Nutritional strategies for minimizing gastrointestinal symptoms during endurance exercise: systematic review of the literature

ABSTRACT

Background

The gastrointestinal (GI) tract plays a critical role in achieving peak athletic performance either during training or in competitions. Despite its significance, the GI tract’s role in the training process of athletes is often neglected, resulting in frequent GI symptoms. These disturbances are particularly prevalent in endurance sports, where GI function is commonly compromised, leading to adverse effects on performance. In this review, we examine potential nutritional causes of the GI symptoms and provide possible solutions to mitigate them, aiming to enhance athletes’ overall performance and well-being.

Methods

PRISMA methodology was used to search through PubMed Database from January 2023 to March 2023. The selected studies were comprised of randomized controlled trials, crossover trials and case studies.

Results

Twenty-nine studies met the inclusion criteria for this systematic review. The studies were categorized into five distinct areas of research on GI symptoms in endurance exercise: gut training protocols, effects of different carbohydrate solutions and mixtures, low FODMAP diet, hydrogel CHO technology, and probiotic supplementation.

Gut training protocols seem promising in improving GI symptoms over time. Optimizing carbohydrate intake during exercise according to current recommendations has been associated with lower incidence and severity of GI symptoms as well. The low FODMAP diet also shows potential to reduce GI symptoms, although its restrictive nature could negatively affect athletes in other ways. Hydrogel carbohydrate products, at present, do not demonstrate any benefits over standard carbohydrate products. Probiotic supplementation shows mixed evidence regarding its effectiveness in alleviating and reducing GI symptoms during endurance exercise.

Conclusion

We have acknowledged that the onset of GI symptoms is very complex, and that onset is influenced by a huge variety of factors. It should be emphasized that the elimination of GI symptoms in each athlete must be approached individually and thoughtfully.

Graphical abstract

1. Introduction

Gastrointestinal (GI) tract represents a key link in delivering fuel and liquid in long duration exercise, therefore it plays a crucial role in maintaining performance in endurance exercise. Sports nutrition emphasizes optimizing carbohydrate intake during exercise based on duration and intensity, with recommendations ranging from small amounts for short-duration exercise to higher intakes (up to 90 g/h) for prolonged endurance events [1]. However, GI symptoms are often present in athletes during different kinds of exercise and can greatly impact their ability to sustain exercise intensity and sports performance in competition, while also making it challenging to achieve the recommended carbohydrate intake [2]. Literature shows that at least 30 to 50 % of endurance athletes experience GI symptoms during exercise on a regular basis [3], with especially high occurrence in long duration endurance exercise [2]. For example, in endurance trained runners it is estimated that between 30 and 90 % may experience them [3,4]. This wide range in incidence highlights the variability of GI symptoms during endurance exercise. Based on the anatomical origin, GI symptoms can be classified into upper GI (heartburn, regurgitation, stomach pain, belching, etc.), lower GI (flatulence, lower abdominal bloating, urge to defecate, intestinal pain, diarrhea, etc.), and other GI-related symptoms that can occur as well (nausea, dizziness, acute transient abdominal pain) [3].

Past research has recognized four main causes of GI symptoms: first, physiological causes due to splanchnic hypoperfusion [5]; second, mechanical causes, related mostly to how force acts on the GI tract during impact and to the influence of posture during exercise [6]; third, psychological causes, where different psychological states are connected with higher occurrence rates of GI symptoms [7]; and fourth, nutritional causes [3,8] which will be the focus of this paper.

Multiple nutritional factors influence the prevalence and incidence of GI symptoms during endurance exercise, including CHO concentration, type, osmolality, and acidity, as well as dietary intake of fiber, protein, and fat [3]. High FODMAP foods, by increasing osmotic load and colonic gas production, may exacerbate symptoms in sensitive individuals [9]. Consequently, a low FODMAP diet has gained attention as a potential strategy, particularly due to its effectiveness in managing irritable bowel syndrome symptoms [10]. Additionally, the ability to absorb fluids and CHO efficiently is crucial for both fueling and reducing GI distress. Gut microbiota composition also plays a role, with probiotics being explored for their potential in lowering symptom severity and occurrence [11]. More recently, hydrogel-based CHO formulations, designed to encapsulate CHO in the stomach and reduce fermentation, have emerged as a novel approach that may reduce the severity of GI symptoms and CHO availability during exercise.

The aim of the present article is to review the literature on the efficacy of different nutritional strategies that could potentially help lower the incidence and severity of GI symptoms during endurance exercise and, with that, improve exercise performance.

2. Methods

This systematic review was completed in accordance with PRISMA (Preferred Reporting Items for Systematic Review and Meta-analysis) guidelines [12].

2.1. Literature search

Database PubMed was searched through from January 2023 to March 2023. There was no limit to publication date. Key terms (and MeSH terms) used for the literature research were “gastrointestinal diseases”, “gastrointestinal tract”, “gastrointestinal problems,” gastrointestinal symptoms, “gastrointestinal distress”, “gastrointestinal complaints”, “gastrointestinal absorption”, “gastrointestinal microbiome”, “exercise”, “carbohydrates”, “nutrition” for English language articles on randomized controlled trials, crossover trials, clinical trials, and case studies. The reference lists of the articles obtained were searched manually to obtain additional studies that were not electronically identified.

2.2. Selection criteria

Studies that met the following criteria were included in this systematic review:

(1) they contain accurate information regarding the type and intensity of exercise during study;

(2) provide detailed explanation of planned intervention, dose/exposure;

(3) provide relevant details regarding reporting of GI symptoms and statistical data;

(4) report the details of participants included in the study.

Studies were excluded if they presented results from a previous publication (duplicated data). Two researchers independently assessed studies for inclusion. Potential studies that could be included based on their abstract were retrieved in full-text and reviewed according to our inclusion criteria. Based on the search and inclusion criteria, 31 studies were selected for inclusion in this systematic review (Figure 1).

Figure 1.

Flow diagram of study selection.

