5


Consequences of Repetitive Head Impacts and Multiple Concussions

In recent years there has been an increase in research on the cognitive and neuropathological consequences of repetitive head impacts and multiple concussions in athletes. Given the frequency of head impacts in contact sports, the public health implications of these consequences may be significant. This chapter addresses those elements of the committee’s statement of task that concern the effects of “subconcussive” head impacts (i.e., head impacts that do not result in symptoms consistent with a diagnosis of concussion) and multiple concussions. The chapter reviews the clinical manifestations, neuroimaging features, risk factors, and animal studies related to repetitive head impacts and multiple concussions. It also discusses the possible long-term neuropathological consequences associated with repetitive head impacts and multiple concussions, including chronic traumatic encephalopathy (CTE), an emerging diagnostic entity associated with retired athletes with a history of head injury as well with as military personnel exposed to repeated brain injury from blast and other causes. The goals of this chapter are to provide a comprehensive review of the current literature, to clarify controversies, and to point out important directions for future research.

NEUROPSYCHOLOGICAL AND NEUROPHYSIOLOGICAL CONSEQUENCES

Studies of Repetitive Head Impacts

As with much of the clinical literature on the consequences of concussions in sports, the generalizability of many studies of the effects of repeti-



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5 Consequences of Repetitive Head Impacts and Multiple Concussions In recent years there has been an increase in research on the cogni- tive and neuropathological consequences of repetitive head impacts and multiple concussions in athletes. Given the frequency of head impacts in contact sports, the public health implications of these consequences may be significant. This chapter addresses those elements of the committee’s statement of task that concern the effects of “subconcussive” head im- pacts (i.e., head impacts that do not result in symptoms consistent with a diagnosis of concussion) and multiple concussions. The chapter reviews the clinical manifestations, neuroimaging features, risk factors, and animal studies related to repetitive head impacts and multiple concussions. It also discusses the possible long-term neuropathological consequences associated with repetitive head impacts and multiple concussions, including chronic traumatic encephalopathy (CTE), an emerging diagnostic entity associated with retired athletes with a history of head injury as well with as military personnel exposed to repeated brain injury from blast and other causes. The goals of this chapter are to provide a comprehensive review of the current literature, to clarify controversies, and to point out important directions for future research. NEUROPSYCHOLOGICAL AND NEUROPHYSIOLOGICAL CONSEQUENCES Studies of Repetitive Head Impacts As with much of the clinical literature on the consequences of concus- sions in sports, the generalizability of many studies of the effects of repeti- 203

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204 SPORTS-RELATED CONCUSSIONS IN YOUTH tive head impacts is limited by methodological weaknesses. For example, helmet-based head impact recording devices are typically set to record only impact forces over a minimum threshold (e.g., 10 g of linear acceleration; see Duma et al., 2005) and, therefore, do not record all impacts to the head. Although recent advances in technical, statistical, and clinical knowledge have helped to improve research on repetitive head impacts, earlier findings have to be viewed in the context of history: Their importance lies more in their groundbreaking attempts to quantify relevant variables and not neces- sarily in their specific findings. Findings from Soccer Studies In soccer, athletes experience repetitive head impacts from using their heads to strike the ball for passing and shooting. Older research involving amateur and professional soccer players indicated an association between cumulative heading and neuropsychological impairments (see, for example, Matser et al., 1998, 1999, 2001; Sortland and Tysvaer, 1989; Tysvaer and Lochen, 1991). One study of 37 former professional soccer players found mild to severe deficits in the areas of attention, concentration, memory, and judgment in 81 percent of the players. The authors speculated that this find- ing could be indicative of permanent organic brain damage resulting from repeated traumas from heading the ball (Tysvaer and Lochen, 1991). In another study involving 53 active professional soccer players, impairments in memory, planning, and visuo-perceptual tasks were observed and com- pared with those in non-contact-sport athlete controls. Among the soccer players, performance on these tasks was inversely related to the frequency of heading the ball (Matser et al., 1998). Computed tomography scans of 33 former professional soccer players identified central brain atrophy in one-third of study participants, although scans were only visually inspected, and there were no baseline or control comparisons (Sortland and Tysvaer, 1989). Several other studies, including more recent ones, involving youth soc- cer players have found no effect of heading on neurocognitive performance (Broglio and Guskiewicz, 2001; Guskiewicz et al., 2002; Kaminski et al., 2007, 2008; Kontos et al., 2011; Stephens et al., 2010; Straume-Naesheim et al., 2005). For example, Guskiewicz and colleagues (2002) found no differences in neurocognitive function or Scholastic Aptitude Test scores between collegiate soccer players (n=91) and groups of athletes from other contact and non-contact sports (n=96) or between the collegiate soccer players and non-athletic controls (n=53), suggesting that soccer players are not differentially affected by soccer playing (and, by extension, heading). Furthermore, studies that have directly assessed changes in cognition related to heading a soccer ball have failed to establish any relationship be-

