Concussions in Soccer: A Current Understanding

Concussions in Soccer: A Current Understanding Michael L. Levy 1,2, Aimen S. Kasasbeh 3, Lissa Catherine Baird 1,2, Chiazo Amene 1,2, Jeff Skeen 1,2, Larry Marshall 2 Key words Concussion Head injury Protective headgear Soccer Trauma Abbreviations and Acronyms AAN: American Academy of Neurology EEG: Electroencephalogram LOC: Loss of consciousness MRI: Magnetic resonance imaging PTA: Post-traumatic amnesia TBI: Traumatic brain injury From the 1 Division of Pediatric Neurosurgery Rady Children s Hospital of San Diego, San Diego, California; 2 Division of Neurosurgery, University of California, San Diego, San Diego, California; and 3 Graduate Program in Neuroscience, University of Arizona, Tucson, Arizona, USA To whom correspondence should be addressed: Michael L. Levy, M.D., Ph.D. [E-mail: mlevy@rchsd.org] Citation: World Neurosurg. (2012) 78, 5:535-544. DOI: 10.1016/j.wneu.2011.10.032 Journal homepage: www.worldneurosurgery.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter 2012 Elsevier Inc. All rights reserved. INTRODUCTION Sports are a major cause of traumatic brain injury (TBI). It is estimated that approximately 300, 000 sport-related TBIs occur each year (121, 122). This is thought to be a drastic underestimate as well, as it includes only TBIs where loss of consciousness (LOC) was reported (70, 71), and more accurate estimates may put sport-related TBI near 1.6 3.8 million annually, on an international level (28, 71, 111). Approximately 90% of TBIs are classified as concussions or mild TBIs (49, 92). Ninety percent of sports-related concussions may go unidentified (1). Soccer is the most popular sport in the world and has a following of millions in the United States, and approximately 16 million registered players in the United States (2, 36, 59, 98). In the United States, it is estimated that 12.5 million (1) to 18.2 million OBJECTIVE: Traumatic brain injury (TBI) is a significant public health problem in the United States, with approximately 1.5 2 million TBIs occurring each year. However, it is believed that these figures underestimate the true toll of TBI. Soccer is the most popular sport in the world and has a following of millions in the United States. Soccer is a sport not traditionally identified as high-risk for concussions, yet several studies have shown that concussion rates in soccer are comparable to, and often exceed those of, other contact sports. As many as 22% of all soccer injuries are concussions. METHODS: Soccer is a sport not traditionally identified as high risk for concussions, yet several studies have shown that concussion rates in soccer are comparable to, and often exceed those of, other contact sports. As many as 22% of all soccer injuries are concussions. Head injury during soccer is usually the result of either direct contact or contact with the ball while heading the ball. Relationships between the number of headers sustained in a single season and the degree of cognitive impairment (attention and visual/verbal memory) have been demonstrated. It is also likely that multiple concussions may cause cumulative neuropsychologic impairment in soccer players. RESULTS: Although our understanding of risk factors for sports-related concussions is far from complete, there is great potential for prevention in sports-related concussions. Several measures must be taken to avert the development of concussions in soccer and, when they take place, reduce their effects. These include the development and testing of effective equipment during play, the maintenance of regulatory standards for all such equipment, educating young athletes on the safe and appropriate techniques used during play, and strict adherence to the rules of competition. CONCLUSIONS: In spite of such preventive measures, concussions in soccer will continue to occur. Considering the frequency of concussions in soccer, the serious sequelae of these concussions, and because almost half of concussed soccer players were noncompliant with recommended American Academy of Neurology return-to-play guidelines, further measures must be taken to protect players, in addition to understanding those criteria that result in removing an injured player from competition and the steps by which to safely return an athlete to competition after injury. (22) people participate in soccer. In terms of participation, the largest number of individuals are involved in boys and girls youth soccer in the United States, with more than 3.5 million players between the ages of 5 and 19 years in the United States Youth Soccer Association, American Youth Soccer Organization, and United Soccer League. The U.S. Consumer Product Safety Commission estimated between 146,000 and 160,000 soccer-related injuries annually for the years 1992 through 1994, with approximately 45% occurring in participants younger than 15 years. Injury rates per 1000 player-hours range from 0.6 to 19.1 per 1000, depending on the level of play and the WORLD NEUROSURGERY 78 [5]: 535-544, NOVEMBER 2012 www.worldneurosurgery.org 535

