EFFECTS OF KARATE-DŌ TRAINING IN OLDER ADULTS COGNITION: RANDOMIZED CONTROLLED TRIAL EFEITOS DO TREINAMENTO DE KARATE-DŌ NA COGNIÇÃO DE IDOSOS: ENSAIO

The aim of this study was to verify the effectiveness of a Karate-Dō training, Wadō-ryū style, on cognition in healthy older adults. We conducted a single-blind randomized controlled trial with 33 older adults divided into Karate Group (KG) and Control Group (CG). In the pre and post-intervention, participants answered a sociodemographic questionnaire, a battery of neuropsychological tests, scales of subjective cognitive complaints, depressive and anxiety symptoms. The intervention was conducted twice per week for 12 weeks (lasting 60 minutes). The CG did not perform any physical activity or cognitive stimulation during the intervention period. Data analysis was performed using descriptive and inferences statistics. Performance comparisons in neuropsychological tests and scales of subjective cognitive complaints, within and between groups, pre and post-intervention, was performed by Mann-Whitney and Wilcoxon tests. KG shows better results than CG in visual memory tasks, executive functions and memory complaints in post-intervention analysis. The results suggest that 3 months of Karate-Dō practice is related to a significant improvement of the cognitive functions in healthy older adults.


Introduction
Cognitive functions are defined as the brain's ability to perform skills needed to carry out different tasks. They concern different mental processes such as attention, perception, memory, language, motor skills and visuoconstrutive abilities in addition to the executive functions 1 . During the aging process, some of these functions have a natural decline, e.g. in explicit memory, working memory, attention, executive functions and fluid intelligence 2 . However, the speed of the cognitive impairment can be influenced by the individual's lifestyle. Physical exercise, in general, is an important factor to reduce the cognitive impairment 3 , by reducing the impact of neurodegenerative diseases associated with aging 4 .
Martial arts are exercises that have a positive impact on physical health, stimulate cognitive and motor skills and can improve the quality of life and the emotional health of practitioners 5,6 . Among the different styles of martial arts, Karate-Dō is a discipline of personal development through struggle practices, which also stimulate memory and motion tasks. It is based on three core educational pillars: kihon (basic techniques), kata (form) and kumite (fight, combat) 7 .
Kihon is the study of the fundamentals of this martial art. The practitioner makes repeated movements (strikes and defenses, walking or standing) in order to enhance technical gestures. Kata are predetermined sequences of techniques that simulate a combat against multiple opponents, individually performed as Kihon, where pre-established attack and defense moves are performed. Kumite explores physical contact between the practitioners, through real or adapted body contact exercises [7][8][9] . It is a global development process where the karateka are entirely focused on the technique and body coordination. This indicates the presence of a demanding cognitive task. When this is associated with the muscle memory, concentration and meditation practices, it should result in increased benefits to the psychological balance of the practitioner 5 .
Physical activity plays a key role on cognitive performance 3 and several studies report cognitive benefits derived from the practice of martial arts, especially in global cognitive function 10 , attention tasks, working memory 11 , delayed recall and subjective cognitive complaints 12 of the practitioner. Such studies focused on Tàijí Quán. However, there are few studies on the therapeutic effects of Karate-Dō regarding cognitive aspects, especially regarding older adults. A better understanding of the effects of this physical activity may contribute to the development of more appropriate interventions for the treatment of neurological conditions through physical activities and sports. Therefore, this study aimed to assess the effectiveness of the training of Karate-Dō Wadō-ryū style on the cognition of older adults.

Methods
This study is characterized as a single-blind randomized controlled trial, approved by the Research Ethics Committee of the Pontifical Catholic University of Rio Grande do Sul (PUCRS) (CAAE number 26742314.8.0000.5336) and registered at the Brazilian Registry of Clinical Trials (REBEC -number 2494). All the requirements of the Ministry of Health's Resolution 466/2012 on research with human beings were met for this study.