2.3. Risk of bias assessment

Quality assessment of included studies was conducted using the Cochrane Collaboration’s risk-of-bias (RoB 2) tool. This was performed independently and in duplicate by two reviewers by referring to the criteria for evaluating risk of bias.

3. Results

In the following tables, brief summaries and details of the studies included in this systematic review are provided.

Table 1 Summarizes the studies examining gut-training protocols.

Table 1.

Characteristics of the studies examining gut-training protocols.

References	No. of subjects	Characteristics of subjects	Exercise type	Type of exercise	Type of intervention	Data collection	Results
Lambert et al., [13]	n = 7	Trained male and female runners	Running	Six 90-min runs (65% VO2max; separated by 7–11 days).	Ingestion of lemon-lime flavored GLU-electrolyte solution (GES) containing 40 g/L (4%; 222 mM) GLU, 20 mEq/L sodium, and 3 mEq/L potassium (osmolality ~275–280 mOsm/every 10 minutes matched to participants sweat rate determined in first run.	GI symptoms-visual analogue scale	Stomach comfort significantly improved (ρ = 0.04) during runs 5 and 6, compared to run 2. GI symptoms did not differ amongst trials.
Costa, Miall, et al., [14]	n = 25	Recreationally competitive male and female runners	Running	Gut-challenge trial (GC) 1–2 h running at 60% VO2max +1 h distance test. 10 days over two weeks performing 1 h running exercise (60 % VO2max) Gut-challenge trial 2–2 h running at 60% VO2max +1 h distance test.	Two weeks gut-training protocol- ingesting 90 g per hour of CHO during running, CHO gel group (CHO-S) (2:1 GLU-FRU, CHO: 30 g), placebo group (PLA) or CHO whole food supplement group (CHO-F) (1:1 GLU-FRU ratio, CHO 30 g, protein: 4 g, fat: 4 g)	Self-reported GI symptom assessment tool, 10-point Likert-type rating scale	GI symptoms reduced in GC2 on CHO-S (60%; ρ = 0.008) and CHO-F (63%; p = 0.046), more than in placebo (ρ < 0.05). H2 peak lower in GC2 on CHO-S compared with CHO-F.
Miall et al., [15]	n = 18	Recreationally competitive male runners	Running	Gut-challenge trial 1–120 min at 60% VO2max +60 min distance test Two weeks daily 1-hour at 60% VO2max Gut-challenge trial 1–120 min at 60% VO2max +60 min distance test	Two weeks gut-training protocol, ingesting 90 g per hour of CHO (2:1 GLU-FRU) with water during running (10% w/v; 316 mOsmol kg − 1) at 0, 20 and 40 minutes.	10-point Likert-type rating scale	Significant reductions in gut discomfort on CHO (ρ < 0.001), no improvements observed in PLA. Lower H2 in GC2 compared with GC1 on CHO, but not on PLA.
King et al., [16] Study 1	n = 19	Elite male race walkers	Race walking	Pre intervention trial 14-day intervention- four long walks (25 km), two interval training sessions and two tempo hill sessions Post intervention trial	Pre intervention trial: Group moderate CHO (CON) or MAX group. CON group daily CHO intake (6.5 g kg BM−1 day−1), MAX group (10 g kg BM−1 day−1). Postintervention trial: 3-day of CHO loading, CON group CHO intake 8 g kg BM−1day−1, MAX group CHO intake 12 g kg BM−1 day−1	Modified visual analogue scale	GI symptoms were greater in post-intervention trial compared to pre-intervention at 13, 19 km, and post exercise (all ρ < 0.01). No differences between trials were evident in CON for GIS (ρ > 0.05)
King et al., [16] Study 2	n = 18	Elite male and female runners	Running	Pre intervention trial 35 km run +7 km time trial Twice-weekly long runs, high intensity running, recovery run, and gym sessions. Post intervention trial 35 km run +7 km time trial	Pre intervention trial 3 days of 8 g kg BM−1 day−1 During 14-day intervention CON group CHO intake 7 g kg BM−1 day−1 , MAX group CHO intake 10 g kg BM−1 day−1. During exercise CON group 30 g per h of CHO drink (2:1 GLU-FRU), MAX group 60–90 g per h CHO drink Pre post intervention trial CON group 3 days CHO intake of 8 g kg BM−1 day−1 , MAX group 3 days CHO intake of 12 g kg BM−1 day−1	Modified visual analogue scale	Total-GI symptoms increased (ρ = 0.002), magnitude of increase was similar between trials (ρ = 0.386) and dietary groups (ρ = 0.068). CON group greater magnitude of upper-GI symptoms compared to MAX (ρ = 0.034). Post intervention trial no difference for lower GI symptoms or peak GI symptoms between dietary groups (ρ > 0.002)

GES: flavored glucose-electrolyte solution, GLU: glucose, FRU: fructose, MAL: maltodextrin, PLA: placebo, VO_2max : maximal oxygen consumption, CHO: carbohydrate, GC: gut challenge trial.

Table 2 Summarizes the studies investigating the impact of various CHO forms and the ratios of multiple CHO forms on GI symptoms.

Table 2.

Characteristics of the studies examining various CHO forms and the ratios of multiple CHO.

