Cognitive functioning and soccer heading: one-year longitudinal assessment among professional players

Abstract

Background Soccer is the most popular sport worldwide, and the only one in which players purposely and repetitively use their head to hit the ball. In recent years, more attention has been given to subconcussive impacts, which are characterized by a cranial impact that does not result in known or diagnosed concussion on clinical grounds.

Objective To investigate the effects of soccer heading on cognitive functioning among professional soccer players.

Methods In a longitudinal case-control study, 22 professional soccer players were compared with 37 non-athletes on 2 occasions (T0 and T1) separated by a 1-year interval. The cognitive assessment consisted of computerized neuropsychological tests and the Brief Neuropsychological Assessment Battery (NEUPSILIN).

Results There was no evidence of cognitive impairment among athletes, who actually outperformed the controls in terms of score, accuracy, and reaction time in certain tests. Moreover, the estimates of heading exposure did not correlate with the cognitive performance of players. The intragroup analyses revealed that while the controls improved their performance on three cognitive variables from T0 to T1, no improvement occurred among players. However, within-group variation in performance from T0 to T1 was similar.

Conclusion Although the present study has not shown an association between soccer heading and cognitive impairment, subconcussive impacts may have a negative effect on brain function, as improvement in cognitive performance was not observed among athletes. Future and longer longitudinal investigations are needed to clarify the relationship between soccer heading and cognition.

Keywords

Cognition - Neurology - Athletes - Soccer - Brain Injuries, Traumatic

INTRODUCTION

Since the twentieth century, the role of concussion in chronic neurodegenerative disease has gained attention, while athletes have shown neuropsychiatric symptoms and cognitive impairment after numerous head impacts throughout their competitive years. Nowadays, those repeated brain injuries are known as a potential cause of chronic traumatic encephalopathy (CTE).[1]

In recent years, more attention has been given to subconcussive impacts. The term “subconcussive” refers to head impacts that could lead to neuronal dysfunction without causing the typical concussive symptoms of confusion, amnesia, dizziness, visual disturbances, or headaches.[2] Moreover, the cumulative effects of repetitive minor injury may not manifest for many years, as in CTE.[3] Therefore, pathological evidence of traumatic brain injury is mixed, and, if detectable, it is likely to present prior to the onset of overt symptoms or disability.[4] [5]

Soccer is the most popular sport worldwide, and the only one in which players purposely and repetitively use their head to hit the ball, on an average of 6 to 12 headings per competitive game, in which the ball reaches high velocities.[6] Therefore, even though concussive events are not common in soccer, we can consider that headings may act as subconcussive impacts which, while not causing immediate symptoms, may contribute to long-term cognitive damage. Moreover, based on field position and career length, professional soccer players are exposed to a higher risk of developing neurodegenerative disease, and a more frequent use of dementia-related medications.[7] [8] [9] Importantly, the possible negative effects of headings may depend on the rate of exposure, the time between exposures, and the vulnerability of individual players.[3]

However, to date, research on the possible effects of soccer headings on brain function has produced controversial results, with some studies[10] [11] [12] suggesting an association between heading and cognitive impairment, while others[13] [14] [15] have found no correlation.

The current one-year longitudinal case-control study aims to investigate the effects of soccer headings on cognitive functioning among professional soccer players. We have previously reported the baseline and cross-sectional results of the study,[16] in which no evidence of cognitive impairment was found among soccer players compared with non-athletes, and no association between heading exposure and neuropsychological performance was observed.

METHODS

Two groups of male participants matched by age and years of schooling participated in the study: 22 active professional soccer players (mean age = 24.1 ± 5.2 years; mean years of schooling = 11.2 ± 1.7 years) from 2 teams playing in the Brazilian A-series championship. We also included 37 non-athletes as controls (mean age = 26.1 ± 4.0 years; mean years of schooling = 10.9 ± 1.7 years).

The athlete's group was composed of 5 goalkeepers, 7 defenders, 7 midfielders and 3 forwards. All athletes performed approximately 15 hours of training sessions per week and usually played one or, during most of the soccer season, two competitive matches per week.

The control group was composed of non-athletes who worked as doormen or security guards and who did not practice soccer or practiced it occasionally and at a recreational level.

To characterize the participants, a sociodemographic questionnaire was applied, as well as parts of the Mini International Neuropsychiatric Interview (MINI),[17] with the aim of investigating possible psychiatric disorders. None of the participants showed a major depressive episode or alcohol dependence, nor reported using any psychotropic drug.

