Carbohydrate and protein intake during exertional heat stress ameliorates intestinal epithelial injury and small intestine permeability

Snipe, Rhiannon M.J.; Khoo, Anthony; Kitic, Cecilia M.; Gibson, Peter R.; Costa, Ricardo J.S.

doi:10.1139/apnm-2017-0361

Cited by 117Thermoregulation and physiological responsesExercise and Physiological ResponsesMuscle metabolism and nutrition

Carbohydrate and protein intake during exertional heat stress ameliorates intestinal epithelial injury and small intestine permeability

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Snipe, Rhiannon M.J., Khoo, Anthony, Kitic, Cecilia M., Gibson, Peter R., Costa, Ricardo J.S.·2017·Applied Physiology Nutrition and Metabolism

DOI 10.1139/apnm-2017-0361

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Abstract

Exertional heat stress (EHS) disturbs the integrity of the gastrointestinal tract leading to endotoxaemia and cytokinaemia, which have symptomatic and health implications. This study aimed to determine the effects of carbohydrate and protein intake during EHS on gastrointestinal integrity, symptoms, and systemic responses. Eleven (male, n = 6; female, n = 5) endurance runners completed 2 h of running at 60% maximal oxygen uptake in 35 °C ambient temperature on 3 occasions in randomised order, consuming water (WATER), 15 g glucose (GLUC), or energy-matched whey protein hydrolysate (WPH) before and every 20 min during EHS. Rectal temperature and gastrointestinal symptoms were recorded every 10 min during EHS. Blood was collected pre- and post-EHS, and during recovery to determine plasma concentrations of intestinal fatty-acid binding protein (I-FABP) as a marker of intestinal epithelial injury, cortisol, endotoxin, and inflammatory cytokines. Urinary lactulose/l-rhamnose ratio was used to measure small intestine permeability. Compared with WATER, GLUC, and WPH ameliorated EHS associated intestinal epithelial injury (I-FABP: 897 ± 478 pg·mL−1 vs. 123 ± 197 pg·mL−1 and 82 ± 156 pg·mL−1, respectively, p < 0.001) and small intestine permeability (lactulose/l-rhamnose ratio: 0.034 ± 0.014 vs. 0.017 ± 0.005 and 0.008 ± 0.002, respectively, p = 0.001). Endotoxaemia was observed post-EHS in all trials (10.2 pg·mL−1, p = 0.001). Post-EHS anti-endotoxin antibodies were higher (p < 0.01) and cortisol and interleukin-6 lower (p < 0.05) on GLUC than WATER only. Total and upper gastrointestinal symptoms were greater on WPH, compared with GLUC and WATER (p < 0.05), in response to EHS. In conclusion, carbohydrate and protein intake during EHS ameliorates intestinal injury and permeability. Carbohydrate also supports endotoxin clearance and reduces stress markers, while protein appears to increase gastrointestinal symptoms, suggesting that carbohydrate is a more appropriate option.

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CHO intake reduces gut damage.
“CHO intake reduces gut damage (Snipe et al., 2017)”
From Contemporary Nutrition Strategies to Optimize Performance in Distance Runners and Race Walkers (2019) · cites this paper as Snipe et al., 2017

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Snipe, R., Kitic, C., Gibson, P., and Costa, R.J.S. 2016. Heat stress during prolonged running results in exacerbated intetsinal epithelial injury and gastrointestinal symptoms. In Proceedings of the Research to Prcatice 2016 Conference, Melbourne Convention and Exhibition Centre, 14-16 April 2016. Edited by Exercise & Sports Science Australia, Qld, Australia. pp. 168.