References	No. of subjects	Characteristics of subjects	Exercise type	Exercise intensity?	Type of intervention	Data collection	Results
Wilson & Ingraham, [17]	n = 20	Recreational male and female endurance runners	Running	Two 120-min submaximal runs followed by a 4-mile time trial (TT).	Consumption of GLU-only or 10.3 % CHO mixture of GLU-FRU (1.2:1 ratio) beverages supplying 1.3 g/min of CHO.	7-point scale from the validated GI symptom Rating scale	Submaximal run belching/ regurgitation/reflux, bloating/fullness, and gas/flatulence were likely lower with GF (Cohen’s ranging from −0.37 to − 0.45), Similar pattern emerged during TT; however, effect sizes were smaller.
Sareban et al., [18]	n = 9	Well trained triathletes	Triathlon	Two simulated long-distance triathlons-race.	Receiving 67.2 ± 7.2 g · h−1 from GEL (2:1 GLU-FRU ratio) and receiving 67.8 ± 4.2 g · h−1 of CHO (2:1 GLU-FRU ratio) from LIQ	Questionnaire asking for common GI symptoms at the end of the trial.	7 of the 9 participants reported GI symptoms in GEL condition. No GI symptoms in the LIQ condition. The difference in the incidence of GI symptoms between conditions was significant (ρ = .016).
Rowlands & Houltham, [19]	n = 74	Well trained triathletes	Triathlon	Two half-ironman triathlon races.	Comparison of ingesting GLU only or GLU/FRU (2:1 ratio) providing 1.4 g of CHO per min. CHO in both groups were provided in mix of solid bar, GEL, LIQ form.	Post-race 0–100 Likert scale for assessing gut comfort and nausea during each leg of the triathlon.	Possibly lowered nausea during the swim and bike with GLU/FRU compared to GLU, otherwise no differences found.
Murray et al., [20]	n = 12	Healthy adults	Cycling	Three sessions of 115 min intermittent cycle ergometer exercise at 65–80% of VO2max, followed by time trial of 600 pedal revolutions.	Comparing responses to ingestion of 6% GLU, 6% FRU, and 6% SUC solutions. 1.27 ± 0.072 L of fluid each session, providing 76.3 + 4.3 g of CHO.	9-point Likert index assessing GI comfort during and after exercise.	Increased rating of stomach upset with FRU ingestion than GLU or SUC (ρ < 0.05).
Pfeiffer et al., [21]	Study 1: n = 34 Study 2: n = 48	Recreational runners and triathletes	Running	Two 16-km outdoor-runs.	Study 1: GLU+FRU gel (1 g/min) or high dose GLU+FRU gel (1.4 g/min). Study 2: GLU gel (1.4 g/min) or GLU+FRU gel (1.4 g/min)	Questionnaire about GI symptoms using 10-point scale, after exercise.	Mean scores for upper abdominal, lower abdominal and systemic symptoms were not significantly different.
Burke et al., [22]	n = 18	Highly trained runners	Running	Two half marathons	Consumption of 426 ± 227 mL flavored placebo or 386 ± 185 mL water with GEL supplying 1.1 ± 0.2 g/kg body mass CHO at two feed zones (7 km and 14 km)	Post-race questionnaire	Three runners experiencing GI symptoms in the GEL trial. GI symptoms were related to slower finishing time (ρ = 0.04).
D. Baur et al., [23]	n = 10	Trained cyclists and triathletes	Cycling	Three experimental trials, (3 h) 1 h at 50% Wmax, 8 × 2-min intervals at 80% Wmax, and 10 maximal sprints.	Hydrothermally modified starch supplement (HMS). Trial 1: 10% G 30 min before exercise, 7.5% G every 15 min during exercise (Iso HMS) Trial 2: 10% HMS consumed 30 min before exercise, 7.5% HMS every 15 min during exercise. Trial 3: 10 % HMS consumed 30 min before exercise and 15 % HMS every 60 min (and after sprint two) (low HMS)	100-mm Likert scale for the assessment of GI distress.	Clear differences for mean ratings of nausea during repeated sprints with HMS (Iso and Low) vs. G (31.2 ± 26.8 (Iso) and 31.9 ± 27.2 (Low) vs 14.0 ± 18.9; ES = 0.83; 0.86. Mean ratings of abdominal cramp (14.3 ± 14.9 vs. 9.4 ± 6.9) were increased (ES = 0.65) with Low HMS vs G during repeated sprints.
Guillochon & Rowlands, [24]	n = 12	Trained cyclists and triathletes	Cycling	4 trials, 140-min variable-intensity simulated road cycling race, followed by a double-blind slow-ramp to exhaustion (0.333 W s−1)	Effects of drink, gel, bar or mixed CHO formats (ingestion every 20 min, 80 g CHO h−1, 2:1 MD- FRU ratio)	Visual analogue scale, ratings were recorder every 20 min and after exercise.	Nausea with bar was certainly higher relative to GEL and likely higher relative to drink (standardized mean increase with Bar: 99.9% and 96.2%, respectively; < 0.01% chance decrease) Stomach fullness was very likely higher with Bar vs. Gel (99.5%; < 0.01% chance decrease), and likely higher vs. Drink (93.8%; < 0.01% chance decrease). Other contrasts were likely small (Mix-Gel) or non-significant.
van Nieuwenhoven et al., [25]	n = 98	Recreationally competitive runners and triathletes males and females	Running	Three times 18-km competitive run	Effects of ingesting non-carbonated mineral water (WAT), carbohydrate-electrolyte solution (CES) 68.8 g of CHO/L (saccharose + MD), or a CES containing 150 mg/l caffeine (CAF).	Questionnaire using 10 points scale, assessment after exercise.	Majority of the subjects reported 1 or more GI complaints during the runs (WAT: 78.5%, CES: 89.8%, CAF 88.8%) CHO sports drinks lead to higher incidences of all types of GI symptoms compared to water, intensities amongst conditions were similar.
O’Brien & Rowlands, [26]	n = 10	Trained cyclists and triathletes	Cycling	Four experimental trials of 150 min cycling at 50% Wmax followed by an incremental test to exhaustion	Effects of different FRU-MD ratios (0.5, 0.8, 1,25 ratio) at 1.8 g/min.	GI markers on linear scale from 0 to 10 during exercise.	Nausea rated less than slight in all conditions, trivial overall differences between conditions. Stomach fulness overall likely small increase (0.5 ± 0.2 scale units) with the 0.5-Ratio, relative to 0.8-Ratio. Abdominal cramping low in all conditions, likely/very likely trivial differences between conditions.
Jentjens et al., [27]	n = 9	Trained cyclists	Cycling	Four experimental trials of 150 min cycling at 50% Wmax	Effects of different solutions providing either 1.2 g/min of GLU, 1.2 g/min of GLU +0.6 g/min of SUC, 1.2 g/min of GLU +0.6 g/min of MAL or water.	Questionnaire using 10 points scale, assessment during exercise.	More subjects reported severe GI discomfort (stomach problems, bloated feeling, and urge to vomit) in the GLU and GLU + MAL trials compared with the GLU + SUC trial.
Jentjens et al., [28]	n = 8	Trained cyclists	Cycling	Four experimental trials of 120 min cycling at 50% Wmax.	Effects of different solutions providing either 1.2 g/min of GLU, 1.8 g/min of GLU, 0.6 g/min of FRU +1.2 g/min of GLU or water.	Questionnaire using 10 points scale, assessment during exercise.	More subjects reported severe GI discomfort (bloated feeling, urge to vomit) in the high – GLU trial compared with other conditions.

