The increase in core body temperature in response to exertional-heat stress can predict exercise-induced gastrointestinal syndrome

References

• Gaskell SK, Lis DM, Costa RJS. Exercise-Induced Gastrointestinal Syndrome. (Chapter 21. 6th. Burke L, Deakin V, Minehan M., Ed. InSydney, NSW, Australia: Clinical Sports NutritionMcGraw-Hill Education; 2021pp. 551–575
   Google Scholar
• Gill SK, Hankey J, Wright A, et al. The impact of a 24-h ultra-marathon on circulatory endotoxin and cytokine profile. Int J Sports Med. 2015;36(8):688–695. DOI:10.1055/s-0034-1398535
   PubMed Web of Science ®Google Scholar
• Gill SK, Teixeira A, Rama L, et al. Circulatory endotoxin concentration and cytokine profile in response to exertional-heat stress during a multi-stage ultra-marathon competition. Exerc Immunol Rev. 2015;21:114–128.
   PubMed Web of Science ®Google Scholar
• Young P, Russo I, Gill P, et al. Reliability of pathophysiological markers reflective of exercise-induced gastrointestinal syndrome (EIGS) in response to prolonged strenuous exercise: a comprehensive methodological efficacy exploration. Frontiers Physiol. 2023;14. In press, DOI:10.3389/fphys.2023.1063335
   Web of Science ®Google Scholar
• Costa RJS, Snipe RMJ, Kitic CM, et al. Systematic review: exercise-induced gastrointestinal syndrome - implications for health and intestinal disease. Aliment Pharmacol Ther. 2017;46(3):246–265. DOI:10.1111/apt.14157
   PubMed Web of Science ®Google Scholar
• Costa RJS, Gaskell SK, McCubbin AJ, et al. Exertional-heat stress-associated gastrointestinal perturbations during Olympic sports: management strategies for athletes preparing and competing in the 2020 Tokyo Olympic Games. Temperature. 2020;7(1):58–88. DOI:10.1080/23328940.2019.1597676
   Google Scholar
• Molinaro A, Holst O, Di Lorenzo FD, et al. Chemistry of lipid A: at the heart of innate immunity. Chemistry. 2015;21(2):500–519. DOI:10.1002/chem.201403923
   PubMed Web of Science ®Google Scholar
• Pietro A, Mervyn S. Pathophysiology of sepsis. Curr Opin Anaesthesiol. 2021;34(2):77–84. DOI:10.1097/ACO.0000000000000963
   PubMed Web of Science ®Google Scholar
• Laitano O, Leon LR, Roberts WO, et al. Controversies in exertional heat stroke diagnosis, prevention, and treatment. J Appl Physiol. 2019;127(5):1338–1348. DOI:10.1152/japplphysiol.00452.2019
   PubMed Web of Science ®Google Scholar
• Costa RJS, Gill SK, Snipe RMJ, et al. Assessment of exercise-associated gastrointestinal perturbations in research and practical settings: methodological concerns and recommendations for better practice. Int J Sport Nutr Exerc Metab. 2022;32(5):387.418. DOI:10.1123/ijsnem.2022-0048
   Web of Science ®Google Scholar
• Costa RJS, Camões-Costa V, Snipe RMJ, et al. The impact of a dairy milk recovery beverage on bacterially-stimulated neutrophil function and gastrointestinal tolerance in response to hypohydration including exercise stress. Int J Sport Nutr Exerc Metab. 2020;30(4):237–248. DOI:10.1123/ijsnem.2019-0349
   PubMed Web of Science ®Google Scholar
• Costa RJS, Mika AS, McCubbin AJ. The impact of exercise modality on exercise-induced gastrointestinal syndrome and associated gastrointestinal symptoms. J Sci Med Sport. 2022;25(10):788–793. DOI:10.1016/j.jsams.2022.07.003
   PubMed Web of Science ®Google Scholar