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Costa, R. J. S., Camões‐Costa, V., Snipe, R. M. J., Dixon, D. J., Russo, I., & Huschtscha, Z. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01032.2018 · Cited by 85 · see citing works
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Considerations for ultra-endurance activities: part 1- nutrition
Costa, R. J. S., Hoffman, M. D., & Stellingwerff, T. (2019) · Research in Sports Medicine · doi:10.1080/15438627.2018.1502188 · Cited by 83 · see citing works
Considerations for ultra-endurance activities: part 2 – hydration
Hoffman, M. D., Stellingwerff, T., & Costa, R. J. S. (2018) · Research in Sports Medicine · doi:10.1080/15438627.2018.1502189 · Cited by 83 · see citing works
The Effects of Exercise on Indirect Markers of Gut Damage and Permeability: A Systematic Review and Meta-analysis
Chantler, S., Griffiths, A., Matu, J., Davison, G., Jones, B. L., & Deighton, K. (2020) · Sports Medicine · doi:10.1007/s40279-020-01348-y · Cited by 80 · see citing works
The Gastrointestinal Exertional Heat Stroke Paradigm: Pathophysiology, Assessment, Severity, Aetiology and Nutritional Countermeasures
Ogden, H. B., Child, R. B., Fallowfield, J. L., Delves, S. K., Westwood, C. S., & Layden, J. D. (2020) · Nutrients · doi:10.3390/nu12020537 · Cited by 76 · see citing works
Impact of 24-h high and low fermentable oligo-, di-, monosaccharide, and polyol diets on markers of exercise-induced gastrointestinal syndrome in response to exertional heat stress
Gaskell, S. K., Taylor, B., Muir, J. G., & Costa, R. J. S. (2019) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2019-0187 · Cited by 70 · see citing works
Does the temperature of water ingested during exertional-heat stress influence gastrointestinal injury, symptoms, and systemic inflammatory profile?
Snipe, R. M. J., & Costa, R. J. S. (2018) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2017.12.014 · Cited by 58 · see citing works
Self-citation
Betaine Supplementation May Improve Heat Tolerance: Potential Mechanisms in Humans
Willingham, B. D., Ragland, T. J., & Ormsbee, M. J. (2020) · Nutrients · doi:10.3390/nu12102939 · Cited by 59 · see citing works
Assessment of Exercise-Associated Gastrointestinal Perturbations in Research and Practical Settings: Methodological Concerns and Recommendations for Best Practice
Costa, R. J. S., Young, P., Gill, S. K., Snipe, R. M. J., Gaskell, S. K., Russo, I., & Burke, L. M. (2022) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2022-0048 · Cited by 56 · see citing works
Self-citation
Gastrointestinal Assessment and Therapeutic Intervention for the Management of Exercise-Associated Gastrointestinal Symptoms: A Case Series Translational and Professional Practice Approach
Gaskell, S. K., Rauch, C., & Costa, R. J. S. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.719142 · Cited by 51 · see citing works
Fucoidans and Bowel Health
Yang, J., & Lim, S. (2021) · Marine Drugs · doi:10.3390/md19080436 · Cited by 50 · see citing works
Exit Gluten-Free and Enter Low FODMAPs: A Novel Dietary Strategy to Reduce Gastrointestinal Symptoms in Athletes
Lis, D. M. (2019) · Sports Medicine · doi:10.1007/s40279-018-01034-0 · Cited by 45 · see citing works
Dietary restrictions in endurance runners to mitigate exercise-induced gastrointestinal symptoms
Parnell, J. A., Wagner–Jones, K., Madden, R. F., & Erdman, K. A. (2020) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-020-00361-w · Cited by 42 · see citing works
Diurnal versus Nocturnal Exercise—Effect on the Gastrointestinal Tract
Gaskell, S. K., Rauch, C., Parr, A., & Costa, R. J. S. (2020) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002546 · Cited by 42 · see citing works
Gastrointestinal pathophysiology during endurance exercise: endocrine, microbiome, and nutritional influences