GLU: glucose, FRU: fructose, MD: maltodextrin, SUC: sucrose, MAL: maltose, PLA: placebo, VO_2max : maximal oxygen consumption, CHO: carbohydrate, LIQ: liquid, HMS: Hydrothermally modified starch supplement.

Table 3 Summarizes the studies exploring the effects of a low-FODMAP diet approach.

Table 3.

Characteristics of the studies examining low FODMAP diet.

References	No. of subjects	Characteristics of subjects	Exercise type	Exercise intensity?	Type of intervention	Data collection	Results
Gaskell & Costa, [29]	n = 1	Female ultra endurance runner	Running	Mountainous multi-stage ultramarathon (MSUM)	Effects of low-FODMAD diet six days before and during MSUM	100 mm validated visual analogue scale.	During lead-in diet period only bloating and flatulence reported to a modest degree (VAS 30 mm). During MSUM, minor bloating and flatulence (VAS 30 mm), moderate to severe level of nausea during rest and running, peaking on day 4 and 5 (VAS 40–80 mm)
D. Lis et al., [30]	n = 1	Recreational multisport athlete	Multisport	Swim 60 min (Tuesday), cycle 60 min (Wednesday); run intervals 70 min (Friday), cycle 180 min and steady state run (Saturday), run intervals 65 min (Sunday).	Effects of 6 days low-FODMAP diet on running specific GI symptoms and wellbeing.	Daily and during exercise GI symptoms were noted using a scale 0–9.	Improvement in the daily GI symptoms severity score compared to habitual diet (0–4 during habitual diet vs 0 during low FODMAP; no symptoms at all) Improvement in during exercise GI symptom severity scores compared to habitual diet (0–4 habitual diet vs 0: no symptoms during low FODMAP)
Gaskell et al., [31]	n = 18	Well endurance trained runners	Running	2 h running at 60% VO2max in 35° ambient temperature.	Effects of 24-h high FODMAP and low FODMAP diets before exertional-heat stress	Modified visual analogue scale, 10-point rating scale. Symptoms were assessed before, during and after exercise.	Severity of gut discomfort (ρ = 0.028), total (ρ = 0.035), upper (ρ = 0.050) and lower (ρ = 0.030) GI symptoms were higher during running on HFOD vs LFOD Severity of gut discomfort (ρ = 0.056), total (ρ = 0.014), upper (ρ = 0.019) and lower (ρ = 0.006) GI symptoms were higher in response to the trial period, on HFOD vs LFOD.
Wiffin et al., [32]	n = 16	Recreational males and females runners	Running	Habitual training	Effects of 7 days low FODMAP diet or high- FODMAP diet on exercise-related GI symptoms	Adapted version of irritable bowel syndrome-Severity Scoring system (IBS-SSS = questionnaire.	Significant differences between dietary conditions in IBS-SSS scores (ρ = 0.007). Significant reduction in IBS-SSS score with LOW fodmap (ρ = 0.004) Non-significant increase in IBS_SSS score with HIGH fodmap (ρ = 0.08). 69% participants reporting positive effects of low FODMAP, in contrast to 25% on the high FODMAP.
D. M. Lis et al., [9]	n = 11	Recreationally competitive male and female runners	Running	days 1 and 2 light-to moderate intensity, day 3 rest, day 4 5 × 1000 m interval pace (100% of predicted vVO2max), day 5 included 7 km at threshold pace (90% of predicted VO2max), day 6 rest or self-selected exercise.	Effects of 6 days low-FODMAP or high FODMAP diet	GI questionnaire using a 10-point scale. Assessment of daily and during GI symptoms., area under the curve for 6 days (AUC)	Individual AUC response: 82% of participants had a smaller AUC for daily GI symptoms scores during LFOD compared with HFOD (ρ = 0.003). Group AUC lower in LFOD (mean ± SD, 31.4 ± 24.6) compared with HFOD (44.6 ± 33.6). Specific daily GI symptoms reduced during LFOD, flatulence (ρ < 0.001), urge to defecate (ρ = 0.04), loose stool (ρ = 0.03), and diarrhea (ρ = 0.004). Burping during strenuous running sessions significantly higher (ρ = 0.04) during LFOD compared with HFOD.

PLA: placebo, VO_2max : maximal oxygen consumption, CHO: carbohydrate, FODMAP: fermentable oligosaccharides, disaccharides, monosaccharides, and polyols, VAS: visual analogue scale, LFOD: low fodmap diet, HFOD: high fodmap diet.

Table 4 Summarizes the studies on hydrogel CHO products.

Table 4.

Characteristics of the studies examining CHO hydrogel products.

