Specific adaptations of patellar and Achilles tendons in male sprinters and endurance runners

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1 Accepted: 21 March 2018 DOI: /tsm2.21 ORIGINAL ARTICLE Specific adaptations of patellar and Achilles tendons in male sprinters and endurance runners H. Ueno T. Suga Y. Miyake K. Takao T. Tanaka J. Misaki M. Otsuka A. Nagano T. Isaka Faculty of Sport and Health Science, Ritsumeikan University, Kusatsu, Japan Correspondence Tadashi Suga, Faculty of Sport and Health Science, Ritsumeikan University, Kusatsu, Japan. Funding information Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Science, Sports and Culture, Grant/Award Number: 15H03077, 15K16497, 16H03238, This study aimed to determine the impact of long-term training on Achilles tendon (AT) and patellar tendon (PT) hypertrophy in sprinters and endurance runners. The cross-sectional area (CSA) of AT and PT in 40 sprinters, 40 endurance runners, and 40 untrained subjects was measured using magnetic resonance imaging. The AT and PT CSAs were calculated at its proximal, middle, and distal portions. Three CSAs of AT and PT were averaged to give an overall absolute CSA for each tendon. To minimize the effect of body size on tendon CSA and obtain relative CSA, overall absolute CSA for each tendon was normalized with body mass. Absolute AT CSA did not differ significantly among all 3 groups. However, we found that relative AT CSA was significantly larger in endurance runners than in sprinters and untrained subjects (P <.001 for both). In contrast, both absolute and relative PT CSAs were significantly larger in sprinters than in endurance runners and untrained subjects (P.001 for all). These findings indicate that AT hypertrophy is characteristic of endurance runners, whereas PT hypertrophy is characteristic of sprinters. Therefore, we suggest that the AT and PT may undergo specific morphological adaptations in these athletes. KEYWORDS cross-sectional area, joint moment, magnetic resonance imaging, tendon stiffness 1 INTRODUCTION Tendons transmit forces from muscles to skeletons. 1 Therefore, tendons play an important role in coordinating complex movements, such as running and sprinting. 2 Tendon hypertrophy can occur in situations when tendons are exposed to chronic mechanical loading in humans. 3 This morphological adaptation is known to be induced via the activation of collagen synthase that results from increased expression of genes related to growth factors, such as insulin-like growth factor 1 and transforming growth factor b. 4 In humans, hypertrophy of the Achilles tendon (AT) and patellar tendon (PT) is observed in athletes who undergo long-term exercise/sports training In particular, previous studies have determined that AT cross-sectional area (CSA) is larger in endurance runners than in untrained subjects. 5,6,10 However, whether tendon hypertrophy also occurs in the PT of endurance runners is poorly understood. To the best of our knowledge, 2 studies have compared the PT CSA between endurance runners and untrained subjects. Wiesinger et al 10 determined that PT CSA was larger in endurance runners than in untrained subjects. In contrast, Couppe etal 9 reported that PT CSA did not differ between endurance runners and untrained subjects. Thus, there are contradictory findings between the 2 previous studies. Additionally, the 2 previous studies included a relatively small number of subjects (n = 8-10 in each group). 9,10 Therefore, to clarify the impact of longterm running raining on PT hypertrophy, a difference in the PT CSA between endurance runners and untrained subjects should be reexamined with a relatively larger number of subjects John Wiley & Sons Ltd wileyonlinelibrary.com/journal/tsm2 Transl Sports Med. 2018;1:

2 UENO ET AL. 105 Only 1 study has compared the AT CSA between sprinters and untrained subjects. 11 Kubo et al 11 determined using ultrasonography that AT CSA did not differ between sprinters and untrained subjects. It is well known that magnetic resonance image (MRI) is more appropriate to evaluate tissue size than ultrasonography. 