definition of injury. The male-to-female ratio of injuries overall is 1:2 for similar levels of exposure (7). Soccer is a sport not traditionally identified as high-risk for concussions (11, 24, 36, 38, 58, 76, 109). However, soccer players are prone to TBI (12, 83, 127), and as high as 22% of all soccer injuries are concussions (31). Furthermore, several studies have shown that concussion rates in soccer are comparable to, and often exceed those of, other contact sports traditionally perceived as inherently more violent, such as football and ice hockey (13, 19, 33, 38, 39, 48, 63, 82, 83, 109, 114, 128, 129). The American Academy of Pediatrics has categorized soccer as a contact/collision sport, along with hockey and football (7). CONCUSSION RATES IN SOCCER Several studies have demonstrated concussion rates in soccer with the trend for concussions in soccer continuing to increase (13, 31). Radelet et al. (103) noted that soccer had the highest injury rate per athleteexposure among 7- to 13-year-old children. Delaney et al. (38) noted that approximately half of university soccer players had experienced concussion symptoms during that season. Only 29.2% of concussed soccer players were aware that they had suffered a concussion. Of concussed players, 75% had experienced multiple concussions during a single season, with 54.2% having had at least three concussions and 8.4% having had five or more concussions. This suggested that more university soccer players may be exposed to concussive injury than football players. Another study of university soccer players during 1 year of soccer participation (39) demonstrated that 62.7% of university soccer players had experienced symptoms of a concussion. Only 19.8% of concussed players were aware that they had suffered a concussion. Furthermore, of the concussed soccer players, 81.7% suffered multiple concussions, 54.8% of concussed soccer players suffered at least three concussions, and 27% of concussed soccer players suffered at least five concussions (39). Of those, 18.8% experienced symptoms for 1 day or longer. Goalies were most commonly affected. In a retrospective study by Sallis and Jones (106), 40% of players reported symptoms of concussion during the prior season, 10% of players reported symptoms of concussion during the final game of the season. Of the players concussed, 58% reported more than one episode. More than 50% of players who developed concussion, failed to report their symptoms. Sideline physicians and trainers diagnosed only 15% of players with concussion. The actual incidence of soccer-related concussion varies in the literature, and likely depends on variables such as age, gender, and level of participation. The incidence of concussion may be as high as 18.91 per 1000 athlete-exposures, in which each game or practice session is equivalent to one athlete-exposure. The literature suggests that there is an increase in injuries with increase in age and level of play (6, 13, 19, 39, 40, 42, 46, 48, 55, 61, 98). Methodologic differences such as in defining, reporting, and grading of concussions must be taken into consideration. Differences in rates of concussion notwithstanding, even lower estimates of concussions in soccer may translate into considerable lifetime risk of brain injury and its sequelae during the course of many years of participation. CONCUSSIONS INCREASE RISK OF FUTURE CONCUSSIONS Studies have demonstrated that athletes with a history of concussion are at increased risk of developing a concussion in the future. Guskiewicz et al. (51, 52) demonstrated that players with a history of three or more concussions were three times more likely to have a future concussion when compared with athletes with no such history. Delaney et al. (38, 39) demonstrated that past history of recognized concussion during soccer increased the odds of suffering a concussion in that season by 11.12 times. In a large prospective cohort study, Zemper (140) reported that the risk of sustaining a concussion was 5.8 times greater for athletes with a history of concussion. Multiple previous concussions were also associated with a slowed recovery of neurological function (51, 52, 80). HOW ARE SOCCER CONCUSSIONS CAUSED? In October 2007, the Journal of Athletic Training published a 15-year review of National Collegiate Athletic Association Injury Surveillance System data for both men s and women s soccer (6, 40). They demonstrated that player-to-player contact was the principal injury mechanism during men s soccer games, accounting for 61% of injuries. Of reported concussions in games, 80.6% resulted from player contact. Concussions accounted for 5.8% of all game injuries, and 3.9% of injuries resulted in 10 or more days of inactivity before return to play. Players were 13 times more likely to experience a concussion during a game compared with practice. In women s soccer, concussions were found