How the vegetarian diet influences recreational and professional athletes’ physical performance: A systematic review

Vegetarianism has been getting increasing attention over the years, in society in general and in sport in particular. However, the growth in the number of people following a meatless diet notwithstanding, vegetarianism should be practiced with caution, especially by professional and recreational athletes, considering the possible lack of certain nutrients and decline in their physical performance. Therefore, the present review aimed to determine whether following a vegetarian diet influences recreational and professional athletes’ physical and sports performance. A search of the databases Medline/Pubmed, Scopus, Web of Science, and Lilacs gave 343 relevant articles; however, only 15 of these focused on the vegetarian diet and physical performance, in accordance with the inclusion criteria. These studies compared the vegetarian diet with the omnivorous diet, and found that it did not negatively influence physical performance. Moreover, those who followed a vegetarian diet seemed to have a higher volume of maximum oxygen (V̇O 2 max), which positively influenced their performance. In conclusion, following a plant-based diet does not seem to harm recreational and professional athletes.


Introduction
Vegetarianism has been receiving increasing attention worldwide; as a result, the number of people practicing it has increased over the years. Approximately 22% of the world's population is vegetarian, while 8% of elite athletes are vegetarian (Collins et al. 2020).
The Brazilian Vegetarian Society (2017) considers vegetarianism as the dietary regime that excludes all types of meat and may, in some categories, include animal derivatives. However, the vegetarian diet can be classified in different ways, depending on the inclusion or exclusion of certain animal products. In this sense, a vegetarian can be categorized under one of the following four classifications: "ovolactovegetarian"-those who consume eggs and dairy products; "lactovegetarian"those who consume dairy products but not eggs; "ovovegetarian"-those who consume eggs but not dairy products; or "strict vegetarian"-those who do not consume any animal products or ingredients such as gelatin, albumin, milk proteins, some dyes, and thickeners (Slywitch 2012). Moreover, according to the definition provided by the Vegan Society. (n.d.), vegans are also considered strict vegetarians in terms of diet. In addition to diet, veganism is a philosophy of life that tries to exclude all things related to animal exploitation, including food, cosmetics, and clothing.
While there are several reasons motivating individuals to become vegetarians, such as religiosity, sustainability, moral beliefs, and being against different treatment in relation to other species; however, according to Courceiro et al. (2008), health seems to be the most common reason. Some studies have associated the vegetarian diets with a lower risk of cardiovascular and metabolic diseases (Orlich et al. 2013;Kim et al. 2019;Qian et al. 2019). Moreover, a balanced vegetarian diet is associated with a higher intake of complex carbohydrates, fiber, fruits, vegetables, antioxidants, phytochemicals, and a lower intake of saturated fat and cholesterol, when compared with the omnivorous diet (Ada 2003; Rauma & Mykkanen 2000;Huang et al. 1999). Conversely, the general population still believes that a diet devoid of animal products may be associated with poor performance due to the lack of certain nutrients, such as protein, creatine, vitamin B12, and vitamin D (Fields et al. 2016;Solis et al. 2017).
According to the American College of Sports Medicine (2016), "the performance of, and recovery from, sporting activities are enhanced by well-chosen nutrition strategies" (p. 543). Therefore, the nutritional aspect must be considered as an important factor for recreational athletes' and professional athletes' physical and sports performance. The American Dietetic Association (2003) argues that vegetarianism and veganism are suitable for different groups of people such as pregnant women, nursing mothers, children, adolescents, adults, and even athletes. However, even in a balanced vegetarian diet, which is considered appropriate for maintaining health throughout one's life cycle (Craig & Mangels 2009), attention should be paid to nutritional adequacy vis-à-vis physical performance in professional and recreational athletes, as many of their necessary and desirable nutritional needs may remain unmet, leading to a decline in performance.
Considering the increasing adherence to plant-based diets, without meat consumption and with regular physical exercise, this systematic literature review aimed to determine whether following a vegetarian diet influences recreational athletes' and professional athletes' physical and sports performance.

Eligibility criteria
The research strategy was defined based on the question "Does following a vegetarian diet influence recreational athletes' and professional athletes' physical and sports performance?" and considered the PICO (Guyatt et al. 2008 All observational studies that sought to identify the effects if vegetarian diets on physical and sports performance were considered eligible. Publications such as letters to the editor, editorials, literature reviews, meta-analyses, and points of view were excluded.