12,13 Additionally, Bohm et al 14 have reported that there was a lack of a significant correlation between ultrasonography and MRI-measured AT CSAs. Thus, a difference in the AT CSA between sprinters and untrained subjects should be reexamined using MRI. Furthermore, to the best of our knowledge, no study has compared the PT CSA between sprinters and untrained subjects. Taken together, the impact of long-term sprint training on AT and PT hypertrophy in sprinters remains unclear. In terms of the difference in the degree of AT and PT hypertrophy between sprinters and endurance runners, because PT CSA is larger than AT CSA, 10 the mechanical stress per unit of CSA during human movements is theoretically mitigated in the PT. 15 In a previous study, Belli et al 16 reported that the joint moment of the knee increased when running (ie, 4.0) to maximal speeds, whereas that of the ankle was not increased throughout these speeds. The mechanical stress to the tendon is associated with the magnitude of the joint moment during movements in humans. 17 Based on these findings, PT hypertrophy may require higher levels of mechanical stress, which occur more readily in sprinters than in endurance runners. Hence, we hypothesized that PT hypertrophy would be greater in sprinters than in endurance runners and untrained subjects. In contrast, when similar degrees of ankle joint moment for running and sprinting are considered, 16 the mechanical stress to AT does not differ. Nevertheless, because mechanical stress per unit of CSA is higher in the AT than in the PT, AT hypertrophy would become more evident with higher volumes of mechanical stress. In general, endurance runners are required to train with longer running distances than sprinters, and therefore, their tendons are exposed to high volumes of mechanical stress throughout the training periods. Hence, we hypothesized that AT hypertrophy would be greater in endurance runners than in sprinters and untrained subjects. To test our hypotheses, this study compared the AT and PT CSAs among sprinters, endurance runners, and untrained subjects. 2 METHODS 2.1 Subjects Forty male sprinters (age, years) and 40 male endurance runners (age, years) participated in this study. They were all well trained, being involved in regular training and competition. The personal best 100-m race times in sprinters ranged from to seconds (mean, seconds). The personal best 5000-m race times in endurance runners ranged from 834 to 959 seconds (mean, seconds). Mean International Amateur Athletic Federation scores (an interindividual score for the comparison of competitive performance in different events) based on these personal best time were the same between sprinters and endurance runners ( and , respectively). In addition, 40 male untrained subjects (age, years) participated as a control group. The untrained control subjects were recreationally active but did not participate in any specific physical training program within the previous 3 years. Nevertheless, many of them had participated in recreational sports and/or physical training for 2-3 hours per week. All subjects were informed of the experimental procedures and provided written consent to participate in the study. None of the subjects had contraindications to MRI. All procedures were approved by the Ethics Committee of Ritsumeikan University (BKC-IRB ). 2.2 MRI measurements Representative axial images for calculating CSAs at 3 different portions of the AT and the PT on MRI are shown in Figure 1. The MRI measurement was performed using a 1.5-T magnetic resonance system (Signa HDxt; GE Medical Systems, WI, USA). To measure the CSA, the subjects were placed in a supine position on the scanner bed, with both knees fully extended and both the ankles set at the neutral position (ie, 0 ). In a measurement of CSA, axial T1-weighted MRI scans of the lower limb were acquired with 8-channel coil. Axial scans were obtained in successive slices with an interdistance of 5 mm from the muscletendon junction of the soleus to the calcaneal tuberosity with a repetition time of 600 ms, echo time of 7.7 ms, slice thickness of 5 mm, field of view of 380 mm, and matrix size of pixels. The CSAs of the AT were measured at 10 mm below the muscle-tendon junction of the AT and soleus (ie, the proximal portion), 10 mm above the distal insertion of the AT (ie, the distal portion), and midway between these 2 portions (ie, the middle portion). The CSA of the PT was measured at 5 mm below the patellar insertion (ie, the proximal portion), 5 mm above the tibial insertion (ie, the distal portion), and midway between these 2 portions (ie, the middle portion). Additionally, the mean of 3 portion CSAs was calculated for each tendon to obtain an overall absolute CSA. Furthermore, to minimize the effect of body size on tendon CSA and obtain relative CSA, overall absolute CSA for each tendon was normalized with body mass to the two-third power. 9,10 The analyses for measuring tendon CSAs were conducted using image analysis software (OsiriX Version 5.6; OsiriX Foundation, Geneva, Switzerland).