The soccer players were also questioned about the average number of headings per game. In the cross-sectional analysis of the project of the present research,[16] the number of headings performed by 16 athletes in 42 matches was directly measured by an observer. Considering this subsample of players, a comparison between the self-reported and the actual number of headings per game revealed no significant differences. Moreover, a significant correlation was found between the self-reported and the actual values.[16] Therefore, we believe that the self-report method used in the current study may be considered a good estimate of headings during official matches.

In relation to previous reports of concussion, 7 players (31.8%) and 4 controls (10.8%) reported history of concussive impacts (p = 0.045).

A total of six professional players reported regular alcohol use, but none used cigarettes or other toxic substances. Only one player was on medication affecting the central nervous system (escitalopram), none had a history of major depressive episodes, and one soccer player had generalized anxiety disorder. Among the controls, no participant reported using drugs with effects on the central nervous system, nor exhibited mood disorder or alcohol dependence. Importantly, no participants from the 2 groups had consumed alcohol in the 12 hours prior to the neurocognitive tests, and only 1 had consumed alcohol in the 24 hours leading up to the tests.

The participants were tested on two occasions, T0 and T1, separated by a 1-year interval. In T0, 7 players and 4 non-athletes referred to a lifetime history of concussion, with a significant difference in the rate of concussed subjects between groups (p = 0.045). No concussion was reported between T0 and T1 analysis. On both occasions, the cognitive assessment consisted of 2 parts: the first part lasted ∼ 35 minutes and was composed of computerized neuropsychological tests designed on the E-Prime (Psychology Software Tools, Inc., Pittsburgh, PA, United States) software,[18] which measure general motor skills, memory, attention, and executive functioning. On each test, the reaction time in milliseconds and the percentage of correct responses were calculated.

Computerized tests

• Simple Reaction Time Test: the participants press the “1” key in response to a “*” symbol appearing on the screen at random intervals. The test contains 40 trials in a single block.

• Immediate Memory Test: the participants memorize 20 words shown on the screen and then identify them from sets of 4 words. The test contains 3 blocks of 20 trials.

• Attention Test: the participants determine whether a target figure appears among four similar figures. The test includes 60 trials in a single block.

• Number-Letter test: the participants categorize numbers as odd/even or letters as consonants/vowels depending on their screen position. The test involves task switching with 32 trials in 2 blocks and 64 in a third block.

• Two-Back test: the participants monitor sequences of numbers, pressing “Enter” when a number matches one from two trials earlier. The test contains 160 trials.

• Stroop test: the participants identify the ink color of incongruent/congruent words, with 72 trials in a single block.

• Delayed memory test: ∼ 30 minutes after the Immediate Memory Test, the participants indicated whether 40 words were in the original list.

The second part of the cognitive assessment was applied immediately after the first one, and it involved the Brief Neuropsychological Assessment Battery (NEUPSILIN),[19] which is composed of 32 short tasks that evaluate different cognitive domains such as time and spatial orientation, attention, perception, memory, arithmetic abilities, language, praxis, problem solving, and verbal fluency. This part also lasted ∼ 35 minutes, and the measured variable was the score on each test.

The statistical analyses were performed using the IBM SPSS Statistics for Windows (IBM Corp., Armonk, NY, United States) software, version 19.0. The normality of each variable was tested with the Kolmogorov-Smirnov test. For independent samples, mean comparisons between groups were performed using the Student's t-test for variables with normal distribution, and the Mann-Whitney U-Test, for non-normally distributed variables. Regarding the dependent samples, the paired Student's t-test was used for variables with normal distribution, and the Wilcoxon test, for those with non-normal distribution. The correlations involving the athletes' cognitive performance in T0 and T1 and the self-reported number of headings were calculated with the Pearson's Correlation Test, controlling for lifetime history of concussion. The categorical variables were compared using the Chi-squared test. Bonferroni correction (p < 0.01) was used in the present study to enable multiple comparisons involving cognitive performance in T0 and T1. In all other analyses, the significance level was set to 5% (p < 0.05).

All subjects provided written informed consent to participate in the study, which was approved by the Ethics Committee of the Universidade Federal de Minas Gerais (under CAAE 51433115.1.0000.5149).

RESULTS

In T0 ([Table 1]), the players performed better than the controls in three variables of the computerized testing, namely reaction time and accuracy in the number-letter test and accuracy in the two-back test. They also outperformed the controls in terms of memory and arithmetic abilities in the NEUPSILIN.