to be the third most commonly reported injury. Player-toplayer contact was the primary injury mechanism during games, accounting for 53.7% of injuries; 67.7% of reported concussions in games resulted from collision with another player. Concussions contributed to 8.6% of total game injuries with 6.0% of injuries resulting in 10 or more days of inactivity before return to play. In both men s and women s soccer, the second most common body area at risk for injury (after lower extremities) was the head and neck. Head-to-head contact results in the majority of concussions in soccer (Table 1), with the forehead and temples being the most common sites of injury (Table 2). The majority of insults occur within a narrow band around the head (Fuller, 100%; Delaney, 83%) (Figure 1) (32, 46). Concussion may occur in the absence of direct impact to the head (66). The penalty area and the midfield line are where most cases of head injury occur (66). In laboratory simulations analyzing head accelerations (47) and maximum head impact power, Withnal et al.(134) demonstrated a low risk of concussion in head-to-upper limb impacts ( 5%), whereas head-to-head impacts were associated with a 67% risk of concussion. As the intentional use of the head to impact another player s head presents a very high risk of concussion, we suggest a harsher position on the part of supervisory bodies in such instances. Namely, immediate removal of the offending athlete (red card) from competition should be mandatory with consideration of further removal from upcoming competition. At the professional level, financial penalties could also be levied as has been recently done in the National Football League and the National Basketball Association. 536 www.sciencedirect.com WORLD NEUROSURGERY, DOI:10.1016/j.wneu.2011.10.032

Table 1. Mechanism of Head Injury in Soccer (in percentages) Impact Boden et al. (19) Andersen et al. (9) Fuller et al. (46) Withnall et al. (134) Delaney et al. (32) Dick et al. (40) Agel et al. (6) Head/head 28 32 30 30 33 68* 81* Head/elbow 14 34 35 38 17 Head/knee 3 3 21 13 6 Head/ground 10 2 2 22 13 8 Head/ball 24 6 9 13 11 18 8 Head/other 21 23 3 6 11 1 3 *Percentages are a combination of impact locations on another player s body (head, elbow, and knee). Impacts from upper extremity, not elbow alone. Most concussions in soccer are associated with transient confusion, no LOC, and symptoms or mental status abnormalities, such as post-traumatic amnesia, that resolve in 15 minutes or less (American Academy of Neurology guidelines grade I injuries) (19, 106). The risk of concussion is a function of the maximum linear acceleration of the head, with the probability of sustaining a concussion at 50% at approximately 750 m/s 2 acceleration (Figure 2)(96). Studies have demonstrated that goalkeepers are at a high risk for concussion, with as many as 80% of goalkeepers reporting sustaining a concussion (19, 38, 39, 125). This is consistent with the distinct role of goalkeepers in soccer, often stopping balls shot from short distances and at very high speeds, frequently exceeding 120 km/h (129). They are also vulnerable to head injury in the penalty area. HEADING AND CONCUSSION Head injury during soccer is usually the result of either direct contact (i.e., head vs. head, head vs. knee, head vs. the ground) or contact with the ball while heading the Table 2. Site of Head Injury in Soccer: Where Impacts Occur on the Head Location Fuller (46) (%) Delaney (32) (%) Forehead 50 6 Temples 37 56 Occiput 11 22 Face 6 Jaw 11 ball. Between 6% and 24% of reported concussions in soccer have been associated with contact with the ball (6, 9, 19, 32, 40, 44-46). A soccer player can be subjected to an average of six to seven incidents of heading the ball per game (59, 104, 126). Matser et al. (83) have estimated a median of 800 occurrences of heading during a single season for professional soccer players. Noteworthy is that these numbers do not include events that take place during practice or training. Studies have coupled heading the ball to neurocognitive impairment in amateur and professional soccer players (14, 57, 82, 83, 127, 128). Witol and Webbe (136) demonstrated that players with the highest exposure rates to heading had significantly poorer performance on neurocognitive tests designed to measure attention, concentration, and other aspects of cognition. In a study of 84 professional soccer players by Matser et al. (84), number of headers in one season correlated with poor performance on tests designed to measure attention, memory, and visuoperceptual processing, suggesting a relationship between headers and cognitive impairment. In addition, a dose-response relationship between the number of headers sustained in a single season and the degree of cognitive impairment (attention and visual/verbal memory) has been demonstrated (84), indicating that heading the ball independently contributes to cognitive impairment. However, other researchers question the