 3). Conservative management for a PCHA aneurysm with symptomatic emboli in the spiking hand showed promising results in one observed case. 190 I Chapter 11

194 Table 3 Overview of the main outcomes of Chapter 9 (PART III) Prevalence Recommendations for clinical management US+Q+ 1.1% * At risk for irreversible tissue damage from prolonged digital ischemia Refer to vascular surgeon for additional imaging and therapy US+Q 5.0% * At risk for distal embolization from the aneurysmal PCHA SPI-US monitoring annually to identify progress of PCHA pathology Consult vascular surgeon in case of thrombus formation SPI-Q monitoring twice a year to detect onset of digital ischemia and to increase awareness Consult vascular surgeon when symptoms arise acutely or are associated with pulse deficits, pallor or differences in temperature between digits in the spiking hand US Q+ 33.5% * Consider other causes of digital ischemia ** At risk for PCHA pathology as the career progresses SPI-Q monitoring yearly to grade severity of digital ischemia and to increase awareness Consult vascular surgeon when symptoms aggravate acutely or are associated with pulse deficits, pallor or differences in temperature between digits in the spiking hand US Q 60.4% * At risk for PCHA pathology when symptoms of digital ischemia arise and as the career progresses SPI-US monitoring biannually to detect the onset of digital ischemia and to increase awareness Consult vascular surgeon when symptoms arise acutely or are associated with pulse deficits, pallor or differences in temperature between digits in the spiking hand Key: US+/, presence or absence of PCHA pathology on SPI-US examination; Q+/, presence or absence of symptoms of digital ischemia on SPI-Q surveillance 11 Conclusions I 191

195

196 11.3 CLINICAL IMPLICATIONS Awareness Aneurysmal degeneration, thrombosis and distal occlusion of the PCHA is a rare vascular shoulder overuse injury mostly found among elite volleyball players, and until a few years ago was not on the radar of volleyball players, national and international volleyball federations and medical professionals. To prevent serious ischemic complications, awareness of the existence of this injury is of vital importance. Through our research we have reached a large international population of elite beach- and indoor volleyball players, ranging from the Dutch under-18 squad to players at national and international top level. Hopefully these athletes now know not to trivialize apparently innocuous symptoms of digital ischemia in the spiking hand, and to seek timely medical attention. Also, we increased awareness through a systematic transfer of knowledge. Team physicians, (para)medical staff members, national and international sports medicine specialists, vascular technologists, radiologists, and the Fédération Internationale de Volleyball (FIVB) and the Dutch Volleyball Association (Nevobo) have been explicitly informed through our on-site research activities, promotional posts, presentations at medical conferences and practice sessions, website ( and national and international publications in the field of sports medicine, occupational medicine, and radiology. In addition, as a result of national and international media attention generated by our first publications 40,41, more amateur volleyball players are aware of PCHA pathology and its concomitant symptoms. For example, a concerned mother from Chicago contacted us wondering if her 14-year-old son, who experienced cold hands during volleyball at an amateur level, was also at risk. As mentioned, a 45-year-old retired Dutch volleyball player contacted us. In the period that he was active at top national level in the 90s, he experienced severe complaints of ischemic digits in his spiking hand for which no cause was found. Ultimately, the third digit in his spiking hand became necrotic and had to be amputated. After reading our article, he recognized the described symptoms and contacted us with his story. This is a worst case example of how lack of awareness of this injury can lead to the loss of a finger. When the treating physician does not consider a proximal cause of signs and symptoms of digital ischemia in the spiking hand, imaging and therapy in the forearm and hand might be applied without treating the actual source of embolization, which might result in a postponed diagnosis and serious ischemic complications as a result of the recurrence of emboli. Hopefully, the international dissemination of this thesis, and its individual articles, will help prevent similar events in the future. We believe a key role in this process of spreading national and worldwide awareness through national volleyball federations and international volleyball tournaments lies with the FIVB. 11 Clinical implications I 193

197 Team physicians and sports medicine specialists Knowledge about PCHA pathology and its concomitant symptoms should enable recognition, which is important for preventing serious ischemic complications. One in every 16 elite volleyball players (6.1%) has PCHA pathology in the dominant shoulder, a known source of digital embolization in the spiking arm in volleyball players, which is the equivalent of two players in every three volleyball teams. Therefore, sports physicians need to have a high index of suspicion when a volleyball player reports symptoms and signs of digital ischemia, especially as the volleyball career progresses. On the other hand, since one in every three elite volleyball players reports symptoms of digital ischemia in the spiking hand, and PCHA pathology was detected with ultrasound in only a small percentage of these athletes, sports physicians need to remain vigilant for other possible (vascular) causes. Two reliable standardized diagnostic instruments for assessing the PCHA and symptoms of digital ischemia, and clinical management recommendations on how to act based on the assessment outcomes, are provided and can be found on We encourage sports physicians to use these instruments and recommendations in daily practice. SPI-US assessment of the PCHA by sports medicine specialists might be possible, and even favourable, in the future, especially with the development of new smartphone ultrasound devices. Of course this should be accompanied by a comprehensive training in performing SPI-US examination given the fact that the reliability of the SPI-US protocol has only been assessed among experienced vascular technologists. Moreover, since PCHA pathology is often under-recognized and similar symptoms will often be caused by, and attributed to, musculoskeletal injuries, PCHA pathology in overhead sports should be addressed in the education of team physicians, sports medicine specialists, general practitioners, and orthopaedic- and vascular surgeons. Vascular technologists and radiologists Worldwide standardization of PCHA imaging will help in targeted and accurate identification and assessment. This thesis provides vascular technologists and radiologists with insights into how ultrasonography can be used for the surveillance of a vascular overuse injury which is prevalent in elite overhead athletes, like volleyball players. When confronted with an elite overhead athlete with symptoms of digital ischemia in whom only forearm and more distal vascular US is requested, proactive vascular sonographers should always consider a proximal cause of emboli and might therefore consider performing the standardized and reliable 5-10 minute SPI-US protocol to assess the PCHA for possible pathology. The four steps of the SPI-US protocol, including illustrative photographs combined with ultrasound images per step, can be found on www. spikestudy.com. We encourage vascular technologists and radiologists to use the SPI-US protocol. However, for targeted and accurate PCHA imaging, good anatomical knowledge of axillary artery branching patterns and its anatomic variations is essential. Moreover, to raise awareness and enable recognition, PCHA pathology in overhead sports should 194 I Chapter 11

198 be addressed in the education of vascular technologists and radiologists. An E-learning programme can play an important role in a timely international dissemination of the SPI-US protocol Prevention The ultimate goal of sports medicine is to prevent injuries so that athletes remain competitive in the arena. 100 According to van Mechelen s model 69, the first step in the sequence of sports injury prevention research is to describe the magnitude of the problem in terms of frequency and severity of injuries. To do so, a comprehensive review of the medical literature was performed, which showed that PCHA pathology with serious ischemic complications is mostly reported among elite volleyball players. Also, multiple cases have been reported in elite baseball, tennis, swimming, kayaking, yoga, trapeze flying, American football, and even one in regular work, namely a mechanic. 13 The second step is to map the possible causes of injuries, and to identify their risk factors and mechanisms. According to the Bradford and Hill criteria for causation 45, a group of minimal conditions is necessary to provide adequate evidence of a causal relationship. This thesis has shown that the relationship between PCHA pathology and volleyball satisfies a number of these criteria, one of them being the strength (effect size) of the association. Case reports previously published on this topic were the first to indicate a causal relationship. Recently, a clear association has been demonstrated (see chapters 8 and 9), in which the prevalence of PCHA pathology among elite volleyball players has been objectified. Moreover, the presence of a time relationship and dose-response effect has also been demonstrated in chapter 9. Biological plausibility is provided by the fact that the vast majority of cases of PCHA pathology are found in sports that involve repetitive powerful overhead movements. The assumption is that these movements for instance spiking and serving in volleyball and throwing in baseball cause chronic vessel wall injury as a result of positional traction and compression of the proximal PCHA. 3,17,95 Lastly, the effect of exposure reduction is demonstrated in chapter 10, since cessation of volleyball activities resulted in the dissolution of intravascular thrombus as well as symptoms in the spiking arm and hand, and normalization of physical examination measurements as well as brachial artery and finger pressure measurements. Therefore, Reekers hypothesis seems to be confirmed in this thesis: PCHA pathology can be classified as a sports-related disease among volleyball players. 11 The final step in the injury prevention sequence, according to van Mechelen s model 69, is to introduce measures that are likely to reduce the future risk and/or severity of sports injuries, and to document whether they are effective. At the moment, the literature on the prevention of PCHA pathology among volleyball players is lacking. A first step to introducing clinical management recommendations in order to prevent onset and worsening of PCHA pathology has been taken in chapter 9. The efficacy and feasibility of these and other yet to be introduced measures has to be evaluated in the future. Clinical implications I 195

199

200 11.4 FUTURE RESEARCH Future research into PCHA pathology among elite volleyball players should address at least the following five topics. Firstly, the cause of unilateral ischemia-related symptoms in the spiking hand among the majority of volleyball players assessed in chapters 2, 3, 5 and 9 remains unknown. The high prevalence of these symptoms among professional athletes at the prime of their career is both unexpected and ominous. Therefore, future studies might address other serious vascular causes such as micro- and macrovascular damage in the fingers, hand, and forearm, which might be due to repeated vascular microtrauma by vigorous ball contact during passing, serving, spiking and blocking in volleyball. Moreover, the high prevalence among volleyball players emphasizes the need for surveillance of other overhead athletes at risk, such as baseball pitchers, to objectify the presence of symptoms of digital ischemia and assess associations with possible risk factors. The same goes for regular jobs with similar risk factors like mechanics and meat processing workers. Similar surveillance of young elite volleyball players might clarify the moment of onset of these symptoms and identify possible risk factors. Furthermore, a prospective assessment of symptoms of digital ischemia at regular intervals among elite volleyball players might reveal possible associations with both PCHA pathology and other causes. 6,122 Secondly, the characteristics that predispose a volleyball player to develop PCHA pathology in the dominant shoulder remain unclear. One identified risk factor is the duration of the volleyball career, a variable which all volleyball players have in common. Additionally, based on the results of chapter 8, it seems that a PCHA originating directly from the axillary artery is another risk factor and that variant anatomy might be protective against PCHA pathology. However, the existence of more still unknown predisposing characteristics seems plausible. Although male sex was thought to be predisposing for PCHA injury among volleyball players, since the large majority of clinical cases have been reported in male volleyball players 17, the prevalence of US-detected PCHA pathology was similar among men and women. Interestingly, female sex was a risk factor for symptoms of digital ischemia among beach volleyball players, which can be attributed to the notably high (50%) prevalence of these complaints in the spiking hand among female beach volleyball players, compared to their male colleagues (24%). Additionally, this prevalence was also much higher than among male indoor volleyball players (31%). Why women are more likely to perceive symptoms of digital ischemia in the spiking hand might be assessed in the future. However, a misleading impression might be provided since the group of participating female volleyball players in this thesis was relatively small. Therefore, it would be interesting for future studies to assess the presence of PCHA pathology, digital ischemia, and associated risk factors among elite female indoor- and beach volleyball players. Another example of a possible predisposing 11 Future research I 197