Smith, K. A., Pugh, J. N., Duca, F. A., Close, G. L., & Ormsbee, M. J. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-021-04737-x · Cited by 41 · see citing works
Perceptions of heat-health impacts and the effects of knowledge and preventive actions by outdoor workers in Hanoi, Vietnam
Lohrey, S., Chua, M., Gros, C., Faucet, J., & LEE, J. K. W. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.148260 · Cited by 40 · see citing works
Assessing Overall Exercise Recovery Processes Using Carbohydrate and Carbohydrate-Protein Containing Recovery Beverages
Russo, I., Gatta, P. D. D., Garnham, A., Porter, J., Burke, L., & Costa, R. J. S. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.628863 · Cited by 35 · see citing works
Sucrose but Not Nitrate Ingestion Reduces Strenuous Cycling–induced Intestinal Injury
Jonvik, K. L., Lenaerts, K., Smeets, J. S. J., Kolkman, J. J., van Loon, L. J. C., & Verdijk, L. B. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001800 · Cited by 36 · see citing works
Effect of prebiotics, probiotics, and synbiotics on gastrointestinal outcomes in healthy adults and active adults at rest and in response to exercise—A systematic literature review
Rauch, C., Mika, A. S., McCubbin, A. J., Huschtscha, Z., & Costa, R. J. S. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.1003620 · Cited by 35 · see citing works
Case Study: Providing Nutritional Support to an Ultraendurance Runner in Preparation for a Self-Sufficient Multistage Ultramarathon: Rationed Versus Full Energy Provisions
Alcock, R., McCubbin, A. J., Camões‐Costa, V., & Costa, R. J. S. (2018) · Wilderness and Environmental Medicine · doi:10.1016/j.wem.2018.06.004 · Cited by 33 · see citing works
Nutritional considerations to counteract gastrointestinal permeability during exertional heat stress
King, M. A., Rollo, I., & Baker, L. B. (2021) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00072.2021 · Cited by 32 · see citing works
Reliability of gastrointestinal barrier integrity and microbial translocation biomarkers at rest and following exertional heat stress
Ogden, H. B., Fallowfield, J. L., Child, R. B., Davison, G., Fleming, S. C., Edinburgh, R. M., Delves, S. K., Millyard, A., Westwood, C. S., & Layden, J. D. (2020) · Physiological Reports · doi:10.14814/phy2.14374 · Cited by 33 · see citing works
Impact of 3-day high and low dietary sodium intake on sodium status in response to exertional-heat stress: a double-blind randomized control trial
McCubbin, A. J., Lopez, M. B., Cox, G. R., Caldwell Odgers, J. N., & Costa, R. J. S. (2019) · European Journal of Applied Physiology · doi:10.1007/s00421-019-04199-2 · Cited by 30 · see citing works
Ad libitum drinking adequately supports hydration during 2 h of running in different ambient temperatures
Hoffman, M. D., Snipe, R. M. J., & Costa, R. J. S. (2018) · European Journal of Applied Physiology · doi:10.1007/s00421-018-3996-7 · Cited by 30 · see citing works
Self-citation
Addition of pectin-alginate to a carbohydrate beverage does not maintain gastrointestinal barrier function during exercise in hot-humid conditions better than carbohydrate ingestion alone
Flood, T. R., Montanari, S., Wicks, M., Blanchard, J., Sharp, H., Taylor, L. K., Kuennen, M. R., & Lee, B. (2020) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2020-0118 · Cited by 31 · see citing works
Impact of exercise duration on gastrointestinal function and symptoms
Gaskell, S. K., Burgell, R., Wiklendt, L., Dinning, P. G., & Costa, R. J. S. (2022) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00393.2022 · Cited by 30 · see citing works
Reliability of pathophysiological markers reflective of exercise-induced gastrointestinal syndrome (EIGS) in response to 2-h high-intensity interval exercise: A comprehensive methodological efficacy exploration