3 106 UENO ET AL. (A) Proximal portion Middle portion Distal portion (B) Proximal portion Middle portion Distal portion FIGURE 1 Representative axial images for the calculation of patellar and Achilles tendon (AT) cross-sectional areas. A, shows crosssectional area (CSA) of the patellar tendon (PT). The PT CSA was measured at 5 mm below the patellar insertion (ie, the proximal portion), 5 mm above the tibial insertion (ie, the distal portion), and midway between the 2 portions (ie, the middle portion). B, shows CSA of the AT. The AT CSA was measured at 10 mm below the muscle-tendon junction of the AT and soleus (ie, the proximal portion), 10 mm above the distal insertion of the AT (ie, the distal portion), and midway between the 2 portions (ie, the middle portion) 2.3 Statistical analysis All data are expressed as mean SD. The differences in variables among 3 groups were analyzed using 1-way analyses of variance after normal distributions were confirmed. If the sphericity assumption was not met, the Greenhouse- Geisser corrections were used. Specific differences were identified with a Bonferroni post-hoc test. The g 2 effect size was calculated to determine the magnitude of difference in outcome variables among the 3 groups. The strength of the effect sizes was interpreted as weak (.10 < g 2 ), moderate (.25 < g 2 ), and strong (.40 < g 2 ). 18 Cohen s d effect size was calculated to determine the magnitude of difference in outcome variables between the 2 groups. The strength of the effect sizes was interpreted as weak (d < 0.40), moderate (0.40 d < 0.80), and strong (0.80 d). 19 All statistical analyses were conducted using IBM SPSS software (version 19.0; International Business Machines Corp, NY, USA), and the statistical significance level was defined at P < RESULT Comparisons of the physical characteristics and the PT and AT CSAs in all 3 groups are shown in Table 1. Body height, body mass, and body mass index analyses revealed a significant difference among group. The body height was significantly higher in sprinters than in endurance runners and untrained subjects. The body mass was significantly higher in sprinters (P <.001, d = 2.065) and untrained subjects (P <.001, d = 1.306) than in endurance runners. Similarly, body mass index was significantly higher in sprinters (P <.001, d = 2.268) and untrained subjects (P <.001, d = 1.448) than in endurance runners. With regard to the AT, proximal CSA analysis revealed a significant difference among group. The proximal CSA was significantly larger in endurance runners than in untrained subjects (P =.019, d = 0.619). In contrast, middle and distal CSA analyses revealed no significant differences among groups. Mean CSA analysis also revealed no significant difference among groups. With regard to the PT, all 3 portion CSA analyses revealed significant differences among groups. Each CSA was significantly larger in sprinters in endurance runners (P <.001, d = for proximal CSA; P <.001, d = for middle CSA; P <.001, d = for distal CSA) and untrained subjects (P =.002, d = for proximal CSA; P <.001, d = for middle CSA; P <.001, d = for distal CSA). Moreover, distal CSA was significantly larger in untrained subjects than in endurance runners (P =.031, d = 0.594). Additionally, mean CSA analysis revealed a significant difference among group (F = , P <.001, g 2 =.351). The mean CSA was larger in sprinters than in endurance runners and untrained subjects (P <.001, d = and P <.001, d = 1.173, respectively). Furthermore, mean CSA was larger in untrained subject than in endurance runners (P =.003, d = 0.574). Following normalization with body mass to the twothird power, the relative value of mean AT CSA analysis revealed a significant difference among group (F = , P <.001, g 2 =.168: Figure 2). The relative AT CSA was