201 characteristic is a familial predisposition for peripheral aneurysms, since these have been reported to be associated with genetic connective tissue disorders such as Marfan syndrome, Behçet disease, acromegaly and arteriomegaly. 42,109 In this light it is worth noting that 15% (2/13) of volleyball players in this thesis in whom a PCHA aneurysm was detected reported the presence of aortic aneurysms in second-degree family members. For a better understanding of individual risk factors that predispose for PCHA pathology, prospective SPI-Q and SPI-US surveillance of volleyball players with asymptomatic PCHA pathology, starting with the 17 cases found in chapter 9, seems appropriate. Moreover, this might clarify the onset and course of symptoms in relation to the progress of PCHA pathology and the development of intravascular thrombus. Additionally, risk factors for similar injuries, such as symptomatic iliac artery compression in cyclists 62,107, might be examined for PCHA pathology among volleyball players. Furthermore, the AMC has a longstanding history in the field of medical research, for instance on wall shear stress in intracranial aneurysms. This knowledge might be useful for a better understanding of aneurysmal hemodynamics and intra-aneurysmal thrombus formation in the PCHA. Thirdly, future studies should focus on preventive measures to prevent PCHA pathology in the dominant shoulder in elite volleyball players. Although only one case of a volleyball player has been described in whom cessation of volleyball activities led to the termination of symptoms and normalization of both physical examination and digital arterial blood pressure measurements (chapter 10), this observation gives rise to speculations concerning prevention. For instance, measures like limited amount of serves, spikes or overhead strength exercises per training session might be protective against PCHA overuse in the dominant shoulder. Moreover, since the intensity of performing strength-increasing weight training was found to be related to symptoms of digital ischemia, and might play a role in vascular overuse in the dominant shoulder, a better insight into biomechanical factors, like the type of movements and ranges of motion, and training characteristics, like intensity, frequency and duration, might be relevant for prevention. Furthermore, it might be interesting to explore the influence of the serve and spike technique on PCHA overuse in the dominant shoulder, with special attention being paid to the extreme shoulder angles achieved during these movements. Fourthly, when diagnosed with PCHA pathology with symptomatic embolization in the spiking arm, elite volleyball players probably want to return to competition as soon as possible, and might therefore have a preference for invasive clinical modalities such as surgery or percutaneous interventional techniques. However, conservative management might be appropriate for a small percentage of these athletes. Therefore, future studies might assess the effect of conservative versus invasive clinical management using for instance interrupted time series studies 106, given the fact that the prevalence of clinical cases of volleyball players with PCHA pathology is low. 198 I Chapter 11

202 Fifthly, although the identification of the dose-response-related risk factors of volleyball career duration and age implies that chronic vessel wall overuse leads to the development of PCHA abnormalities, this has still to be confirmed in future studies. In conclusion, although the first steps into the unexplored entity of PCHA pathology among elite volleyball players have been made in this thesis, plenty of territory remains uncharted, which provides a wide range of opportunities for future research. Finally, the international dissemination of this thesis and its individual articles will encourage new research initiatives. We believe an important role in this process lies with the FIVB, and its collaboration with International Olympic Committee (IOC) accredited Research Centres, such as the Academic Center of Evidence based Sports medicine (ACES), which is part of the Amsterdam Collaboration on Health & Safety in Sports together with the VU University. The mission of ACES as part of one of the nine worldwide expert centres for prevention of injury and protection of athlete health is the continuous improvement of health care for injured top-level athletes through integrated diagnostics, patient-tailored treatment and monitoring of treatment outcomes. This is the first AMC thesis from this platform on which synergetic collaboration between experts in several clinical and preclinical disciplines, such as Orthopaedic surgery, Sports medicine, Human Movement Sciences and Radiology, fosters new insights and breakthrough research. This thesis is a prime example of how the ACES umbrella facilitates synergetic collaboration between medical professionals and students to perform scientific research through bachelor- and master thesis and PhD projects. 11 Future research I 199

203

204 CHAPTER 12 Samenvatting Conclusies

205

206 12.1 SAMENVATTING In 1993 was Reekers 95 de eerste die een traumatische verwijding van de Arteria circumflexa humeri posterior (ACHP) bij een volleyballer beschreef en een causaal verband suggereerde. Vijftien jaar later, tussen 2008 en 2010, presenteerden zes volleyballers zich in het AMC met zuurstoftekort (ischemie) in de vingers van de slaghand als gevolg van kleine bloedpropjes (trombo-embolieën) in de slagaderen van deze vingers. Na verder onderzoek bleek dat deze trombo-embolieën waren ontstaan in een afwijkende (pathologische) slagader in de dominante schouder, de ACHP. Bij deze volleyballers was de ACHP verwijd (aneurysma) en in deze verwijding zat een bloedprop (trombus) die het bloedvat afsloot. Na operatieve afbinding van het bloedvat en drie tot vier maanden revalideren keerden ze terug op hun oorspronkelijke niveau. Allen waren mannelijke topvolleyballers spelend in de hoogste nationale competitie. Tot dat moment waren wereldwijd slechts vijf patiënt-beschrijvingen (case-reports) gepubliceerd in de medische literatuur over volleyballers met deze aandoening. Meer internationale kennis over deze aandoening is van essentieel belang omdat deze jonge, gezonde en fitte topvolleyballers in de bloei van hun carrière risico lopen op onherstelbare weefselschade in de vingers als gevolg van langdurig zuurstoftekort. Dit kan uiteindelijk leiden tot weefseldood (necrose) en het verliezen van een vinger. Een voorbeeld hiervan is het verhaal van een 45-jarige Nederlandse oud-volleyballer die contact met ons opnam na het lezen van onze eerste publicatie. Hij volleybalde op nationaal topniveau in de jaren negentig en had toentertijd veel last van koude, ontkleurde, tintelende en pijnlijke vingers in zijn slaghand. Hiervoor werd destijds geen oorzaak gevonden. Uiteindelijk werd de middelvinger van zijn slaghand necrotisch en moest deze geamputeerd worden. In dit proefschrift worden de eerste stappen gezet in de ontrafeling van de onbekende aandoening van Shoulder PCHA pathology and digital Ischemia in Known Elite volleyball players, met als doel om in een effectieve bijdrage aan kennis over dit vasculair overbelastingsletsel te voorzien. Een smash (in het Engels spike) is een volleybalterm die staat voor een aanvallende techniek waarbij gepoogd wordt een punt te scoren door de bal hard en effectief op de helft van de tegenstander te slaan. Vandaar de titel SPIKE the PCHA. 12 Dit proefschrift onderzoekt in het eerste deel (Deel I) de symptomen van zuurstoftekort in de vingers, hoe vaak die optreden bij topzaal- en topbeachvolleyballers en welke risicofactoren in volleybal bestaan voor deze symptomen. Deel II beschrijft hoe ACHP letsel goed in beeld kan worden gebracht. Deel III richt zich op hoe vaak ACHP letsel optreedt bij topvolleyballers en geeft aanbevelingen voor hoe een arts kan handelen bij deze patiënten. Samenvatting I 203

207 Deel I Symptomen en risicofactoren Volleyballers presenteren zich over het algemeen in een vergevorderd stadium van de ziekte met invaliderende symptomen van ischemische vingers in de slaghand, zoals kou, ontkleuring, tintelingen en pijn. Deze symptomen veroorzaken een onvermogen om te volleyballen en verminderen de dagelijkse kwaliteit van leven. In een vroeg stadium van de ziekte manifesteren de symptomen zich mogelijk alleen na bovenhandse bewegingen tijdens het volleyballen, zoals smashen en serveren. Tijdens deze bewegingen brokkelen de trombo-embolieën namelijk af van de trombus in het bloedvat en wordt het ACHP aneurysma als een tube tandpasta samengeknepen, waardoor de trombo-embolieën terug in de grote slagader van de schouder (de bovenarmslagader) geduwd worden, en vervolgens met de bloedstroom meegevoerd worden tot in de kleinste slagaderen van de slaghand, waar ze vastlopen. Dit kan leiden tot de hierboven genoemde klachten zowel tijdens als direct na het volleyballen. Vergelijkbare symptomen worden vaak veroorzaakt door, en toegeschreven aan, blessures aan het bewegingsapparaat. Het kan daarom zo zijn dat de volleyballer deze symptomen in eerste instantie bagatelliseert en negeert. Omdat er een risico op necrose en amputatie bestaat, is tijdige herkenning en signalering van symptomen die passen bij trombo-embolieën van groot belang. De doelstelling van hoofdstuk 2 was tweeledig. Het eerste doel was om te bepalen welke symptomen het best passen bij ACHP letsel met trombo-embolieën in de slaghand bij volleyballers. Hiervoor zijn de symptomen geselecteerd die werden beschreven in de case-reports van volleyballers met ischemische vingers door ACHP letsel met tromboembolieën in de slaghand. Ook de symptomen die werden gerapporteerd in de medische dossiers van de in het AMC behandelde volleyballers zijn meegenomen. Op basis hiervan is besloten dat klachten van koude, blauwe en bleke vingers tijdens of direct na het volleyballen het best passen bij trombo-embolieën in de slaghand door ACHP letsel. Vragen over deze symptomen zijn opgenomen in een speciaal ontwikkelde vragenlijst genaamd de Shoulder PCHA pathology and digital Ischemia - Questionnaire (SPI-Q). De tweede doelstelling was om het vóórkomen (de prevalentie) van deze symptomen in de slaghand bij topvolleyballers in Nederland te bepalen. Negenennegentig van de 107 mannelijke volleyballers actief op het hoogste niveau in Nederland vulden tijdens een nationaal vragenlijstonderzoek in 2011 de SPI-Q in: 91 zaalvolleyballers en 8 beachvolleyballers, een deelnamepercentage van 93%. Een onverwacht hoog percentage van 31% van deze topvolleyballers rapporteerde symptomen van ischemische vingers in de slaghand. Deze klachten hangen samen met ACHP letsel met trombo-embolieën in de slaghand. Omdat deze klachten passen bij een vroeg stadium van ACHP letsel, lopen deze volleyballers mogelijk het risico op het ontwikkelen van ernstig zuurstoftekort in de vingers. Daarom is het belangrijk dat de aanwezigheid van ACHP letsel in de dominante schouder en trombo-embolieën in de slaghand verder onderzocht wordt. Ook is het voor preventie noodzakelijk om te weten wat de risicofactoren voor deze aandoening zijn. In hoofdstuk 3 onderzochten we welke kenmerken van de persoon, sport en werk 204 I Chapter 12