Table 1 Cognitive performance of soccer players and controls at T0 and T1

Test	Variable	T0			T1
		Players	Controls	p	Players	Controls	p
Age	Years	24.13 ± 5.29	26.13 ± 4.09	0.110	25.32 ± 5.38	27.19 ± 4.09	0.137
Schooling	Years	11.22 ± 1.75	10.94 ± 1.74	0.888	11.34 ± 1.77	11.08 ± 1.87	0.816
Computerized tests
Simple reaction time	Reaction time	290 ± 28	309 ± 39	0.047	280 ± 21	316 ± 37	0.000
	Accuracy	100.00 ± 0.00	99.96 ± 0.20	0.441*	100 ± 0.00	100 ± 0.00	−
Attention	Reaction time	2,364 ± 580	2,725 ± 679	0.042	2,323 ± 526	2,504 ± 579	0.235
	Accuracy	94.39 ± 4.22	94.09 ± 5.23	0.823	95.83 ± 2.94	95.08 ± 3.38	0.396
Immediate memorya	Reaction time	2,377 ± 565	2,935 ± 917	0.013	2,453 ± 492	2,736 ± 768	0.128
	Accuracy	89.39 ± 7.17	86.71 ± 10.55	0.296	91.36 ± 5.26	88.56 ± 8.03	0.150
Number-lettera	Reaction time	494 ± 137	656 ± 231	0.004	481 ± 116	628 ± 197	0.056
	Accuracy	−1.35 ± 2.78	−5.02 ± 6.76	0.005	−0.28 ± 2.14	−1.87 ± 4.10	0.001
Two-back	Reaction time	518 ± 103	561 ± 100	0.126	503 ± 115	564 ± 129	0.074
	Accuracy	98.66 ± 1.48	94.60 ± 4.95	0.000	98.92 ± 1.51	96.37 ± 3.76	0.000*
Stroopa	Reaction time	172 ± 97	163 ± 142	0.784	115 ± 138	126 ± 119	0.731
	Accuracy	−2.14 ± 2.96	−1.95 ± 2.92	0.842*	−0.76 ± 3.34	−1.43 ± 3.18	0.842*
Delayed memory	Reaction time	874 ± 147	1,049 ± 318	0.019	2,453 ± 492	2,736 ± 768	0.094
	Accuracy	93.75 ± 5.16	92.16 ± 7.68	0.394	91.36 ± 5.26	88.56 ± 8.03	0.617*
NEUPSILIN battery
Time and spatial orientation	Score (Total: 8)	8.00 ± 0.00	7.97 ± 0.16	0.441*	7.77 ± 0.43	7.97 ± 0.16	0.441*
Attention	Score (Total: 27)	24.31 ± 2.12	23.13 ± 1.90	0.031	24.27 ± 1.69	23.76 ± 1.85	0.056*
Perception	Score (Total: 12)	11.00 ± 1.11	11.08 ± 0.92	1.000*	11.41 ± 0.79	11.22 ± 0.75	1.000*
Memory	Score (Total: 84)	61.72 ± 6.18	56.29 ± 7.95	0.008	64.09 ± 7.07	60.05 ± 8.28	0.061
Arithmetic skills	Score (total: 8)	7.59 ± 0.73	6.18 ± 1.94	0.002*	7.63 ± 0.73	6.40 ± 2.06	0.002*
Language	Score (total: 53)	50.72 ± 1.69	49.91 ± 2.34	0.164	51.31 ± 1.13	50.43 ± 1.74	0.037
Praxis	Score (total: 22)	18.72 ± 1.77	17.62 ± 2.13	0.046	19.18 ± 1.59	18.35 ± 2.08	0.113
Problem-Solving	Score (total: 2)	1.81 ± 0.39	1.56 ± 0.55	0.073*	1.86 ± 0.35	1.51 ± 0.55	0.073*
Verbal fluency	Score (total: 11)	5.36 ± 1.49	5.08 ± 1.21	0.431	5.77 ± 1.44	5.14 ± 1.39	0.515*

Abbreviation: NEUPSILIN, Brief Neuropsychological Assessment Battery.