4 UENO ET AL. 107 TABLE 1 subjects Physical characteristics and patellar and Achilles tendon cross-sectional areas in sprinters, endurance runners, and untrained Sprinters Endurance runners Untrained subjects F P value g 2 Body height, cm ** * Body mass, kg *** < Body mass index, kg/m *** < PT CSA, mm 2 Proximal portion *** ** < Middle portion *** *** < Distal portion *** ***, < AT CSA, mm 2 Proximal portion Middle portion Distal portion AT, Achilles tendon; CSA, cross-sectional area; PT, patellar tendon. Values are presented as mean SD. *P <.050, **P <.010, and ***P <.001 compared with sprinters; P <.050 and P <.001 compared with endurance runners. significantly higher in endurance runners than in sprinters and untrained subjects. In contrast, the relative values of mean PT CSA revealed a significant difference among group (F = , P <.001, g 2 =.241). The relative PT CSA was larger in sprinters than in endurance runners and untrained subjects. 4 DISCUSSION The primary findings of the present study were that AT CSA was larger in endurance runners than in sprinters and untrained subjects, whereas PT CSA was larger in sprinters than in endurance runners and untrained subjects. Additionally, AT CSA did not differ between sprinters and untrained subjects, and PT CSA did not differ between endurance runners and untrained subjects. These findings suggest that the AT and PT may undergo specific morphological adaptations in sprinters and endurance runners. Previous studies have determined using MRI that AT CSA is larger in endurance runners than in untrained subjects. 5,6,10 Similarly, the present study also determined that although absolute AT CSA did not differ among the 2 groups, AT CSA relative to body mass was larger in endurance runners than in untrained subjects. Furthermore, we found that absolute and relative AT CSAs did not differ between sprinters and untrained subjects. To the best of our knowledge, in only 1 study, Kubo et al 11 have compared AT CSA between sprinters and untrained subjects. They reported using ultrasonography that AT CSA was Patellar tendon P <.001 Achilles tendon Relative CSA (mm 2 /kg 2/3 ) Sprinters P <.001 Endurance runners Untrained subjects Relative CSA (mm 2 /kg 2/3 ) Sprinters P <.001 P =.001 Endurance runners Untrained subjects FIGURE 2 Comparison of relative PT and AT CSAs among sprinters, endurance runners, and untrained subjects. The 3 portion CSAs of PT and AT were averaged and then normalized with body mass to the two-third power. The relative values of mean PT and AT CSA analyses revealed a significant difference among group (F = , P <.001, g 2 =.241 and F = , P <.001, g 2 =.168, respectively). AT, Achilles tendon; CSA, cross-sectional area; PT, patellar tendon

5 108 UENO ET AL. similar between sprinters and untrained subjects. However, Bohm et al 14 have reported there is a lack of a significant correlation between ultrasonography and MRI-measured AT CSAs. Nevertheless, the results of MRI measurements in the present study appear to support those of ultrasonography by Kubo et al. 11 Thus, the present and previous findings suggest that AT hypertrophy is characteristic of endurance runners but not sprinters. With regard to the PT, Wiesinger et al 10 reported that PT CSA was larger in endurance runners than in untrained subjects. In contrast, Couppe etal 9 determined that PT CSA did not differ between the 2 groups. This discrepancy may be accounted for by the relatively small sample size (n = 8-10 in each group) utilized in these studies. 9,10 In the present study, we determined with a relatively large number of subjects (n = 40 in each group) that PT CSA did not differ between endurance runners and untrained subjects. This supports the findings by Couppe etal 9 and indicates that PT hypertrophy may be not induced in endurance runners. Additionally, to the best of our knowledge, the present study is also the first to determine that PT CSA is larger in sprinters than in endurance runners as well as untrained subjects. Therefore, we suggest that hypertrophy of the PT, but not of the AT, is characteristic of sprinters. The present findings indicate that the PT and AT may undergo specific morphological adaptations in sprinters and endurance runners. As we hypothesized prior to our study, these adaptations might result from differences in the magnitude and volume of mechanical stress imposed on these tendons during sprinting and running. Theoretically, mechanical stress per unit of CSA during human movement is lower in the PT than in the AT, 15 because of a larger CSA of the former. As such, a higher intensity of mechanical stress to the tendon