208 samenhangen met de symptomen van ischemische vingers in de slaghand. Een vragenlijstonderzoek werd uitgevoerd bij 99 mannelijke volleyballers actief op het hoogste niveau in Nederland: 91 zaalvolleyballers en 8 beachvolleyballers. Twee sportgerelateerde risicofactoren bleken samen te hangen met de symptomen van ischemische vingers in de slaghand: een totale volleybalcarrière van 18 jaar of meer gaf een 7x zo hoog risico op deze klachten (Odds Ratio (OR) 6,70; 95% BetrouwbaarheidsInterval (BI) 1,12-29,54) en het vaak of altijd uitvoeren van krachttraining voor de slagarm gaf een 3x zo hoog risico op deze klachten (OR 2,70; 95%BI 1,05-6,92). Deze sport-gerelateerde risicofactoren bieden een kans voor preventie voor deze ogenschijnlijk onschuldige symptomen van ischemische vingers in de slaghand bij volleyballers. Voordat de SPI-Q voor preventief medisch onderzoek kan worden gebruikt bij topvolleyballers die risico lopen op ischemische vingers, dient eerst de testhertest betrouwbaarheid te worden bepaald. In hoofdstuk 4 is deze test-hertest betrouwbaarheid onderzocht bij 65 mannelijke zaalvolleyballers actief op het hoogste niveau in Nederland. De volleyballers vulden de vragenlijst twee keer in met een tussenperiode van twee weken. Na 2 weken werd gekeken in hoeverre ze vergelijkbare antwoorden gaven op vragen over klachten van koude, bleke en blauwe vingers in de slaghand tijdens of direct na het volleyballen. De resultaten toonden aan dat de SPI-Q een betrouwbare vragenlijst is voor: 1) het detecteren van mannelijke zaalvolleyballers met symptomen van ischemische vingers in de slaghand (kappa 0,83; 95%Bl 0,69-0,97); en 2) het inschatten van de ernst van deze symptomen (Intra-class Correlatie Coëfficiënt (ICC) 0,82; 95%Bl 0,72-0,88). Deze bevindingen geven aan dat de SPI-Q gebruikt kan worden voor periodiek preventief medisch onderzoek van symptomen van ischemische vingers in de slaghand bij topvolleyballers. Omdat de sport-specifieke eisen bij beachvolleybal anders zijn dan bij zaalvolleybal, was het doel van hoofdstuk 5 om de prevalentie van symptomen van ischemische vingers in de slaghand, en mogelijke risicofactoren, te bepalen bij beachvolleyballers actief op mondiaal niveau. Tijdens het jaarlijkse internationale beachvolleybaltoernooi in Den Haag werd een vragenlijstonderzoek uitgevoerd waaraan 60 beachvolleyballers deelnamen: 26 mannen en 34 vrouwen uit 17 landen, een deelnamepercentage van 49%. De prevalentie van symptomen van ischemische vingers in de slaghand was 38%. Twee risicofactoren bleken samen te hangen met symptomen van ischemische vingers in de slaghand: een totale volleybalcarrière van 14 jaar of meer gaf een 4x zo hoog risico op deze klachten (OR 4,42; 90%BI 1,30-15,07) en vrouw zijn een 5x zo hoog risico op deze klachten (OR 4,62; 90%BI 1,15-18,57). Vergeleken met de nationaal actieve zaalvolleyballers onderzocht in hoofdstukken 2 en 3 was de prevalentie van symptomen van ischemische vingers hoger bij internationaal actieve beachvolleyballers (38% versus 31%), en was de totale duur van de volleybalcarrière een zelfde risicofactor. DEEL II - Beeldvorming 12 Samenvatting I 205

209 Echografie is een techniek die door het zenden van geluidsgolven structuren in het lichaam zichtbaar kan maken zoals aneurysma s in de bloedvaten van de ledematen. Deze beeldvormende techniek is overal toepasbaar, goedkoop, patiëntvriendelijk en maakt het mogelijk om bloedvatdiameters niet-invasief te meten, en trombus in een bloedvat op te sporen. Momenteel is er geen gestandaardiseerd, echografisch protocol beschikbaar voor de beeldvorming van de ACHP. Een dergelijk protocol zou wereldwijde uniforme beeldvorming van de ACHP mogelijk maken. Bovendien is het zo dat de beeldvorming wordt bemoeilijkt door de complexe lokale anatomie, zoals de soms nabijgelegen oorsprong van de, en sterk op de ACHP gelijkende, Arteria brachialis profunda (ABP). Daarom kunnen evidence based aanbevelingen en instructies voor beeldvorming van de ACHP helpen bij een accurate echografische beoordeling. In hoofdstuk 6 presenteren we een gestandaardiseerd 4-staps protocol voor echografische beeldvorming en beoordeling van de proximale ACHP: het Shoulder PCHA pathology and digital Ischemia UltraSound (SPI-US) protocol. Internationale standaardisatie van beeldvorming van de ACHP zal bijdragen aan gerichte en nauwkeurige echografische beoordeling. Voordat het SPI-US protocol kan worden gebruikt voor ACHP beeldvorming moet de betrouwbaarheid worden bepaald. In hoofdstuk 7 testen we de betrouwbaarheid van het SPI-US protocol voor ACHP en ABP bloedvat-diameter bepaling. Bij 32 gezonde vrijwilligers werd door twee ervaren vaatlaboranten onafhankelijk van elkaar de diameter van de ACHP en ABP bepaald met behulp van het SPI-US protocol. De resultaten laten zien dat het SPI-US protocol accurate, precieze en vaatlaborantonafhankelijke diameter bepaling van de ACHP (ICC 0,70; 95%BI 0,50-0,83) en ABP (ICC 0,60; 95%BI 0,30-0,80) mogelijk maakt. Bovendien is de Minimaal Waarneembare Verandering (MWV) van 0,90 mm zo klein dat het SPI-US protocol bruikbaar is voor opsporing van ACHP aneurysma s. Dit protocol maakt het mogelijk om zowel in een klinische setting, als bij periodiek preventief medisch onderzoek op locatie, ACHP letsel te detecteren. Het eerste doel van hoofdstuk 8 was om de prevalentie van ACHP aneurysma s in de dominante schouder bij topvolleyballers te bepalen. De tweede doelstelling was om de anatomie, het aftakkingspatroon, het beloop en de diameters van de ACHP en ABP te beschrijven. Bij 280 topzaal- en topbeachvolleyballers werden de ACHP en ABP in de dominante schouder onderzocht met behulp van het SPI-US protocol. De ACHP werd in 100% van de gevallen gevonden in de okselplooi. Een aneurysma van de proximale ACHP werd gevonden bij 13 van de 280 topvolleyballers (4,6%) en bleek gerelateerd aan een specifiek aftakkingstype, namelijk een ACHP die rechtstreeks van de bovenarmslagader aftakt. De ACHP bleek in 81% (228/280) van de gevallen direct uit de bovenarmslagader te ontspringen, en vertoonde in 93% (211/228) van deze gevallen een gekromd verloop naar achteren (dorsaal) richting de opperarmbeenkop (caput humeri). De gemiddelde diameter van de ACHP was 3,8 mm (95%BI 3,7-3,9) bij mannen en 3,5 mm (95%BI 3,3-3,7) 206 I Chapter 12

210 bij vrouwen. De ABP werd in 93% (260/280) van de gevallen gevonden in de okselplooi, allen zonder aneurysma s. De ABP bleek in 73% (190/260) van deze gevallen direct uit de bovenarmslagader te ontspringen, en vertoonde in 93% (177/190) van deze gevallen een recht verloop parallel aan de bovenarmslagader. De gemiddelde diameter van de ABP was 2,3 mm (95%BI 2,2-2,3) bij mannen en 3,5 mm (95%BI 3,3-3,7) bij vrouwen. De beschreven vaatkarakteristieken en diameters kunnen worden gebruikt om accurate echografische identificatie en beoordeling van de ACHP en ABP te vergemakkelijken. De hoge prevalentie van gevonden ACHP aneurysma s bij topvolleyballers vraagt om actief beleid op het gebied van periodiek preventief medisch onderzoek. Deel III Medisch handelen Het vergroten van de bekendheid van dit vasculaire letsel onder medische professionals door verspreiding van kennis zal herkenning bevorderen. Dit is belangrijk om te voorkomen dat er een vergevorderd stadium van de ziekte ontstaat met ernstige schade in de slaghand als gevolg van zuurstoftekort. Operaties van de ACHP leiden tot enkele maanden revalidatie en onvermogen om te volleyballen. Als een ACHP aandoening in een vroeg stadium wordt ontdekt, dan is het wellicht mogelijk om trombo-embolieën in de slaghand, onherstelbare weefselschade en ook een operatieve ingreep aan de ACHP te voorkomen. Aangezien volleyballers risico lopen op het ontwikkelen van kritiek zuurstoftekort in de vingers is het noodzakelijk om de aanwezigheid van ACHP letsel in de dominante schouder te bepalen. Als bovendien duidelijk wordt welke risicofactoren er zijn, kan ook aan preventie worden gewerkt. Uiteindelijk zou het opstellen van individuele risicoprofielen het klinisch beleid kunnen ondersteunen. De doelstelling van hoofdstuk 9 was viervoudig namelijk het bepalen van: (1) de prevalentie van ACHP letsel in de dominante schouder bij topvolleyballers; (2) de relatie tussen ACHP letsel en symptomen van ischemische vingers in de slaghand; (3) de relatie tussen ACHP letsel en kenmerken van persoon, sport en werk; en (4) het opstellen van individuele risicoprofielen voor medisch handelen bij ACHP letsel. Tweehonderdachtenzeventig topzaal- en topbeachvolleyballers vulden eerst de SPI-Q vragenlijst in, waarna vervolgens de ACHP in de dominante schouder onderzocht werd op verwijding en occlusie (verstopping) met behulp van het SPI-US protocol. ACHP letsel werd gevonden bij 17 volleyballers (6,1%). Van de 278 deelnemers rapporteerden er 96 symptomen van ischemische vingers, die opmerkelijk genoeg niet bleken samen te hangen met de ACHP letsel (OR 0,39; 95%BI 0,13-1,13). Een totale duur van de volleybalcarrière van 17 jaar of meer en een leeftijd van 27 jaar of ouder verhoogden respectievelijk met 9x (OR 9,21; 90%BI 1,61-52,63) en met 14x (OR 13,61; 90%BI 2,43-76,40) het risico op ACHP letsel. Op basis van de combinatie van de aanwezigheid van (1) met echografie gevonden ACHP letsel (US+ of US ) en (2) symptomen van ischemische vingers vastgesteld met de vragenlijst (Q+ or Q ) konden vier risicoprofielen voor topvolleyballers worden opgesteld, namelijk I) 1,1% US+Q+ (n=3), II) 5,0% US+Q (n=14), III) 33,5% US Q+ (n=93), 12 Samenvatting I 207

211 en IV) 60,4% US Q (n=168). Om de zorg rondom deze potentieel vinger-bedreigende blessure te optimaliseren zijn per risicoprofiel aanbevelingen voor medisch handelen voorgesteld, bijvoorbeeld periodiek preventief medisch onderzoek met behulp van de SPI-Q en het SPI-US protocol en verwijzing naar de vaatchirurg. Hoofdstuk 10 beschrijft een casus van een 34-jarige mannelijke topvolleyballer met symptomatische trombo-embolieën in de slaghand en een ten dele getromboseerd ACHP aneurysma in zijn dominante schouder. Bij follow-up na 15 maanden, waarin hij gestopt was met volleyballen, was de bloeddruk in de vingers vrijwel genormaliseerd. Ook liet een nieuw Magnetische Resonantie Angiografie (MRA) protocol zien dat het ACHP aneurysma onveranderd was en dat de trombo-embolieën in de bloedvaten van de slaghand opgelost waren. De bloedvaten lieten wel restschade zien. Deze patiëntbeschrijving (n=1) laat als eerste bemoedigende resultaten zien voor een conservatief beleid als alternatief voor invasieve behandeling van dit vasculair overbelastingsletsel in de schouder. 208 I Chapter 12