References	No. of subjects	Characteristics of subjects	Exercise type	Exercise intensity?	Type of intervention	Data collection	Results
D. A. Baur et al., [33]	n = 9	Endurance trained cyclists	Cycling	Three experimental trials, 98-min varied intensity cycling protocol, followed by 10 consecutive sprint intervals.	Effects of MD-FRU hydrogel supplementing 78 g hr−1 CHO, ratio 2:1 MD: FRU	100-mm Likert scales were administered during exercise.	GI symptoms increased over time (ρ = 0.05 for all symptoms). From extremely weak (≤10 mm) to weak or mild (≤30 mm). No significant treatment ×time interactions observed for any GI symptoms.
Pettersson et al., [34]	n = 12	Elite cross-country males and females ski athletes	Roller-skiing	120.min submaximal roller skiing and maximal time-trial (2000 m for females, 2400 m for males).	Effects of 18% multiple-transportable CHO-hydrogel solution (1:0.8 MD: FRU) or PLA	GI symptoms scale using rating from 0–20.	No differences observed between trials for any of GI discomfort variables.
Rowe et al., [35]	n = 11	Trained runners	Running	Three experimental trials, 120-min steady state run at 68% VO2max, followed by a 5-km time-trial.	Effects of multiple transportable CHO hydrogel, 90 g h−1, ratio 2:1 GLU: FRU in comparison with standard CHO solution or CHO-free PLA	GI questionnaire with a 10-point scale, during and after exercise.	GI symptom score for the hydrogel and placebo were lower compared with non-hydrogel (ρ = 0.001). Upper GI symptoms significantly greater during non-hydrogel compared with hydrogel (ρ = 0.025) and placebo (ρ = 0.001). Lower GI symptom significantly greater during non-hydrogel compared with hydrogel (ρ = 0.006) and placebo (ρ < 0.001).
Barber et al., [36]	n = 9	Well trained runners	Running	120 min run at 60% VO2peak	Effects of multiple transportable CHO hydrogel, 90 g h−1, MD: FRU	GI Symptoms Rating Scale using a 7-point scale.	Upper, central, and lower GI symptoms ratings increased to a similar extent across time in both trials (time effect, all ρ < 0.01) (treatment effect and time-treatment interaction, all, ρ > 0.07)
Mears et al., [37]	n = 8	Well trained cyclists	Cycling	120 min cycling at 55% Wmax followed by 20 min time trial	Effects of multiple transportable CHO (MD-FRU) drink with addition of sodium alginate, pectin, and sodium chloride	GI symptoms were rated on a scale from 1 to 10, during exercise.	GI symptoms were not different between trials, except stomach fulness higher in CHO-ALG (ρ = 0.020)

GLU: glucose, FRU: fructose, MD: maltodextrin, PLA: placebo, VO_2max : maximal oxygen consumption, CHO: carbohydrate.

Table 5 Summarizes the studies on probiotic supplementation.

Table 5.

Characteristics of the studies examining probiotics supplementation.

References	No. of subjects	Characteristics of subjects	Exercise type	Exercise intensity?	Type of intervention	Data collection	Results
Smarkusz-Zarzecka et al., [38]	n = 70	Recreational long-distance male and female runners	Long distance running	Habitual running training.	Effects of a three-month multi-strain probiotic supplementation: B. lactis W52, Levilactobacillus brevisW63, L. caseiW56, Lactococcus lactisW19, Lc. lactisW58, L. acidophilus 109 W37, B. bifidumW23, Ligi lactobacillus salivariusW24 in a dose of 2.5 CFU/g (1 capsule).	GI symptoms questionnaire containing single and multiple-choice questions during the study period.	Regurgitation of gastric contents, no difference was observed between groups. Diarrhoea, reduction in symptoms occurred in both groups similarly.
West et al., [39]	n = 99	Recreationally competitive female and male cyclists	Cycling	Subjects recorded information on all types of physical activity during the study.	Effect of 11 weeks probiotic supplementation: Lactobacillus fermentum	Subjects recorded symptoms of GI on a daily illness log over the study period.	Two-fold increase in the number and duration of mild (low grade) GI symptoms in supplementation group. No substantial effect of supplementation between groups on moderate and severe GI symptoms.
Pugh et al., [40]	n = 24	Recreational runners	Running	Marathon training and racing	Effect of 4 weeks probiotic supplementation: Lactobacillus acidophilus CUL60, L. acidophilus CUL21, Bifidobacterium bifidum CUL20, and Bifidobacterium animalis subsp. Lactis CUL34	Daily GI symptom questionnaire using a 10-point scale.	Differences between conditions groups were not significant for the first (ρ = 0.722), or second (ρ = 0.205) third of the race, GI symptoms were significantly lower in PRO compared to PLA during the final third of the race (ρ = 0.010). No significant difference between thirds of the race for PRO. For PLA significant difference between thirds of the race (ρ < 0.001).
Schreiber et al., [41]	n = 27	Elite and well-trained cyclists	Cycling	Normal training and competing through the study period	3 months supplementation period	Online questionnaire, assessing GI symptoms prior, during and after training and competitions.	Significantly lower incidence of GI symptoms during training in group E compared with group C (−27 %±47 % vs. 8 %±29 %, ρ = 0.04) Significantly fewer incidences of nausea (−16 %±43 % vs. 71 %±119 %, ρ = 0.01, d = 0.9), belching (−14 %±53 % vs. 62 %±115 %, ρ = 0.04, d = 1) and vomiting (−7 %±30 % vs. 49 %±114 %, ρ = 0.04, d = 0.7) at rest in the E group compared with the C group after supplementation.
Kekkonen et al., [42]	n = 141	Recreational endurance trained runners	Running	Normal training through the study period	3 months supplementation period	Daily diary questionnaire	The mean number of GI symptoms episode, 0.4 LGG group and 0.6 PLA group (ρ = 0.48). Duration of GI symptom episode was 33% shorter in LGG than in PLA (2.9 vs. 4.3 d, ρ = 0.35) 2 wk after marathon no differences between groups for GI symptom episodes. Duration of GI symptom episodes was 57% shorter in LGG group vs PLA (2.9 vs. 4.3 d, ρ = 0.35)

PLA: placebo, LGG: Limosilactobacillus rhamnosus GG, PRO: probiotic.

3.1. Risk of bias

The majority of studies presented an overall low risk of bias (Supplementary table S1). However, some studies did not provide clear details regarding their blinding and randomization processes. In some cases, complete blinding of participants or researchers was challenging, leading to ‘some concerns’ in specific areas such as period and carryover effects, intervention adherence, and outcome measurement. Risk of bias is available in supplementary material.