role of heading on neurocognitive function. Some investigators have attributed this to various confounding factors such as the use of heavier soccer balls or selection bias of control groups (9, 50, 66, 88, 100). Additional methodologic flaws have been noted, such as failure to control for aging, prior head trauma, and alcohol intake (14, 65, 67, 105). Jordan et al. (59) in a review of repetitive heading in elite players of the U.S. Men s National Soccer team found no statistical difference in symptoms or magnetic resonance imaging (MRI) findings between the players and the control groups. They suggested that encephalopathy in soccer players is more closely correlated with acute head injuries than from repetitive heading. Naunheim et al. (95) showed that peak acceleration exposure to the head when heading a soccer ball averaged a gravitational force of 54.7g compared with 29.2g and 35g for football and hockey, respectively. Thus soccer players experience significantly greater accelerations of 160% 180% greater from heading a soccer ball compared with head impacts sustained during hockey or football. The force required to result in concussion has been estimated to be 22 N/s (110). Levendusky et al. (72) dem- Figure 1. Stripe around head where most impacts occur. WORLD NEUROSURGERY 78 [5]: 535-544, NOVEMBER 2012 www.worldneurosurgery.org 537

Figure 2. Probability of concussion as a function of maximum linear acceleration (A max ). (From: Newman Newman J, Barr C, Beusenberg M, Fournier E, Shewchenko N, Welbourne E, Withnall C: A New Biomechanical Assessment of Mild Traumatic Brain Injury, Part 2 - Results and Conclusions. International Research Council on the Biomechanics of Impact. Proceedings of the 2000 International IRCOBI Conference on the Biomechanics of Impact; 2000:223-233 [96].) onstrated that the majority of cases of heading occur at ball velocities of less than 40 mph (65 km/h), or an impact force between 12.4 and 13.7 N/s (72), indicating that they are of inadequate force (68, 93, 102). In addition, heading a soccer ball has less impact than head-to-head contact and is less likely to result in concussion. Heading a ball was found to result in head accelerations of less than 1000 rad/s 2 (less than 10g), rendering them incapable of reaching the threshold of sport-related concussions of 3500 5000 rad/s 2 (40 60g) (88, 91, 95). This is in contrast to head-to-head impacts, where contact produces enough force to result in concussive injury (88). Whereas repetitive heading may result in the exacerbation of brain injury in the presence of underlying pathology (99, 102), the cumulative effect of repeated subconcussive insults to the brain remains to be determined. CONSEQUENCES OF HEAD INJURY IN SOCCER Barnes et al. (13) have shown that with increased exposure to soccer, the incidence of head injuries is increased. From 1990 to 1999, 86,697 patients presented to emergency departments in the United States with head injuries resultant from their participation in soccer. The annual rates of head injuries and concussions presenting to emergency departments were often comparable with football and ice hockey (33). The highest incidence of skull base fractures and maxillofacial fractures was found to be resulted mostly from soccer (59%), and the most common diagnosis associated with skull base fractures and maxillofacial fractures were concussion (43). Deaths have been reported in soccer, often from heading the ball, especially when the ball was wet (117, 124). There is risk for significant intracranial insult in soccer, especially in the presence of underlying pathology (99). NEUROPSYCHOLOGIC DEFICITS AND SOCCER Short-Term Cognitive Deficits The immediate neurocognitive effects of concussions are well documented (80, 85-87, 138). Straume-Naesheim et al. (118) examined whether minor head trauma caused measurable neuropsychologic impairment in professional soccer players. They reported increased durations of reaction time in athletes who sustained head trauma. This reduced performance after minor head injury was found to be most significant in players reporting acute symptoms after the initial injury head impact. Deficits were also found in asymptomatic athletes. It has been recognized for decades that LOC is not a required feature of concussion (30). Lovell et al. (78) found no significant differences in any neuropsychologic measures between patients with LOC, those without LOC, and those with an uncertain history of LOC, suggesting that LOC is a poor predictor of subsequent neurocognitive function after concussion. Furthermore, Webbe et al. (133) found that players with highest reported estimates of heading frequency were found to score significantly lower on a battery of neurocognitive tests, suggesting a contribution of heading to short-term cognitive impairment. McCrea et al. (86) demonstrated a correlation between recognized indicators of injury severity (e.g., LOC and post-traumatic amnesia [PTA]) and severity of