Feeding Tolerance to a Running Gut-Challenge Protocol: a Cross-Sectional Exploration

Abstract

This study examined gastrointestinal function, substrate utilization, and exercise performance differences in response to a gut-challenge between (1) female and male athletes, (2) young adult versus masters athletes, and (3) athletes with or without exercise-associated gastrointestinal symptom history (Ex-GIS). Fifty-three endurance athletes (43 males and 10 females) completed a gut-challenge involving a 2-hour run (60% V̇O_2max) with 90 g/h carbohydrate intake, followed by a 1-hour self-paced distance test (DT) with ad libitum water. Blood and breath samples were collected pre- and post-exercise. Blood glucose and substrate utilization during exercise were measured, while Ex-GIS and feeding tolerance were assessed pre-, during, and post-exercise. Interest in food and appetite during exercise was lower in symptomatic athletes than asymptomatic athletes (p<0.05). Females had a higher blood glucose concentration during exercise (p=0.037) and immediately after exercise (p=0.003) and a lower whole-body fat oxidation rate during exercise (p=0.009). Exercise performance did not differ based on the biological sex, age, and Ex-GIS history. Overall, gastrointestinal functional markers were comparable between groups, while feeding tolerance and substrate availability and utilization appear to be influenced by the Ex-GIS history and biological sex, respectively. Tailored management of gastrointestinal issues in athletes should be based on an individual basis as opposed to general demographic characteristics.

Keywords

exercise-induced gastrointestinal syndrome - gastrointestinal symptoms - breath hydrogen - glucose - carbohydrate oxidation - running performance