Participants, Randomization and Blinding
The study included older adults (between 60 and 85 years old) residents of the city of Porto Alegre, recruited by convenience sampling and in newspaper advertisements. In total, 123 individuals were selected, and 73 agreed to participate. Of these, 11 were deemed ineligible, leaving 62 subjects (59 females and 3 males) who completed the first tests and were randomized, in a one by one draw. All researchers involved in the study were blindfolded. However, the Karate-Dō teacher and the trained participantes were not blindfolded.
The groups were named Karate Group (KG) and Control Group (CG). After the training, some participants have withdrawn from the study, and the final sample consisted of 33 older adults (16 participants in KG and 17 in the CG). This withdrawal had different reasons, as follows: 1) some participants did not complete the second evaluation session (after training) on a timely basis; 2) health problems (subjects or family members); 3) some respondents did not attend the minimum number of intervention sessions; 4) some subjects simply quit the study.
Inclusion criteria were: being literate; have 60 years of age or older; submited of a medical certificate authorizing them to practice exercises; signed the consent form. Exclusion criteria were: alcoholism; practice of physical exercises on a regular basis; use of drug(s) antidepressant(s); submission of a score below the cut-off point of the Mini-Mental State Examination (MMSE) 13 ; use of crutches, canes, walkers, wheelchairs or similar devices; selfreported walking difficulties to perform the practice of intervention, or participants who needed accessories to assist in displacement. All participants had no previous experience with Karate-Dō and were classified as a "white belt".

Cognitive Battery
The older adults participated individually in 90-minute sessions, approximately, for the completion of a sociodemographic and clinical questionnaire and a cognitive battery. This battery was reapplied after the training period (12 weeks), in both groups, to verify the results. The cognitive battery was applied by a psychologist and scored by another expert to avoid conflicts. Both were trained in the application and correction of tests. The assesments was applied in a private room (whitout interferences) in the Post Graduate Program in Psychology of PUCRS.
The cognitive battery included: (1) MMSE: which evaluates time and spatial orientation, registration, attention and calculation, delayed recall and language. The Portuguese version 13 27 . The instruments administered had the objective of evaluating a wide range of cognitive functions, since some skills could show improvement with the training and others did not. All the instruments are extremely recognized in neuropsychology, demonstrating robust evidence of validity and reliability in the cognitive evaluation of older adults, besides being validated for the Brazilian context.

Intervention
After the initial assessment, the KG participated in 24 intervention sessions over 12 weeks, conducted in groups, twice a week and lasting 60 minutes. The training was conducted by a trained teacher, with black belt (1st Dan) in Karate-Dō, Wadō-ryū style. The training session consisted of: (1) brief warmup -5-10 minutes; (2) kihon exercises, kata (sequences of Karate-Dō movements), kumite and breathing techniques -40-45 minutes and (3) relaxation through brief meditation exercises tailored to the needs of the participants -10 minutes.
The technical exercises of Karate-Dō covered in the training sessions were the same exercises of the first belt (white or Mu Kyū) in Wadō-ryū style. In kihon: Jun Zuki (straight punch), Gyaku Zuki (reverse punch), Gedan Barai Uke (low defense), Jodan Age Uke (high defense), Mae Geri (front kick) and Zenkutsu Dachi (advanced posture); in kata: Kihon Kata (basic form); in kumite: applications of the exercises in pairs. Breathing exercises were inserted into the kihon. The meditation practice was performed in the supine position on the mats (lying flat on their backs) in order to accommodate all the participants, helping prevent the discomfort of the standing or sitting position.
The practices occurred in an appropriate room. During the intervention period the CG were instructed to continue performing their daily activities. After the end of all sessions, both groups were re-evaluated with the previously used instruments. Figure 1 shows the study design and its steps.

Outcome
The outcome measures were performance in cognitive assessment battery, subjective cognitive complaint scales and functional capacity scales, between and within groups, in pre and post-intervention.

Sample Size
The sample size was calculated using the Winpepi software version 11.26 28 , based on studies of Lam et al 12 and Nguyen and Kruse 10 , considering the cognitive functions investigated by these two studies. A sample size of 16 participants per group would be required for the study to have 95% power to show intervention improvements. All p values were two-sided, and a p value of 0.05 or less was considered to indicate statistical significance.