neurocognitive impairment immediately after concussion. They found that athletes who experienced a short period of PTA manifested more severe impairments than athletes who did not. Athletes who demonstrated LOC manifested the most severe neurocognitive impairment after concussion. In the absence of PTA or LOC, no significant neurocognitive impairment was evident 15 minutes after concussion. These results further support that PTA and LOC are indicative of more significant injury after concussion (62). This is in contrast with the results of Lovell et al. (78). Other investigators have suggested that the neurocognitive impairment in the immediate post-concussion period is characterized by initial disruption of neurocognitive function followed by steady recovery in the following hours and return to baseline cognitive function within days. Considerable neurocognitive changes may be detected immediately after concussion in the absence of LOC, PTA, or alteration of gross neurological status (86). Of sports-related concussions, 85% occur without evidence of LOC, PTA, or changes in gross neurological function. However, as previously noted, the presence of LOC or PTA indicates a more severe injury during the immediate post-concussion phase (86). In a study of an 8-year-old girl who sustained a concussion while playing soccer reported that cognitive impairment (noted at 24 hours after injury), resolved within 22 weeks. Visual evoked potentials demonstrated cortical impairment that persisted up to 1 year after the concussion and was associated with poorer school performance (20). In more significant injuries (American Academy of Neurology [AAN] grade 3) or in players with persistent compromise after 538 www.sciencedirect.com WORLD NEUROSURGERY, DOI:10.1016/j.wneu.2011.10.032

concussion, neuropsychologic assessment is imperative. Routine neurological examination alone has not been found to be sensitive at predicting underlying cognitive impairment. In addition, most injuries are not associated with intracranial lesions on imaging after a concussion (116). Glasgow coma scale (120) is sensitive for more serious cases of head trauma, but is not suitable for subtle cognitive deficits after concussion (116). Detailed neurocognitive evaluation is necessary, and is capable of identifying elusive neurocognitive deficits after a concussion (25). Long-Term Cognitive Deficits Repetitive head injury in soccer has long been believed to adversely affect certain aspects of cognitive functioning (126). Neuropsychological screening tests are becoming more commonly used to evaluate impairment and recovery from concussion in all athletes before and after injury (15, 81). Tysvaer and Lochen (128) used an extensive battery of neuropsychologic tests to examine retired soccer players. They found that 81% of studied soccer players had deficits in attention, concentration, memory, and judgment. Matser et al. (83) found that performance in memory, planning, and visuoperceptual processing tasks was inversely related to the number of concussions and frequency of heading the ball in professional soccer players studied. Killam et al. (64), using a battery of neuropsychologic tests to study the residual effects of sport-related head trauma in all athletes, showed that recently concussed athletes scored lower than controls in immediate memory, delayed memory, and total Repeatable Battery for the Assessment of Neuropsychological Status scores. They further conclude that subclinical cognitive impairment, even in the absence of a diagnosis of concussion, may result from the cumulative effect of repeated mild head injuries. Collie et al. (27) demonstrated that athletes who have sustained concussion demonstrated impaired attention and motor function, with poorer improvement over time on neurocognitive testing compared with asymptomatic and noninjured athletes. Matser et al. (82, 83) studied the neuropsychologic sequelae in amateur and professional soccer players with a prior history of head injury and documented impairment of memory, planning, and motor tasks in amateur players, and impairment of memory, planning and visuoperceptual processing in professional players. Colvin et al. (29) found that soccer players who had sustained a concussion had significantly worse neurocognitive scores. Using computer-based neuropsychologic testing to evaluate memory, reaction time, and visual motor speed, Colvin et al. (29) found that soccer players who had sustained a concussion had significantly worse neurocognitive scores compared with controls. Female soccer players performed worse than their male counterparts. Although the effects of playing soccer and its role in chronic brain damage continue to be evaluated (53), the majority of related literature supports the relationship of such with its effect on long-term cognitive compromise. This decline in neurocognitive function mirrors reports of decline found in American football (77). Also, it has been proposed that multiple