212 12.2 CONCLUSIES Deel I Symptomen en risicofactoren (Hoofdstukken 2-5) Van de topzaal- en topbeachvolleyballers die een vragenlijst invulden rapporteerde respectievelijk 31% en 38% symptomen van koude en ontkleurde vingers in de slaghand tijdens of direct na het volleyballen. De lengte van de volleybalcarrière, de frequentie waarmee krachttraining wordt uitgevoerd en het vrouwelijk geslacht zijn gerelateerd aan een verhoogd risico op deze symptomen (Tabel 1). Deze symptomen en risicofactoren van ischemische vingers, die geassocieerd zijn met ACHP letsel, kunnen bevraagd worden met de Shoulder PCHA pathology and digital Ischemia Questionnaire (SPI-Q) vragenlijst: een betrouwbaar instrument voor het detecteren van topvolleyballers met symptomen van ischemische vingers in de slaghand en voor het inschatten van de ernst van deze symptomen. Tabel 1 Overzicht van de belangrijkste resultaten van Hoofdstukken 2, 3, 5 (Deel I), en 9 (Deel III) Prevalentie Samenhangende risicofactoren Totaal Zaal Beach Beach Verhoogd risico Symptomen van ischemische vingers PCHA pathologie 35% 31% 23% 50% Zaalvolleybal: volleybalcarrière van 18 jaar* frequentie van krachttraining om kracht te vergroten* Beachvolleybal: volleybalcarrière van 14 jaar* vrouwelijk geslacht 6,1% 6,0% 7,7% 5,7% volleybalcarrière van 17 jaar * leeftijd van 27 jaar* 7-voudig 3-voudig 4-voudig 5-voudig 9-voudig 14-voudig * dosis-respons relatie aanwezig DEEL II Beeldvorming (Hoofdstukken 6-8) Standaardisatie van echografisch ACHP onderzoek met behulp van het Shoulder PCHA pathology and digital Ischemia UltraSound (SPI-US) protocol, gecombineerd met gedetailleerde kennis van ACHP en ABP vaatkarakteristieken en diameters, maakte gerichte, accurate en precieze diameter metingen mogelijk, alsmede detectie van ACHP aneurysma s (Tabel 2). Een aneurysma van de ACHP werd gevonden bij 4,6% van de onderzochte topvolleyballers en bleek gerelateerd aan een specifiek aftakkingstype, namelijk een ACHP die rechtstreeks van de bovenarmslagader aftakt. 12 Conclusies I 209

213 Tabel 2 Overzicht van de belangrijkste resultaten van Hoofdstukken 7 en 8 (Deel II) ACHP ABP ICC van diameter meting 0,70 (95%BI 0,50-0,83) 0,60 (95%BI 0,30-0,80) SM 0,32 mm 0,29 mm MWV 0,90 mm 0,80 mm Aneurysma s Ja (4,6% prevalentie) Nee Aneurysma s bij anatomische varianten Locatie van aneurysma s Nee Proximaal (binnen 1,5 cm van origo) Nee n.v.t. Aanwezigheid in okselplooi Altijd aanwezig Vaak aanwezig (afwezig bij 7% van de gevallen) Direct uit de AA aftakkend 81% van de gevallen 75% van de gevallen Locatie van origo Verloop bij origo Dorsaal van de AA, proximaal van de ABP Gekromd richting de dorsale zijde van de humerus Dorsaal van de AA, distaal van de ACHP Recht en parallel aan de AA Intra-individuele ratio >1,0 (ACHP dm / ABP dm) <1,0 (ABP dm / ACHP dm) Gemiddelde diameter (in mm) Gemiddelde diameter (gecorrigeerd voor BSA) 3,8 ( ) 3,5 ( ) 1,8 ( ) 1,8 ( ) 2,3 ( ) 2,0 ( ) 1,1 ( ) 1,1 ( ) Legenda: ICC, intra-class correlatie coëfficiënt; BI, betrouwbaarheidsinterval; SM, standaard meetfout; MWV, minimaal waarneembare verandering; AA, Arteria axillaris (bovenarmsslagader); mm, millimeter; cm, centimeter; dm, diameter;, mannen;, vrouwen; BSA, body surface area (lichaamsoppervlak); n.v.t., niet van toepassing Deel III Medisch handelen (Hoofdstukken 9 en 10) Om de zorg rondom deze potentieel vinger-bedreigende blessure te optimaliseren, en om onherstelbare weefselschade als gevolg van langdurig zuurstoftekort in de slaghand te voorkomen, zijn aanbevelingen voor medisch handelen opgesteld op basis van de aan- of afwezigheid van zowel ACHP letsel, samenhangende risicofactoren, en symptomen van ischemische vingers (Tabel 1 & 3). Conservatief beleid voor ACHP letsel met symptomatische trombo-embolieën in de slaghand liet bemoedigende resultaten voor herstel zien in een patiëntbeschrijving van een topvolleyballer. 210 I Chapter 12

214 Tabel 3 Overzicht van de belangrijkste resultaten van Hoofdstuk 9 (Deel III) Prevalentie Aanbevelingen voor medisch handelen US+Q+ 1,1% * Risico op onherstelbare weefselschade in de slaghand als gevolg van langdurig zuurstoftekort Verwijs naar de vaatchirurg voor beeldvorming en behandeling US+Q 5,0% * Risico op trombo-embolieën in de slaghand vanuit het ACHP aneurysma Jaarlijks echografische controle m.b.v. SPI-US protocol om progressie ACHP pathologie te evalueren Overleg met vaatchirurg bij vorming van trombus in ACHP Halfjaarlijkse controle met SPI-Q vragenlijst om het ontstaan van symptomen te evalueren en om de herkenning te bevorderen Overleg met vaatchirurg bij acuut ontstaan van symptomen of wanneer deze gepaard gaan met een verzwakte pols, bleekheid of temperatuurverschil tussen vingers van de slaghand US Q+ 33,5% * Overweeg andere oorzaken van symptomen van ischemische vingers ** Risico op ACHP pathologie neemt toe met de carrièreduur Jaarlijkse controle met SPI-Q vragenlijst om de ernst van symptomen te evalueren Overleg met vaatchirurg bij acute verergering van symptomen of wanneer deze gepaard gaan met een verzwakte pols, bleekheid of temperatuurverschil tussen vingers van de slaghand US Q 60,4% * Risico op ACHP pathologie wanneer symptomen van ischemische vingers ontstaan en bij toename van de carrièreduur Tweejaarlijkse controle met SPI-Q vragenlist om het ontstaan van symptomen te evalueren en om de herkenning te bevorderen Overleg met vaatchirurg bij acuut ontstaan van symptomen of wanneer deze gepaard gaan met een verzwakte pols, bleekheid of temperatuurverschil tussen vingers van de slaghand Legenda: US+/, aan- of afwezigheid van ACHP pathologie in de dominante schouder bij echografisch onderzoek met behulp van het SPI-US protocol; Q+/, aan- of afwezigheid van symptomen van ischemische vingers in de slaghand bij onderzoek met de SPI-Q vragenlijst 12 Conclusies I 211

215

216 REFERENCES

217

218 REFERENCES 1. Aagaard H, Scavenius M, Jørgensen U. An epidemiological analysis of the injury pattern in indoor and in beach volleyball. Int J Sports Med. 1997;18(03): doi: /s Arko FR, Harris EJ, Zarins CK, Olcott C. Vascular complications in high-performance athletes. J Vasc Surg. 2001;33(5): doi: /mva Atema JJ, Ünlü Ç, Reekers JA, Idu MM. Posterior circumflex humeral artery injury with distal embolisation in professional volleyball players: a discussion of three cases. Eur J Vasc Endovasc Surg. 2012;44(2): doi: /j.ejvs Augustsson SR, Augustsson J, Thomeé R, Svantesson U. Injuries and preventive actions in elite Swedish volleyball. Scand J Med Sci Sports. 2006;16(6): doi: /j x. 5. Bagoji IB, Hadimani GA, Bannur BM, Patil BG, Bharatha A. A unique branching pattern of the axillary artery: a case report. J Clin Diagn Res. 2013;7(12): doi: / JCDR/2013/ Bahr R. No injuries, but plenty of pain? On the methodology for recording overuse symptoms in sports. Br J Sports Med. 2009;43(13): doi: /bjsm Bahr R, Krosshaug T. Understanding injury mechanisms: a key component of preventing injuries in sport. Br J Sports Med. 2005;39(6): doi: /bjsm Bahr R, Lian O, Bahr IA. A twofold reduction in the incidence of acute ankle sprains in volleyball after the introduction of an injury prevention program: a prospective cohort study. Scand J Med Sci Sports. 1997;7(3): doi: /j tb00135.x. 9. Bahr R, Reeser JC. Injuries among world-class professional beach bolleyball players the Fédération Internationale de Volleyball beach volleyball injury study. Am J Sports Med. 2003;31(1): doi: /j Bartelink ML, Wollersheim H, van de Lisdonk E, Spruijt R, van Weel C. Prevalence of Raynaud s phenomenon. Neth J Med. 1992;41(3-4): Bastiaansen CA, Jochems AAF, Tervoort MJ, Jüngen IJD. Body temperature and thermoregulation. In: Fysiologie En Anatomie [Physiology and Anatomy]. 1st ed. Houten: Bohn Stafleu van Loghum; 2007: Baumgarten KM, Dines JS, Winchester PA, et al. Axillary artery aneurysm with distal embolization in a major league baseball pitcher. Am J Sports Med. 2007;35(4): doi: / R 13. Beers L. Posterior circumflex humeral artery injury: a systematic review on risk factors in work and sports. Bachelorthesis Academic Medical Center Nov Supervisors: Kuijer PPFM, van de Pol D, Daams JG, Maas M. 14. Block JA, Sequeira W. Raynaud s phenomenon. The Lancet. 2001;357(9273): doi: /s (00) References I 215

219 15. Brennan PF, Hays BJ. The kappa statistic for establishing interrater reliability in the secondary analysis of qualitative clinical data. Res Nurs Health. 1992;15(2): doi: / nur Briner WWJ, Kacmar L. Common injuries in volleyball. Mechanisms of injury, prevention and rehabilitation. Sport Med. 1997;24(1): Brown SA, Doolittle DA, Bohanon CJ, et al. Quadrilateral Space Syndrome. Mayo Clin Proc. 2015;90(3): doi: /j.mayocp Bruton A, Conway JH, Holgate ST. Reliability: what is it, and how is it measured? Physiotherapy. 2000;86(2): doi: /s (05) Buckhout BC, Warner MA. Digital perfusion of handball players. Effects of repeated ball impact on structures of the hand. Am J Sports Med. 1980;8(3): doi: / Çavdar S, Zeybek A, Bayramiçli M. Rare variation of the axillary artery. Clin Anat. 2000;13(1): doi: /(sici) (2000)13:1<66::aid-ca8>3.0.co;2-m. 21. Chloros GD, Smerlis NN, Li Z, Smith TL, Smith BP, Koman LA. Noninvasive evaluation of upper-extremity vascular perfusion. J Hand Surg. 2008;33(4): doi: /j. jhsa Conijn AP, Loukachov VV, Bipat S, Koelemay MJW. Test retest reliability and measurement error are excellent for the Dutch version of the VascuQol questionnaire in patients with intermittent claudication. Eur J Vasc Endovasc Surg. 2015;50(4): doi: /j. ejvs Conn JJ, Bergan JJ, Bell JL. Hypothenar hammer syndrome: posttraumatic digital ischemia. Surgery. 1970;68(6): `. 24. Descatha A, Roquelaure Y, Chastang J-F, Evanoff B, Cyr D, Leclerc A. Description of outcomes of upper-extremity musculoskeletal disorders in workers highly exposed to repetitive work. J Hand Surg. 2009;34(5): doi: /j.jhsa Du Bois D, Du Bois EF. A formula to estimate the approximate surface area if height and weight be known Nutrition. 1989;5(5): Durham JR, Yao JST, Pearce WH, Nuber GM, McCarthy WJ. Arterial injuries in the thoracic outlet syndrome. J Vasc Surg. 1995;21(1): doi: /s (95)70244-x. 27. Duwayri YM, Emery VB, Driskill MR, et al. Positional compression of the axillary artery causing upper extremity thrombosis and embolism in the elite overhead throwing athlete. J Vasc Surg. 2011;53(5): doi: /j.jvs Fleiss JL. Design and Analysis of Clinical Experiments. 1 edition. New York: Wiley- Interscience; Fleiss JL. Repeated measurements studies. In: The Design and Analysis of Clinical Experiments. John Wiley & Sons, Inc.; 1999: I References