• References

• 1 Stellingwerff T, Cox GR. Systematic review: Carbohydrate supplementation on exercise performance or capacity of varying durations. Appl Physiol Nutr Metab 2014; 39: 998-1011
• 2 Rauch CE, McCubbin AJ, Gaskell SK. et al. Feeding tolerance, glucose availability, and whole-body total carbohydrate and fat oxidation in male endurance and ultra-endurance runners in response to prolonged exercise, consuming a habitual mixed macronutrient diet and carbohydrate feeding during exercise. Front Physiol 2022; 12: 2217-2217
• 3 Martinez IG, Mika AS, Biesiekierski JR, Costa R. The effect of gut-training and feeding-challenge on markers of gastrointestinal status in response to endurance exercise: A systematic literature review. Sports Med 2023; 53: 1175-1200
• 4 Costa R, Snipe RMJ, Kitic CM, Gibson PR. Systematic review: Exercise-induced gastrointestinal syndrome—implications for health and intestinal disease. Aliment Pharmacol Ther 2017; 46: 246-265
• 5 Ter Steege RWF, Van Der Palen J, Kolkman JJ. Prevalence of gastrointestinal complaints in runners competing in a long-distance run: An internet-based observational study in 1281 subjects. Scand J Gastroenterol 2009; 43: 1477-1482
• 6 Costa R, Young P, Gill SK. et al. Assessment of exercise-associated gastrointestinal perturbations in research and practical settings: Methodological concerns and recommendations for best practice. Int J Sport Nutr Exerc Metab 2022; 32: 387-418
• 7 Costa R, Miall A, Khoo A. et al. Gut-training: The impact of two weeks repetitive gut-challenge during exercise on gastrointestinal status, glucose availability, fuel kinetics, and running performance. Appl Physiol Nutr Metab 2017; 42: 547-557
• 8 Miall A, Khoo A, Rauch C. et al. Two weeks of repetitive gut-challenge reduce exercise-associated gastrointestinal symptoms and malabsorption. Scand J Med Sci Sports 2018; 28: 630-640
• 9 Snipe RMJ, Costa RJS. Does biological sex impact intestinal epithelial injury, small intestine permeability, gastrointestinal symptoms and systemic cytokine profile in response to exertional-heat stress?. J Sports Sci 2018; 36: 2827-2835
• 10 Gaskell SK, Rauch CE, Costa RJS. Gastrointestinal assessment and therapeutic intervention for the management of exercise-associated gastrointestinal symptoms: A case series translational and professional practice approach. Front Physiol 2021; 12: 1-28
• 11 Young P, Henningsen K, Snipe R. et al. Does age influence gastrointestinal status responses to exertional-heat stress?. Int J Sports Med 2024; 45: 272-281
• 12 Bitar K, Greenwood-Van Meerveld B, Saad R, Wiley JW. Aging and gastrointestinal neuromuscular function: Insights from within and outside the gut. Neurogastroenterol Motil 2011; 23: 490-501
• 13 Man AL, Bertelli E, Rentini S. et al. Age-associated modifications of intestinal permeability and innate immunity in human small intestine. Clin Sci 2015; 129: 515-527
• 14 Stuempfle KJ, Hoffman MD. Gastrointestinal distress is common during a 161-km ultramarathon. J Sports Sci 2015; 33: 1814-1821
• 15 Smith ES, McCormick R, McKay AKA. et al. Perceived negative menstrual cycle symptoms, but not changes in estrogen or progesterone, are associated with impaired cycling race performance. Med Sci Sports Exerc 2024; 57: 590-599
• 16 Bruinvels G, Goldsmith E, Blagrove R. et al. Prevalence and frequency of menstrual cycle symptoms are associated with availability to train and compete: A study of 6812 exercising women recruited using the strava exercise app. Br J Sports Med 2021; 55: 438-443
• 17 Teff KL, Alavi A, Chen J, Pourdehnad M, Townsend RR. Muscarinic blockade inhibits gastric emptying of mixed-nutrient meal: Effects of weight and gender. Am J Physiol 1999; 276: R707-R714
• 18 Meier R, Beglinger C, Dederding JP, Meyer-Wyss B. et al. Influence of age, gender, hormonal status and smoking habits on colonic transit time. Neurogastroenterol Motil 1995; 7: 235-238
• 19 Graff J, Brinch K, Madsen JL. Gastrointestinal mean transit times in young and middle-aged healthy subjects. Clin Physiol 2008; 21: 253-259
• 20 Rao SS, Sadeghi P, Beaty J, Kavlock R, Ackerson K. Ambulatory 24-h colonic manometry in healthy humans. Am J Physiol 2001; 280: G629-G639
• 21 Datz FL, Christian PE, Moore J. Gender-related differences in gastric emptying. J Nucl Med 1987; 28: 1204-1207
• 22 Freire AC, Basit AW, Choudhary R, Piong CW, Merchant HA. Does sex matter? The influence of gender on gastrointestinal physiology and drug delivery. Int J Pharm 2011; 415: 15-28
• 23 Kuikman MA, Smith ES, McKay A, Ackerman KE. et al. Fueling the female athlete: Auditing her representation in studies of acute carbohydrate intake for exercise. Med Sci Sports Exerc 2023; 55: 569-580
• 24 Horowitz M, Maddern GJ, Chatterton BE, Collins PJ, Harding PE, Shearman DJ. Changes in gastric emptying rates with age. Clin Sci 1984; 67: 213-218
• 25 O’Donovan D, Hausken T, Lei Y. et al. Effect of aging on transpyloric flow, gastric emptying, and intragastric distribution in healthy humans—impact on glycemia. Dig Dis Sci 2005; 50: 671-676
• 26 Madsen JL, Graff J. Effects of ageing on gastrointestinal motor function. Age Ageing 2004; 33: 154-159
• 27 Madsen JL. Effects of gender, age, and body mass index on gastrointestinal transit times. Dig Dis Sci 1992; 37: 1548-1553
• 28 Alcock R, McCubbin A, Camões-Costa V, Costa R. Case study: Providing nutritional support to an ultraendurance runner in preparation for a self-sufficient multistage ultramarathon: Rationed versus full energy provisions. Wilderness Environ Med 2018; 29: 508-520
• 29 Snipe RMJ, Khoo A, Kitic CM, Gibson PR, Costa R. Carbohydrate and protein intake during exertional heat stress ameliorates intestinal epithelial injury and small intestine permeability. Appl Physiol Nutr Metab 2017; 42: 1283-1292
• 30 Gaskell SK, Snipe RMJ, Costa RJS. Test–retest reliability of a modified visual analog scale assessment tool for determining incidence and severity of gastrointestinal symptoms in response to exercise stress. Int J Sport Nutr Exerc Metab 2019; 29: 411-419
• 31 Smith RE, Smoll FL, Schutz RW. Measurement and correlates of sport-specific cognitive and somatic trait anxiety: The sport anxiety scale. Anxiety Stress Coping 1990; 2: 263-280
• 32 Martinez IG, Houghton MJ, Forte M, Williamson G, Biesiekierski JR, Costa R. Development of a low-fructose carbohydrate gel for exercise application. Heliyon 2024; 10: e33497
• 33 Péronnet F, Massicotte D. Table of nonprotein respiratory quotient: An update. Can J Sport Sci 1991; 16: 23-29
• 34 Martinez IG, Biesiekierski JR, Rauch CE, Costa RJS. Repetitive Feeding-Challenge With Different Nutritional Densities on Markers of Gastrointestinal Function, Substrate Oxidation, and Endurance Exercise Performance. Int J Sport Nutr Exerc Metab 2025;
• 35 Calles-Escandón J, Poehlman ET. Aging, fat oxidation and exercise. Aging Clin Exp Res 1997; 9: 57-63
• 36 Leiper JB. Fate of ingested fluids: Factors affecting gastric emptying and intestinal absorption of beverages in humans. Nutr Rev 2015; 73: 57-72
• 37 Noakes TD, Rehrer NJ, Maughan RJ. The importance of volume in regulating gastric emptying. Med Sci Sports Exerc 1991; 23: 307-313
• 38 Farmer AD, Aziz Q. Gut pain & visceral hypersensitivity. Br J Pain 2013; 7: 39-47
• 39 Gibson PR, Newnham E, Barrett JS, Shepherd SJ, Muir JG. Review article: Fructose malabsorption and the bigger picture. Aliment Pharmacol Ther 2007; 25: 349-363
• 40 Mitsui T, Shimaoka K, Kanao Y, Kondo T. Colonic fermentation after ingestion of fructose-containing sports drink. J Sports Med Phys Fitness 2001; 41: 121-123
• 41 Knowles SR, Apputhurai P, Palsson OS, Bangdiwala S, Sperber AD, Mikocka-Walus A. The epidemiology and psychological comorbidity of disorders of gut–brain interaction in australia: Results from the rome foundation global epidemiology study. Neurogastroenterol Motil 2023; 35: e14594