There were 9 studies examining the psychological function.2,21–28 In all studies, psychological functioning was called as depression. These studies were performed in a relatively old sample of players, ranging from a mean age of 44 to 71 years. All studies examined a sample of retired players, except for Amen et al (2011),22 who studied a group including younger active players. Most of the studies used BDI-II as a method for measuring depression. Of the 9 studies, 5 showed a significant relation between exposure to concussion and depression.2,21–24 Guskiewicz et al (2007)23 revealed that retirees with 1 or 2 concussion had an RR of 1.5 to have been diagnosed with depression, and retirees with 3 or more concussions had an RR of 3 to have been diagnosed with depression, relative to retired players with no concussion history (P < 0.005). Kerr et al (2012)24 examined the 9-year risk of a depression diagnosis and found a significant linear dose–response relationship between the number of concussions and risk of depression diagnosis (P < 0.001). Overall, there is strong evidence that there is a relationship between MTBI and depression later in life. In addition, these results are highly suggestive that there is a positive dose–response relationship between the number of concussions endured by a player and the risk of depression diagnosis.
Three studies examined the relation between concussion and sports-related functioning.3,14,16 This functional outcome was translated to “on-field performance” and “return to play.” All studies had a longitudinal design and studied active players. None of the studies found a significant relationship between concussion and a sports-related outcome measure. Kumar et al (2014)3 found no significant difference between preinjury and postinjury on-field performance. Pellman et al (2006)14 showed that players recover quickly from acute concussion and that they can return to play within a week. Overall, there is inconclusive evidence that there is an association between concussions and impaired sports-related functioning.
The relation between concussions and physical functioning was subject of 3 studies.17,18,27 Two of these studies showed significant relations between concussion and physical functioning.17,18 These studies showed that concussed players had significantly more deficits in balance control and had lower voluntary muscle activation and a declined muscle force, compared with their healthy counterparts. We can conclude that there is strong evidence that concussion is related to a declined physical function.
For cognitive functioning, there was such a great variety in outcome variables that we decided to split this category up into 5 subthemes of cognitive functioning: memory impairment, mild cognitive impairment (MCI), executive dysfunction, reaction time, and visual-motor speed. In total, 13 articles focused on cognitive functioning. With all subthemes combined, the overall evidence for the effect of concussion on cognitive functioning is inconclusive.
Mild Cognitive Impairment
Mild cognitive impairment is a diagnostic classification to describe cognitive decline in usually older individuals. It is frequently described as a transitional state between the cognitive impairments that normally come with age, and dementia. The cognitive decline found in MCI is usually in the domain of memory, but it can also be a generally lower score on neurocognitive testing.29 Three cross-sectional studies examined MCI.22,26,29 Two of the studies found a significant correlation between concussion exposure and MCI.22,29 Guskiewicz et al (2005)29 found that retired players with a concussion history of ≥3 concussions were twice as likely to have MCI, compared with players with a history of 1 to 2 concussions, and 5 times more likely to have MCI compared with players with no concussion history whatsoever (P = 0.02). Hart et al (2013)26 compared cognitively impaired players with nonimpaired players, and found no differences between concussion history in these groups. In conclusion, we found moderate evidence that a history of concussion is associated with MCI.
Nine studies examined the relation between concussion and memory impairment.4,6,14,15,19–21,27,29 Several methods for measuring memory impairment were used. These are described in Supplemental Digital Content 1 (see Appendix 1, http://links.lww.com/JSM/A129). Four studies found a significant relation between concussion and memory impairment.6,21,27,29 Some interesting significant findings were that retired players with ≥3 previous concussions had an RR of 3 to report significant memory problems, compared with retired players without a history of concussion.29 Seichepine et al (2013)6 found significantly impaired working memory in retired players, compared with normal healthy adults. Because of the great proportion of nonsignificant results, we conclude that there is inconclusive evidence for the relationship between concussion and memory impairment.
