Use of Carbohydrate (CHO), Gluten-Free, and FODMAP-Free Diets to Prevent Gastrointestinal Symptoms in Endurance Athletes: A Systematic Review

nd: Gastrointestinal symptoms (GISs) can affect the performance of endurance athletes (EAs). This study aims to analyze the ef cacy of carbohydrate (CHO), gluten-free, and low-mono-saccharide and polyol (FODMAP) diets in preventing GISs in adult EAs of both sexes. Methods: A systematic search was conducted prior to 30 June 2024 in accordance with the PRISMA statement. We searched for original studies from the last eight years, in English or Spanish, that looked at the effect of CHO, gluten-free, or FODMAP diets on the GISs of EAs. In PubMed, the MeSH (medical subject heading) categories were used. The search was repeated in EBSCO, Google Scholar, and Web of Science. The inclusion criteria were determined using the PICOS framework and the risk of bias in each paper was assessed using the PEDro scale quality criteria checklist (systematic review registration: INPLASY202490080). Results: Of 289 articles identi ed, only 3.5% met the eligibility criteria. All studies found that GISs are common in EAs. We found that 60% of the articles used an experimental method; moreover, based

determined using the PICOS framework and the risk of bias in each paper was assessed using the PEDro scale quality criteria checklist (systematic review registration: INPLASY202490080). Results: Of 289 articles identi ed, only 3.5% met the eligibility criteria. All studies found that GISs are common in EAs. We found that 60% of the articles used an experimental method; moreover, based on 80% of the articles, following a bowel training diet, like CHO, reduced ber and dairy products, or a low-FODMAP diet, has the potential to reduce gastrointestinal symptoms and improve the athletic performance of EA. Conclusions: We found that low-FODMAP diets, gut training with CHO intake, and decreased ber and dairy intake may have favorable effects in preventing GISs. No studies support a gluten-free diet in reducing GISs in EAs. Keywords:sports nutrition; sports performance; gastrointestinal upset; athletes' preferences 1. Introduction Endurance athletes (EAs) often experience gastrointestinal symptoms (GISs) [1,2] that affect their performance and health [3,4]. Previous ndings suggest that up to 70% of EAs, during rest and moderate and vigorous exercise, can have a high frequency and intensity of symptoms [5,6]. These multifactorial symptoms involve mechanical, physiological, and nutritional factors [2,7]. They may occur before, during, or after exercise and manifest as upper symptoms (including nausea, vomiting, and re ux) or lower symptoms (including abdominal pain, bloating, atulence, diarrhea, and rectal bleeding) [8]. Appropriate nutrition could help with managing the symptomology of GISs. The implementation of popular diets has increased rapidly in recent years due to their perceived ergogenic and health bene ts [9–11]. A recently published exploratory study found that the self-reported nutritional strategies used more commonly by EAs are those related to dif- ferent types of carbohydrates (CHOs) (dietary ber reduction, dairy avoidance, FODMAP diet) [12]. In addition, a recent review [1] showed that the FODMAP diet and employing repetitive gut training using carbohydrates are the most used approaches by Ultra-EAs to alleviate exercise-induced GISs. Interestingly, over recent years, adherence to a gluten-free Nutrients2024,16, 3852.

addition, a recent review [1] showed that the FODMAP diet and employing repetitive gut training using carbohydrates are the most used approaches by Ultra-EAs to alleviate exercise-induced GISs. Interestingly, over recent years, adherence to a gluten-free Nutrients2024,16, 3852.