Notes: The p-values refer to the Student's t-test for independent samples, except those marked with the asterisk (*), which refer to the Mann-Whitney's U-test. Bold p-values indicate significant differences at a 1% level. In the computerized testing, the variables measured are the mean reaction time, expressed in milliseconds, and the mean accuracy, expressed in the percentage of correct answers. In the NEUPSILIN, the variable measured is the mean score on each test. ªIn the immediate memory, number-letter, and Stroop tests, reaction time and accuracy are calculated as described in the “Methods” section.

In T1 ([Table 1]), the players outperformed the controls in three variables of the computerized testing: reaction time in the general motor skills test and accuracy in the number-letter and two-back tests. They also showed a better performance in the arithmetic abilities test from the NEUPSILIN.

Intragroup analyses ([Table 2]) revealed that, while the controls improved their performance in three variables from T0 to T1 (reaction time in the Attention Test and accuracy in the two-back test, and score on the NEUPSILIN memory test), no improvement was observed among soccer players. However, a comparison involving variation in performance between T0 and T1 showed no significant differences between the groups.

Table 2 Variation in cognitive performance of soccer players and controls between T0 and T1

Test	Variable	Players			Controls			T1-T0
		T0	T1	p	T0	T1	p	Players	Controls	p
Computerized tests
Simple reaction time	Reaction time	290 ± 28	280 ± 21	0.025	309 ± 39	316 ± 37	0.213	−9.64 ± 18.72	6.65 ± 31.86	0.033
	Accuracy	100.00 ± 0.00	100.00 ± 0.00	−	99.96 ± 0.20	100.00 ± 0.00	0.317*	0.00 ± 0.00	0.03 ± 0.20	0.441*
Attention	Reaction time	2364 ± 580	2323 ± 526	0.687	2725 ± 679	2504 ± 579	0.003	−41.18 ± 472.06	−220.57 ± 413.64	0.132
	Accuracy	94.39 ± 4.22	95.83 ± 2.94	0.078	94.09 ± 5.23	95.08 ± 3.37	0.256	1.43 ± 3.64	0.99 ± 5.21	0.725
Immediate memorya	Reaction time	2377 ± 565	2453 ± 492	0.546	2935 ± 917	2736 ± 768	0.030	76.36 ± 583.28	−199.30 ± 534.69	0.069
	Accuracy	89.39 ± 7.17	91.35 ± 5.26	0.176	86.71 ± 10.55	88.55 ± 8.03	0.172	1.96 ± 6.58	1.84 ± 8.04	0.952
Number-lettera	Reaction time	494 ± 137	481 ± 116	0.608	656 ± 231	628 ± 197	0.406	−13.55 ± 121.85	−27.43 ± 198.39	0.740
	Accuracy	−1.35 ± 2.78	−0.28 ± 2.14	0.239	−5.02 ± 6.76	−1.87 ± 4.10	0.013	1.06 ± 4.13	3.15 ± 7.32	0.226
Two-back	Reaction time	518 ± 103	503 ± 115	0.352	561 ± 100	564 ± 129	0.783	−15.14 ± 74.55	3.32 ± 72.72	0.354
	Accuracy	98.66 ± 1.48	98.91 ± 1.50	0.511*	94.60 ± 4.95	96.36 ± 3.75	0.003	0.25 ± 1.67	1.75 ± 3.39	0.058
Stroopa	Reaction time	175 ± 97	115 ± 138	0.053	163 ± 142	126 ± 119	0.120	−57.41 ± 131.47	−36.16 ± 138.20	0.563
	Accuracy	−2.14 ± 2.96	−0.75 ± 3.34	0.155*	−1.95 ± 2.92	−1.42 ± 3.18	0.420*	1.39 ± 4.26	0.52 ± 4.13	0.446
Delayed memory	Reaction time	874 ± 147	888 ± 170	0.605	1049 ± 318	990 ± 249	0.057	13.82 ± 123.38	−58.14 ± 179.57	0.103
	Accuracy	93.75 ± 5.16	96.47 ± 3.59	0.029	92.16 ± 7.68	92.97 ± 7.72	0.486*	2.72 ± 5.45	0.81 ± 7.04	0.278
NEUPSILIN
Time and spatial orientation	Score (total: 8)	8.00 ± 0.00	7.77 ± 0.42	0.025*	7.97 ± 0.16	7.97 ± 0.16	1.000*	−0.22 ± 0.42	0.00 ± 0.23	0.012*
Attention	Score (total: 27)	24.31 ± 2.12	24.27 ± 1.69	0.935	23.13 ± 1.90	23.75 ± 1.84	0.167*	−0.04 ± 2.57	0.72 ± 2.34	0.315*
Perception	Score (total: 12)	11.00 ± 1.11	11.40 ± 0.79	0.117*	11.08 ± 0.92	11.21 ± 0.75	0.415*	0.40 ± 1.25	0.18 ± 1.04	0.290*
Memory	Score (total: 84)	61.72 ± 6.18	64.09 ± 7.07	0.069	56.29 ± 7.95	60.05 ± 8.27	0.002	2.36 ± 5.78	3.89 ± 6.89	0.387
Arithmetic skills	Score (total: 8)	7.59 ± 0.73	7.63 ± 0.72	0.860*	6.18 ± 1.94	6.40 ± 2.06	0.471*	0.04 ± 0.78	0.27 ± 1.78	0.717*
Language	Score (total: 53)	50.72 ± 1.69	51.31 ± 1.12	0.034	49.91 ± 2.34	50.43 ± 1.74	0.100	0.59 ± 1.22	0.59 ± 1.83	0.993
Praxis	Score (total: 22)	18.72 ± 1.77	19.18 ± 1.59	0.226	17.62 ± 2.13	18.35 ± 2.08	0.011	0.45 ± 1.71	0.94 ± 1.91	0.326
Problem-Solving	Score (total: 2)	1.81 ± 0.39	1.86 ± 0.35	0.655*	1.56 ± 0.55	1.51 ± 0.55	0.414*	0.04 ± 0.48	−0.05 ± 0.40	0.399*
Verbal fluency	Score (total: 11)	5.36 ± 1.49	5.77 ± 1.44	0.215	5.08 ± 1.21	5.13 ± 1.39	0.777	0.40 ± 1.50	0.08 ± 1.21	0.362