• Gaskell SK, Taylor B, Muir J, et al. Impact of 24-h and low fermentable oligo-, di-, monosaccharide, and polyol diets on markers of exercise-induced gastrointestinal syndrome in response to exertional heat stress. Appl Physiol Nutr Metab. 2020;45(6):569–580. DOI:10.1139/apnm-2019-0187
   PubMed Web of Science ®Google Scholar
• Gaskell SK, Rauch CE, Parr A, et al. Diurnal versus nocturnal exercise—effect on the gastrointestinal tract. null. 2021;53(5):1056–1067. DOI:10.1249/MSS.0000000000002546
   Google Scholar
• Russo I, Della Gatta PA, Garnham A, et al. Does the nutritional composition of dairy milk based recovery beverages influence post-exercise gastrointestinal and immune status, and subsequent markers of recovery optimisation in response to high intensity interval exercise? Frontiers Nutr. 2021;7(622270):1–17. DOI:10.3389/fnut.2020.622270
   Google Scholar
• Russo I, Della Gatta PA, Garnham A, et al. Assessing overall exercise recovery processes using carbohydrate and carbohydrate-protein containing recovery beverages. Front Physiol. 2021;12(62863):1–18. DOI:10.3389/fphys.2021.628863
   Google Scholar
• Russo I, Della Gatta PA, Garnham A, et al. The effects of an acute “train-low” nutritional protocol on markers of recovery optimization in endurance-trained male athletes. Int J Sport Physiol. 2021;16(12):1764–1776. DOI:10.1123/ijspp.2020-0847
   PubMed Web of Science ®Google Scholar
• Snipe RMJ, Khoo A, Kitic CM, et al. The impact of exertional-heat stress on gastrointestinal integrity, gastrointestinal symptoms, systemic endotoxin and cytokine profile. Eur J Appl Physiol. 2018;118(2):389–400. DOI:10.1007/s00421-017-3781-z
   PubMed Web of Science ®Google Scholar
• Snipe RMJ, Khoo A, Kitic CM, et al. The impact of mild heat stress during prolonged running on gastrointestinal integrity, gastrointestinal symptoms, systemic endotoxin and cytokine profiles. Int J Sports Med. 2018;39(4):255–263. DOI:10.1055/s-0043-122742
   Web of Science ®Google Scholar
• Snipe RMJ, Costa RJS. Does the temperature of water ingested during exertional-heat stress influence gastrointestinal injury, symptoms, and systemic inflammatory profile? J Sci Med Sport. 2018;21(8):771–776. DOI:10.1016/j.jsams.2017.12.014
   PubMed Web of Science ®Google Scholar
• Pals KL, Chang RT, Ryan AJ, et al. Effect of running intensity on intestinal permeability. J Appl Physiol. 1997;82(2):571–576. DOI:10.1152/jappl.1997.82.2.571
   PubMed Web of Science ®Google Scholar
• Bennett CJ, Henry R, Snipe RMJ, et al. Is the gut microbiota bacterial abundance and composition associated with intestinal epithelial injury, systemic inflammatory profile, and gastrointestinal symptoms in response to exertional-heat stress? J Sci Med Sport. 2020;23(12):1141–1153. DOI:10.1016/j.jsams.2020.06.002
   PubMed Web of Science ®Google Scholar
• Costa RJS, 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(5):547–557. DOI:10.1139/apnm-2016-0453
   PubMed Web of Science ®Google Scholar
• Costa RJS, Camões-Costa V, Snipe RMJ, et al. The impact of exercise-induced hypohydration on intestinal integrity, function, symptoms, and systemic endotoxin and inflammatory responses. J Appl Physiol. 2019;126(5):1281–1291. DOI:10.1152/japplphysiol.01032.2018
   PubMed Web of Science ®Google Scholar
• 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(2):630–640. DOI:10.1111/sms.12912
   PubMed Web of Science ®Google Scholar
• 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. Frontiers Physiol. 2021;12:773054.