Young, P., Russo, I., Gill, P. A., Muir, J. G., Henry, R., Davidson, Z. E., & Costa, R. J. S. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1063335 · Cited by 29 · see citing works
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
Rauch, C., McCubbin, A. J., Gaskell, S. K., & Costa, R. J. S. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2021.773054 · Cited by 29 · see citing works
Sports Dietitians Australia and Ultra Sports Science Foundation Joint Position Statement: A Practitioner Guide to the Prevention and Management of Exercise-Associated Gastrointestinal Perturbations and Symptoms
Costa, R. J. S., Gaskell, S. K., Henningsen, K., JEACOCKE, N. A., Martinez, I. G., Mika, A. S., Scheer, V., Scrivin, R., Snipe, R. M. J., Wallett, A. M., et al. (2025) · Sports Medicine · doi:10.1007/s40279-025-02186-6 · Cited by 31 · see citing works
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Intestinal Barrier Dysfunction in the Absence of Systemic Inflammation Fails to Exacerbate Motor Dysfunction and Brain Pathology in a Mouse Model of Parkinson's Disease
Jackson, A., Engen, P. A., Forsyth, C. B., Shaikh, M. W., Naqib, A. D., Wilber, S., Frausto, D. M., Raeisi, S., Green, S. J., Bradaric, B. D., et al. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.882628 · Cited by 27 · see citing works
A protocol for an observational cohort study of heat strain and its effect on fetal wellbeing in pregnant farmers in The Gambia
Bonell, A., Hirst, J. E., Vicedo-Cabrera, A. M., Haines, A., Prentice, A. M., & Maxwell, N. (2020) · Wellcome Open Research · doi:10.12688/wellcomeopenres.15731.2 · Cited by 25 · see citing works
A systematic review: Role of dietary supplements on markers of exercise-associated gut damage and permeability
Chantler, S., Griffiths, A., Matu, J., Davison, G., Holliday, A., & Jones, B. L. (2022) · PLoS ONE · doi:10.1371/journal.pone.0266379 · Cited by 30 · see citing works
Gastrointestinal Complaints and Correlations with Self-Reported Macronutrient Intake in Independent Groups of (Ultra)Marathon Runners Competing at Different Distances
Hoogervorst, D., van der Burg, N., Versteegen, J. J., Lambrechtse, K. J., Redegeld, M. I., Cornelissen, L. A. J., & Wardenaar, F. C. (2019) · Sports · doi:10.3390/sports7060140 · Cited by 24 · see citing works
Exercise hyperthermia induces greater changes in gastrointestinal permeability than equivalent passive hyperthermia
Walter, E. J., Watt, P., Gibson, O. R., Willmott, A. G. B., Mitchell, D., Moreton, R., & Maxwell, N. (2021) · Physiological Reports · doi:10.14814/phy2.14945 · Cited by 23 · see citing works
Short-Term Very High Carbohydrate Diet and Gut-Training Have Minor Effects on Gastrointestinal Status and Performance in Highly Trained Endurance Athletes
King, A. J., Etxebarria, N., ROSS, M. L. R., Garvican‐Lewis, L. A., Heikura, I. A., McKay, A. K. A., Tee, N., Forbes, S. F., Beard, N. A., Saunders, P. U., et al. (2022) · Nutrients · doi:10.3390/nu14091929 · Cited by 28 · see citing works
Plasma measurements of the dual sugar test reveal carbohydrate immediately alleviates intestinal permeability caused by exertional heat stress
Houghton, M. J., Snipe, R. M. J., Williamson, G., & Costa, R. J. S. (2023) · The Journal of Physiology · doi:10.1113/jp284536 · Cited by 25 · see citing works
Self-citation
The Effect of Gut-Training and Feeding-Challenge on Markers of Gastrointestinal Status in Response to Endurance Exercise: A Systematic Literature Review
Martinez, I. G., Mika, A. S., Biesiekierski, J. R., & Costa, R. J. S. (2023) · Sports Medicine · doi:10.1007/s40279-023-01841-0 · Cited by 29 · see citing works
Pre-Exercise Carbohydrate or Protein Ingestion Influences Substrate Oxidation but Not Performance or Hunger Compared with Cycling in the Fasted State