Abbreviation: NEUPSILIN, Brief Neuropsychological Assessment Battery.

Notes: Soccer players and controls at T0 and T1: the p-values refer to the paired t-test, except those marked with the asterisk (*), which refer to the Wilcoxon test. Soccer players and controls at T1-T0: the p-values refer to the Student's t-test for independent samples, except those marked with the asterisk (*), which refer to the Mann-Whitney's U-test. Bold p-values indicate significant differences at a 1% level. In the computerized testing, the variables measured are the mean reaction time, expressed in milliseconds, and the mean accuracy, expressed in the percentage of correct answers. In the NEUPSILIN, the variable measured is the mean score on each test. ªIn the immediate memory, number-letter, and Stroop tests, reaction time and accuracy are calculated as described in the “Methods” section.

Among soccer players ([Table 3]), no significant correlations were found between the self-reported number of headings per game and cognitive performance in T0 nor T1, controlling for concussion history.

Table 3 Correlations between cognitive performance of soccer players and self-report of headings per game

Test	Variable	Correlation coefficient (T0)	p	Correlation coefficient (T1)	p
Computerized tests
Simple reaction timea	Reaction time	0.005	0.983	0.039	0.868
	Accuracy	−	−	−	−
Attention	Reaction time	−0.398	0.074	−0.188	0.415
	Accuracy	0.178	0.439	−0.130	0.574
Immediate memoryb	Reaction time	−0.208	0.366	−0.264	0.247
	Accuracy	0.138	0.551	0.194	0.401
Number-letterb	Reaction time	0.144	0.533	−0.156	0.500
	Accuracy	−0.217	0.345	0.327	0.148
Two-back	Reaction time	0.125	0.589	−0.160	0.488
	Accuracy	−0.006	0.981	0.049	0.832
Stroopb	Reaction time	−0.160	0.489	0.084	0.718
	Accuracy	0.288	0.205	0.243	0.287
Delayed memory	Reaction time	−0.065	0.780	−0.298	0.189
	Accuracy	0.105	0.650	−0.081	0.726
NEUPSILIN battery
Time and spatial orientationa	Score	−	−	0.085	0.714
Attention	Score	−0.409	0.066	0.133	0.566
Perception	Score	0.179	0.437	−0.106	0.648
Memory	Score	−0.263	0.250	−0.063	0.785
Arithmetic skills	Score	0.103	0.657	0.405	0.069
Language	Score	0.059	0.800	0.208	0.367
Praxis	Score	0.228	0.321	0.117	0.613
Problem-Solving	Score	0.320	0.157	0.172	0.456
Verbal fluency	Score	−0.112	0.628	0.105	0.652

Abbreviation: NEUPSILIN, Brief Neuropsychological Assessment Battery.