220 30. Frans FA, Nieuwkerk PT, Met R, et al. Statistical or clinical improvement? Determining the minimally important difference for the Vascular Quality of Life questionnaire in patients with critical limb ischemia. Eur J Vasc Endovasc Surg. 2014;47(2): doi: /j. ejvs Frans FA, van Wijngaarden SE, Met R, Koelemay MJW. Validation of the Dutch version of the VascuQol questionnaire and the Amsterdam linear disability score in patients with intermittent claudication. Qual Life Res. 2012;21(8): doi: /s z. 32. Galland RB, Magee TR. Popliteal aneurysms: distortion and size related to symptoms. Eur J Vasc Endovasc Surg. 2005;30(5): doi: /j.ejvs Gelabert HA, Machleder HI. Diagnosis and management of arterial compression at the thoracic outlet. Ann Vasc Surg. 1997;11(4): doi: /s Gellhorn AC, Carlson MJ. Inter-rater, intra-rater, and inter-machine reliability of quantitative ultrasound measurements of the patellar tendon. Ultrasound Med Biol. 2013;39(5): doi: /j.ultrasmedbio Gouttebarge V, Plat M-CJ, Kuijer PPFM, Sluiter JK, Frings-Dresen MHW. The reproducibility of two task-specific functional capacity evaluation protocols for household waste collectors. Work. 2015;51(2): doi: /wor Gouttebarge V, Wind H, Kuijer PPFM, Frings-Dresen MH. Reliability and validity of functional capacity evaluation methods: a systematic review with reference to Blankenship system, Ergos work simulator, Ergo-Kit and Isernhagen work system. Int Arch Occup Env Health. 2004;77(8): doi: /s Gouttebarge V, Wind H, Kuijer PPFM, Sluiter JK, Frings-Dresen MH. Reliability and agreement of 5 Ergo-Kit functional capacity evaluation lifting tests in subjects with low back pain. Arch Phys Med Rehabil. 2006;87(10): doi: /j.apmr Grams ST, von Saltiél R, Mayer AF, et al. Assessment of the reproducibility of the indirect ultrasound method of measuring diaphragm mobility. Clin Physiol Funct Imaging. 2014;34(1): doi: /cpf Greenspan JD, Craft RM, LeResche L, et al. Studying sex and gender differences in pain and analgesia: a consensus report. Pain. 2007;132:S26-S45. doi: /j.pain Grens K. Artery injury signs common in pro volleyballers. Reuters Health. September article/2012/09/07/us-artery-volleyball -idinbre88617t ?feedtype =RSS&feedName=health. 41. de Groot P. Smashen tot vingers blauw zien. Wegener Nieuws Media. September 17, R 42. Hall HA, Minc S, Babrowski T. Peripheral artery aneurysm. Surg Clin North Am. 2013;93(4): doi: /j.suc Hattori Y, Doi K, Sakamoto S, Satbhai N. Anatomic variations in branching patterns of the axillary artery: a multidetector-row computed tomography angiography study. J Reconstr Microsurg. 2013;29(08): doi: /s References I 217

221 44. Higgins JP, McClinton MA. Vascular insufficiency of the upper extremity. J Hand Surg. 2010;35(9): doi: /j.jhsa Hill AB. The environment and disease: association or causation? Proc R Soc Med. 1965;58: Ho PK, Dellon AL, Wilgis EF. True aneurysms of the hand resulting from athletic injury. Report of two cases. Am J Sports Med. 1985;13(2): doi: / Ikezawa T, Iwatsuka Y, Asano M, Kimura A, Sasamoto A, Ono Y. Upper extremity ischemia in athletes: embolism from the injured posterior circumflex humeral artery. Int J Angiol. 2000;9(3): doi: /bf Itoh Y, Wakano K, Takeda T, Murakami T. Circulatory disturbances in the throwing hand of baseball pitchers. Am J Sports Med. 1987;15(3): doi: / Jackson MR. Upper extremity arterial injuries in athletes. Semin Vasc Surg. 2003;16(3): doi: /s (03) Johnston KW, Rutherford RB, Tilson MD, Shah DM, Hollier L, Stanley JC. Suggested standards for reporting on arterial aneurysms. J Vasc Surg. 1991;13(3): doi: / mva Junge A, Langevoort G, Pipe A, et al. Injuries in team sport tournaments during the 2004 Olympic Games. Am J Sports Med. 2006;34(4): doi: / Kalashyan H, Shuaib A, Gibson PH, et al. Single sweep three-dimensional carotid ultrasound: Reproducibility in plaque and artery volume measurements. Atherosclerosis. 2014;232(2): doi: /j.atherosclerosis Kane KY, Shutze WP, Vines T, Pearl GJ. Duplex-guided diagnosis and surgical repair of a posterior circumflex humeral artery aneurysm in a Major League Baseball pitcher. J Vasc Ultrasound. 2013;37(3): Kappa as a Measure of Concordance in Categorical Sorting: kappa.html. Accessed Kee ST, Dake MD, Wolfe-Johnson B, Semba CP, Zarins CK, Olcott C 4th. Ischemia of the throwing hand in major league baseball pitchers: embolic occlusion from aneurysms of axillary artery branches. J Vasc Interv Radiol. 1995;6(6): doi: /s (95) Koch C, Tilp M. Beach volleyball techniques and tactics: a comparison of male and female playing characteristics. Kinesiology. 2009;41: Kostianen S, Orava S. Blunt injury of the radial and ulnar arteries in volleyball players. A report of three cases of the antebrachial-palmar hammer syndrome. Br J Sports Med. 1983;17(3): doi: /bjsm Kottner J, Audige L, Brorson S, et al. Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were proposed. Int J Nurs Stud. 2011;48(6): doi: /j. ijnurstu I References

222 59. Kugler A, Krüger-Franke M, Reininger S, Trouillier HH, Rosemeyer B. Muscular imbalance and shoulder pain in volleyball attackers. Br J Sports Med. 1996;30(3): doi: / bjsm Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33(1): doi: / Lee JT, Chandra V, McAdams T, Olcott C. Axillary branch artery aneurysms: a rare cause of upper extremity ischemia in high-performance athletes. J Vasc Surg. 2012;56(2):581. doi: /j.jvs Lim CS, Gohel MS, Shepherd AC, Davies AH. Iliac artery compression in cyclists: mechanisms, diagnosis and treatment. Eur J Vasc Endovasc Surg. 2009;38(2): doi: /j. ejvs Lindholt JS, Vammen S, Juul S, Henneberg EW, Fasting H. The validity of ultrasonographic scanning as screening method for abdominal aortic aneurysm. Eur J Vasc Endovasc Surg. 1999;17(6): doi: /ejvs Maas M, van Delden OM, Reekers JA. [Sports-related vascular problems in the shoulder: role for angiography and endovascular therapy] [article in Dutch]. Geneeskd en Sport. 2004;37(1): Massada M, Aido R, Magalhaes C, Puga N. Hypothenar hammer syndrome in a middle blocker a case report and brief review. Br J Sports Med. 2011;45:549. doi: / bjsm McCarthy WJ, Yao JST, Schafer MF, et al. Upper extremity arterial injury in athletes. J Vasc Surg. 1989;9(2): doi: / (89) McClelland D, Paxinos A. The anatomy of the quadrilateral space with reference to quadrilateral space syndrome. J Shoulder Elbow Surg. 2008;17(1): doi: /j. jse McIntosh A, Hassan I, Cherry K, Dahm D. Posterior circumflex humeral artery aneurysm in 2 professional volleyball players. Am J Orthop Belle Mead NJ. 2006;35(1): Mechelen W, Hlobil H, Kemper HC. Incidence, severity, aetiology and prevention of sports injuries. A review of concepts. Sports Med. 1992;14(2): doi: / Melchior M, Roquelaure Y, Evanoff B, et al. Why are manual workers at high risk of upper limb disorders? The role of physical work factors in a random sample of workers in France (the Pays de la Loire study). Occup Environ Med. 2006;63(11): doi: / oem R 71. Mochizuki T, Isoda H, Masui T, et al. Occlusion of the posterior humeral circumflex artery: detection with MR angiography in healthy volunteers and in a patient with quadrilateral space syndrome. Am J Roentgenol. 1994;163(3): doi: /ajr References I 219

223 72. Mokkink LB, Terwee CB, Patrick DL, et al. The COSMIN checklist for assessing the methodological quality of studies on measurement properties of health status measurement instruments: an international Delphi study. Qual Life Res. 2010;19(4): doi: / s de Mooij T, Duncan AA, Kakar S. Vascular injuries in the upper extremity in athletes. Hand Clin. 2015;31(1): doi: /j.hcl Morgan MBF, Crayford T, Murrin B, Fraser SCA. Developing the Vascular Quality of Life Questionnaire: a new disease-specific quality of life measure for use in lower limb ischemia. J Vasc Surg. 2001;33(4): doi: /mva Mosley JG. Arterial problems in athletes. Br J Surg. 2003;90(12): doi: / bjs Naveen K, Jyothsna P, Nayak SB, et al. Variant origin of an arterial trunk from axillary artery continuing as profunda brachii artery - a unique arterial variation in the axilla and its clinical implications. Ethiop J Health Sci. 2014;24(1):93. doi: /ejhs.v24i Ndoye JM, Armstrong O, Rogez JM, Sow ML, Le Borgne J. [Update on lateral and medial spaces of the dorsal wall of the axillary fossa] [article in French]. Dakar Med. 2002;47(2): Nguyen LL, Moneta GL, Conte MS, Bandyk DF, Clowes AW, Seely BL. Prospective multicenter study of quality of life before and after lower extremity vein bypass in 1404 patients with critical limb ischemia. J Vasc Surg. 2006;44(5): doi: /j.jvs Nuber GW, McCarthy WJ, Yao JST, Schafer MF, Suker JR. Arterial abnormalities of the shoulder in athletes. Am J Sports Med. 1990;18(4): doi: / Olinger A, Benninger B. Branching patterns of the lateral thoracic, subscapular, and posterior circumflex humeral arteries and their relationship to the posterior cord of the brachial plexus. Clin Anat. 2010;23(4): doi: /ca Palao JM, Gutiérrez D, Frideres JE. Height, weight, Body Mass Index, and age in beach volleyball players in relation to level and position. J Sports Med Phys Fitness. 2008;48(4): Palao JM, Valades D, Ortega E. Match duration and number of rallies in men s and women s FIVB world tour beach volleyball. J Hum Kinet. 2012;34(1). doi: /v Pedersen OM, Aslaksen A, Vik-Mo H. Ultrasound measurement of the luminal diameter of the abdominal aorta and iliac arteries in patients without vascular disease. J Vasc Surg. 1993;17(3): doi: /mva Planken RN, Keuter XHA, Hoeks APG, et al. Diameter measurements of the forearm cephalic vein prior to vascular access creation in end-stage renal disease patients: graduated pressure cuff versus tourniquet vessel dilatation. Nephrol Dial Transplant. 2006;21(3): doi: /ndt/gfi I References