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CONSEQUENCES OF REPETITIVE HEAD IMPACTS 205 tween heading and neurocognitive changes. Following detailed observation of heading frequencies by 63 high school soccer players and the adminis- tration of Immediate Post-Concussion Assessment and Cognitive Testing (ImPACT), Kontos and colleagues (2011) found no differences in neurocog- nitive performance or symptoms among low-, moderate-, and high-exposure header groups. Similarly, Putukian and colleagues (2000) found no changes in neuropsychological test scores between pairs of collegiate soccer players who headed the ball in practice for 20 minutes compared with those who did not head in practice. Kaminski and colleagues conducted two studies with 71 (2007) and 393 (2008) female collegiate soccer players. Using heading counts as the independent variable and pre- and post-season balance and neuropsychological tests to determine neuropsychological changes, they found no significant relationships on any test measure. Early research using magnetic resonance imaging (MRI) and cognitive tests found no significant cognitive impairments or differences on MRI scans among soccer players, boxers, and track and field athletes (Haglund and Ericksson, 1993). In a recent study using diffusion tensor imaging (DTI) scans on 12 German soccer players and 11 swimmers, several group differences in brain white matter were noted, including increased radial diffusivity and axial diffusivity in soccer players compared to swimmers (­ oerte et al., 2012). Although the authors of the study suggest that head- K ing in soccer may lead to neurophysiological changes in the brain, this study’s generalizability is limited because of the small number of partici- pants and because it did not include a baseline scan. Furthermore, it is not clear what the functional significance of such findings would be. In summary, studies of the consequences of heading in soccer have obtained mixed results, with more recent studies showing no relationship between heading and neuropsychological impairment. The positive findings of some older studies may have been due in part to the more frequent use in the 1980s and 1990s of soccer balls that absorbed more water, increas- ing the weight of the ball by up to 20 percent and potentially making them more dangerous for heading (Smodlaka, 1984). Today, players use water- proof synthetic soccer balls that absorb less water (Kirkendall and Garrett, 2001). The DTI study (Koerte et al., 2012) appeared to show neurological differences in a very small sample. Due to small sample sizes and other methodological limitations, caution is required in interpretation of these studies’ findings. Findings from Football and Ice Hockey Studies As is the case with soccer players, football and ice hockey players can incur repetitive head impacts (Brainard et al., 2012; Crisco et al., 2010, 2011, 2012). For example, a lineman in football who tackles another

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206 SPORTS-RELATED CONCUSSIONS IN YOUTH player with his head in successive plays experiences a series of repetitive head impacts. Hockey players may experience repetitive head impacts from collisions with the board and with other players. McAllister and colleagues (2012) examined repetitive head impacts over a single season in collegiate football and ice hockey athletes and compared those athletes with a group of athletes who played a non-contact sport on a variety of measures. Contact athletes wore accelerometer-instrumented helmets and took pre- and post-season ImPACT tests. A subset from one of the three Division I universities also completed a paper-and-pencil neu- ropsychological battery and had preseason and postseason neuroimaging. There were no group differences on cognitive tasks over a sport season. The researchers also examined baseline neurocognitive tests scores across three sport seasons and found no differences on baseline assessments among the sport groups, suggesting that previous exposures to contact did not affect test scores negatively. However, the researchers did report that a higher percentage of the contact sport athletes performed worse than those in the non-contact group on a measure of new learning (California Verbal Learning Test), with no ImPACT composites showing significant change. Furthermore, the authors found that impact exposure above the 95th per- centile in frequency during the last week of the season was related to poorer performance on the Trail Making test, a measure of visual attention and task switching, and that the peak linear acceleration for the season was related to slower ImPACT reaction times. A relationship among recent bio- mechanical exposures, brain white matter integrity, and lower scores was also found, although the absolute value of (significant) test score decline did not reach impairment level. Other studies of the effects of repetitive head impacts in high school and collegiate football players have found no association with neurocog- nitive impairment or physiological changes (see, for example, Broglio et al., 2011; Gysland et al., 2012; Miller et al., 2007). However, these stud- ies all have methodological weaknesses. Only McAllister and colleagues (2012) used non-contact controls and adjusted neurocognitive test scores for practice effects, baseline levels, regression to the mean, and relevant demographic factors, while also comparing seasonal exposure and recent exposures across biomechanical measurements of magnitude and frequency. A few small studies of high school and collegiate football and hockey players have looked at DTI, neurocognitive test scores, and biomechanical data; these have found axonal changes but mixed neuropsychological find- ings (Bazarian et al., 2012; Breedlove et al., 2012; Talvage et al., 2010). Evidence for the effects of repetitive head impacts on diffuse axonal injury in humans comes largely from DTI studies that measure directionality (frac- tional anisotropy, or FA) and regularity (mean diffusivity, or MD) of white matter tracts. This technique showed pre-season to post-season changes in