Search sources and strategies
The databases searched were Medline/Pubmed, Scopus, Web of Science, and Lilacs by employing independent search strategies. The references of the eligible articles were checked to select studies of interest. The search strategies using keywords, other terms, and Boolean language are described in Table 1, which was conducted in accordance with the guideline described by the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) (Liberati et al, 2009 76 Scopus (TITLE-ABS-KEY (adult* OR athlete* OR "practicing sports" OR "practicing physical activities") AND TITLE-ABS-KEY ("Diet, Vegetarian" OR vegetarian OR vegan OR "energy restricted diets") AND TITLE-ABS-KEY ("Athletic Performance" OR "Sports performance" OR "physical performance" OR performance)) 04/19/2021 186 Web of Science (Adult* OR athlete* OR "practicing sports" OR "practicing physical activities") AND TÓPICO: ("Diet, Vegetarian" OR vegetarian OR vegan OR "energy restricted diets") AND TÓPICO: ("Athletic Performance" OR "Sports performance" OR "physical performance" OR performance)

Risk of bias
After the articles were selected, duplicate records were removed. Subsequently, the three authors selected the articles independently, starting with the title. The reviewers then analyzed the articles, and disagreements were resolved in accordance Research, Society andDevelopment, v. 10, n. 9, e26910917952, 2021 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v10i9.17952 4 with all authors. Thereafter, the three authors read the abstracts of the selected articles and independently selected the eligible ones, thus ensuring greater accuracy. Disagreements were resolved by consensus, and the eligible articles were then read in full.

Article selection
The initial search yielded 343 articles, of which 15 were selected after following all the steps. Figure 1 shows the entire process.

Summary of results
Among the 15 articles, one (5.6%) reported that the vegetarian diet negatively influences physical and sports performance, while eight (44.4%) reported the opposite, and nine (50%) reported that the diet had no influence on the physical and sports performance (the abovementioned percentages were obtained by considering a total of 18 results in the 15 articles as three articles presented more than one result and, thus, were mentioned in different tables; consequently, these articles had to be counted twice). The studies in which the diet worsened performance, or which showed a negative association between the two are presented in Table 2; those in which the diet improved performance, or which showed a positive association between the two are presented in Table 3; and those in which the diet had no effect on performance, or which showed no association between the two are presented in Table 4. Legend: a) Professional athletes are professional competitors, federates. While, recreational athletes do not necessarily participate in competitions. b) * The study by Hebbelinck et al. (1999) identifies contrasting results that can be applied to other tables. There was a negative influence in relation to vegetarian participants in the strength tests, but there was no negative association in relation to the aerobic test for vegetarians in the same study, which can be seen in Table 3. Source: Authors.
To assess the association between protein intake and physical performance in a general population sample. As the main outcome measure was used the 6-min walking test and the distance walked in metres. Their mean vegetable and animal proteins intake for gram/kg of body weight/day were, respectively, 0.4 and 0.7. After adjusting for all the potential confounders, there was a significant increase of 20.0 m in the distance walked for an increase in 10 g/day of vegetable proteins and non-significant variations of −1.8m for an increase in 10 g/day of animal proteins and of 0.5 for an increase in 10 g/day of total proteins. The result suggests a positive role of vegetable proteins on physical performance.
Research, Society and Development, v. 10, n. 9, e26910917952, 2021 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v10i9.17952 8 Król et al. (2020) To assess the differences in the athletes' heart morphology and function and the correlation of these with dietary habits. Legend: a) Professional athletes are professional competitors, federates. While, recreational athletes do not necessarily participate in competitions. b) * The studies identify contrasting results that could be applied to other tables. c) The study by Lynch et al. (2016) demonstrate a difference in the maximum V O2 variable for women, nevertheless there was no such difference for males in the study. d) Boutros et al. (2020) verify a difference in the variable of maximum V O2 and submaximal endurance time to exhaustion, however there were no significant differences in relation to the other variables. The other results of the articles could be seen in Table 4. Source: Authors. Table 4. List of the studies included in the review in which the diet had no effect on performance, or which showed no association between the two (author name, year, aim, sample characteristics, study design and main results). There was a significant diet 9 trainings interaction in soleus carnosine content, which was non-significantly increased with mixed diet and non-significantly decreased with vegetarian diet. Carnosine content in other muscles and gastrocnemius buffer capacity were not influenced by training. The performance during the repeated sprint ability test improved by training, without difference between groups.

Reference
Both groups were supplemented with 1 g/day of creatine monohydrate for 5 weeks. Shomrat et al. (2000) To determine the effect of creatine feeding on maximal exercise performance in vegetarians.