4. Discussion

In the world of endurance exercise, GI symptoms are a prevalent concern that can significantly impact performance and overall well-being. Our investigation explored the efficacy of various nutritional strategies in mitigating GI symptoms during endurance exercise. Throughout our analysis, we found studies examining gut training protocols and the effects of different CHO types, ratios of multiple transportable CHO, and osmolality on GI comfort. Furthermore, we investigated the potential of low FODMAP diets, hydrogel CHO products, and probiotic supplementation in relation to GI symptoms during exercise, specifically their association with lower incidence, prevalence, or severity of symptoms. Through this comprehensive exploration, we aim to provide valuable insights into optimizing nutritional interventions for minimizing GI symptoms in endurance athletes.

The GI tract is known to be adaptable and responsive to daily diet. Intentionally training the gut by consuming large amounts of food or drink during exercise may enhance the absorption of macronutrients and reduce the severity and frequency of GI symptoms over time [2]. Several studies looked at different gut training protocols and showed promising results. Two weeks of purposeful repetitive intake of CHO during running lowered the severity of GI symptoms and, furthermore, a lowered breath H₂ response was observed in participants indicating a lowered malabsorption of CHO after the gut training protocol [14,15]. Repetitive running sessions with an intentional ingestion of a higher volume of liquid during running produced a gradual improvement in tolerating fluid intake during running through time and a reduction of GI symptoms [13]. In contrast, minor effects on GI status were observed with a gut-training protocol in race walkers and runners, and high intake of CHO in their daily diet and during exercise did not lead to an increase in GI symptoms compared to lower CHO intake [16].The results of these studies suggest that the GI tract can adapt to ingestion of higher amounts of CHO and a higher volume of liquid during exercise in a short period of time. Therefore, athletes should meet the minimum CHO guidelines for training and competition goals, noting that, with practice, increased CHO intake can be tolerated, and may contribute to performance outcomes. On the other hand, the literature provides evidence that exercise can impair intestinal nutrient absorption mechanisms, potentially leading to malabsorption [43,44]. However, for now it is unclear if the mechanisms underlying impaired nutrient absorption are due to intestinal ischemic injury, down-regulated intestinal transporter activity, or a combination of both [45]. It can be hypothesized that regular intake of CHO and fluids during exercise may minimize these adverse effects on the GI tract, and this hypothesis is supported by findings from studies investigating gut training protocols. One mechanism which could contribute to improved GI status after gut training protocols is the increased expression and function of specific CHO transporters SGLT1 and GLUT5 at the brush-border membrane of the intestinal epithelial cells [46]. This could lead to improved CHO absorption and, with that, a reduction in GI symptoms, higher oxidation of exogenous CHO and consequently improved exercise performance of an athlete. We know that transporters SGLT1 and GLUT5 are responsive to the quantity of CHO in the diet [47]. Therefore, for appropriate functional capabilities and maintenance of higher number of transporters on the luminal membrane, it is important that endurance athletes have a high daily intake of CHO in their diet. It was elegantly shown in one study that high daily CHO intake in a diet can influence exogenous CHO oxidation [48]. The study compared cyclists through a 28-day training cycle on a high-CHO diet (8.5 g/kg/bw) and low-CHO diet (5.3 g/kg/bw). The group of cyclists that were on the high-CHO diet showed improved exogenous CHO oxidation at the end of the time trial in comparison with the group that were on the low-CHO diet (ρ < 0.01). However, if athletes regularly consume higher amounts of CHO in their daily diet, SGLT1 and GLUT5 transporters should be present in high quantities at the brush-border membrane of intestinal epithelial cells. Gut training protocols alone are unlikely to influence their number. Instead, these protocols are likely to reduce the incidence and severity of GI symptoms by reducing CHO malabsorption and increasing tolerance to higher CHO intakes during exercise [49].

De Oliveria and others pointed out that the intake of CHO on its own might not be the sole cause of GI symptoms, and they are more likely the result of the combined action of several different factors such as concentration of CHO, type of CHO, osmolality, and acidity of sports beverages, all of which are linked with a higher occurrence of GI symptoms [3]. In the study the effect of consuming CHO in the form of energy bar, gel, liquid, or a mixture of all three forms during intensive cycling was investigated [24]. Intake of CHO in the form of a bar proved to be the worst of all the forms. In comparison with other forms, a CHO bar intake caused higher occurrence of GI symptoms, lowered maximum power and induced an increased feeling of fatigue. They found that perceived GI symptoms of nausea, full stomach and/or abdominal cramps may negatively affect the ability to perform high-intensity exercise. CHO-bars contain a low amount of fats and protein, which could influence the emptying rate from the stomach and slow down the absorption of CHO in the small intestine. Furthermore, it is known that a meal in solid form is digested in the stomach more slowly when compared to a meal in liquid form. CHO oxidation from CHO-bar and the same form of CHO in liquid form (FRU+MAL) were compared, observing a 0.11 g/min difference in CHO oxidation between the CHO-bar and CHO-liquid [50]. Rowlands & Hultman reported negative comments by participants regarding the difficulty of eating CHO bars because of the requirement for chewing, and mouth dryness. There were three comments relating to vomiting following bar ingestion [19]. There was an interesting small correlation observed in this study that faster race times were associated with higher GI discomfort.

Another factor that could lead to higher occurrence of GI symptoms when ingesting CHO in a form of a bar is a limited blood supply to the GI tract during exercise. Average intensity in this study was 70% VO_2max, for which it is known that there is a greatly reduced blood circulation in the GI tract [51]. In a simulated triathlon, a greater proportion of subjects reported the occurrence of GI symptoms when consuming CHO gel, while these symptoms were not detected when consuming CHO in liquid form in a less concentrated CHO solution [18]. In general, symptoms occurred more often when consuming highly concentrated CHO solutions.

It is not only the concentration of CHO solution that impacts GI symptoms, but also the type of sugar. It has long been known that 6% solutions of GLU, SUC and FRU impact GI comfort differently [20].