Statistical Analysis
The following variables were investigated: (1) cognition and (2) sociodemographic data. Data was analyzed using the statistic package SPSS version 22.0 for Windows. Chi Square test was used to verify differences in categorical sociodemographic characteristics and Mann-Whitney U test was used for the continuous characteristics. This analysis was performed between groups (KG versus CG) in the pre-intervention. Descriptive analysis included frequencies, means, standard deviations and percentage.
Performance on cognitive tests and subjective cognitive complaints of questionnaires between groups in the pre and post-interventions were investigated using Mann Whitney U test, since the data did not present normal distribution according to the Kolmogorov-Smirnov test. Performance on cognitive tests and subjective cognitive complaints questionnaires, pre and post-interventions within the groups, were analyzed by Wilcoxon test. The effect size was calculated with Cohen's d test. The results were considered significant when p ≤0.05. Table 1 shows the sociodemographic characteristics and clinical data of KG and CG. There were no statistically significant differences between groups regarding age, education, socioeconomic status and gender distribution between the groups. The KG was composed by 93.75% women and 6.25% men, and CG by 94.12% women and 5.88% men. Also, the groups did not differ in subjective perception of health, general cognitive ability, number of depressive and anxiety symptoms in the pre-intervention period.  Table 2 shows the performance of both groups in the cognitive assessment battery, in the pre and post-intervention, and between and within groups analysis. In the pre-intervention, KG obtained significantly higher scores compared to CG in ROCF copy (score) and WCST-64 (failure to maintain context); whereas CG had higher scores in ROCF delayed recall (time in seconds) and VMS (forward). In the post-intervention was identified that KG obtained significantly higher scores compared to GC in ROCF delayed recall (score). This group also improved their performance in the VMS (forward), eliminating the previous difference. The other data retained its behavior in relation to the pre-intervention.

Results
In within groups analysis, CG did not show significant differences. However KG presented a superior performance in the post-intervention in the following tasks: RAVLT A1-A5, ROCF delayed recall (score), WCST-64 (conceptual level responses) and TMT-B (time in seconds). The effect size of these improvements ranged from moderate (d between 0.7 and 0.5) to small (d ≥ 0.4). Table 3 shows the scores of the subjective cognitive complaint scales and of functional capacity from both groups (pre and post intervation). No significant differences were found in the analysis between groups (pre-intervention); however, KG performed much better than CG in the MAC-Q questionnaire (informant) in the post-intervention. There was also a significant difference with strong effect between the initial performance and the final results of the KG group in the same task.

