Introduction
The study of repeated head trauma (RHT) in contact sports has recently become more relevant because association between chronic RHT and long-term development of serious neurodegenerative diseases such as chronic traumatic encephalopathy (CTE), but also due to recent studies, suggests an increase in the incidence of concussion related to sports activities in the past decades, particularly in young women1-3. This global concern has led to the recent publication of several guidelines for the diagnosis and management of concussion associated with sports activities4,5, as well as an effort to develop and validate the use of serum, cerebrospinal fluid, and neuroimaging biomarkers to support the diagnosis of CTE in vivo6,7.
The development of cognitive and behavioral disturbances in RHT related to contact sports seems to require a significant exposure time, such as CTE, whose presentation latency ranges from a few years to several decades after stopping the sports activity8. In this sense, various studies have shown that the number of years of sports practice as well as the age of onset in sport activity have an influence on the cognitive alterations that are present in sport-related brain trauma9,10. Acute alterations (0-24 h) after trauma have been consistently demonstrated in concussive and subconcussive trauma, including cognitive and other post-concussional symptoms (headache, dizziness, sleep disturbances, etc.). Nevertheless, the follow-up reports show a reversal of those alterations in a period of a few days to 1 month11. Despite this, some studies reported that subjects with a history of prior trauma display a slower recovery, suggesting a cumulative effect of repeated injuries12.
However, most populations of athletes previously studied often have multiple “neuroprotective” factors (youth, regular physical activity, diet, educational level, etc.). The effects of RHT are challenging to detect especially in the short term, because the subjects may compensate cognitive deficits until the damage reaches a “threshold” level13. On the other hand, amateur athletes may have different conditions than professional athletes: (a) fewer hours of physical preparation and training (which makes them more prone to suffer injuries) and (b) having a lesser quality of protective equipment or neuroprotective factors (especially in developing countries).
In the study of cognitive alterations in RHT, emphasis has been placed on the processes that have shown sensitivity to indicate alterations in athletes, such is the case of working memory, decision-making, planning, inhibition, and reaction times14,15. In this sense, the use of computerized tests represents an advantage in the study of repeated blows to the head, since it allows the randomized presentation of the stimuli to avoid the learning effect of a pencil and paper test and the measurement of times reaction rate as a measure of processing speed16.
For all of the above, it is important to study the cognitive effects of RHT on this group of athletes, especially in developing countries, where this type of research is practically non-existent17,18. With all these in mind, the objective of the present research was to determine the association between the performance of executive functions with variables related to sports practice in amateur American football players.
Methods
The present study was adhered to the principles of the Helsinki Declaration revised in 2008 and was approved by the research and ethics committee of the School of Medicine at the Universidad Nacional Autónoma de México (UNAM), and all participants signed and received a copy of the informed consent. An observational, cross-sectional pilot study was carried out in 14 amateur American football players belonging to the team from the School of Medicine at UNAM, Mexico City. The inclusion/exclusion criteria were as follows: male sex, being an active and regular player, without: previous neurological or psychiatric illnesses (included non-sport-related brain trauma), drug abuse, or consumption of psychotropic medications; high levels of stress, impulsivity, or important traits of anxiety and depression that may affect cognitive performance were discarded by the assessment of Hamilton, Beck's, SISCO inventory, and Barratt impulsivity scales. All evaluations were applied before the start of the game season and in an examination-free period. Executive functions (visual-spatial and verbal working memory, inhibition, and speed processing) were assessed by automated tests of the PEBL version 2.1 software (http://pebl.sourceforge.net/). The digit span, Flanker test. and Corsi cubes were the selected sub-tests. These tasks require the subject to identify, remember, and effectively manipulate information about numbers, words, and figures quickly and with increasing complexity. These tasks were chosen because the previous studies suggest that they are more sensitive in detecting changes in patients with sport-related concussion16; in addition, the use of the PEBL software allowed to quantify very precisely the errors made in the tasks and also the reaction times of participants, which would not be possible using traditional pencil and paper tests16; Likewise, different variables related to their sports activity (age of onset, years of sports practice, position in the game, amount of training days, previous sports concussions, etc.) were collected. Statistical analysis: The data analysis was performed with the statistical package SPSS version 23 (IBM Corp., 2014). To assess the association between variables related to sport activity on score and reaction time in every executive task (dependent variable), with a robust estimator of the maximum likelihood. a generalized linear model of main effects was made. For analyses, the decision rule was set to a value p ≤ 0.05 with two-tailed hypothesis tests.