Nutrients2024,16, 3852 2 of 12 diet in non-celiac athletes has become increasingly popular [13]. Surprisingly, forty percent of non-celiac athletes report following this diet at least half the time, and 60% have a self-reported “gluten intolerance” [10,14]. CHO is a fuel source oxidized by skeletal muscle tissue during prolonged exercise [15]. The consumption of CHOs during exercise can improve endurance and performance during prolonged exercise (>2 h) [16]. Additionally, previous studies have reported that ef cient oxidation is associated with a lower accumulation of CHO in the gastrointestinal tract, reducing the risk of developing GIS discomfort [17,18]. Gastrointestinal training with a high amount of CHO is a strategy that can help athletes improve their tolerance to CHO intake and reduce GISs during exercise [19,20]. This involves the consumption of CHO during training to enhance absorption and utilization during prolonged exercise [16]. Gluten is a complex mixture of proteins present in foods such as wheat, rye, barley, and oats that are incompletely digested by intestinal enzymes [21]. A gluten-free diet is essential for managing symptoms in people diagnosed with celiac disease or gluten sensitivity [22]. This diet has also been popularized among non-celiac athletes [10] due to the belief that it is a healthy and balanced diet [13]. However, there is no scienti c evidence that this diet supports improved mental or physical performance in healthy people [23]. FODMAPs are CHOs that are poorly absorbed and highly fermentable by the intestinal ora, and are present in fruits, vegetables, cereals, milk, dairy products, legumes, and sweeteners [24]. The main types of FODMAPs are fructose, lactose, oligosaccharides, and polyols, each with a distinct action mechanism [25]. The low-FODMAP diet [24,26,27] involves the reduced consumption of fermentable short-chain CHOs and is used in people with non-speci c digestive symptoms such as irritable bowel syndrome [28,29]. In athletes who perform strenuous exercise, undigested molecules can increase the osmotic load in the small intestine, leading to increased stool volume or diarrhea [30]. The low-FODMAP diet is associated with improved GISs in 50–80% of patients. However, following this diet is not often easy due to an unintuitive

with non-speci c digestive symptoms such as irritable bowel syndrome [28,29]. In athletes who perform strenuous exercise, undigested molecules can increase the osmotic load in the small intestine, leading to increased stool volume or diarrhea [30]. The low-FODMAP diet is associated with improved GISs in 50–80% of patients. However, following this diet is not often easy due to an unintuitive and very restrictive list of foods that can increase the risk of de ciencies and imbalances in the microbiota [31]. The relationship between nutritional interventions and the maintenance or alteration of intestinal integrity is still unclear. Even though the intake of CHOs could bene t the performance of athletes, their impact on GISs is yet unknown, making it dif cult to develop recommendations [32]. In addition, gluten-free and low-FODMAP diets are popularly suggested to improve gastrointestinal health [33]. Based on previous reviews, it is evident that a substantial number of athletes are not diagnosed with a clinical condition necessitating a gluten-free diet to prevent gastrointestinal issues [34]. Additionally, athletes who adhere to a gluten-free diet inadvertently reduce their intake of high-FODMAP foods, effectively reducing gastrointestinal symptoms [11,35]. This approach depends on the athletes' characteristics and the severity of gastrointestinal issues [36]. Given this context, the following question arises: Are CHO, gluten-free, and low-FODMAP diets effective in mitigating GISs in EAs? Consequently, this review aims to analyze the ef cacy of CHO, gluten-free, and low-FODMAP diets in preventing GISs in adult EAs of both sexes. 2. Materials and Methods 2.1. Search Strategy A systematic search was carried out for articles published before June 30, 2024, follow- ing the criteria of the PRISMA declaration [37]. We used generic terms to identify all studies addressing the ef cacy of CHO, gluten-free, and low-FODMAP diets in preventing GISs in adult EAs of both sexes. The search criteria were (((“Diet, Carbohydrate-Restricted”))) OR (“Diet, Gluten-Free” AND (“Gastrointestinal Diseases”)) AND (“Athletes”). In PubMed, the MeSH (Medical Subject Heading) terms were used. The same search strategy and com- bination of terms was repeated in EBSCO, Google Scholar, and Web of Science. A PRISMA ow diagram was used to

diets in preventing GISs in adult EAs of both sexes. The search criteria were (((“Diet, Carbohydrate-Restricted”))) OR (“Diet, Gluten-Free” AND (“Gastrointestinal Diseases”)) AND (“Athletes”). In PubMed, the MeSH (Medical Subject Heading) terms were used. The same search strategy and com- bination of terms was repeated in EBSCO, Google Scholar, and Web of Science. A PRISMA ow diagram was used to show the search strategy steps for this systematic review.