Discussion
In a single-blind randomized controlled trial with healthy and sedentary older adults, the impact of the Karate-Dō Wadō-ryū style practice on cognitive abilities was investigated. The KG performed better than CG in visual memory ability (delayed recall). This was also observed in the comparison within groups. Such behavior can be explained by the characteristics of Karate-Dō practice: in a typical training session, the student watches the teacher perform the movements, then memorizes and performs these sequential tasks themselves. This repetition begins in non-automated form, evolving until the student is able to use only their memory to perform the techniques 7,8 .
In within group comparisons, the KG did not achieve significant results in VMS test (forward), but the significant difference in the analysis between groups (pre-intervention) is not observed in post-intervention, suggesting a possible improvement in the KG. The VMS test evaluates, among other functions, concentrated attention and visuospatial memory 18 . Furthermore, significant improvements were reported in the alternating attention function (TMT-B -Time in seconds), in KG within group comparison. Such improvements can be associated to the kata (form) and kumite (fight) practices. Concurrent to visual stimulation provided by the teacher, kata practitioners should perform sequence movements in the environment in multiple directions 8 . They should be very careful to perform the task correctly to avoid clashing with their colleagues during the process. In kumite the student is supposed to calculate strength, speed and distance, in defense and attack exercises with arms and legs, in order to move in harmony with the partner 9 . Overall, it is a task of great attentional demand and visuospatial ability.
Also, significant improvements were observed in KG regarding the episodic verbal memory (immediate recall) in the RAVLT A1-A5 task, in comparisons within group. This improvement may be related to the social interaction provided by the activity 29 : conversation and interaction among participants was always encouraged during the intervals. The specific verbal content of the martial art discussed in the sessions may have also influenced the results of episodic verbal memory; the techniques and movements of Karate-Dō are named in Japanese, and these terms should be learned by the participants. This is a brief experience of speaking a foreign language.
Regarding to the executive functions, the WCST-64 tests (conceptual responses) and TMT-B (Time in seconds) has identified improvements in logical-abstract reasoning ability and visual processing speed in the KG in comparisons within groups. The visual stimulation associated to the coordination skills required in Karate-Dō may provide a strong stimulus for visual processing speed. The practice of kumite (combat) may be responsible for the improvement of this executive function: in addition to performing the movements correctly, the participant must perform defenses and counter attacks effectively 9 ; such tasks stimulate the reaction time, which also depends of the visual stimulus 30 . The logical-abstract reasoning ability is strongly associated with the kata (form) practice: it is a sequence of predetermined movements, which simulates a fight against imaginary opponents. The student should perform the movements in the correct order, trying to hit his "enemies" at specific points of the body 8 . There are similar demands in kihon exercises (basic movements) and kumite (combat) 9 , for it is necessary to choose and perform the techniques (attacks, defenses and dodges) that are most appropriate for each situation. The use of a cognitive process that involves logicalabstract reasoning is clear in these tasks and may be responsible for the improvement.
A substantial improvement of subjective memory complaints was identified in KG in comparison within groups, as reported by family members in the MAC-Q questionnaire (informant). There was also a noteworthy improvement in this questionnaire compared to CG in post-intervention. It is a functional measure of the intervention, suggesting that the improvements in the assessment instruments may have impacted the daily routine of the participants. This data is very relevant because the outstanding performances in a retest maybe associated to the learning of these tasks, rather than to a real improvement in the older adult's condition 31 . Taking into account the aforementioned data, these results reinforce the improvements detected in the visual and verbal memory.
Several studies show significant improvements in cognition after several protocols of physical training. A recent study 32 investigated the effects of systematized physical exercise for 282 older adults, within a three-year period, which showed benefits related to executive functions and processing speed. The study of Antunes et al. 33 conducted a six-month fitness program, with emphasis on aerobic metabolism, in which the experimental group improved significantly in attention process, memory and motor skills (agility). Another study was conducted with two groups (46 volunteers) subjected to resistance training for eight weeks. This survey identified moderate improvements on psychological well-being and cognitive functions of older adults, especially in memory. The intervention group maintained its improvement one year after the training period compared to the control group 34 .
In the field of martial arts, Kasai and contributors 35 found significant improvements in memory abilities in a 6-month training pilot study of Tàijí quán with 26 older adults. In another study on the same martial art, during a 10-week intervention, the researchers found significant benefits in concentrated attention, episodic verbal memory, visual memory and visuospatial memory in the older adults 11 . Several studies on Tàijí quán showed significant improvements in global cognitive function, delayed recall and subjective cognitive complaints 12 , as well as in executive functions 10 and speed processing 36 .
Regarding Karate-Dō, there are few studies conducted that have investigated cognitive functions. A survey found improvements in children's confidence in their own abilities and memory function by parental report 37 . However, the martial art investigated was the Kenpō Karate, a practice with a similar name but different formative contents. Another study that investigated the Karate-Dō Shōtōkan-ryū style practice found no positive effects 5 . Improvement in cognition obtained with the practice of Karate-Dō demonstrated by this study was corroborated in the studies of Tàijí quán and others types of physical exercises. This can be explained by the presence of a memory training in which the subject learns the complex tasks sequences performed in an intervention session. It is a coordinated pathway between memory, attention, postural control, voluntary motor actions, verbal and visual imagery, which constitute the learning process 12 . In addition, Tàijí quán is assumed as an effective activity to prevent cognitive impairment (in normal or pathological aging) because their practice stimulates neurogenesis and angiogenesis processes in the brain 36 . As shown, the results of this survey are consistent with the literature, indicating that Karate-Dō can be classified as a cognitive training activity with an efficacy similar to that of Tàijí quán.

Study Limitations
This study does has some limitations. One of the greatest difficulties consisted in obtaining a sample that would meet all the inclusion criteria and maintaining the number of participants until the end. Also, additional results could have been obtained if there is the presence of a third group of participants, practicing another type of physical exercise.
Such points may have affected the results in some way. However, despite the limitations, this is the first study that investigated the effects of the practice of Karate-Dō Wadō-ryū style in cognition in the older adults. In addition to finding benefits for cognition, it was possible to find the functions that the practice of Karate-Dō affects specifically.

Conclusions
According to the findings, the results suggest that 3 months of Karate-Dō, Wadōryū style practice is related to a significant improvement of the cognitive functions in healthy older adults. Substantial improvements were observed in abilities of visual memory (delayed recall), alternative attention, episodic verbal memory (immediate recall), executive functions (logic-abstract reasoning and visual processing speed), and a decrease of subjective cognitive complaints by informants.
Thus, the present study shows evidence that Karate-Dō may serve as a cognitive stimulation activity. Additional studies with longer training periods or longer weekly frequency are still needed to fully understand the impacts of its effects on cognitive functions. Another strategy is to work with a third sample group, practicing another type of physical exercise. It is also necessary to investigate the maintenance of these benefits in long term. For future studies, we would like to further examine the cognitive functions investigated, as well as other factors that may impact health, which include strength, flexibility and biological markers.