FRU solution was connected with an increased incidence of GI symptoms, higher ratings of perceived exertion and poorer exercise performance in comparison with GLU and SUC. The reason for greater incidence of GI symptoms with higher doses of FRU ingestion is believed to be related to the absorption mechanisms of FRU in the small intestine [20]. GLU uses active transport to cross the intestinal epithelium whereas FRU is absorbed via facilitated diffusion. Consequently, FRU is absorbed in the proximal intestine at a slower rate than GLU. The slower rate of FRU absorption is therefore considered to be the cause of increased GI symptoms often reported with ingestion of fructose.

GI symptoms during endurance exercise can also occur with the intake of large amounts of only one type of CHO, such as GLU [27,28]. The inhibition of gastric emptying that occurs with high GLU intake could be the cause of bloating and distention. The limitation here is the limited ability of SGLT1 transporters to absorb GLU, which is around 60 g/h [47]. SGLT1 transporters can become saturated with higher GLU intakes, which can cause malabsorption of CHO and osmotic fluid passage into the intestine.

With the ingestion of mixed CHOs, the recruitment of an additional transporter, GLUT5, occurs, through which FRU absorption takes place. As a result, CHO absorption increases and the possibility of CHO malabsorption and GI symptoms decrease [52]. In addition, the presence of GLU may stimulate FRU absorption [53].

O’Brian & Rowlands examined the effects of ingesting different MD-FRU solutions [26]. The obtained evidence shows that the ingestion of a 0.8 ratio solution proved to be better in terms of increasing performance and GI comfort when compared to the 1.25 and 0.5 ratio solutions. Additionally, a relative increase in exogenous CHO oxidation was observed only with the 0.8 ratio solution. It is worth noting that although the ratio of 2:1 of MD:FRU has been suggested and used for some time now, the ratios close to unity have been shown to be superior in this study [54].

A GLU-FRU mixture (1.2:1 ratio) (1.3 g/min) was observed to have a high probability of lowering GI symptoms compared to GLU (1.3 g/min), influence physiological state during prolonged running and time trial efforts and consequently increase exercise performance in runners [17]. On the other hand, no substantial differences were observed between the ingestion of GLU or GLU-FRU based CHO during a triathlon except for a small reduction in perception of nausea during the swimming and cycling stages of the race [19]. Similarly, tolerance of a high intake of mixed GLU-FRU CHO in gel form during running and a low incidence of GI symptoms were reported, with similar results observed with the ingestion of just GLU [21]. In a study of 18 runners, three complained of GI symptoms after consuming CHO in gel form, and this slightly impaired their half-marathon performance [22]. Symptoms appeared mainly in subjects who already had a history of GI symptoms during exercise. These data suggest that there may be an individual predisposition to the occurrence of GI symptoms during exercise.

A study involving cyclists and triathletes looked at how ingestion of slow-absorbing modified starch before and during cycling would affect substrate oxidation, GI comfort, and performance [23]. Hydrothermally modified starch supplement (HMS) was connected with statistically significant higher occurrence and severity of GI symptoms during exercise and led to decrease in performance during cycling exercise in comparison with SUC/GLU supplement. From these results we can conclude that ingestion of highly absorbable CHO is superior, especially for high intensity endurance exercise to minimize the possibility of GI symptoms and improve exogenous CHO oxidation.

Despite the fact that there is a lack of research examining the effect of a low-FODMAP diet on exercise-related GI symptoms, there are some interesting results from conducted studies [29–32,55]. All the studies show an improvement in either incidence or severity or both of GI symptoms when there is a reduction of FODMAP in the diet of the research participants. Care must be taken when an endurance athlete follows a low FODMAP diet, as it can also have negative consequences if it is not systematically designed and adapted to the individual [9]. Moreover, in one of the studies too-low CHO intake and overall negative energy intake was detected in the participants who followed a low FODMAP diet [32]. Sufficient CHO intake is crucial for endurance athletes both for exercise performance and for the athlete’s physical health in general. Many endurance athletes have problems consuming sufficient CHO even when following a normal diet [56]. The strict and restrictive nature of the low FODMAP diet will only exacerbate this symptom in the long term, negating the positive benefits of a reduction in GI symptoms. A reduction in the incidence and severity of GI symptoms during endurance exercise in a hot environment was found with just 24 hours of following a low-FODMAP diet, while the rest of the research mostly adopted a protocol of six or more days of dietary intervention [31]. Therefore, short-term implementation of a low-FODMAP diet would be a better choice than multi-day long-term protocols. By only using a low FODMAP diet just before competitions or only on intensive training days the possible negative consequences, including the risk of reduced energy intake, can be avoided [57]. The literature suggests to identify the nutrient in the athlete that possibly causes GI symptoms and determine at what exercise intensities this occurs [57]. For example, the symptom trigger may be FRU, LAC, or any of the other fermented CHO. As a result, simply reducing the intake of LAC as an example could contribute to a reduction in the incidence of GI symptoms without a strict and restrictive diet.

Contrary to marketing hype, scientific research has so far failed to significantly demonstrate the benefits of hydrogel CHO products in improving GI symptoms, exogenous CHO oxidation, or exercise performance compared to consuming conventional CHO during exercise [33–35,36, 37, 58]. However, at this point it should be noted that the scientific literature in this field so far is only comprised of a small number of conducted studies. The advantage of consuming CHO in the form of a hydrogel could be shown only when introducing larger amounts of CHO ( < 90 g/h) during long-term exercise of relatively high intensity. A possible reason for the unsuccessful results in some studies could be insufficient exercise intensity where CHO hydrogel could possibly be effective [33,36,37]. To date, only one study has demonstrated a statistically significant improvement in exercise performance with the consumption of CHO in hydrogel form compared to the conventional form [35]. Additionally, this study reported increased oxidation of exogenous CHO and a reduction in GI symptoms relative to standard CHO consumption. There could be several possible reasons for the discrepancy in the results with the rest of the research: higher exercise intensity (running at 68% VO_2max), exercise duration, type and dose of CHO, and training status of the subjects. An additional differentiating factor from other studies was the use of a mixture of GLU and FRU, while others used mixture of MD and FRU. Petterson and others obtained interesting results in their experiment with cross country skiers and high intake of CHO-hydrogel [34]. Despite a very high intake (2.2 g/min) of a highly concentrated (18%) mixture of MAL and FRU in the form of CHO-hydrogel, cross-country skiers reported no serious GI symptoms during cross-country skiing. A contributing factor could be the cold environment in which the research was conducted. In a cold environment, the incidence and severity of GI symptoms are reduced compared to hot conditions [59]. Another contributing factor could be the superior physical fitness of the research participants. Typically, highly trained endurance athletes are already adapted to consuming larger amounts of CHO during exercise and experience fewer symptoms than recreational athletes or those not familiar with a higher intake of CHO. However, if the hydrogel form is the cause of the successful high intake of CHO, this could have great implications for the future of consuming CHO in larger quantities during endurance exercise. Current guidelines recommend an intake of up to 90 g/h of CHO mixture during endurance exercise longer than two hours [1]. Many endurance athletes do not meet these guidelines. It is known that a proportion of athletes experience GI symptoms with such high CHO intake and avoid it if possible. At this point, further research with appropriately designed protocols and higher exercise intensities is warranted to critically assess any potential benefits of high CHO hydrogel intake during endurance exercise.

