Sports-Related Concussions in Youth Improving the Science, Changing the Culture (2014) / Chapter Skim
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5 Consequences of Repetitive Head Impacts and Multiple Concussions
5 Consequences of Repetitive Head Impacts and Multiple Concussions
Pages 203-238
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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)
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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)
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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)
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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 neurocognitive impairment or physiological changes (see, for example, Broglio et al., 2011; Gysland et al., 2012; Miller et al., 2007)
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studies have begun to examine blood-oxygen-level dependent brain activity following repetitive head impacts. Talvage and colleagues (2010)
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The largest DTI studies to date on repetitive head impacts are those involving professional boxers (ages 20 to 52) , with sample sizes ranging from 24 to 81.
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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.
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Overall the findings from studies of the effects of multiple concussions on high school athletes are mixed. In addition to the number of concussions, the interval between concussions may be an important recoveryrelated factor to consider.
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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.
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. 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.
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. 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.
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Oquendo and colleagues (2004) examined a clinical sample of depressed patients and found that while a past history of TBI was a risk factor for suicidal behavior, this increased risk for suicidal behavior was explained by the higher rates of substance abuse, cluster B personality disorder, and higher self-reported aggression and hostility in those with TBI.
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EXPERIMENTAL MODELS Behavioral and Cognitive Consequences Several experimental models of repeat TBI have demonstrated changes in behavioral outcome in the absence of overt pathology (DeFord et al., 2002; Prins et al., 2010; Shitaka et al., 2011)
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impacts caused ventricular enlargement and white matter atrophy. Both reactive astrocytosis throughout the cortical layers and axonal swellings increased with repeat TBI.
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mice were given either a sham injury, a single injury, or two injuries 24 hours apart, and axonal damage and astrocytic reactivity were histologically assessed 24 hours post injury. The bAPP immunohistochemical labeling was positive in the ipsilateral white matter and was significantly greater in animals exposed to repeat TBI than in the single-injury or sham-injury animals.
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These studies emphasize the need for establishing age-appropriate biomarkers for cerebral vulnerability to help inform return-to-play guidelines. The human findings concerning the effects of repetitive head impact on brain physiology are supported by controlled animal studies which show increased vulnerability to axonal damage and cognitive impairment with repeated mild head injury (Barkhoudarian et al., 2011; Laurer et al., 2001)
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has been used to examine the effects of multiple concussions on brain metabolites. This research shows that changes in NAA, a marker of neuronal injury, take longer to resolve following a second concussion in nonprofessional athletes -- an average of 45 days (n=13)
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LONG-TERM NEURODEGENERATIVE CONSEQUENCES In general there is a paucity of literature on the long-term neuropathological consequences of repeated or chronic traumatic brain injury in athletes. However, the recent interest in the effects of repeat head injury on professional athletes, many of whom began playing sports in their youth, has prompted a series of studies aimed at identifying the neuroanatomical and neuropathological substrates that underlie the behavioral outcomes in these athletes.
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. Chronic Traumatic Encephalopathy The identification of tau-positive NFTs in boxers with dementia pugilistica raises the question of whether this is an early and a consistent diagnostic feature in repeated traumatic brain injury.
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Clinical history and comorbid factors, such as complications from other medical conditions and exposures (e.g., substance use) may make it difficult to determine whether the features of CTE are a result of head impacts or of other factors, which complicates the development of diagnostic criteria for CTE.
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. Plassman and colleagues showed that both moderate and severe head injuries sustained during early adulthood are associated with increased risk of Alzheimer's disease, whereas the relationship between mild head injury and Alzheimer's disease was inconclusive (Plassman et al., 2000)
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. The association of ALS with both severe and repeated traumatic brain injury is supported by another case-control study from a population-based registry (Pupillo et al., 2012)
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Results from the Ab and tau transgenic mice studies provide some of the first evidence that repeat TBI can increase accumulation of these proteins and increase the risk of neurocognitive complications. In addition to the implications of Ab and tau in the pathogenesis of TBI, there is emerging evidence that reactive astrogliosis and microgliosis may contribute to neuronal injury following TBI.
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Preliminary imaging research suggests that there are changes in brain white matter following repetitive head impacts. This finding is supported by the animal literature.
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2012. Gender differences in head impacts sustained by collegiate ice hockey players.
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2013. Repetitive traumatic brain injury, psychological symptoms, and suicide risk in a clinical sample of deployed military personnel.
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2006. Co-morbid traumatic brain injury and substance abuse disorders: Childhood predictors and adult correlates.
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1999. Neuronal cytoskeletal changes are an early consequence of repetitive head injury.
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1997. Apolipoprotein E epsilon4 associated with chronic traumatic brain injury in boxing.
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2012. White matter integrity in the brains of professional soccer players without a symptomatic concussion.
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2009. Chronic traumatic en cephalopathy in athletes: Progressive tauopathy after repetitive head injury.
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2010. Repeat traumatic brain injury in the juvenile rate is associated with increased axonal injury and cognitive impair ments.
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2011. Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity.
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2011. Suicide prevention after traumatic brain injury: A randomized controlled trial of a program for the psychologi cal treatment of hopelessness.
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A neuropsychologic study of former soccer players. American Journal of Sports Medicine 19(1)
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2003. Increased diffusion in the brain of professional boxers: A preclinical sign of traumatic brain injury.
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