Four studies examined reaction time,14,19,20,25 which is a component of the ImPACT. Only Casson et al (2014)25 found a significant relationship between concussion history and a slower reaction time. They studied a sample of retired NFL players. All nonsignificant studies had active NFL players as their subjects. There is inconclusive evidence for a relationship between concussion and a slower reaction time.
Five studies focused on the association between visual-motor speed,14,15,19,20,25 for example, the processing speed of visual input into motor output, which is also a composite score of the ImPACT. Again, only Casson et al (2014),25 the only study examining retired players, showed a significant relation between concussion and an impaired visual-motor speed, and the evidence for this relation is therefore inconclusive.
The association between concussion and executive dysfunction, or the inability to perform complex tasks, was subject of 3 studies.5,6,21 Two studies6 found a significant positive relation between concussion and executive dysfunction. Hampshire et al (2013)5 used functional MRI whereas the subjects were performing “the Spatial Planning Task” (SP-task), a test commonly used to asses executive functioning. Compared with controls, the NFL alumni did not perform significantly worse on the SP-task. Seichepine et al (2013)6 compared NFL retirees with normal healthy adults, evaluating 9 areas of executive functioning. National Football League retirees scored significantly worse on 7 of the 9 areas. Because of the low number of significant findings, it can be concluded that there is limited evidence for the association between TBI and executive dysfunction.
This systematic review found strong evidence for the association between repetitive brain trauma in professional American football players and depression later in life. There is also strong evidence for the correlation with physical dysfunctions. However, these dysfunctions were subclinical of nature and the results for the association between concussion and sports-related functioning showed that it did not affect players' time to return to play or their on-field performance. The evidence for the effect of concussion on several aspects of cognitive functioning remains inconclusive, although there was moderate evidence for the relationship between concussions and MCI.
Interestingly, when we looked at players' ages, the most significant associations were found in the older age groups, involving retirees. The overall effect for cognitive dysfunctions was found to be inconclusive, but when the studies involving active players are removed from the evidence synthesis, there would have been strong evidence for the relation between TBI and cognitive dysfunctions. Moreover, the strongest relation we have discovered, between concussion and depression, all occurred in retired players older than 45 years. Depression is a common consequence of brain injury. It has even been reported as a consequence of a single mild traumatic injury,30 but the biological or psychological pathway of that association has not yet been clarified. One possible explanation of the relationship between repeated concussions and depression can be found in the occurrence of a disease called Chronic traumatic encephalopathy (CTE). Chronic traumatic encephalopathy is a neurodegenerative disease, characterized by atrophy of various regions of the brain and deposition of tau protein, also called tauopathy.27 It was first identified in boxers as a long-term effect of repetitive TBI, and later also in other contact sports such as hockey, soccer, martial arts, and American football.31 Chronic traumatic encephalopathy causes various behavioral symptoms, cognitive decline, and mood disorders, such as depression, suicidality, irritability, disinhibition, aggression, and substance abuse.27 Remarkably is that these symptoms typically present in the fourth to fifth decade of life, after a latency period of decades after the exposure to multiple TBIs. The disease can eventually develop into dementia.6,27 This supports our findings of a higher chance of depression later in life and a higher risk for developing MCI in older individuals. However, CTE may be the explanation for the symptoms we observe and can be suspected clinically, CTE remains a pathological diagnosis, and it can only be diagnosed at autopsy in deceased individuals.21 Therefore, early detection of this disease is not yet possible which may impede early clinical diagnosis and associated early interventions.
Because we considered TBI in football as an occupational disease, the question arises whether concussion really does affect optimal functioning in work. As we revealed, performance in current work of players is not affected. However, depression can affect an optimal performance in work after retirement from the NFL. Depression can negatively influence one's ability to maintain relationships, to be productive and concentrated at work, and to maintain an acceptable level of self-care.24 Furthermore, it is expected that MCI in retired players is also not conducive to optimal work functioning, as it is accompanied with memory loss and cognitive decline.