Nutrients2024,16, 3852 3 of 12 2.2. Inclusion and Exclusion Criteria The inclusion criteria were determined using the PICOS (population, intervention, comparators, outcomes, study design) model (Table). Table 1.PICOS model for determination of inclusion criteria. Topic Criteria P Population Adult endurance athletes or runners with GISs of both sexes. I Intervention Use of CHO, gluten-free, and low-FODMAP diets in preventing GISs or the application of a dietary questionnaire for determining the incidence and severity of GISs related to exercise. C Comparators None/placebo. O Outcomes GI reports (self-reported gut symptoms). S Study design Original studies from the last eight years (cross-sectional studies, randomized controlled trials, crossover trials, case studies), written in English or Spanish, available to the authors as a full text that includes results about the relationship between the use or intake of CHO, gluten-free, and low-FODMAP diets with GISs in EAs or runners. A researcher (KNMC) reviewed, in detail, whether the articles met the inclusion criteria established in two phases: (a) reading the title and abstract and (b) reading the full text of the articles included in the previous phase. The exclusion criteria were (a) narrative or systematic reviews; (b) studies on athletes diagnosed with celiac disease; (c) articles related to non-athletes or other sports disciplines; and (d) studies that included results of the use or intake of CHO, gluten, and FODMAP diets not related to GISs. 2.3. Quality Assessment of Studies The risk of bias and quality in each paper was assessed by KNMC using the (Table) PEDro Scale (Physiotherapy Evidence Database) checklist [38] containing 11 criteria (eligi- bility, random allocation, concealed allocation, baseline comparability, blind subjects, blind therapies, blind assessors, adequate follow-up, intention-to-treat analyses, between-group comparations, and point estimates and variability). A score > 6 was considered acceptable to be considered in this review. Further details regarding the PEDro Scale methodology can be found elsewhere [38]. Table 2.Scienti c quality of studies according to PEDro Scale [38]. PEDro Scale Costa et al. [39] Lis et al. [40] Miall et al. [41] Wif n et al. [25] Hoogervorst et al. [42] Parnell et al. [43] Gaskell et al. [44]

to be considered in this review. Further details regarding the PEDro Scale methodology can be found elsewhere [38]. Table 2.Scienti c quality of studies according to PEDro Scale [38]. PEDro Scale Costa et al. [39] Lis et al. [40] Miall et al. [41] Wif n et al. [25] Hoogervorst et al. [42] Parnell et al. [43] Gaskell et al. [44] Rauch et al. [45] Etxebarria et al. [46] Scrivin et al. [12] 1. 2.3.4.5.6.7.8.9.10.Between-group comparisons11.Point estimates and variabilityTOTAL 8/10 9/10 7/10 6/10 8/10 6/10 10/10 10/10 7/10 7/10 contains the criteria;does not contain the criteria.

Nutrients2024,16, 3852 4 of 12 2.4. Process of Extraction of Information After the inclusion criteria and PEDro scale checklist were applied, information on the author and year of publication, objective, type of diet, methodology, results, and conclusion were extracted by two authors (KNMC, MJAT), and the systematic review was registered at INPLASY202490080. 3. Results A total of 651 articles were identi ed, of which 55% (n= 362) were duplicated in the different databases. In this phase, 289 articles were selected by reading the title and abstract. Moreover, 93% (n= 271) were excluded because they were systematic reviews or did not include results that would allow for an analysis of the ef cacy of CHO, gluten-free, and low-FODMAP diets in preventing GISs in adult EAs of both sexes. The remaining 18 articles were evaluated using the PEDro Scale [38]. Of these, eight articles were excluded because they did not score 6 on the PEDro Scale. The PRISMA ow diagram (Figure) shows the steps of the search strategy and the 10 articles considered for this systematic review.Nutrients 2024, 16, x FOR PEER REVIEW 4 of 12 9. Intention-to-treat analysis 10. Between-group comparisons 11. Point estimates and variability TOTAL 8/10 9/10 7/10 6/10 8/10 6/10 10/10 10/10 7/10 7/10 contains the criteria; does not contain the criteria. 2.4. Process of Extraction of Information After the inclusion criteria and PEDro scale checklist were applied, information on the author and year of publication, objective, type of diet, methodology, results, and conclusion were extracted by two authors (KNMC, MJAT), and the systematic review was registered at https://inplasy.com/inplasy-2024-9-0080/ (accessed on 18 September 2024) , identifier INPLASY202490080. 3. Results A total of 651 articles were identified, of which 55% (n = 362) were duplicated in the different databases. In this phase, 289 articles were selected by reading the title and abstract. Moreover, 93% (n = 271) were excluded because they were systematic reviews or did not include results that would allow for an analysis of the efficacy of CHO, gluten- free, and low-FODMAP diets in preventing GISs in adult EAs of both sexes. The remaining 18 articles were