Rothschild, J. A., Kilding, A. E., Broome, S. C., Stewart, T. I., Cronin, J. B., & Plews, D. J. (2021) · Nutrients · doi:10.3390/nu13041291 · Cited by 21 · see citing works
Nutrition and Supplementation Considerations to Limit Endotoxemia When Exercising in the Heat
Guy, J. H., & Vincent, G. E. (2018) · Sports · doi:10.3390/sports6010012 · Cited by 21 · see citing works
Carbohydrate Hydrogel Products Do Not Improve Performance or Gastrointestinal Distress During Moderate-Intensity Endurance Exercise
King, A. J., Rowe, J., & Burke, L. M. (2020) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2020-0102 · Cited by 20 · see citing works
An exploratory study of the management strategies reported by endurance athletes with exercise-associated gastrointestinal symptoms
Scrivin, R., Costa, R. J. S., Pelly, F. E., Lis, D. M., & Slater, G. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.1003445 · Cited by 19 · see citing works
A protocol for an observational cohort study of heat strain and its effect on fetal wellbeing in pregnant farmers in The Gambia
Bonell, A., Hirst, J. E., Vicedo-Cabrera, A. M., Haines, A., Prentice, A. M., & Maxwell, N. (2020) · Wellcome Open Research · doi:10.12688/wellcomeopenres.15731.1 · Cited by 18 · see citing works
The increase in core body temperature in response to exertional-heat stress can predict exercise-induced gastrointestinal syndrome
Henningsen, K., Mika, A. S., Alcock, R., Gaskell, S. K., Parr, A., Rauch, C., Russo, I., Snipe, R. M. J., & Costa, R. J. S. (2023) · Temperature · doi:10.1080/23328940.2023.2213625 · Cited by 18 · see citing works
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Intestinal damage following short-duration exercise at the same relative intensity is similar in temperate and hot environments
Sheahen, B., Fell, J. W., Zadow, E. K., Hartley, T. F., & Kitic, C. M. (2018) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2018-0057 · Cited by 19 · see citing works
High Fermentable Oligosaccharides, Disaccharides, Monosaccharides, and Polyols (FODMAP) Consumption Among Endurance Athletes and Relationship to Gastrointestinal Symptoms
Killian, L. A., Muir, J. G., Barrett, J. S., Burd, N. A., & Lee, S. Y. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.637160 · Cited by 21 · see citing works
Dietary Patterns in Runners with Gastrointestinal Disorders
Erdman, K. A., Jones, K. W., Madden, R. F., Gammack, N., & Parnell, J. A. (2021) · Nutrients · doi:10.3390/nu13020448 · Cited by 17 · see citing works
Amino Acid-Based Beverage Interventions Ameliorate Exercise-Induced Gastrointestinal Syndrome in Response to Exertional-Heat Stress: The Heat Exertion Amino Acid Technology (HEAAT) Study
Costa, R. J. S., Henningsen, K., Gaskell, S. K., Alcock, R., Mika, A. S., Rauch, C., Cheuvront, S. N., Blazy, P., & Kenefick, R. W. (2023) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2023-0025 · Cited by 17 · see citing works
The Impact of a 24-h Low and High Fermentable Oligo- Di- Mono-Saccharides and Polyol (FODMAP) Diet on Plasma Bacterial Profile in Response to Exertional-Heat Stress
Gaskell, S. K., Henningsen, K., Young, P., Gill, P. A., Muir, J. G., Henry, R., & Costa, R. J. S. (2023) · Nutrients · doi:10.3390/nu15153376 · Cited by 17 · see citing works
Potato ingestion is as effective as carbohydrate gels to support prolonged cycling performance
Salvador, A. F., McKenna, C. F., Alamilla, R. A., Cloud, R., Keeble, A. R., Miltko, A., Scaroni, S. E., Beals, J. W., ULANOV, A. V., Dilger, R. N., et al. (2019) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00567.2019 · Cited by 17 · see citing works
The impact of 48 h high carbohydrate diets with high and low FODMAP content on gastrointestinal status and symptoms in response to endurance exercise, and subsequent endurance performance