Discussion
Only one study showed that the vegetarian diet had a negative influence on athletes' physical performance. Hebbelinck et al. (1999) initiated the use of strength tests to evaluate performance: a hand grip strength test (static strength), a standing long jump test (explosive strength), and abdominal flexion (abdominal strength) test, and found that the performance of the vegetarian participants was poorer than that of those in the control group, the daily energy intake of the vegetarians was significantly lower than that of the omnivores, which could explain the significant difference observed in the strength test performance of the two groups. Thus, each type of exercise and diet requires a different dietary regime to fulfill the energy requirements necessary for optimum performance. Conversely, Boutros et al. (2020) performed the one repetition maximum (1RM) test for upper and lower limbs to analyze muscle strength in vegetarians and omnivores, and found no significant difference between the two groups. It is worth noting that of the 15 studies reviewed, strength tests had been conducted as an analysis resource in only five articles in the present analyze.
Considering that strength athletes have specific needs when it comes to training and nutrients in their diet, future studies should investigate the association between resistance exercises and the vegetarian diet, thus expanding the literature on the topic, which is currently scarce.
In this review, studies indicating that the vegetarian diet is beneficial for performance had conducted aerobic tests to analyze performance, and in most of these, the participants were endurance athletes. Gazanni et al. (2019) evaluated their participants in the short term through only the diets suggested as part of their investigation; furthermore, Veleba et al. (2016) randomly distributed their study participants into a control group and vegetarian group, including the diets suggested only in the investigation.
According to Nieman (1998), vegetarian diets usually have higher levels of carbohydrates, which can be beneficial for endurance athletes as they enhance the body's glycogen reserves, thereby improving performance. Some studies present in this review that showed a positive correlation between the vegetarian diet without supplementation and with aerobic performance, reported an increase in V O2 max and vagal cardiac activity, which suggests several benefits for the cardiovascular system of these athletes. Nonetheless, some of these studies possess limitations, such as different levels of physical conditioning and uncontrolled diet. Furthermore, Mujika (2019) observed an improvement in the performance of the athletes under analysis in endurance tests using a vegetarian diet, compared with a low-carbohydrate and high-fat diet, however, some questions remain unanswered, as food was the only factor analyzed, and other internal and external variables may have interfered with the athlete's performance.
Only one of the studies reviewed had participants with chronic disease, Veleba et al. (2016) enrolled only diabetics, and after following the vegetarian diet along with aerobic exercise, they showed lower visceral fat levels, which may suggest a decrease in muscle fat, indicating a positive association with physical conditioning; the authors also reported a correlation between lower intracellular fat rates in vegetarians and increased insulin sensitivity, and an increase in metabolic flexibility was also observed, indicating a possible correlation between metabolic flexibility and V O2 max. According to Olfert and Wattick (2018), diets devoid of animal products, prioritizing whole grains, fruits, vegetables, legumes, and nuts, and low in saturated and trans-fat, which can be characterized as vegetarian diets, are associated with a lower risk of metabolic diseases such as diabetes, and provide physical benefits to patients.
Other studies showed that the vegetarian diet had no influence on performance. In most, the common analysis resource used was the blood test associated with performance tests; variables such as skeletal muscle carnitine content and creatine supplementation were analyzed. Furthermore, the study by Baguet et al. (2011) included omnivorous participants who only after a five-week intervention were able to follow a diet devoid of animal products.
Some of the studies in which the vegetarian diet did not influence physical and sports performance investigated the respective influences of creatine and carnosine on anaerobic activities. According to Barr et al. (2004), creatine is found mainly in poultry, fish, and meat, and is synthesized endogenously; its highest concentration is in the muscle, mainly in the form of phosphocreatine. During exercise, phosphocreatine breaks down to generate energy to resynthesize adenosine triphosphate (ATP). Thus, a high concentration of creatine can prolong the exercise's supra-maximal intensity or shorten the recovery time.
Subsequently, Burke et al. (2008) showed that omnivores have higher levels of creatine. However, vegetarians, because they have lower levels of it, seem to be more receptive to the supplementation of this amino acid and absorb it more, having similar adaptations, and without any impact on athletes who wish to follow this type of a plant-based diet. Shomrat et al. (2000) too conducted a study with creatine supplementation among vegetarians and omnivores, comparing peak and average potency during the Wingate test, found lower creatine levels in vegetarians; however, potency during the test was not significantly affected after supplementation, both groups increased their average potency, but only omnivores increased their peak potency. In contrast to the studies analyzed in the present review, Barr et al. (2004) showed a significantly higher increase in total muscle creatine, lean mass, and better performance in knee flexion and extension among vegetarians after supplementation, suggesting that vegetarian athletes who supplement creatine and participate in sports requiring the ATP/phosphocreatine system may show better results than omnivores. Almannai et al. (2019) reported that one of the fundamental functions of carnitine is to produce cellular energy. It is primarily found in animal protein and dairy products, which is favorable to omnivores, who absorb it in greater amounts through food. Vegetarians, on the other hand, obtain carnitine mainly through endogenous synthesis. Novakova et al. (2016) compared body carnitine reserves and physical performance in people following diets with and without animal protein. Although vegetarians had lower plasma carnitine levels, carnitine reserves in skeletal muscle were similar between the two groups. Furthermore, although L-carnitine supplementation led to a slight increase in muscle carnitine, skeletal muscle function and energy metabolism were not affected; thus, performance results did not differ between the groups.

Conclusion
In conclusion, the present review indicates that there is no consensus on the topic in the literature. However, it should be noted that only one study, which used strength tests to analyze performance, showed that the vegetarian diet worsened physical and sports performance. To date, few studies have investigated vegetarian diets using strength tests. Moreover, a significant number of those reviewed found that the vegetarian diet had a positive influence on performance, noting a possible improvement in the cardiorespiratory system of the participants engaging in aerobic activities; while others showed that a diet devoid of animal products did not influence recreational and professional athletes' performance many of the variables analyzed had even values, and in the variables in which a difference was observed, such as creatine levels, supplementation was found to reduce such deficiencies.
For future researchers and works, it would be interesting to analyze larger samples of groups considered vegetarian and greater attention to physical methods, such as V O2 max and muscle strength is encouraged. In addition, a better leveling of participants in terms of physical conditioning and dietary monitoring will be beneficial.