Another area of research that lacks literature is the effect of probiotic supplementation on exercise-related GI symptoms. A significantly lower incidence of GI symptoms during training was demonstrated in the experimental group that consumed a multi-strain probiotic supplement [41]. Significantly fewer incidences of nausea, belching and vomiting was noticed in the experimental group, and this decrease was more pronounced as exercise intensity increased. Moreover, significant differences in the subjective response to exercise before reaching fatigue were observed, with the experimental group reporting lower RPE values during the time-to-fatigue test. The authors stated that this may be related to changes in GI symptoms and/or immune system function [41]. A two-fold increase in the number and duration of mild (low grade) GI symptoms was observed in the supplementation group using a strain of Lactobacillus fermentum [39]. A potential reason for the increase in number and duration of mild GI symptoms could be remodeling of the microbiome in the GI tract as a response to probiotic supplementation. Using a self-reported severity score for GI symptoms, probiotic supplementation was associated with a reduction in symptoms at higher training loads in male participants, but this effect was not noticed in female participants. In another study involving recreational long-distance runners, a multi-strain probiotic supplement did not significantly impact GI symptoms, except for a notable reduction in the incidence of constipation [38]. However, a high percentage of participants reported subjective improvement in their general health after 3-month supplementation period and this can have an effect on sustaining high training load in athletes. On the other hand, another study noted a significantly shorter duration of GI symptom episodes with probiotic supplementation in comparison with placebo, however, no influence on the incidence of GI symptoms were observed [42]. Moreover, another study reports that runners in a probiotic supplementation group experienced significantly fewer GI symptoms in comparison with a placebo group both in training and in a marathon race when using standardized, recommended CHO loading and in-race CHO and hydration strategies [40]. Runners supplementing with probiotics were able to maintain their running speed better in a marathon race, possibly due to the attenuation of GI symptoms leading to less of a performance decrement toward the end of the race. One reason could be that maintaining the integrity of GI tract wall helps to sustain adequate absorption and oxidation of exogenous CHO throughout the marathon race [60]. The exact mechanisms of action of probiotics have not yet been determined. The literature suggests that chronic supplementation with probiotics in endurance athletes could reduce the incidence and severity of GI symptoms by maintaining the stability of tight junctions in enterocytes and maintaining intestinal impermeability. Further research is warranted to discover any mechanisms through which probiotics could prevent the onset of GI symptoms [60].

Conducting scientific research in the field of GI symptoms during exercise comes with some limitations. Symptoms of GI dysfunction are highly individual, and a variety of different factors influence their occurrence. Consequently, it is very difficult to conduct standardized research studies to obtain accurate and reliable data outcomes. One limitation is that there is no consistency in the definition of what constitutes a severe or non-severe GI symptom. In addition, studies use different questionnaires and approaches for evaluating GI symptoms which creates additional confusion. For these reasons we have also included case studies in this systematic review. In addition, we have focused on potential nutritional interventions applicable to a broad population of endurance athletes. While we acknowledge that there are other potential nutritional interventions for minimizing the occurrence and severity of GI symptoms during endurance exercise, such as gluten and dairy avoidance, this was not within the scope of this paper. These interventions are usually relevant for individuals with specific medical conditions or sensitivities, such as gluten or lactose intolerance.

In conclusion, gut training protocols, involving the regular intake of CHO and fluids during training, show promise in enhancing nutrient absorption and reducing GI discomfort over time. Studies indicate that higher CHO intake, both during daily diet and exercise, can be well-tolerated and may contribute to improved performance through increased CHO absorption and oxidation during exercise. Different CHO forms and mixtures, such as GLU-FRU combinations, appear more effective in minimizing GI symptoms when compared to single CHO types at high intake levels. The form of CHO intake is also crucial, with liquid forms generally causing fewer unfavorable GI symptoms than solid forms like CHO bars. A low FODMAP diet shows potential to reduce GI symptoms but it requires careful implementation to avoid negative consequences such as reduced energy intake. Instead of strictly following a low FODMAP diet, we recommend identifying and excluding specific nutrients from the FODMAP group that may be causing symptoms. Hydrogel CHO products, despite limited supporting evidence, may offer benefits at higher exercise intensities and high CHO intake levels, however for now we remain highly skeptical of their effects. Probiotic supplementation shows a small potential to reduce the incidence and severity of GI symptoms, probably through maintaining intestinal integrity and perhaps improving immune function. However, this area is currently under-researched, and much more investigation is needed to fully understand the mechanisms and efficacy of different types of probiotics in endurance athletes.

Funding Statement

The study was supported by the Slovenian Research and Innovation Agency (ARIS) Research Programme P5–0443 (Javna agencija za znanstvenoraziskovalno in inovacijsko dejavnost Republike Slovenije (ARIS) [P5–0443]).

Disclosure statement

No potential conflict of interest was reported by the author(s).