Notes: The correlations were measured through the Pearson's correlation test, controlling for the variable “lifetime history of concussion.” ^aCorrelation tests were not performed for accuracy in the simple reaction time test at T0 and T1 and for score in the time and spatial orientation test at T0, since all subjects had 100% of correct responses and achieved the maximum score respectively. ^bIn the immediate memory, number-letter, and Stroop tests, reaction time and accuracy are calculated as described in the “Methods” section.

DISCUSSION

The inconclusive findings on the effects of headings on cognitive impairment among soccer players underscore the need for more robust data on this topic.[20] In the present study, professional soccer players performed better than controls in neuropsychological tests that require task-switching and working-memory abilities, as well as in general motor skills, memory, and arithmetic skills. We believe that this may be related to team sport practice, which demands strategic decision-making in complex and quickly changing contexts. Besides, there is evidence that participation in sports relates to faster processing speed in measures of simple reaction time.[21] This can explain the advantage of professional soccer players in reaction-time measures in T0 (number-letter test) and T1 (general motor skills test).

The present study shows no evidence of impairment in the cognitive functioning of professional soccer players. In fact, athletes displayed shorter reaction times and greater accuracy in some computerized tests, as well as better results in memory and arithmetic skills of the NEUPSILIN. This may be explained by the improvement in motor skills and ability to develop a strategy that comes from sports practice. However, the longitudinal analysis of the participants draws attention. Although there was no setback in the athletes' performance, they showed a less expressive learning curve than the control group.

The relationship between soccer practice and brain function remains controversial, and further studies involving larger samples and longer follow-up are needed to achieve a better understanding of the effects of subconcussive impacts on brain function.

One strength of the present study is the participation of active high-level professional soccer players, since most studies addressing the effects of soccer headings on cognition have not investigated this population. Thus, in the current study, we analyzed individuals who are constantly exposed to many head impacts.

Nevertheless, we must acknowledge that the present study has limitations, such as the fact that soccer players were compared with non-athletes, which is not an ideal comparison group, given the well-established cognitive benefits of physical activity.[22] Hence, physical activity could act as a confounding variable and compromise the study analysis. Moreover, only headings during competitive matches were considered in the study, excluding the training sessions, and possibly underestimating the number of subconcussive impacts. This may have had an influence on our results, which showed no significant differences between soccer players who reported a greater or smaller number of headings per game. Another limitation is that the number of headings was estimated through self-report by the soccer players, which is potentially biased or imprecise. History of concussion was also more frequent among players than controls. Finally, the sample size was small, but this was related to the number of players who agreed to participate and who were available for both the baseline and the one-year evaluations.

In conclusion, the soccer players evaluated in the present study did not show signs of cognitive impairment and actually outperformed the controls in certain tests. However, given the body of evidence linking professional soccer activity with later-life dementia, efforts to optimize head trauma prevention for soccer players need to be considered to reduce long-term risks.[23]

Conflict of Interest

The authors have no conflict of interest to declare.

Acknowledgments

The authors would like to thank all the soccer players and technical commissions from Clube Atlético Mineiro and América Futebol Clube. We extend our gratitude to all non-athletes who composed the control group.

Authors' Contributions

ACOR: conceptualization, data curation, formal analysis, investigation, software, supervision, validation, visualization, and writing – original draft; CFAF and RCPL: conceptualization, data curation, formal analysis, investigation, methodology, project administration, supervision, validation, and visualization; PC: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, software, supervision, validation, visualization, writing – original draft, and writing – review & editing; MDML: data curation, formal analysis, investigation, software, validation, visualization, and writing – original draft; CVF: data curation, formal analysis, investigation, methodology, and software; and GBP: software, writing – original draft, and writing – review & editing.

Financial Support

Paulo Caramelli is supported by a productivity in reasearch grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil.