224 85. Planken RN, Keuter XH, Kessels AG, Hoeks AP, Leiner T, Tordoir JH. Forearm cephalic vein cross-sectional area changes at incremental congestion pressures: towards a standardized and reproducible vein mapping protocol. J Vasc Surg. 2006;44(2): doi: /j. jvs Pleumeekers HJCM, Hoes AW, Mulder PGH, et al. Differences in observer variability of ultrasound measurements of the proximal and distal abdominal aorta. J Med Screen. 1998;5(2): doi: /jms van de Pol D, Alaeikhanehshir S, Kuijer PPFM, et al. Reproducibility of the SPI-US protocol for ultrasound diameter measurements of the Posterior Circumflex Humeral Artery and Deep Brachial Artery: an inter-rater reliability study. Eur Radiol [Epub ahead of print]. doi:0.1007/s van de Pol D, Alaeikhanehshir S, Maas M, Kuijer PPFM. Self-reported symptoms and risk factors for digital ischaemia among international world-class beach volleyball players. J Sports Sci. 2015;5:1-7 [Epub ahead of print]. doi: / van de Pol D, Kuijer PPFM, Langenhorst T, Maas M. High prevalence of self-reported symptoms of digital ischemia in elite male volleyball players in the Netherlands: a cross-sectional national survey. Am J Sports Med. 2012;40(10): doi: / van de Pol D, Kuijer PPFM, Langenhorst T, Maas M. Risk factors associated with self-reported symptoms of digital ischemia in elite male volleyball players in the Netherlands. Scand J Med Sci Sports. 2014;24(4):e230-e237. doi: /sms van de Pol D, Kuijer PPFM, Terpstra A, et al. The international SPIKE study on Posterior Circumflex Humeral Artery pathology among elite volleyball players: four profiles for clinical management (4P4M). 2015:Manuscript submitted for publication. 92. van de Pol D, Maas M, Terpstra A, et al. Ultrasound assessment of the Posterior Circumflex Humeral Artery in elite volleyball players: aneurysm prevalence, anatomy, branching pattern and vessel characteristics. Eur Radiol. 2016:Conditionally accepted. 93. van de Pol D, Maas M, Terpstra A, Pannekoek-Hekman MJC, Kuijer PPFM, Planken RN. B-mode ultrasound assessment of the Posterior Circumflex Humeral Artery - the SPI-US protocol: a technical procedure in 4-steps. J Ultrasound Med. 2015;Accepted. doi: / ultra van de Pol D, Zacharian T, Maas M, Kuijer PPFM. Test-retest reliability of the SPI- Questionnaire to detect symptoms of digital ischemia in elite volleyball players. 2015:Manuscript submitted for publication. 95. Reekers JA, den Hartog BM, Kuyper CF, Kromhout JG, Peeters FL. Traumatic aneurysm of the posterior circumflex humeral artery: a volleyball player s disease? J Vasc Interv Radiol. 1993;4(3): doi: /s (93) R 96. Reekers JA, Koedam N. Re: Volleyball-related ischemia of the hand. Cardiovasc Intervent Radiol. 1998;21(3):261. doi: /s References I 221

225 97. Reeser JC. Diagnosis and management of vascular injuries in the shoulder girdle of the overhead athlete. Curr Sports Med Rep. 2007;6(5): doi: /s Reeser JC. Introduction: a brief history of the sport of volleyball. In: J.C. Reeser & R. Bahr (Eds.). In: Handbook of Sports Medicine and Science: Volleyball. Chichester: Wiley; 2008: Reeser JC, Joy EA, Porucznik CA, Berg RL, Colliver EB, Willick SE. Risk factors for volleyball-related shoulder pain and dysfunction. PM&R. 2010;2(1): doi: /j. pmrj Reeser JC, Verhagen E, Briner WW, Askeland TI, Bahr R. Strategies for the prevention of volleyball related injuries. Br J Sports Med. 2006;40(7): doi: / bjsm Reutter D, Husmann M, Thalhammer C, et al. The pitcher-syndrom: aneurysm of the posterior circumflex humeral artery - a rare source for upper limb ischemia. Vasa. 2010;39: doi: /eurheartj/ehq Robinson DJ, Marks P, Schneider-Kolsky ME. Occlusion and stenosis of the posterior circumflex humeral artery: detection with ultrasound in a normal population. J Med Imaging Radiat Oncol. 2011;55(5): doi: /j x Robinson DJ, Marks P, Schneider-Kolsky ME. Ultrasound of the posterior circumflex humeral artery. J Med Imaging Radiat Oncol. 2010;54(3): doi: /j x Rohrer MJ, Cardullo PA, Pappas AM, Phillips DA, Wheeler HB. Axillary artery compression and thrombosis in throwing athletes. J Vasc Surg. 1990;11(6): doi: / (90)90071-h Rosi G, Pichot O, Bosson JL, Calabrese G, Carpentier P. Echographic and Doppler screening of the forearm arteries in professional volleyball players. Am J Sports Med. 1992;20(5): doi: / Schelvis RM, Oude Hengel KM, Burdorf A, Blatter BM, Strijk JE, van der Beek AJ. Evaluation of occupational health interventions using a randomized controlled trial: challenges and alternative research designs. Scand J Work Environ Health. 2015;41(5): doi: / sjweh Schep G, Bender MH, van de Tempel G, de Vries WR, Eikelboom BC. Detection and treatment of claudication due to functional iliac obstruction in top endurance athletes: a prospective study. Lancet. 2002;359(9305): doi: /s (02) Schneider K, Kasparyan NG, Altchek DW, Fantini GA, Weiland AJ. An aneurysm involving the axillary artery and its branch vessels in a Major League Baseball pitcher - a case report and review of the literature. Am J Sports Med. 1999;27(3): doi: / Seinturier C, Blaise S, Maufus M, Magne J-L, Pasquier B, Carpentier P-H. [A rare cause of embolic ischemia of the hand: an isolated aneurism of a branch of the axillary artery] [article in French]. J Mal Vasc. 2008;33(4-5): doi: /j.jmv I References

226 110. Seminati E, Minetti AE. Overuse in volleyball training/practice: a review on shoulder and spine-related injuries. Eur J Sport Sci. 2013;13(6): doi: / Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86(2): doi: / Sim J, Wright CC. The kappa statistic in reliability studies: use, interpretation, and sample size requirements. Phys Ther. 2005;85(3): Sluiter JK, Rest KM, Frings-Dresen MH. Criteria document for evaluating the workrelatedness of upper-extremity musculoskeletal disorders. Scand J Work Environ Health. 2001;27(1): doi: /sjweh Solgård L, Nielsen AB, Møller-Madsen B, Jacobsen BW, Yde J, Jensen J. Volleyball injuries presenting in casualty: a prospective study. Br J Sports Med. 1995;29(3): doi: /bjsm Stänz K, Wedler V, Köpfli P, Künzi W, Pfammatter T. [Compression syndrome of the arteria circumflexa humeri posterior in a volleyball player] [article in German]. Vasa. 2001;30(3): Sugawara M, Ogino T, Minami A, Ishii S. Digital ischemia in baseball players. Am J Sports Med. 1986;14(4): doi: / Suter LG, Murabito JM, Felson DT, Fraenkel L. The incidence and natural history of Raynaud s phenomenon in the community. Arthritis Rheum. 2005;52(4): doi: / art Terwee CB, Bot SDM, de Boer MR, et al. Quality criteria were proposed for measurement properties of health status questionnaires. J Clin Epidemiol. 2007;60(1): doi: /j. jclinepi Tilp M, Wagner H, Müller E. Differences in 3D kinematics between volleyball and beach volleyball spike movements. Sports Biomech. 2008;7(3): doi: / Todd GJ, Benvenisty AI, Hershon S, Bigliani LU. Aneurysms of the mid axillary artery in major league baseball pitchers - a report of two cases. J Vasc Surg. 1998;28(4): doi: /s (98) Vanbelle S. A New Interpretation of the Weighted Kappa Coefficients. Psychometrika. 2014;[Epub ahead of print]:1-12. doi: /s Verhagen EALM, Beek AJV der, Bouter LM, Bahr RM, van Mechelen W. A one season prospective cohort study of volleyball injuries. Br J Sports Med. 2004;38(4): doi: /bjsm R 123. de Vet HC, Terwee CB, Knol DL, Bouter LM. When to use agreement versus reliability measures. J Clin Epidemiol. 2006;59(10): doi: /j.jclinepi de Vet HCW, Terwee CB, Mokkink LB, Knol DL. Reliability. In: Meausurement in Medicine. Cambridge: Cambridge University Press; 2011:pp References I 223

227 125. Visnes H, Bahr R. Training volume and body composition as risk factors for developing jumper s knee among young elite volleyball players: Training and body composition and jumper s knee. Scand J Med Sci Sports. 2013;23: doi: /j x Vlychou M, Spanomichos G, Chatziioannou A, Georganas M, Zavras GM. Embolisation of a traumatic aneurysm of the posterior circumflex humeral artery in a volleyball player. Br J Sports Med. 2001;35(2): doi: /bjsm Volckaert K, Geukens L, Peers K, Lysens R. [Thromboembolism of the posterior circumflex humeral artery in a professional volleyball player] [article in Dutch]. Tijdschr Voor Geneeskd. 2014;70(18): doi: /tvg de Vries M, Ouwendijk R, Kessels AG, et al. Comparison of generic and disease-specific questionnaires for the assessment of quality of life in patients with peripheral arterial disease. J Vasc Surg. 2005;41(2): doi: /j.jvs Wigley FM. Clinical practice. Raynaud s phenomenon. N Engl J Med. 2002;347(13): doi: /nejmcp Wikipedia. Volleyball spiking Wilson JMG, Jungner G. Principles and Practice of Screening for Disease. Geneva World Health Organ. 1968;Public Health Paper No. 34. doi: / _ Wolf YG, Kobzantsev Z, Zelmanovich L. Size of normal and aneurysmal popliteal arteries: a duplex ultrasound study. J Vasc Surg. 2006;43(3): doi: /j.jvs van der Worp H, van Ark M, Zwerver J, van den Akker-Scheek I. Risk factors for patellar tendinopathy in basketball and volleyball players: a cross-sectional study. Scand J Med Sci Sports. 2012;22(6): doi: /j x van der Worp H, Zwerver J, Kuijer PPFM, Frings-Dresen MH, van den Akker-Scheek I. The impact of physically demanding work of basketball and volleyball players on the risk for patellar tendinopathy and on work limitations. J Back Musculoskelet Rehabil. 2011;24(1): doi: /bmr Ye Y, Mauro M, Bovenzi M, Griffin MJ. Acute effects of mechanical shocks on finger blood flow: influence of shock repetition rate and shock magnitude. Int Arch Occup Environ Health. 2012;85(6): doi: /s x. 224 I References