concussions may cause cumulative neuropsychologic impairment in athletes (129, 132). Symptoms of concussion typically resolve spontaneously. However, a subset of athletes who sustain a concussion develop post-concussive syndrome (66) and continue to have symptoms of headache, dizziness, impairment of recent memory and concentration for prolonged periods of time. Another potential correlate after concussion is the second impact syndrome. This was first described by Schneider in 1973 (81, 107). The second impact syndrome is an uncommon but serious occurrence in which a disturbance of cerebrovascular autoregulation and consequent intracranial vasodilatation and cerebral edema can overcome the brain s compensatory mechanisms resulting in uncal or central herniation (23, 66, 108). The incidence of second impact syndrome in soccer is unknown, but is always a consideration given the potential for athletes with minimally symptomatic or missed concussive injuries who return to play too quickly after an injury. IMAGING ABNORMALITIES Structural changes in the brain after a concussion have been demonstrated in soccer players (5, 60). Sortland and Tysvaer (114) demonstrated that one-third of former elite soccer players had cerebral atrophy as demonstrated on computerized tomography scan. Autti et al. (12) demonstrated that 11 of 15 amateur soccer players had abnormal findings on MRI that were thought to correlate with cognitive dysfunction (16). Jordan et al. (59) noted that nearly half of the U.S. Men s National Soccer team demonstrated abnormal findings on MRI that were believed to be the result of repetitive heading. These studies suggest that soccer players who have not manifested a definitive concussive injury still demonstrate radiographic evidence of brain injury that is probably the result of the cumulative effect of repeated subconcussive impacts to the head (16, 36). Electrophysiologic studies have also demonstrated abnormal findings after a concussion, especially in the presence of LOC. This has been found to be followed by a period of cortical depression before recovery of electroencephalogram (EEG) (112). Tysvaer Storli (129, 130) performed EEG studies in active and retired professional soccer players and found a significantly increased incidence of EEG disturbances in these players compared with controls. Interestingly, EEG disturbances were found to be most pronounced among younger players. EEG recordings have not been found to be strongly predictive of post-concussive symptoms (131). Stalnacke et al. (115) reported that serum concentrations of biochemical markers of brain tissue damage S-100B and neuronspecific enolase were significantly increased after games compared with baseline before game values. In addition, S-100B levels were found to be significantly correlated to the number of headers during play. HOW CAN BE REDUCED? Although our understanding of risk factors for sports-related concussions is far from complete, a number of considerations from other contact sports can be gleaned (1). Of primary importance, is the development and testing of effective equipment during play. In addition, educating young athletes on the safe and appropriate techniques used during play is of the utmost importance (18, 56). This must progress in conti- WORLD NEUROSURGERY 78 [5]: 535-544, NOVEMBER 2012 www.worldneurosurgery.org 539

nuity with the understanding on the part of the families and caching staff as to what skills are too advanced and/or aggressive for young players to use during play. Soccer balls allowed to be used should be of specific properties. The size of the soccer ball used must be age-appropriate (66, 113). This is particularly important for children who, because of their inexperience at heading and immature skull and neck anatomy, have been suggested to be more at risk of concussion (7, 8, 37, 79, 101). In addition, appropriate inflation pressures of soccer balls need to be ensured as it has been suggested that hyperinflation may be responsible for headache and concussion (66, 101). Strict adherence to the rules of competition can further enhance safety by minimizing the impact of those players with poor skills or a dangerously aggressive approach to the game (66). Finally, preparation by the coaching staff as to how to evaluate young players for concussive injury in addition to understanding those criteria that result in removing an injured player from competition and the steps by which to safely return an athlete to competition after injury. Of critical importance is the prompt and accurate diagnosis of a concussion once it occurs. This is vital as concussions are largely underdiagnosed (1, 39). This is of significant importance in players with a prior history of head trauma during play, given their increased risk for future concussions (39, 51, 52, 140). ON FIELD MANAGEMENT Whether it be for soccer or any other athletic endeavor, initial evaluation and diagnosis is crucial in both identifying the occurrence