Limitations and Strengths
There are a number of limitations to this systematic review. The main limitation is the great heterogeneity between the studies. The included studies differ in sample size, concussion history, outcome measures, and measurement methods. This heterogeneity makes good comparison difficult. Another limitation is that more than half of the studies had a relatively small population size of <100 participants. It is not known whether larger population sizes would have shown the same results. However, the 3 largest studies23,24,29 with over 1000 participants, all showed a significant dose–response relationship between concussion and a functional outcome. There were also limitations to the individual included studies. First, almost all information about concussion history was based on self-report measures. It can be questioned whether the participants recalled the number of concussions they endured correctly, especially when there might be memory impairments in some players. One study participant even reported 20 000 concussions retrospectively.6 The recall of symptoms and functional problems may be inaccurate as well. This might underestimate or overestimate the results. Second, many of the methods for measuring functional outcomes were based on questionnaires and tests performed by the player itself. Participants were rarely assessed by a blinded physician or researcher. Participants were obviously aware of their concussion history, which could have affected their responses on questionnaires and tests. Third, selection bias may have played a role in an overestimation of the results. Many studies recruited their participants from the NFL players' association, which was almost always through self-referral, local advertising, and word of mouth. Because (retired) athletes were aware of the study purpose, athletes who were already experiencing functional impairments may have been more likely to apply to a study.
The main strength of this systematic review is the broad search strategy in 2 databases, with almost no limitations to study design and no less than 4 outcome measures. This is, to our knowledge, the first review to assess and compare such a broad range of functional outcome measures. With 21 included studies, we can give a complete overview of the literature on this subject so far. Another major strength is that levels of evidence were used to synthesize the results, which enabled us to create more transparency and draw more objectivized conclusions.
Implications for Research
In our included studies, the age group from 30 to 45 years was under-represented, and we recommend more studies in this age group. The typical career of an American football player ends at an average age of 28 years.32 Therefore, the 30 to 45 years age group is the postathletic period in which the retirees need to start pursuing some other career. As for now, it remains unclear whether the consequences of TBI affect functions in this age group and whether this would make it harder for these retired players to start a new career. Furthermore, more longitudinal studies on long-term effects of concussion on cognitive and physical functioning are needed. Only 1 study,24 which assessed depression, had a long follow-up period of 9 years. Longer follow-up periods will enhance the evidence for certain associations. Finally, the use of more heterogeneous populations and standardized outcome measures in future research would enable meta-analyses to be performed.
Implications for Practice
This review may be of practical relevance for American football players, coaches, team physicians, and future employers of NFL retirees. It is clear that the consequences of TBI need to be limited. The first step into tackling this problem is prevention of TBIs. This can be achieved by properly informing players and their coaches. Raising awareness may cause players to be more careful during practice or games and to make more informed choices about their health. Furthermore, this review provides input for the NFL to develop more stringent game rules preventing high-impact collisions, to increase medical surveillance and to design better protective equipment. These results can also be used to achieve early detection and intervention of consequences in retired athletes. Future employers can take into account that employees with a history of concussions may experience early cognitive or psychological decline and apply accurate interventions. Finally, the findings of this study may be applicable for other high-contact sports.
There is strong evidence for a relationship between a history of concussion in American football and depression diagnosis later in life, and there are strong hints that this is a dose–response relationship. Also cognitive dysfunctions such as MCI are seen in older American football players with a history of TBI. These dysfunctions may be related to occurrence of Chronic Traumatic Encephalopathy in these players. On the short term, concussion mainly causes subclinical physical dysfunctions like balance control deficits and decreased muscle force. These findings provide insights on the consequences of TBI in other high-contact sports, as well as input for actions to prevent TBI and their consequences in American football players.
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traumatic brain injury; cognitive functioning; physical functioning; sports-related functioning; post-concussion syndrome; football
Supplemental Digital Content
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