228

229

230 APPENDICES List of abbreviations List of publications PhD portfolio Dankwoord Curriculum vitae

231

232 LIST OF ABBREVIATIONS AA ABER ABP ACES ACHA ACHP AMC AV BI BSA CE-MRA CI cm CTA DBA DE DI dm DSA FIVB HHS ICC IOC IRB κ kg Loa LTA m 2 MDC MIC mm mm/m 2 MRA MWV n.a. Nevobo PCHA PCHAP axillary artery abduction and external rotation arteria brachialis profunda academic center of evidence based sports medicine anterior circumflex humeral artery arteria circumflexa humeri posterior academic medical center axillary vein betrouwbaarheidsinterval body surface area contrast-enhanced magnetic resonance angiography confidence interval centimetres computed tomography angiogram deep brachial artery distal embolization digital ischemia diameter digital subtraction angiography Fédération Internationale de VolleyBall hypothenar hammer syndrome intra-class correlation coefficient international Olympic committee institutional review board kappa kilogram limits of agreement lateral thoracic artery square meter minimal detectable change minimally important change millimetres millimetres per square meter magnetic resonance angiography maximaal waarneembare verandering not applicable Dutch volleyball association posterior circumflex humeral artery posterior circumflex humeral artery pathology A List of abbreviations I 229

233 POA PPG OR Q QoL QS QSS RVT SDC SEM SF-36 SM SPIKE SPI-Q SPI-US SSA TAA TOS US VARCOMP VascuQol WMO percentage of agreement photoplethysmography odds ratio questionnaire quality of life quadrilateral space quadrilateral space syndrome registered vascular technologist smallest detectable change standard error of measurement short form-36 standaard meetfout Shoulder PCHA pathology and digital Ischemia in Known Elite volleyball players Shoulder PCHA pathology and digital Ischemia Questionnaire Shoulder vascular Pathology with digital Ischemia UltraSound subscapular artery thoracoacromial artery thoracic outlet syndrome ultrasound variance components vascular quality of life medical research involving human subjects act 230 I Appendices

234 LIST OF PUBLICATIONS Publications in this thesis Van de Pol D, Kuijer PPFM, Langenhorst T, Maas M. High prevalence of self-reported symptoms of digital ischemia in elite male volleyball players in the Netherlands: a crosssectional national survey. American Journal of Sports Medicine 2012;40: doi: / Van de Pol D, Kuijer PPFM, Langenhorst T, Maas M. Risk factors associated with selfreported symptoms of digital ischemia in elite male volleyball players in the Netherlands. Scandinavian Journal of Medicine & Science in Sports 2014;24:e230-e237. doi: / sms Van de Pol D, Alaeikhanehshir S, Maas M, Kuijer PPFM. Self-reported symptoms and risk factors for digital ischaemia among international world-class beach volleyball players. Journal of Sports Sciences 2015;5:1-7. doi: / Van de Pol D, Alaeikhanehshir S, Kuijer PPFM, Terpstra A, Pannekoek-Hekman MJC, Planken RN*, Maas M*. Reproducibility of the SPI-US protocol for ultrasound diameter measurements of the Posterior Circumflex Humeral Artery and Deep Brachial Artery: an inter-rater reliability study. European Radiology [Epub ahead of print]. doi:0.1007/ s (*contributed equally) Van de Pol D, Maas M, Terpstra A, Pannekoek-Hekman MJC, Kuijer PPFM, Planken RN. B-mode ultrasound assessment of the Posterior Circumflex Humeral Artery - The SPI-US protocol: a technical procedure in 4-steps. Accepted for publication in The Journal of Ultrasound in Medicine. doi: /ultra Van de Pol D, Maas M, Terpstra A, Pannekoek-Hekman MJC, Alaeikhanehshir S, Kuijer PPFM, Planken RN. Ultrasound assessment of the Posterior Circumflex Humeral Artery in elite volleyball players: aneurysm prevalence, anatomy, branching pattern and vessel characteristics. Conditionally accepted for publication in European Radiology. Van de Pol D, Zacharian T, Maas M, Kuijer PPFM. Test-retest reliability of the SPI- Questionnaire to detect symptoms of digital ischemia in elite volleyball players. Submitted. A List of publications I 231

235 Van de Pol D, Kuijer PPFM, Terpstra A, Pannekoek-Hekman MJC, Alaeikhanehshir S, Bouwmeester O, Planken RN, Maas M. The international SPIKE study on Posterior Circumflex Humeral Artery pathology among elite volleyball players: four profiles for clinical management (4P4M). Submitted. Van de Pol D*, Planken RN*, Kuijer PPFM, Terpstra A, Pannekoek-Hekman MJC, Maas M. Conservative management of a vascular shoulder overuse injury in a professional volleyball player: use of novel MR Angiography in diagnosis and treatment follow-up. Submitted. (*contributed equally) Publications related to this thesis Van de Pol D, Kuijer PPFM, Langenhorst T, Maas M. Hoge prevalentie van zelfgerapporteerde koude en ontkleurde vingers bij mannelijke topvolleyballers in Nederland. Sport & Geneeskunde Beers L, Van de Pol D, Daams JG, Maas M, Kuijer PPFM. Posterior Circumflex Humeral Artery injury; a systematic review on risk factors in work and sports. Submitted. Bouwmeester O, van de Pol D, Kuijer PPFM, Alaeikhanehshir S, Terpstra A, Pannekoek- Hekman MJC, Planken RN, Maas M. Ultrasound imaging versus questionnaire survey for detection of Posterior Circumflex Humeral Artery pathology in elite volleyball players - A cross-sectional diagnostic accuracy study. Submitted. 232 I Appendices

236 PHD PORTFOLIO Name: Daan van de Pol PhD period: February 2015 December 2015 Promotors: Prof. dr. M. Maas Co-promotores: Dr. P.P.F.M. Kuijer, Dr. R.N. Planken PhD training Year Workload (ECTs) General courses Expert Management of Medical Literature Practical Biostatistics (not completed) Specific courses EPIC Course, OLVG West, Amsterdam Seminars, workshops and master classes Master Class Sports Medicine, Papendal th Symposium Impaired Mobility, Amsterdam MoveMed meeting, Amsterdam Oral presentations Maas Research meeting, AMC Amsterdam. Prevalence of symptoms of digital ischemia among elite volleyball players Maas Research meeting, AMC Amsterdam. Risk factors for symptoms of digital ischemia among elite volleyball players VSG sportwetenschappelijk jaarcongres, Ermelo. Opvallend hoog voorkomen van koude en ontkleurde vingers onder mannelijke topvolleyballers in Nederland Symposium Impaired Mobility, AMC Amsterdam. Topvolleybal: een slag voor de vaten Maas Research meeting, AMC Amsterdam. Is pathology of the posterior circumflex humeral artery associated with symptoms of digital ischemia? VSG sportwetenschappelijk jaarcongres, Ermelo. Verschilt beachvolleybal van zaalvolleybal voor de prevalentie en risicofactoren voor ischemische klachten bij professionals? Radiologendagen, Rotterdam. Ultrasound assessment of the posterior circumflex humeral artery in elite volleyball aneurysm prevalence, anatomy, branching pattern and vessel characteristics A PhD portfolio I 233

237 Maas Research meeting, AMC Amsterdam. Symptoms and risk factors among world-class beach volleyball players & the SPI-US protocol for diameter measurement of the PCHA Signaal bijeenkomst Nederlands Centrum voor Beroepsziekten, Coronel Instituut voor Arbeid & Gezondheid, AMC Amsterdam. SPIKE the PCHA Is there a causal relationship between overuse injury of the posterior circumflex humeral artery and elite volleyball? Onderzoek-refereerbijeenkomst Coronel Instituut voor Arbeid & Gezondheid, AMC Amsterdam. The international SPIKE study on posterior circumflex humeral artery pathology among elite volleyball players: four profiles for clinical management (4P4M) VSG sportwetenschappelijk jaarcongres, Eindhoven. The international SPIKE study: overbelastingsletsel van de arteria circumflexa humeri posterior bij topvolleyballers: prevalentie & risicofactoren Congress of Radiological Society of North America (RSNA), Chicago. Ultrasound assessment of the posterior circumflex humeral artery in elite volleyball aneurysm prevalence, anatomy, branching pattern and vessel characteristics Werkoverleg afdeling Radiologie, AMC Amsterdam. Ultrasound assessment of the posterior circumflex humeral artery in elite volleyball players Ultrasound in Focus, Ede. SPIKE the PCHA Ultrasound assessment of the posterior circumflex humeral artery in elite volleyball players Poster presentations Max Taks Vaatsymposium, Doetinchem. Echografische beoordeling van de arteria circumflexa humeri een gestandaardiseerd 4 stappen protocol in 10 minuten National and international conferences VSG sportwetenschappelijk jaarcongres, Ermelo VSG sportwetenschappelijk jaarcongres, Ermelo Max Taks Vaatsymposium, Doetinchem Radiologendagen - Rotterdam Signaal bijeenkomst Nederlands Centrum voor Beroepsziekten, Amsterdam VSG sportwetenschappelijk jaarcongres, Ermelo Congress of Radiological Society of North America (RSNA), Chicago Ultrasound in Focus, Ede I Appendices

238 Other Presentation: Elite beach volleybal an attack on the vessels? FIVB medical commission meeting, Lausanne, Switzerland by dr. Nau, orthopaedic surgeon Teaching Year Workload (ECTs) Lecturing Guest lecturer for 2nd year medical students at elective course Topsport, dans en muziek als werk, Academical Medical Centre, Amsterdam, the Netherlands Tutoring, Mentoring Sena Alaeikhanehshir, bachelortheses Do international elite male and female volleyball players differ regarding prevalence of ischemic symptoms in their dominant hand and associated personal and sportsrelated risk factors? Sena Alaeikhanehshir, scientifical internship Reproducibility of ultrasound diameter measurements of the posterior circumflex humeral artery and the deep brachial artery: an inter-rater reliability study Tigran Zacharian, scientifical internship Test-retest reliability of the Shoulder PCHA pathology and digital Ischemia Questionnaire (SPI-Q) in male elite volleyball players in the Netherlands Olivier Bouwmeester, bachelortheses Can ultrasound imaging be replaced by a questionnaire to detect posterior circumflex humeral artery pathology in elite volleyball players? Lisa Beers, scientifical internship Posterior circumflex humeral artery injury; a systematic review on risk factors in work and sports. Eva de Rye, bachelortheses Prevalence and risk factors for symptoms of digital ischemia in talented volleyball players Supervising Mark Broos, scientifical internship PET-CT & DWI for diagnosis and follow-up of disease activity in spondylodiscitis Other Profielwerkstuk SPIKE R. Neate & M. Langezaal, Leidsche Rijn College A PhD portfolio I 235