may be required to induce PT hypertrophy. In a previous study, Belli et al 16 reported that the increases in running speed accompanied increases in the knee joint moment. Because the mechanical stress to the tendon is associated with the magnitude of joint moment during human movement, 17 PT hypertrophy might be expected to be seen in sprinters rather than endurance runners. In other words, differences in the magnitude of mechanical stress experienced between sprinters and endurance runners may, at least partially, explain our findings of larger PT CSA in sprinters than in endurance runners and untrained subjects. In contrast, a study by Belli et al 16 showed that that ankle joint moment was not changed despite increases in running speed. Considering their findings, the mechanical stress to the AT is not different between running and sprinting. Nevertheless, because mechanical stress per unit per CSA is higher in the AT than in the PT, AT hypertrophy may be more evident with higher volumes of mechanical stress, which relates to longer running distances during training for endurance runners. Therefore, differences in the volume of mechanical stress experienced between sprinters and endurance runners could, at least partially, explain our findings of larger AT CSA in endurance runners than in sprinters and untrained subjects. In addition to the differences in mechanical stress patterns imposed on the tendons, long-term training experience may be useful to explain the differences in the hypertrophy of tendons, especially the PT, between sprinters and endurance runners. Sprinters include resistance training as part of their habitual training routine. 20 Previous studies have demonstrated that resistance training with knee extension induced PT hypertrophy in untrained subjects; 7 however, no study has examined this in sprinters. In general, the knee extensor strength is greater in sprinters than in endurance runners and untrained subjects, 21 which may be partially due to the long-term resistance training. Compared with other groups, greater knee extensor strength may be associated with hypertrophy of the PT, potentially by increasing itself mechanical stress, in sprinters. Therefore, in addition to sprint training, habitual resistance training may contribute to the PT hypertrophy in sprinters. Nevertheless, in the present study, we did not obtain detailed data regarding resistance training history throughout long-term training period in sprinters and endurance runners. Further studies are needed to examine the relationship between long-term training history and tendon size in athletes. 5 CONCLUSION AND PERSPECTIVE The present study demonstrated that AT CSA was larger in endurance runners than in sprinters and untrained subjects, whereas PT CSA was larger in sprinters than in endurance runners and untrained subjects. Therefore, we suggest that the AT and PT may undergo specific morphological adaptations, namely hypertrophy, in these athletes. These adaptations may be beneficial as larger tendon CSAs can decrease the mechanical stress to tendons during human movement, 15 which may help prevent tendon injuries. Indeed, Couppe etal 22 determined that although PT CSA was larger in the lead than non-lead leg in badminton players without patellar tendinopathy, it did not differ between these legs in those with patellar tendinopathy. Additionally, they found that PT CSA in the lead leg was smaller in players with injury than in players without injury. Their findings indicate that a relatively small PT CSA may be a risk factor for some tendon injuries. This is of relevance to our study as patellar and Achilles tendinopathy commonly occur among track and field athletes, 23,24 with the former being particularly common in endurance runners. 24 To the best of our knowledge, a direct relationship between tendon