Results
In this study, a total of 22 male players were evaluated (the entire team), however, when applying the inclusion and exclusion criteria, eight participants were eliminated (due to personal history or use of psychotropic drugs) and a final sample of 14 men players was included, with an average age of 20.57 (standard deviation [SDí ± 1.61) years, played 7 (50%) in an offensive position, 7 (50%) in defensive position, and 3 (21%) presented previous brain trauma. The average time of practice football was of 35.07 (SD ± 43.10) months, starting age of football playing 17.71 (SD ± 3.64), and hours of training during the week 5.75 (SD ± 2.83). There were no differences between offensive and defensive players in time of practice, p = 0.989, starting age of football playing, p = 0.773, and hours of training during the week, p = 0.353. Furthermore, there were no differences between offensive and defensive players regarding global performance of digit span test, flanker test, and Corsi test (Table 1). Finally, a significant effect of offensive position controlled for previous cranial trauma was found in the Omnibus test c2 (2) = 10.81, p =0.004, but only in the highest span of visual working memory task (Corsi task level 5) (Table 2).
Offensive (n = 7) | Defensive (n = 7) | Stat. | p. | |
---|---|---|---|---|
Span digit test* | ||||
Total corrects | 7.29 ± 2.4 | 7.71 ± 1.1 | 20.50 | 0.62 |
Total time (ms) | 4.08 ± 0.4 | 3.79 ± 0.7 | 18.01 | 0.45 |
Flanker test* | ||||
Total errors | 48.2 ± 76.3 | 50.7 ± 71.4 | 23.50 | 0.90 |
Total time (ms) | 514.8 ± 196 | 545.6 ± 174 | 17.50 | 0.38 |
Corsi test* | ||||
Total corrects | 9.8 ± 1.5 | 10.5 ± 1.2 | 18.00 | 0.45 |
Total time (ms) | 4.85 ± 1.4 | 4.95 ± 0.4 | 19.50 | 0.53 |
*Data reported by mean (standard deviation)) and compared using the MannWhitney U-test. Stat.: statistic.
Parameter | B | β | SE (β) | CI 95% (β) | χ2 Wald | p |
---|---|---|---|---|---|---|
Intersection | 4913 | 0.030 | 0.1590 | (−0.28, 34) | 0.035 | 0.85 |
Position (offensive) | −771 | 0.536 | 0.1650 | (0.21, 0.85) | 10.54 | 0.001 |
TCE (presence) | 1032 | −0.552 | 0.0876 | (−0.72, −0.38) | 39.79 | 0.0001 |
(Scale) | 232,992 | 0.402 | 0.1521 | (0.19, 0.84) |
B: beta no standardized; β: beta standardized; SE: standard error; CI: confidence interval.
Discussion
The results of the present pilot study suggest a significant association between player's offensive position (controlled by previous cranial trauma), with a low cognitive performance but only in the highest span of visual memory task. Likewise, the tasks that evaluate visuospatial working memory with higher cognitive demand (greater number of elements) may be more sensitive to detect the early alterations in amateur athletes who receive repetitive cranial trauma and have multiple factors of neuroprotection.
Our findings are in agreement with that reported by Baugh et al., 2015, who point out that the player's position is a risk factor in athletes exposed to RHT, since according to their location on the playing field, athletes are exposed to a greater or lesser number of head trauma19,20.
Another factor observed in this research is the history of previous head trauma, since a player who previously suffered a trauma is more prone and more vulnerable to the effects of a second trauma, and may also have a cumulative effect21.
On the other hand, neuropsychological assessment is considered crucial in the assessment of RHT in athletes22. The evidence suggests cognitive impairments in specific processes such as working memory, inhibition, cognitive flexibility, planning, and processing speed23. This emphasis on the evaluation of executive (frontal) functions is mainly related to the biomechanics of trauma, in which it is proposed that there is greater damage in frontal orbital and dorsolateral regions, as well as in the anterior and basal portion of the temporal lobes24,25.
Based on our preliminary results, we suggest that future research emphasizes on the evaluation of the right frontal functions, especially in tasks with high cognitive demand, and in a larger group of amateur football players. On the other hand, regarding amateur sports practice, we can suggest the rotation of offensive and defensive positions to try to reduce the risk of brain damage. The final purpose of this type of studies is to generate alternatives so that players can carry out a safer sports practice.