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CONSEQUENCES OF REPETITIVE HEAD IMPACTS 207 a small sample of high school athletes (n=10, 16 to 18 years old, hockey or football) relative to controls (n=5, 16 to 35 years old) following self- reported repetitive head impacts (Bazarian et al., 2012). While pre- and post-season FA and MD changes (calculated as the percentage of white matter voxels showing either a significant increase or a significant decrease) were largest in a concussed player with greater than 3 percent change, those athletes with repetitive head impacts had intermediary changes of more than 1 percent on average, while the controls had insignificant changes of less than 0.5 percent on average. These findings warrant further investiga- tion in larger samples with same-aged comparison groups. Traumatic brain injury may result in disruption of the blood-brain bar- rier (i.e., increased permeability of the brain vasculature) (Neuwelt et al., 2011). Marchi and colleagues used DTI and serum measurements of S100B (a protein secreted by cells in the central nervous system and used as a marker of blood-brain barrier disruption [Blyth et al., 2009, 2011; Marchi et al., 2004]) and S100B auto-antibodies, to evaluate whether head impacts below the threshold for a diagnosis of concussion can disrupt the blood- brain barrier. Sixty-seven college football players were enrolled. In a subset of players (n=15) for whom pre- and post-game blood samples were avail- able, only those players with the most subconcussive head impacts based on self-report and post-game review of the game film had detectable serum levels of S100B and elevated levels of auto-antibodies against S100B. Serum S100B antibodies predicted lasting changes in mean brain white matter dif- fusivity in a subset of players (n=10) who had preseason and postseason and 6-month follow-up DTI scans. Post-season S100B auto-antibodies also correlated with impulse control and balance problems. Although the study sample is too small to make firm inferences, this research provides prelimi- nary evidence that repetitive head impacts that do not result in a diagnosis of concussion may disrupt the blood-brain barrier. It is important to note that there are sources of serum S100B outside of the central nervous system (e.g., fat cells), although this does not preclude use of S100B as a biomarker of brain injury (Marchi et al., 2013). Functional magnetic resonance imaging (fMRI) studies have begun to examine blood-oxygen-level dependent brain activity following repeti- tive head impacts. Talvage and colleagues (2010) prospectively followed 11 male high school football players ages 15 to 19 both preseason and postseason. A negative association was observed between the number of subconcussive repetitive impacts to the front of the head and activity in the prefrontal cortex, as indicated by blood-oxygen-level dependent signals on the fMRI during the performance of a working memory test. These players also exhibited neurocognitive deficits as measured by ImPACT scores on visual memory. Together these studies suggest changes in cognitive function the brain