• References

• 1 McKee AC, Stein TD, Huber BR. et al. Chronic traumatic encephalopathy (CTE): criteria for neuropathological diagnosis and relationship to repetitive head impacts. Acta Neuropathol 2023; 145 (04) 371-394
• 2 Bailes JE, Petraglia AL, Omalu BI, Nauman E, Talavage T. Role of subconcussion in repetitive mild traumatic brain injury. J Neurosurg 2013; 119 (05) 1235-1245
• 3 Lipton ML, Kim N, Zimmerman ME. et al. Soccer heading is associated with white matter microstructural and cognitive abnormalities. Radiology 2013; 268 (03) 850-857
• 4 Ling H, Morris HR, Neal JW. et al. Mixed pathologies including chronic traumatic encephalopathy account for dementia in retired association football (soccer) players. Acta Neuropathol 2017; 133 (03) 337-352
• 5 Lee EB, Kinch K, Johnson VE, Trojanowski JQ, Smith DH, Stewart W. Chronic traumatic encephalopathy is a common co-morbidity, but less frequent primary dementia in former soccer and rugby players. Acta Neuropathol 2019; 138 (03) 389-399
• 6 Spiotta AM, Bartsch AJ, Benzel EC. Heading in soccer: dangerous play?. Neurosurgery 2012; 70 (01) 1-11 , discussion 11
• 7 Koerte IK, Mayinger M, Muehlmann M. et al. Cortical thinning in former professional soccer players. Brain Imaging Behav 2016; 10 (03) 792-798
• 8 Mackay DF, Russell ER, Stewart K, MacLean JA, Pell JP, Stewart W. Neurodegenerative Disease Mortality among Former Professional Soccer Players. N Engl J Med 2019; 381 (19) 1801-1808
• 9 Russell ER, Mackay DF, Stewart K, MacLean JA, Pell JP, Stewart W. Association of Field Position and Career Length With Risk of Neurodegenerative Disease in Male Former Professional Soccer Players. JAMA Neurol 2021; 78 (09) 1057-1063
• 10 Di Virgilio TG, Hunter A, Wilson L. et al. Evidence for acute electrophysiological and cognitive changes following routine soccer heading. EBioMedicine 2016; 13: 66-71
• 11 Stewart WF, Kim N, Ifrah C. et al. Heading frequency is more strongly related to cognitive performance than unintentional head impacts in amateur soccer players. Front Neurol 2018; 9: 240
• 12 Matser JT, Kessels AG, Jordan BD, Lezak MD, Troost J. Chronic traumatic brain injury in professional soccer players. Neurology 1998; 51 (03) 791-796
• 13 Oliveira TG, Ifrah C, Fleysher R, Stockman M, Lipton ML. Soccer heading and concussion are not associated with reduced brain volume or cortical thickness. PLoS One 2020; 15 (08) e0235609
• 14 Kemp S, Duff A, Hampson N. The neurological, neuroimaging and neuropsychological effects of playing professional football: Results of the UK five-year follow-up study. Brain Inj 2016; 30 (09) 1068-1074
• 15 Strauss SB, Fleysher R, Ifrah C. et al. Framing potential for adverse effects of repetitive subconcussive impacts in soccer in the context of athlete and non-athlete controls. Brain Imaging Behav 2021; 15 (02) 882-895
• 16 Rodrigues AC, Lima MDM, de Souza LC. et al. No Evidence of Association Between Soccer Heading and Cognitive Performance in Professional Soccer Players: Cross-Sectional Results. Front Neurol 2019; 10: 209
• 17 Sheehan DV, Lecrubier Y, Sheehan KH. et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 1998; 59 (Suppl. 20) 22-33 , quiz 34–57
• 18 Schneider W, Eschman A, Zuccolotto A. E-Prime User's Guide. Pittsburgh, PA: Psychology Software Tools Inc; 2002
• 19 Fonseca RP, Salles JF, Parente MAMP. Development and content validity of the Brazilian Brief Neuropsychological Assessment Battery Neupsilin. Psychol Neurosci 2008; 1 (01) 55-62
• 20 Rodrigues AC, Lasmar RP, Caramelli P. Effects of soccer heading on brain structure and function. Front Neurol 2016; 7: 38
• 21 Chaddock L, Neider MB, Voss MW, Gaspar JG, Kramer AF. Do athletes excel at everyday tasks?. Med Sci Sports Exerc 2011; 43 (10) 1920-1926
• 22 Zhang M, Jia J, Yang Y, Zhang L, Wang X. Effects of exercise interventions on cognitive functions in healthy populations: A systematic review and meta-analysis. Ageing Res Rev 2023; 92: 102116
• 23 Asken BM, Rabinovici GD. Professional Soccer and Dementia Risk-The Ugly Side of the Beautiful Game. JAMA Neurol 2021; 78 (09) 1049-1051

Publikationsverlauf

Eingereicht: 08. Juli 2024

Angenommen: 29. November 2024

Artikel online veröffentlicht:
19. März 2025