Scrivin, R., Slater, G., Mika, A. S., Rauch, C., Young, P., Martinez, I. G., & Costa, R. J. S. (2024) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2023-0508 · Cited by 16 · see citing works
Changes in surrogate markers of intestinal epithelial injury and microbial translocation in young and older men during prolonged occupational heat stress in temperate and hot conditions
Lee, B., Flood, T. R., Galán-López, N., McCormick, J. J., King, K. E., Fujii, N., & Kenny, G. P. (2023) · European Journal of Applied Physiology · doi:10.1007/s00421-023-05329-7 · Cited by 15 · see citing works
Markers of enterocyte damage, microbial translocation, and systemic inflammation following 9 h of heat exposure in young and older adults
Lee, B. J., Russell, S. L., Meade, R. D., McCormick, J. J., King, K. E., & Kenny, G. P. (2024) · Applied Physiology Nutrition and Metabolism · doi:10.1139/apnm-2024-0094 · Cited by 15 · see citing works
Systematic literature review: The effect of dairy milk on markers of recovery optimisation in response to endurance exercise
(2019) · Monash University Research Portal (Monash University) · doi:10.5923/j.sports.20190904.01 · Cited by 15 · see citing works
Anthocyanin-Rich Blackcurrant Extract Preserves Gastrointestinal Barrier Permeability and Reduces Enterocyte Damage but Has No Effect on Microbial Translocation and Inflammation After Exertional Heat Stress
Lee, B., Flood, T. R., Hiles, A. M., Walker, E. F., Wheeler, L., Ashdown, K., Willems, M. E. T., Costello, R., Greisler, L. D., Romano, P. A., et al. (2022) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2021-0330 · Cited by 15 · see citing works
Plasma Endogenous Endotoxin Core Antibody Response to Exercise in Endurance Athletes
Young, P., Rauch, C., Russo, I., Gaskell, S. K., Davidson, Z. E., & Costa, R. J. S. (2022) · International Journal of Sports Medicine · doi:10.1055/a-1827-3124 · Cited by 15 · see citing works
Exertional heat stroke: nutritional considerations
LEE, J. K. W., Tan, B., Ogden, H. B., Chapman, S., & Sawka, M. N. (2022) · Experimental Physiology · doi:10.1113/ep090149 · Cited by 14 · see citing works
Dietary Intake and Gastrointestinal Integrity in Runners Undertaking High-Intensity Exercise in the Heat
Etxebarria, N., Beard, N. A., Gleeson, M., Wallett, A. M., MCDONALD, W. A., Pumpa, K. L., & Pyne, D. B. (2021) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2020-0367 · Cited by 13 · see citing works
The Effects of Beverage Intake after Exhaustive Exercise on Organ Damage, Inflammation and Oxidative Stress in Healthy Males
Tominaga, T., Ikemura, T., Yada, K., Kanda, K., Sugama, K., Ma, S., Choi, W., Araya, M., Huang, J., Nakamura, N., et al. (2021) · Antioxidants · doi:10.3390/antiox10060866 · Cited by 12 · see citing works
Sport Supplements and the Athlete’s Gut: A Review
Wilson, P. B. (2021) · International Journal of Sports Medicine · doi:10.1055/a-1704-3086 · Cited by 15 · see citing works
The effects of low and normal dose ice slurry ingestion on endurance capacity and intestinal epithelial injury in the heat
Alhadad, S. B., Chua, M., LEE, J. K. W., & Low, I. C. C. (2023) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2023.04.008 · Cited by 11 · see citing works
How to integrate recovery during heat acclimation
Ihsan, M., Périard, J. D., & Racinais, S. (2020) · British Journal of Sports Medicine · doi:10.1136/bjsports-2020-102390 · Cited by 11 · see citing works
The Effects of Prebiotic Supplementation on Markers of Exercise-Induced Gastrointestinal Syndrome in Response to Exertional Heat Stress
Rauch, C., Henningsen, K., Martinez, I. G., Young, P., Mika, A. S., Huschtscha, Z., McCubbin, A. J., Henry, R., Anderson, D., & Costa, R. J. S. (2025) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2024-0127 · Cited by 10 · see citing works