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208 SPORTS-RELATED CONCUSSIONS IN YOUTH following repetitive head impacts in football and hockey players. However, the types of cognitive impairment and brain changes that are observed vary by study, and the results are based on small sample sizes, which raises ques- tions about the reliability of these studies. Findings from Boxing Studies Many youth continue to participate in boxing even though several medical groups have called for its discontinuation due to the incidence of brain injury (Purcell and LeBlanc, 2012). Although many youth and ama- teur boxers wear protective gear and follow rules that are different from those for professional boxers, a primary goal of boxing is to attack the head and face of the opponent, which often results in a concussion or more severe brain injury (Jordan, 1987). Indeed, the association of boxing and traumatic brain injury (TBI) is very well-recognized in the medical litera- ture. The so-called punch-drunk syndrome was first recognized as early as 1928 (Wilberger and Maroon, 1989), and it is associated with personality disturbances, dysarthria, or Parkinson-like disturbances. There is ample evidence supporting the association of boxing with chronic traumatic brain injury. Several researchers have found brain abnor- malities in professional boxers (see, for example, Casson et al., 1984; Drew et al., 1986; Kaste et al., 1982; Morrison, 1986; Ross et al., 1983). Jordan and colleagues (1997) examined boxers who had a high exposure to head contact (defined as having had 12 or more professional bouts) to boxers with low exposure to head contact (defined by less than 12 professional bouts) on neurocognitive performance, symptoms, and genetic testing. The authors reported that athletes with a high exposure to head contact had lower cognitive function than did those with low head contact exposure. The largest DTI studies to date on repetitive head impacts are those in- volving professional boxers (ages 20 to 52), with sample sizes ranging from 24 to 81. Across these studies, microstructural abnormalities were found as indicated by increased regional and whole brain diffusion and decreased FA in boxers relative to control subjects (Chappell et al., 2006; Zhang et al., 2003, 2006). These findings are further supported by a high-resolution MRI study of 100 boxers (85 with complete data, ages 19 to 42 years) showing a significant correlation between years of boxing and diffuse axonal injury (Orrison et al., 2009). Together these studies suggest that boxing is associated with possible long-term cognitive decline and axonal injury. Although boxing is an ex- treme example of a contact sport, the neuropsychological and imaging findings from studies of boxers supplement those of athletes who play other contact sports such as football and hockey.

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CONSEQUENCES OF REPETITIVE HEAD IMPACTS 209 Studies of Multiple Concussions As discussed in Chapter 2, there is some evidence from both animal studies and research involving humans that the brain is at increased risk while recovering from a concussion. Thus, a repeat injury while recovering from a prior concussion may occur with less force, take longer to resolve, and in rare cases lead to catastrophic results (e.g., second impact syndrome) (Bey and Ostick, 2009; Simma et al., 2013, Slobounov et al., 2007). Indeed, this is the purpose of the advice “When in doubt, sit them out” (McCrory et al., 2013). A related concern is the effect of a history of concussions on cognition and brain physiology. In a retrospective survey of 223 high school athletes, 20 percent reported a history of at least one concussion (Moser et al., 2005), suggesting that many youth sustain multiple concussions over the course of their athletic careers. The committee reviewed 16 studies that attempted to answer various questions regarding the effects of multiple concussions. Four additional studies focused on professional and adult athletes and so were not in- cluded. Most of the 16 studies assessed the neurocognitive function and symptom load of “stable” athletes (those not currently concussed) and compared groups based on the reported histories of previous concussions. This cross-sectional approach has many limitations, as noted by Iverson and colleagues (2012). A primary difficulty is finding enough athletes with a history of three or more concussions to provide sufficient statistical power. Concussions are a relatively low-base-rate phenomenon, which means that obtaining a large enough sample of individuals who have sustained multiple concussions is particularly difficult. High School–Age Athletes Five studies of high school athletes compared symptom presentations, and three compared neurocognitive findings. Schatz and colleagues (2011) compared baseline symptoms of 251 high school athletes who had no reported concussions with 260 athletes who had had one concussion and 105 athletes who had had two or more. The athletes with a history of two or more concussions had significantly more cognitive problems, physical symptoms, and sleep problems at the time of pre-season baseline evaluation than those with no history of concussions. On the other hand, in a study of 867 male high school and college athletes with no (n=664), one (n=149), and two (n=54) previous concussions, Iverson and colleagues (2006) found no group differences in neuropsychological test performance or symptom reporting. Collins and colleagues (2002) attempted to study the effect of previous concussions in high school athletes by characterizing the on-field signs and