   PubMed Web of Science ®Google Scholar
• 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;26(24):2827–2835. DOI:10.1080/02640414.2018.1478612
   Google Scholar
• Snipe RMJ, Khoo A, Kitic CM, et al. Carbohydrate and protein intake during exertional heat stress ameliorates intestinal epithelial injury and small intestine permeability. Appl Physiol Nutr Metab. 2017;42(12):1283–1292. DOI:10.1139/apnm-2017-0361
   PubMed Web of Science ®Google Scholar
• Ogden HB, Fallowfield JL, Child RB, et al. Reliability of gastrointestinal barrier integrity and microbial translocation biomarkers at rest and following exertional heat stress. Physiology Reports. 2020;8(5). DOI:10.14814/phy2.14374
   PubMed Web of Science ®Google Scholar
• Ogden HB, Fallowfield JL, Child RB, et al. Influence of aerobic fitness on gastrointestinal barrier integrity and microbial translocation following a fixed-intensity military exertional heat stress test. Eur J Appl Physiol. 2020;120(10):2325–2337. DOI:10.1007/s00421-020-04455-w
   PubMed Web of Science ®Google Scholar
• Sheahen BL, Fell JW, Zadow EK, et al. Intestinal damage following short-duration exercise at the same relative intensity is similar in temperature and hot environments. Appl Physiol Nutr Metab. 2018;43(12):1314–1320. DOI:10.1139/apnm-2018-0057
   PubMed Web of Science ®Google Scholar
• Pires W, Veneroso CE, Wanner SP, et al. Association between exercise-induced hyperthermia and intestinal permeability: a systematic review. Sports Med. 2017;47(7):1389–1403. DOI:10.1007/s40279-016-0654-2
   PubMed Web of Science ®Google Scholar
• Costa RJS, Snipe RMJ, Camões-Costa V, et al. The impact of gastrointestinal symptoms and dermatological injuries on nutritional intake and hydration status during ultramarathon events. Sports Med-Open. 2016;2(16):1–14. DOI:10.1186/s40798-015-0041-9
   Google Scholar
• 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. Frontiers Physiol. 2021;12:719142. DOI:10.3389/fphys.2021.719142
   PubMed Web of Science ®Google Scholar
• Jeukendrup AE, Vet-Joop K, Sturk A, et al. Relationship between gastrointestinal complaints and endotoxaemia, cytokine release and the acute-phase reaction during and after a long-distance triathlon in highly trained men. Clin Sci. 2000;98(1):47–55. DOI:10.1042/CS19990258
   PubMed Web of Science ®Google Scholar
• Roberts WO, Armstrong LE, Sawka MN, et al. ACSM expert consensus statement on exertional heat illness: recognition, management, and return to activity. Curr Sports Med Rep. 2021;20(9):470–484. DOI:10.1249/JSR.0000000000000878
   PubMed Web of Science ®Google Scholar
• Costa RJS, Henningsen K, Gaskell S, et al. Amino acid-based beverage interventions ameliorates exercise-induced gastrointestinal syndrome in response to exertional-heat stress: the HEAAT™ study. Int J Sport Nutr Exerc Metab. 2023;In press.
   PubMed Web of Science ®Google Scholar
• Costa RJ, Oliver SJ, Laing SJ, et al. Influence of timing of postexercise carbohydrate-protein ingestion on selected immune indices. Int J Sport Nutr Exerc Metab. 2009;19(4):366–384. DOI:10.1123/ijsnem.19.4.366
   PubMed Web of Science ®Google Scholar
• 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(4):411–419. DOI:10.1123/ijsnem.2018-0215
   PubMed Web of Science ®Google Scholar
• Adriaanse MP, Tack GJ, Passos VL, et al. Serum I-FABP as marker for enterocyte damage in coeliac disease and its relation to villous atrophy and circulating autoantibodies. Aliment Pharmacol Ther. 2013;37(4):482–490. DOI:10.1111/apt.12194