Acute L‐glutamine supplementation does not improve gastrointestinal permeability, injury or microbial translocation in response to exhaustive high intensity exertional‐heat stress
Ogden, H. B., Fallowfield, J. L., Child, R. B., Davison, G., Fleming, S. C., Delves, S. K., Millyard, A., Westwood, C. S., & Layden, J. D. (2021) · European Journal of Sport Science · doi:10.1080/17461391.2021.2001575 · Cited by 10 · see citing works
Nourishing Physical Productivity and Performance On a Warming Planet - Challenges and Nutritional Strategies to Mitigate Exertional Heat Stress
McCubbin, A. J., Irwin, C. G., & Costa, R. J. S. (2024) · Current Nutrition Reports · doi:10.1007/s13668-024-00554-8 · Cited by 8 · see citing works
The Impact of a Short-Term Ketogenic Low-Carbohydrate High-Fat Diet on Biomarkers of Intestinal Epithelial Integrity and Gastrointestinal Symptoms
McKay, A. K. A., Wallett, A. M., McKune, A. J., Périard, J. D., Saunders, P. U., Whitfield, J., Tee, N., Heikura, I. A., ROSS, M. L. R., Sharma, A. P., et al. (2023) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2023-0009 · Cited by 8 · see citing works
Exertional heat stress promotes the presence of bacterial DNA in plasma: A counterbalanced randomised controlled trial
Henningsen, K., Henry, R., Gaskell, S. K., Alcock, R., Mika, A. S., Rauch, C., Cheuvront, S. N., Blazy, P., Kenefick, R. W., & Costa, R. J. S. (2024) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2024.05.010 · Cited by 8 · see citing works
Author’s Reply to Kitic: Comment on: “Association Between Exercise-Induced Hyperthermia and Intestinal Permeability: A Systematic Review”
Pires, W., Wanner, S. P., Soares, D. D., & Coimbra, C. C. (2018) · Sports Medicine · doi:10.1007/s40279-018-0954-9 · Cited by 8 · see citing works
No protective benefits of low dose acute L-glutamine supplementation on small intestinal permeability, epithelial injury and bacterial translocation biomarkers in response to subclinical exertional-heat stress: A randomized cross-over trial
Ogden, H. B., Fallowfield, J. L., Child, R. B., Davison, G., Fleming, S. C., Delves, S. K., Millyard, A., Westwood, C. S., & Layden, J. D. (2021) · Temperature · doi:10.1080/23328940.2021.2015227 · Cited by 8 · see citing works
The Influence of Dietary Supplements on Exercise-Induced Gut Damage and Gastrointestinal Symptoms: A Systematic Review and Meta-Analysis
Aitkenhead, R., Waldron, M., Conway, G. E., Horner, K. M., & Heffernan, S. M. (2025) · Nutrients · doi:10.3390/nu17030443 · Cited by 7 · see citing works
From Metabolism to Medals: Contemporary Perspectives and Revisiting Carbohydrate Guidelines for Fueling Endurance Athletes during Exercise
Morton, J. P., Fell, J. M., Gonzalez, J. T., Hearris, M. A., Podlogar, T., Pugh, J. N., & Wallis, G. A. (2026) · Journal of Nutrition · doi:10.1016/j.tjnut.2026.101442 · Cited by 9 · see citing works
The effects of collagen peptides on exercise-induced gastrointestinal stress: a randomized, controlled trial
Taylor, G., Leonard, A. N., TANG, J. C. Y., Dunn, R. K., Fraser, W. D., Virgilio, N., Prawitt, J., Stevenson, E., & Clifford, T. (2022) · European Journal of Nutrition · doi:10.1007/s00394-022-03051-2 · Cited by 8 · see citing works
The association between gastrointestinal injury, complaints, and food intake in 60-km ultramarathon runners
van Venrooij, N., Wardenaar, F. C., Hoogervorst, D., Senden, J. M., van Dijk, J., & Jonvik, K. L. (2022) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2021-0711 · Cited by 7 · see citing works
The effect of dietary supplements on core temperature and sweating responses in hot environmental conditions: a meta-analysis and meta-regression
Peel, J., McNarry, M. A., Heffernan, S. M., Nevola, V. R., Kilduff, L. P., & Waldron, M. (2025) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00186.2024 · Cited by 6 · see citing works