In this phase, 289 articles were selected by reading the title and abstract. Moreover, 93% (n = 271) were excluded because they were systematic reviews or did not include results that would allow for an analysis of the efficacy of CHO, gluten- free, and low-FODMAP diets in preventing GISs in adult EAs of both sexes. The remaining 18 articles were evaluated using the PEDro Scale [38]. Of these, eight articles were excluded because they did not score ≥6 on the PEDro Scale. The PRISMA flow diagram (Figure 1) shows the steps of the search strategy and the 10 articles considered for this systematic review. Figure 1. Flow diagram according to PRISMA 2020. Table 3 summarizes the selected articles. Of the studies included in this review, 60% included males and females, and 90% involved trained or recreational adult runners. One study incorporated EAs from a discipline other than running [47]. Figure 1.Flow diagram according to PRISMA 2020. Table included males and females, and 90% involved trained or recreational adult runners. One study incorporated EAs from a discipline other than running [47]. Of the 10 articles, 60% used an experimental method to search for results that sup- ported the bene t of dietary interventions based on a CHO diet, gluten-free diet, or low- FODMAP diet. In contrast, the other 40% implemented validated questionnaires or diary records to collect background information on the strategies used to mitigate gastrointestinal discomfort in EAs. It is worth mentioning that two of the studies used dietary records as a tool that was complementary to the experimental intervention. In addition, for de- termining the incidence and severity of GISs related to exercise, scales or questionnaires were used. The instruments used by the authors were (i) a 10-point Likert-type rating scale (n= 3), (ii) the Syndrome Severity Scoring System (n= 1), (iii) web-based questionnaires (n= 1), (iv) the visual analog scale (n= 3) [48], (v) a questionnaire to assess GI symptoms exercise-induced (without Likert-scale items) (n= 1), and (vi) a gut comfort questionnaire (validate by prior authors) (n= 1).

rating scale (n= 3), (ii) the Syndrome Severity Scoring System (n= 1), (iii) web-based questionnaires (n= 1), (iv) the visual analog scale (n= 3) [48], (v) a questionnaire to assess GI symptoms exercise-induced (without Likert-scale items) (n= 1), and (vi) a gut comfort questionnaire (validate by prior authors) (n= 1).

Nutrients2024,16, 3852 5 of 12 Table 3.Studies examining the ef cacy of gluten-free, FODMAP, and CHO-free diets in the prevention of GISs in adult endurance athletes of one or both sexes. Author Objective Methodology Population Results ConclusionsCharacteristics of Diet Questionnaire or Scale to Quantify GIS Intervention Costa et al. [39] To determine the impact of two-week bowel training with CHOs on gastrointestinal status and sports performance. CHO diet. A 10-point Likert-type rating scale. The bowel challenge test was applied to the initial condition (GC-1) and repeated after 2 weeks of bowel training (GC2). Bowel training intervention with (a) CHO-S gel disc. (b) food with CHO-F. (c) Placebo (PLA). 25 (10 women) recreationally competitive endurance and ultra-endurance runners. GIS reduction in GC2: CHO-S (60%;p= 0.008) CHO-F (63%;p= 0.046) PLA (p 0.05). Improvement in the distance test in GC2: CHO-S (5.2%). CHO-F (4.3%). But not in PLA ( 2.1%). (test time:p= 0.009). Two weeks of gut training with CHO-S and CHO-F improved GISs compared to PLA. Lis et al. [40] To investigate the effects of an LFOD in runners with a history of non-clinical exercise-associated GIS. FODMAP diet. A 10-point Likert-type rating scale. LFOD diet + 2 session of 5 1000 m running sessions + 7 km threshold race. One day of stomach lavage HFOD + 2 5 1000 m running sessions + 7 km threshold run. GI symptoms was measured during exercise and daily. 11 recreationally (6 women) competitive runners. During LFOD, a signi cantly lower AUC was observed for daily GISs. The daily GISs that decreased signi cantly were atulence (p< 0.001), urge to defecate (p= 0.04), loose stools (p= 0.03), and diarrhea (p= 0.004). No signi cant differences in exercise symptoms or DALDA responses were observed between diets (p> 0.05). LFOD may be a bene cial intervention to minimize daily GISs in runners with exercise-related discomfort. Miall et al. [41] To determine whether two weeks of repetitive bowel challenge during running can reduce exercise-associated GISs and CHO malabsorption. CHO diet. 10-point Likert-type rating scale. Initial bowel challenge test (GC1) with 30 g CHO (2:1 glucose/fructose, 10% w/v) every 20

The review evaluates dietary interventions for gastrointestinal symptoms in endurance athletes.