   PubMed Web of Science ®Google Scholar
• Blaser A, Padar M, Tang J, et al. Citrulline and intestinal fatty acid-binding protein as biomarkers for gastrointestinal dysfunction in the critically ill. Anaesthesiol Intensive Ther. 2019;51(3):230–239. DOI:10.5114/ait.2019.86049
   PubMed Web of Science ®Google Scholar
• Al-Saffar AK, Meijer CH, Gannavarapu VR, et al. Parallel changes in Harvey-Bradshaw index, TNF α, and intestinal fatty acid binding protein in response to infliximab in Crohn’s disease. Gastroenterol Res Pract. 2017;2017:1–8. Article 1745918. DOI:10.1155/2017/1745918
   Web of Science ®Google Scholar
• Linsalata M, Riezzo G, D’Attoma B, et al. Noninvasive biomarkers of gut barrier function identify two subtypes of patients suffering from diarrhoea predominant- IBS: a case-control study. BMC Gastroenterol. 2018;18(1):167. DOI:10.1186/s12876-018-0888-6
   PubMedGoogle Scholar
• Pelsers MM, Hermens WT, Glatz JF. Fatty acid-binding proteins as plasma markers of tissue injury. Clin Chim Acta. 2005;352(1–2):15–35. DOI:10.1016/j.cccn.2004.09.001
   PubMed Web of Science ®Google Scholar
• Grootjans J, Lenaerts K, Buurman WA, et al. Life and death at the mucosal-luminal interface: new perspectives on human intestinal ischemia-reperfusion. World J Gastroentero. 2016;22(9):2760–2770. DOI:10.3748/wjg.v22.i9.2760
   PubMed Web of Science ®Google Scholar
• Rehrer NJ, Smets A, Reynaert H, et al. Effect of exercise on portal vein blood flow in man. null. 2001;33(9):1533–1537. DOI:10.1097/00005768-200109000-00017
   Google Scholar
• van Wijck K, Lenaerts K, van Loon LJ, et al. Exercise-induced splanchnic hypoperfusion results in gut dysfunction in healthy men. PLos One. 2011;6(7):e22366. Article e22366. doi:10.1371/journal.pone.0022366.
   PubMed Web of Science ®Google Scholar
• Carr KE, Hume SP, Marigold JC, et al. Scanning and transmission electron microscopy of the damage to small intestinal mucosa following X irradiation or hyperthermia. Scan Electron Microsc. 1982;Pt 1. 393–402.
   PubMedGoogle Scholar
• Kamel HM, Carr KE, Hume SP, et al. Structural changes in mouse small intestinal villi following lower body hyperthermia. Scan Electron Microsc. 1985;Pt 2. 849–858.
   PubMedGoogle Scholar
• Young P, Rauch CE, Russo I, et al. Plasma endogenous endotoxin core antibody response to exercise in endurance athletes. Int J Sports Med. 2022;43(12):1023–1032. DOI:10.1055/a-1827-3124
   PubMed Web of Science ®Google Scholar
• Hudson ASR, Soares AND, Horta NAC, et al. The magnitude of physical exercise-induced hyperthermia is associated with changes in intestinal permeability and expression of tight junction genes in rats. J Therm Biol. 2020;91(2020):102610. DOI:10.1016/j.jtherbio.2020.102610
   PubMedGoogle Scholar
• Selkirk GA, McLellan TM, Wright HE, et al. Expression of intracellular cytokines, HSP72, and apoptosis in monocyte subsets during exertional heat stress in trained and untrained individuals. Am J Physiol - Regul Integr Comp Physiol. 2009;296(3):575–586. DOI:10.1152/ajpregu.90683.2008
   PubMed Web of Science ®Google Scholar
• Bosenberg AT, Brock-Utne JG, Gaffin SL, et al. Strenuous exercise causes systemic endotoxemia. J Appl Physiol. 1988;65(1):106–108. DOI:10.1152/jappl.1988.65.1.106
   PubMed Web of Science ®Google Scholar
• Brock-Utne JG, Gaffin SL, Wells MT, et al. Endotoxaemia in exhausted runners after a long-distance race. S Afr Med J. 1988;73(9):533–536.