of concussion and determining the timeline for return to play. After a concussion, the ABCs of resuscitation must be followed, and, in an unconscious player, stabilization of the spine is required. Determining the mechanism of injury (if possible) and duration of unresponsiveness is necessary. This should be followed by serial neurological examinations, including mental status examination, with specific attention to focal signs that may suggest a more significant injury. A neuropsychologic examination should be conducted, with specific attention given to the concussed player s orientation to time, place, and person. Examination of the face and neck for lacerations and fractures is also necessary. Players should be observed for at least 15 minutes, and should not be left unattended during this period. Repeat evaluations should be performed as are necessary, and return to play criteria must be followed. Any player with AAN grade 3 concussion or demonstrating focal signs should undergo additional evaluation at a qualified medical center (3, 11, 22, 37, 62, 66, 73, 80). We have previously outlined the several role of the neurosurgeon in the management of concussion in American football, which remains valid in cases of concussions sustained in soccer (73). Neurosurgeons, in conjunction with the trainers, must play a strong leadership role in the multidisciplinary approach to management of concussions sustained in soccer or any athletic event. In spite of such primary and secondary preventive measures, concussions in soccer will continue to occur. Considering the frequency of concussions in soccer, the serious sequelae of these concussions, and the fact that almost half of concussed soccer players were noncompliant with recommended AAN return-to-play guidelines (137), further measures must be taken to protect players. BENEFITS OF HEADGEAR During the past three decades, there has been developing interest in the potential role of headgear in soccer (21, 34, 90, 95). The International Federation of Association Football, the U.S. Soccer Federation, the National Collegiate Athletic Association, and the National Federation of State High School Associations all permit the use of protective headgear during soccer (4, 35). In addition, protective headgear has become a requirement by some soccer leagues (10, 21). The U.S. Soccer Federation announced that protective headgear provides a measurable benefit in head-to-head injuries and permits players to wear headgear at their own discretion. The assumption is that the use of headgear will reduce the risk of concussion by lessening impact acceleration and, consequently, reducing neurological sequelae as a result of head injuries incurred during soccer (75). Improvements in headgear used in American football and the introduction of regulatory standards for their use have resulted in a considerable decrease in the incidence and severity of head injuries and resultant fatalities (41, 73, 74, 139). In a laboratory model designed to simulate head acceleration after impact from a propelled soccer ball at differing velocities, Naunheim et al. (94) found that the use of protective headgear resulted in significant decreases in head acceleration after the highest impact velocities and pressures. However, there were no such decreases after head blows of less intensity in this study. Broglio et al. (21) evaluated the efficacy of three brands of protective headgear used in soccer: the Full90 (Full90 Sports, Inc., San Diego, California, USA), Headblast (Benian s Enterprises LLC, St. Louis, Missouri, USA), and Protector (soccerheadband.com, Brandon, South Dakota, USA). For a soccer ball travelling at 35 mph (approximately 56.5 km/h) their data demonstrated a significant decrease in peak impact force of about 12.5% (approximately 400 N) in all brands compared with no headgear. No specific headgear was found to be significantly more protective. Time-to-peak force was most effectively reduced by the Protector headgear. In a biomechanical analysis, McIntosh et al. (89) demonstrated considerable improvement in impact energy attenuation with only minor design changes in headgear, although current designs of headgear for soccer did not reduce the probability of concussion (90). Whether these improvements translate into a reduction in frequency or severity of concussion sustained during soccer and other contact sports remains to be determined. Other studies of clinical efficacy have also demonstrated benefit. Withnall et al. (135) showed that the use of headgear commercially available in North America (Full90, Head Blast, Kangaroo) conferred protection against head-to-head impacts, with an overall protection of nearly 33% for linear acceleration and maximum value of head impact power. However, they also demonstrated that the headgear tested did not significantly mitigate impacts from ball contact alone. This was attributed to the considerable ball deformation that occurs on contact relative to the thickness of the protective headgear being studied. In a recent cross-sectional study of adolescent soccer players, Delaney et al. (34) demonstrated a reduced incidence of concussion in players who wore headgear during 540 www.sciencedirect.com WORLD NEUROSURGERY, DOI:10.1016/j.wneu.2011.10.032