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210 SPORTS-RELATED CONCUSSIONS IN YOUTH symptoms of a subsequent concussion. Sixty athletes with no concussion history were compared with 28 athletes who had had three or more concus- sions. Those with a history of three or more concussions were significantly more likely to suffer loss of consciousness, anterograde amnesia, and men- tal status changes lasting longer than 5 minutes. Among studies that examined neuropsychological test scores, two had conflicting results (Iverson et al., 2006; Moser et al., 2005), and two had too few subjects to have confidence in the results (Elbin et al., 2012; Moser and Schatz, 2002). Moser and colleagues (2005) compared 82 athletes with no concussions to 56 with one concussion, 45 with two or more (although they had had no injuries for at least 6 months), and 40 recently concussed athletes. Athletes were compared on neuropsychological test scores (Re- peatable Battery for the Assessment of Neuropsychological Status, Trail Making). While there was a significant difference between groups, the only post hoc result reported was that those with two or more concussions were not different from the recently concussed. Inspection of the data indicates that scores of the recently concussed athletes were lower than those of the no- and one-concussion groups. In contrast, Iverson and colleagues (2006) compared baseline ImPACT scores for 664 athletes with no history of concussion, 149 with a history of one previous concussion, and 54 with a history of two. After controlling for education level, no significant differ- ences were found between the groups. Overall the findings from studies of the effects of multiple concussions on high school athletes are mixed. In addition to the number of concus- sions, the interval between concussions may be an important recovery- related factor to consider. College-Age Athletes Ten studies of college-age athletes were reviewed. Four studies used symptom presentation as the dependent variable (Collins et al., 1999; Covassin et al., 2008; Guskiewicz et al., 2003; Iverson et al., 2012). Collins and colleagues (1999) found increased symptoms among those athletes with more concussions at baseline, while Guskiewicz assessed the time to symptom resolution of a current concussion based on the number of previ- ous concussions. Neither Covassin and colleagues (2008) nor Iverson and colleagues (2012) found a relationship between symptom levels at baseline testing and the number of previous concussions. However, among those studies that looked at neuropsychological test scores, four found signifi- cant differences between previously concussed and non-concussed athletes (Collins et al., 1999; Covassin et al., 2008, 2010; De Beaumont et al., 2009), while four failed to find differences (Broglio et al., 2006; Bruce and Echemendia, 2009; Guskiewicz et al., 2002; Iverson et al., 2012). Three

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CONSEQUENCES OF REPETITIVE HEAD IMPACTS 211 studies had too few cases to be considered (De Beaumont et al., 2007; Elbin et al., 2012; Killam et al., 2005). In 1999, Collins and colleagues compared baseline symptom totals among 179 athletes with no concussion history, 129 with one, and 78 with a history of two or more. Significant differences were found for symptoms. The researchers also noted that baseline symptom scores increased with the frequency of previous concussions. In a large sample of 184 college football players who suffered concussions, Guskiewicz and colleagues (2003) found that 30 percent of the athletes with more than three concussions took lon- ger than 1 week for symptoms to resolve, compared to only 15 percent of those with one concussion taking more than a week to resolve. Collins and colleagues (1999) also compared baseline neuropsychologi- cal test scores. Significant differences were found on two tests of process- ing speed. However, the average neuropsychological test scores for the group with two or more concussions were within normal limits. In 2002, Guskiewicz and colleagues compared collegiate soccer players with histories of concussion to soccer players, other athletes, and non-athletes with no histories of concussion. He found no significant differences at baseline on any of a battery of neuropsychological tests. Broglio and colleagues (2006) compared baseline test scores of 163 athletes with no history of concus- sions to 43 athletes with one previous concussion, 18 with two, and 11 with three. The researchers administered both the Concussion Resolution Index (CRI), an Internet-based neurocognitive test that assesses “simple” and “complex reaction time and process speed, and ImPACT and found no differences in any scores. The small number of athletes with two or more concussions limited the study. Covassin and colleagues (2010) found no differences on any ImPACT composite test between athletes with no previous concussions and those with one previous concussion. However, both the two-concussion (n=50) and three-plus concussion (n=48) groups scored significantly lower on the verbal memory test than did the no-concussion group (n=50); furthermore, visual memory scores were significantly lower for those with a history of three or more concussions (n=48) than those with no concussion history. The authors concluded that they had demonstrated a partial dose-response relationship for those tests. In a prospective study Guskiewicz and colleagues (2003) followed a large sample of collegiate football players over 3 years; of those athletes, 184 experienced concussions during the study. The researchers reported that athletes with a history of three or more previous concussions had three times the risk of getting a subsequent concussion than those with no previous history. In a study of the effects of concussion history on recovery after a sub- sequent concussion, Covassin and colleagues (2008) compared post-injury