   PubMed Web of Science ®Google Scholar
• Camus G, Nys M, Poortmans JR, et al. Endotoxemia production of tumor necrosis factor alpha and polymorphonuclear neutrophil activation following strenuous exercise in humans. Eur J Appl Physiol. 1998;79(1):62–68. DOI:10.1007/s004210050474
   Web of Science ®Google Scholar
• da Luz Scheffer D, Latini A. Exercise-induced immune system response: anti-inflammatory status on peripheral and central organs. Biochim Biophys Acta Mol Basis Dis BBA-MOL BASIS DIS. 2020;1866(10):165823. DOI:10.1016/j.bbadis.2020.165823
   PubMed Web of Science ®Google Scholar
• Kistler EB, Alsaigh T, Chang M, et al. Impaired small-bowel barrier integrity in the presence of lumenal pancreatic digestive enzymes leads to circulatory shock. Shock. 2012;38(3):262–267. DOI:10.1097/SHK.0b013e31825b1717
   PubMed Web of Science ®Google Scholar
• Fung AA, Zhou A, Vanos JK, et al. Enhanced intestinal permeability and intestinal co-morbidities in heat strain: a review and case for autodigestion. Temperature. 2021;8(3):223–244. DOI:10.1080/23328940.2021.1922261
   Google Scholar
• Rav-Acha M, Hadad E, Epstein Y, et al. Fatal exertional heat stroke: a case series. Am J Med. 2004;328(2):84–87. DOI:10.1097/00000441-200408000-00003
   Google Scholar
• Camus G, Poortmans J, Nys M, et al. Mild endotoxaemia and the inflammatory response induced by a marathon race. Clin Sci. 1997;92(4):415–422. DOI:10.1042/cs0920415
   PubMed Web of Science ®Google Scholar
• Gutsmann T, Müller M, Carroll SF, et al. Dual role of lipopolysaccharide (LPS)-binding protein in neutralization of LPS and enhancement of LPS-induced activation of mononuclear cells. Infectious Immunol. 2001;69(11):6942–6950. DOI:10.1128/IAI.69.11.6942-6950.2001
   PubMed Web of Science ®Google Scholar
• Wang X, Wu L, Wu K, et al. Roles of endotoxin-related signaling molecules in the progression of acute necrotizing pancreatitis in mice. Pancreas. 2005;31(3):251–257. DOI:10.1097/01.mpa.0000175179.62916.17
   PubMed Web of Science ®Google Scholar
• Bradford CD, Cotter JD, Thorburn MS, et al. Exercise can be pyrogenic in humans. Am J Physiol- Regul Integr Comp Physiol. 2007;292(1):R143–149. DOI:10.1152/ajpregu.00926.2005
   PubMed Web of Science ®Google Scholar
• Rowsey PJ. Thermoregulation: cytokine involved in fever and exercise. Annu Rev Nurs Res. 2013;31(1):20–46.
   Google Scholar
• Boden BP, Fine KM, Spencer TA, et al. Nontraumatic exertional fatalities in football players, Part 2: excess in conditioning kills. Orthop J Sports Med. 2018;8(8):2325967120943491. DOI:10.1177/2325967120943491
   Web of Science ®Google Scholar
• Lim CL Heat sepsis precedes heat toxicity in the pathophysiology of heat stroke-a new paradigm on an ancient disease. Antioxidants. 7(11)149.
   Google Scholar
• Gaskell SK, Burgell R, Wiklendt L, et al. Impact of exercise duration on gastrointestinal function and symptoms. J Appl Physiol. 2022;134(1):160–171. DOI:10.1152/japplphysiol.00393.2022
   PubMed Web of Science ®Google Scholar
• Gaskell SK, Burgell R, Wiklendt L, et al. Does exertional heat stress impact gastrointestinal function and symptoms? J Sci Med Sport. 2022;25(12):960–967. DOI:10.1016/j.jsams.2022.10.008
   PubMed Web of Science ®Google Scholar
• Barberio MD, Elmer DJ, Laird RH, et al. Systemic LPS and inflammatory response during consecutive days of exercise in heat. Int J Sports Med. 2015;36(03):262–270. DOI:10.1055/s-0034-1389904
   PubMedGoogle Scholar
• Lee BJ, Clarke ND, Hankey J, et al. Whole body precooling attenuates the extracellular HSP72, IL-6 and IL-10 responses after an acute bout of running in the heat. Nutr Biochem. 2017;36(4):414–421. DOI:10.1080/02640414.2017.1313441
   Google Scholar
• Sumi D, Nagatsuka H, Matsuo K, et al. the impact of heat acclimation on gastrointestinal function following endurance exercise in a hot environment. Nutrients. 2023;15(1):215. DOI:10.3390/nu15010216
   PubMed Web of Science ®Google Scholar
• Alhadad SB, Chua MCY, Lee JKW, et al. The effects of low and normal dose ice slurry ingestion on endurance capacity and intestinal epithelial injury in the heat. J Sci Med Sport. In press, S1440-2440(23)00078–6. DOI:10.1016/j.jsams.2023.04.008.
   Web of Science ®Google Scholar