239

240 DANKWOORD De afgelopen jaren heb ik met veel plezier aan mijn onderzoek gewerkt. Graag wil ik iedereen bedanken die daar of één of andere manier aan bijgedragen heeft. Veel waardering gaat uit naar mijn vrienden en schoon-(familie) voor hun steun en interesse in mijn onderzoek. In het bijzonder wil ik de volgende mensen bedanken voor hun bijdrage aan dit proefschrift. Mijn promotor, prof. dr. M. Maas. Beste Mario, jij bent de geestelijk vader van dit proefschrift, en degene die altijd de grote lijnen en het brede perspectief in de gaten hield. Jij bent degene die mij de mogelijkheid hebt geboden om sportmedisch wetenschappelijk onderzoek te doen, en tevens het brein achter het hiervoor samengestelde team. Jij bent ook degene die mij overtuigd heeft om mijn succesvolle individuele onderzoeksstage voort te zetten in dit promotietraject, waar ik je heel dankbaar voor ben. De brainstormsessies in jouw kamer hebben dit proefschrift gevormd en resulteerden vaak in veel antwoorden en nog meer nieuwe ideeën. Als ik onder Pauls begeleiding weer eens tien versies van een artikel had geschreven, dan was jij altijd degene die met een scherpe en kritische blik (en een paar onleesbare krabbels) de verdere koers van het artikel wist uit te stippelen. Ik bewonder jouw visie, jouw vriendelijke en persoonlijk betrokken benadering en jouw vermogen om mensen te verbinden. Mijn diplomering in 2015, waarbij jij me ten overstaan van mijn familie en vrienden na een persoonlijke toespraak mijn bul overhandigde, maakte jij tot een absoluut hoogtepunt in mijn leven. Mijn co-promotor, dr. P.P.F.M. Kuijer. Beste Paul, het begon allemaal in juni 2010 tijdens het door jou opgezette en geleide keuzeonderwijs Topsport, Dans en Muziek als Werk. Jij bent zonder twijfel de drijvende kracht achter dit promotietraject geweest. Ik koester de tientallen koffiemomenten die we al filosoferend en discussiërend over (toekomstige) artikelen doorbrachten op het Voetenplein. Jouw enthousiaste en gedreven manier van werken vind ik uniek en erg aanstekelijk. Ik heb veel van je geleerd zowel op onderzoekstechnisch, als op persoonlijk gebied, zoals: altijd positief blijven, altijd laagdrempelig bereikbaar zijn en altijd feedback beginnen met een positief punt (en soms een ballonnetje tekenen als het écht goed is). Een aantal keer heb ik de wanhoop nabij op jouw drempel gestaan als ik er niet uit kwam of het niet meer zag zitten. Jij nam dan altijd de tijd om me met een kop koffie en een aantal stimulerende woorden weer hernieuwde energie en vertrouwen in te praten. Je bent een fantastisch begeleider en een geweldig mens. Mijn co-promotor, dr. R.N. Planken. Beste Nils, jij sloot in 2014 aan bij ons team en hebt op radiologisch gebied een enorme meerwaarde gehad, onder andere door het imaging deel van dit proefschrift vorm te geven. Een van de artikelen hieruit mocht ik in december 2015 presenteren op een internationaal radiologie congres, de RSNA in Chicago, een hoogtepunt in mijn carrière als promovendus. Ik heb de momenten waarop wij samen achter de computer aan artikelen zaten te schrijven (en ik de kunst van jou af kon kijken) als zeer leerzaam ervaren. A Dankwoord I 237

241 De promotiecommissie: prof. dr. C.M.A.M. van der Horst, prof. dr. G.M.M.J. Kerkhoffs, prof. dr. J.A. Reekers, prof. dr. J. Gielen, prof. dr. W. van Mechelen en dr. J.L. Tol. U allen dank ik voor het feit dat u in de commissie zitting hebt willen nemen en voor de moeite die U hebt genomen mijn proefschrift te bestuderen. Aart Terpstra & Marja Pannekoek-Hekman. Jullie zijn in mijn ogen onlosmakelijk verbonden aan dit proefschrift. Jullie hebben, grotendeels buiten kantooruren, meer dan 25 volleybal teams verspreid door heel Nederland bezocht en bij zo n 350 volleyballers echo s gemaakt. Tijdens de ritjes van en naar de trainingslocaties leerden we elkaar beter kennen en was het altijd gezellig. Ook in het AMC hebben jullie een belangrijke bijdrage geleverd door alle gemaakte beelden te analyseren, nog meer volleyballers en vrijwilligers te echoën, en te helpen bij het ontwikkelen van het scanprotocol. Samen hebben we hoogte- en dieptepunten beleefd in de afgelopen 5 jaar, waar we uiteindelijk sterker uit gekomen zijn, en die dit proefschrift mede vorm gegeven hebben. Ik heb enorm veel respect voor jullie enorme inzet en passie voor het vak, en heb hier veel van geleerd. Ton Langenhorst en Claire Verheul. Jullie waren degenen die in 2010 alert reageerden toen een aantal volleyballers zich in korte tijd met dezelfde klachten presenteerden. Ton, jij hebt ook actief meegeschreven aan de eerste twee artikelen, die de opmaat tot dit promotietraject gevormd hebben. Zo stonden jullie stonden aan het fundament van dit proefschrift. Dank voor jullie kritische blik. Sena Alaeikhanehshir en Tigran Zacharian. Tijdens meerdere onderzoeksstages hebben jullie een bijdrage geleverd aan dit proefschrift door data te verzamelen, te analyseren en mee te schrijven aan artikelen. Mede door jullie harde werk is het mij gelukt om mijn promotie in negen maanden af te ronden. Jullie hebben je ontpopt tot kritische onderzoekers in spe. Dank voor jullie bijdrage en inzet. Mirjam van Bavel. Dank voor je hulp met de logistiek rondom alle onderzoeksactiviteiten de afgelopen jaren. Of het nou ging om het regelen van parkeerpassen, het verlengen van mijn aanstelling, het opdiepen van stapels multomappen, of het helpen bij het verzenden van mijn proefschriften, altijd was je bereikbaar en bereid om te helpen. Tim van Slooten. Dank voor je hulp bij het vormgeven van de website com. Zonder jouw hulp was het absoluut niet gelukt. Collega s van G1: Robert, Charlotte N, Laura, Charlotte G, Anouk en alle anderen. Dank voor de collegiale sfeer op de afdeling. Ook al was mijn periode als fulltime promovendus maar kort en was ik niet vaak op het AMC aanwezig, als ik er was kon ik altijd bij jullie terecht voor vragen en hulp. Ik wil Dynamic B.V. en de Universiteit van Amsterdam bedanken voor de financiële bijdrage aan dit proefschrift. I would like to thank the Fédération Internationale de Volleyball (FIVB) for its support for this thesis. In particular, I would like to thank the medical delegate for the FIVB Bernard Nau, who has been one of the biggest supporters and the voice of the SPIKE study within the FIVB. 238 I Appendices

242 Graag wil ik ook mijn paranimfen bedanken. Tim, je was mijn paranimf maar moest door omstandigheden passen. Desalniettemin heb je actief geholpen en meegedacht om 1 april 2016 een geslaagde dag te laten worden. Je bent al bijna 20 jaar een trouwe vriend en een van de meest ambitieuze en positieve personen die ik ken. Ik ben er van overtuigd dat we samen nog tientallen jaren onze kinderen zullen zien opgroeien in goede vriendschap. Stag, je bent met veel overtuiging ingevallen voor Tim. Ondanks dat je in het begin geen idee had wat er van je verwacht werd als paranimf, zei je volmondig ja en stond je voor me klaar. Iemand vroeg ons ooit of we broers waren, niet geheel onterecht, want voor mij voelt het wel zo. Dank voor je onvoorwaardelijke vriendschap. Joke, de afgelopen 30 jaar ben je heel belangrijk geweest in mijn leven. Je was erbij toen ik op de wereld kwam, je was er gedurende mijn jeugd als suikertante, oppas, huisarts en werkgever, en nu sta je naast me als paranimf, wat me heel trots maakt. Je hebt deze rol met verve vervuld en niets aan het toeval over gelaten: bij jou is het paranimf-schap in goede handen. Je bent mijn tweede moeder en een voorbeeldfiguur voor mij. Opa en Oma Stiphout, jullie beiden maken dit hoogtepunt in mijn carrière helaas niet meer mee. Mede dankzij het geld waar jullie altijd hard voor gewerkt en zuinig voor geleefd hebben, heb ik mijn promotie kunnen bekostigen. Ik weet zeker dat jullie heel trots geweest zouden zijn. Nikkie, mijn lieve zusje, wat ben ik blij dat jij mijn zusje bent, ik heb het getroffen. Van kinds af aan zijn wij maatjes en steunen elkaar door dik en dun. Dank voor je warmte en betrokkenheid. Paul en Nel, mijn lieve ouders, waar was ik geweest zonder jullie. Ik heb het jullie niet altijd even makkelijk gemaakt de afgelopen 30 jaar. Desondanks bleven jullie in mij geloven en mij onvoorwaardelijk steunen. Van jullie heb ik geleerd door te zetten en vertrouwen in eigen kunnen te hebben. Ik hoop dat ik zo n goede ouder wordt als dat jullie altijd voor mij geweest zijn. Joanne, mijn grote liefde en aanstaande bruid. Sinds is jou ken is mijn leven alleen maar mooier geworden. Ik kan alles bij je kwijt, je bent mijn steun en toeverlaat en de stabiele factor in mijn leven. Ik kijk uit naar de geboorte van onze dochter en een heel lang en gelukkig leven samen. A Dankwoord I 239

243

244 CURRICULUM VITAE Daan van de Pol werd geboren op 6 november 1985 in Amsterdam als eerste kind van Paul van de Pol en Nel van Neerven. Samen met zijn zus Nikkie groeide hij op in Amsterdam-West. In 2003 slaagde hij voor het eindexamen aan het Vossius Gymnasium te Amsterdam, waarna hij in 2004 startte met de Academie voor Lichamelijke Opvoeding aan de Hogeschool van Amsterdam. In 2008 werd zijn afstudeeronderzoek naar kniestabiliteit bij patiënten met voorste kruisband letsel genomineerd voor de scriptieprijs van de Hogeschool van Amsterdam en behaalde hij ook de 1 e graads docent Lichamelijk Opvoeding bevoegdheid. In datzelfde jaar startte hij met de studie geneeskunde aan de Universiteit van Amsterdam. Tijdens zijn studie werkte hij in een huisartsenpraktijk, voetbalde hij in een vriendenteam en leerde hij zijn aanstaande bruid Joanne kennen. Ook deed hij naast zijn studie en coschappen onderzoek naar een bloedvatafwijking bij topvolleyballers op de AMC afdelingen Radiologie en Arbeid & Gezondheid, waarmee hij de aandacht trok van binnen- en buitenlandse pers. Na het behalen van het artsexamen in februari 2015 werd dit onderzoek in de vorm van een promotietraject voorgezet. Ruim 9 maanden na zijn artsexamen heeft hij dit proefschrift afgerond. Momenteel is Daan werkzaam als arts-assistent Cardiologie in het Medisch Centrum Haaglanden. In mei 2016 zal hij voor het eerst vader worden. A Curriculum vitae I 241

245

246

247