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212 SPORTS-RELATED CONCUSSIONS IN YOUTH neurocognitive test scores 1 day out and 5 days out from the injury between 56 athletes with no previous concussion and 21 with a history of two or more concussions. While they found significant differences in all four com- posite scores at day 1 and in two composite scores at day 5 (verbal memory and reaction time), they did not control for baseline scores or compare the number of significantly changed scores (CRI) between groups. There were no symptom level differences at any point. Methodological differences make comparisons among these studies difficult. Differences in how concussion history is measured (e.g., two and more, three and more, etc.) may obscure an important threshold. Variable controls, small sample sizes, and cross-sectional designs make generaliza- tions difficult. Group-level studies are mixed in terms of results, and better methodologies are needed to identify the timing and cumulative effects of multiple concussions. Longitudinal studies and studies highlighting indi- vidual differences are lacking. Collaborative studies may be needed to ac- cumulate larger samples of multiply concussed athletes. MULTIPLE CONCUSSIONS AND DEPRESSION AND SUICIDE Surveys of retired professional athletes provide some evidence that a history of multiple concussions increases risk for depression (Didehbani et al., 2013; Guskiewicz et al., 2007; Kerr et al., 2012). In a survey of more than 2,500 retired professional football players, 269 of the respondents (11.1 percent) reported having had a prior or current diagnosis of clinical depression. After controlling for parameters such as age, number of years since retirement, number of years played, physical condition, and diag- nosed comorbidities such as osteoarthritis, coronary heart disease, stroke, cancer, and diabetes (but not substance abuse or intervening psychosocial issues), the authors found an increasing linear relationship between history of concussion and diagnosis of lifetime depression (p < 0.005). Compared with retired players with no history of concussion, retired players report- ing three or more previous concussions (24.4 percent) were three times more likely to have been diagnosed with depression; those with a history of one or two previous concussions (36.3 percent) were 1.5 times more likely to have been diagnosed with depression (Guskiewicz et al., 2007). In another study of 30 retired professional football players with a history of concussion versus 29 age- and IQ-matched controls without a history of concussion, a significant correlation was observed between number of lifetime concussions and current cognitive symptoms of depression as measured by the Beck Depression Inventory II. These findings suggest that the number of concussions an individual has sustained may be related to later depressive symptomology (Didehbani et al., 2013). Imaging research is beginning to explore the relationship between depression symptoms and

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CONSEQUENCES OF REPETITIVE HEAD IMPACTS 213 brain white matter abnormalities in retired athletes (Hart et al., 2013; Strain et al., 2013). Athletes who retire as a result of suffering multiple concussions may experience distress and reduced quality of life, similar to outcomes reported following other serious athletic injuries (Caron et al., 2013; Kuehl et al., 2010; Mihovilovic, 1968). Social support has been identified as important to psychological recovery following more severe brain injuries (Gan et al., 2006) as well as within the sport injury and rehabilitation process (Bianco, 2001; Clement and Shannon, 2011; Wiese-Bjornstal et al., 1998). Individu- als who have sustained concussions are also likely to benefit from social support. However, little is known about the role of social support in manag- ing athletes’ concussion symptoms and related psychosocial outcomes. The effect of support may be complicated in situations where norms encourage athletes to play through their injuries and when athletes fear being stig- matized by peers as lacking toughness (Safai, 2003; Young et al., 1994). Qualitative interviews with five retired National Hockey League players who had retired due to symptoms following multiple concussions revealed that they were significantly affected by their injuries in their postathletic careers and in their personal relationships. They continued to feel debili- tated by post-concussive symptoms and experienced symptoms of anxiety and depression. Three of the participants reported thoughts of suicide in the months immediately following their retirement. Though it is difficult to distinguish whether the experiences of these former athletes were a result of multiple concussions or the end of their careers in professional ice hockey, these findings indicate a need for professional support for athletes when they are recovering from concussions and during the transition to their post-athletic careers (Caron et al., 2013). Recently, after several highly publicized suicides by professional ath- letes who showed evidence of CTE, there has been growing interest in understanding the relationship between multiple concussions and suicide (Omalu et al., 2006; Reider, 2012). Though there is some indication of a relationship between number of previous concussions and risk of develop- ing depression, very little research has evaluated the relationship between concussions and suicidal thoughts and behaviors. There are certainly theo- retical reasons why individuals who have sustained concussions might be predisposed to suicidal ideation and behavior. For example, there is grow- ing evidence that individuals who attempt suicide, particularly those who engage in high lethality attempts, show deficits in attention, working mem- ory, and risk assessment, which overlap with the neurocognitive residua of concussions, both in the short term and, for those with longer-lasting post- concussive symptoms, in the long term as well (Bridge et al., 2012; Jollant et al., 2005; Keilp et al., 2001, 2013). Thus, the deficits associated with a concussion may lower the threshold for a person with suicidal thoughts to

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