Table 3. American Society for Testing and Materials Headgear Requirements for Soccer ASTM F2439 06 Requirements Anvils Head to head, ground, post simulators Velocities 2.0 3.8 m/s Upper limit 80g Multiple impacts 6 impacts at 1-min intervals, 15% decrease in performance Coverage Tilted stripe, forehead to occiput Labeling ID of product, manufacturer, ASTM standard; use only in football ASTM, American Society for Testing and Materials. play. Players that did not wear protective headgear were 2.65 times more likely to become concussed during play. Furthermore, the study demonstrated that the frequency of lacerations, abrasions, and contusions was reduced in players who wore protective headgear, suggesting that players wearing headgear do not play more aggressively. It has been suggested that soccer protective headgear may not provide proper protection for all players, especially female players who demonstrate more pronounced head accelerations when wearing headgear (123). This issue becomes very important considering that female soccer players may be more prone to developing concussions when compared with their male counterparts (31, 35, 46). Delaney et al. (36) outline groups of soccer players that would most likely benefit from wearing headgear during soccer practice and games. This includes goalkeepers, athletes who have previously sustained concussion considering their increased risk of further concussions (39, 51, 140), and children. Children are also believed to benefit greatly from wearing headgear during soccer. Having weaker neck muscles, thinner skulls, and proportionately larger heads (17, 36, 127), children are at higher risk of injury after head trauma when compared with adults. This is compounded by the fact that children are less skilled at heading the ball. Goalkeeping is a position that is particularly high risk for concussions (19, 39, 119, 125) as a result of being exposed to oncoming shots at high speeds (129), and the additional risk from goalposts (8, 22, 26). STANDARD FOR SOCCER HEADGEAR Headguards have numerous designs that offer partial or full padding. These protective headgear are legal, provided that they do not pose a risk to other players (69). Some designs may, in fact, prove dangerous, as they may facilitate transmission of the impact to the brain (54, 97). The American Society for Testing and Materials has established specific requirements for headgear in soccer (Table 3). CONCLUSION Soccer is the most popular sport in the world and has a following of millions in the United States. Soccer is a sport not traditionally identified as high risk for concussions, yet several studies have shown that concussion rates in soccer are comparable with, and often exceed those of, other contact sports. Head injury during soccer is usually the result of either direct contact (i.e., head vs. head, head vs. knee, head vs. the ground) or contact with the ball while heading the ball. Relationships between the number of headers sustained in a single season and the degree of cognitive impairment (attention and visual/verbal memory) have been demonstrated. It is also likely that multiple concussions may cause cumulative neuropsychologic impairment in soccer players. Although our understanding of risk factors for sports-related concussions is far from complete, a number of measures can be addressed to potentially reduce the incidence. Of primary importance is the development and testing of effective equipment during play. The assumption is that the use of headgear will reduce the risk of concussion by lessening impact acceleration and, consequently, reducing neurological sequelae as a result of head injuries incurred during soccer. The introduction of regulatory standards has been associated with an increase safety in a number of sports. The American Society for Testing and Materials has established specific requirements for headgear in soccer. Soccer balls allowed to be used should also be age-appropriate. Educating young athletes on the safe and appropriate techniques used during play is also of the utmost importance. They must progress in continuity with the understanding on the part of the families and coaching staff as to what skills are too advanced and/or aggressive for young players to use during play. Strict adherence to the rules of competition can further enhance safety by minimizing the impact of those players with poor skills or a dangerously aggressive approach to the game. As the intentional use of the head to impact another player s head presents a very high risk of concussion, we suggest a harsher position on the part of supervisory bodies in such instances. 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