Letter: low‐ FODMAP diet for exercise‐induced gastrointestinal syndrome—Authors’ reply
Costa, R. J. S., Snipe, R. M. J., Kitic, C. M., & Gibson, P. R. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.14358 · Cited by 6 · see citing works
Self-citation
Carbohydrate knowledge, beliefs, and intended practices, of endurance athletes who report exercise-associated gastrointestinal symptoms
Scrivin, R., Costa, R. J. S., Pelly, F. E., Lis, D. M., & Slater, G. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1133022 · Cited by 5 · see citing works
Acute or Short-term Effects of Whey Protein Alone or Along with Carbohydrate on Inflammation: A Systematic Review of Clinical Trials
Moazen, M., Babajafari, S., Akbari, A., Abdollahzadeh, S. M., Zahedani, M. R., Sasani, N., & Kazemi, A. (2023) · Galen Medical Journal · doi:10.31661/gmj.v12i.2441 · Cited by 5 · see citing works
A Warm Environment Reduces Exogenous Glucose Oxidation and Endurance Performance during Cycling with Facing Airflow
Reynolds, K. M., Funnell, M. P., Collins, A. J., Mears, S. A., Pugh, J. N., & James, L. J. (2024) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000003632 · Cited by 6 · see citing works
Case Series: Management of Exercise-Associated Gastrointestinal Symptoms in Endurance Athletes Using a High-Carbohydrate Low-FODMAP Therapeutic Intervention
Scrivin, R., Slater, G., & Costa, R. J. S. (2025) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2024-0133 · Cited by 5 · see citing works
Compression Socks Reduce Running-Induced Intestinal Damage
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Dietary Intake and Gastrointestinal Integrity in Runners Undertaking High-Intensity Exercise in the Heat
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Authors: Snipe, R. M. J., Khoo, A., Kitic, C. M., Gibson, P. R., & Costa, R. J. S.
Affiliations: Monash University (AU)
University of Tasmania (AU)
The Alfred Hospital (AU)
ORCID: Snipe, Rhiannon M.J.
Kitic, Cecilia M.
Costa, Ricardo J.S.
Venue: Applied Physiology Nutrition and Metabolism
Publisher: Canadian Science Publishing
Published: 2017-12
Volume: 42
Issue: 12
Pages: 1283-1292
ISSN: 1715-5312 (ISSN-L)
1715-5320
DOI: 10.1139/apnm-2017-0361
OpenAlex: W2743575529
Cited by: 117
References: 69
Citations by year: 2026: 14 · 2025: 15 · 2024: 8 · 2023: 11 · 2022: 15 · 2021: 18 · 2020: 12 · 2019: 12 · 2018: 11 · 2017: 1
FWCI: 7.28
Type: journal article
Language: en
Open access: green
hdl.handle.net
Licence: www.nrcresearchpress.com/page/about/CorporateTextAndDataMining (tdm)
Locations: Applied Physiology, Nutrition, and Metabolism (publishedVersion)
PubMed (publishedVersion)
UTAS Research Repository (acceptedVersion)
TSpace (University of Toronto) (acceptedVersion)
eCite Digital Repository (University of Tasmania) (submittedVersion)
Figshare (submittedVersion, cc-by)
Funders: Monash University (SGS15-0128)
Topics: Health Sciences › Medicine › Physiology › Thermoregulation and physiological responses
Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Keywords: exertional heat stress, carbohydrate intake, whey protein hydrolysate, intestinal epithelial damage, intestinal permeability, endotoxemia, intestinal fatty acid binding protein, gastrointestinal symptoms, endurance running, anti-endotoxin antibodies, interleukin-6, cortisol, heat acclimation, sports nutrition
MeSH terms: Organism Hydration Status, Adult, Blood Glucose, Body Temperature, Dietary Carbohydrates, Dietary Proteins, Female, Gene Expression Regulation, Humans, Hydrocortisone, Intestinal Mucosa, Intestine, Small, Male, Permeability, Running, Exercise, Cytokines

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Carbohydrate and protein intake during exertional heat stress ameliorates intestinal epithelial injury and small intestine permeability

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