6 UENO ET AL. 109 morphology and tendon injury is yet to be determined. Clarifying this relationship may be useful in understanding the features of individual sprinters and endurance runners, facilitating the outlining of personalized programs for their training and rehabilitation to improve outcomes and performance. ACKNOWLEDGEMENTS This study was supported by a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Science, Sports, and Culture (#15K16497 to T.S; #16H03238 to A.N; # and #15H03077 to T.I). CONFLICT OF INTEREST No potential conflict of interest was reported by the authors. ORCID T. Suga M. Otsuka REFERENCES 1. Benjamin M, Toumi H, Ralphs JR, Bydder G, Best TM, Milz S. Where tendons and ligaments meet bone: attachment sites ( entheses ) in relation to exercise and/or mechanical load. J Anat. 2006;208: Bramble DM, Lieberman DE. Endurance running and the evolution of Homo. Nature. 2004;432: Bohm S, Mersmann F, Arampatzis A. Human tendon adaptation in response to mechanical loading: a systematic review and metaanalysis of exercise intervention studies on healthy adults. Sports Med Open. 2015;1:7. 4. Kjaer M, Langberg H, Heinemeier K, et al. From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand J Med Sci Sports. 2009;19: Rosager S, Aagaard P, Dyhre-Poulsen P, Neergaard K, Kjaer M, Magnusson SP. Load-displacement properties of the human triceps surae aponeurosis and tendon in runners and non-runners. Scand J Med Sci Sports. 2002;12: Magnusson SP, Kjaer M. Region-specific differences in Achilles tendon cross-sectional area in runners and non-runners. Eur J Appl Physiol. 2003;90: Kongsgaard M, Reitelseder S, Pedersen TG, et al. Region specific patellar tendon hypertrophy in humans following resistance training. Acta Physiol. 2007;191: Seynnes OR, Erskine RM, Maganaris CN, et al. Training-induced changes in structural and mechanical properties of the patellar tendon are related to muscle hypertrophy but not to strength gains. J Appl Physiol. 2009;107: Couppe C, Svensson RB, Grosset JF, et al. Life-long endurance running is associated with reduced glycation and mechanical stress in connective tissue. Age (Dordr). 2014;36: Wiesinger HP, Rieder F, K osters A, M uller E, Seynnes OR. Are sport-specific profiles of tendon stiffness and cross-sectional area determined by structural or functional integrity? PLoS One. 2016;11:e Kubo K, Miyazaki D, Ikebukuro T, Yata H, Okada M, Tsunoda N. Active muscle and tendon stiffness of plantar flexors in sprinters. J Sports Sci. 2017;35: Miyatani M, Kanehisa H, Ito M, Kawakami Y, Fukunaga T. The accuracy of volume estimates using ultrasound muscle thickness measurements in different muscle groups. Eur J Appl Physiol. 2004;91: Wachi M, Suga T, Higuchi T, et al. Applicability of ultrasonography for evaluating trunk muscle size: a pilot study. J Phys Ther Sci. 2017;29: Bohm S, Mersmann F, Schroll A, M akitalo N, Arampatzis A. Insufficient accuracy of the ultrasound-based determination of Achilles tendon cross-sectional area. J Biomech. 2016;49: Butler DL, Grood ES, Noyes FR, Zernicke RF. Biomechanics of ligaments and tendons. Exerc Sport Sci Rev. 1978;6: Belli A, Kyr ol ainen H, Komi PV. Moment and power of lower limb joints in running. Int J Sports Med. 2002;23: Muramatsu T, Muraoka T, Takeshita D, Kawakami Y, Hirano Y, Fukunaga T. Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo. J Appl Physiol. 2001;90: Cohen J. Statistical Power Analysis for the Behavioral Sciences, 2nd edn. Hillsdale, MI: Lawrence Erlbaum Associates; Cohen J. A power primer. Psychol Bull. 1992;112: Bolger R, Lyons M, Harrison AJ, Kenny IC. Sprinting performance and resistance-based training interventions: a systematic review. J Strength Cond Res. 2015;29: Maughan RJ, Watson JS, Weir J. Relationships between muscle strength and muscle cross-sectional area in male sprinters and endurance runners. Eur J Appl Physiol. 1983;50: Couppe C, Kongsgaard M, Aagaard P, et al. Differences in tendon properties in elite badminton players with or without patellar tendinopathy. Scand J Med Sci Sports. 2013;23:e89-e Taunton JE, Ryan MB, Clement DB, McKenzie DC, Lloyd-Smith DR, Zumbo BD. A prospective study of running injuries: the Vancouver Sun Run In Training clinics. Br J Sports Med. 2003;37: Pierpoint LA, Williams CM, Fields SK, Comstock RD. Epidemiology of injuries in United States high school track and field: through Am J Sports Med. 2016;44: How to cite this article: Ueno H, Suga T, Miyake Y, et al. Specific adaptations of patellar and Achilles tendons in male sprinters and endurance runners. Transl Sports Med. 2018;1: /tsm2.21