Download PDF
Int J Sports Med 2018; 39(04): 255-263
DOI: 10.1055/s-0043-122742
Physiology & Biochemistry
© Georg Thieme Verlag KG Stuttgart · New York

The Impact of Mild Heat Stress During Prolonged Running On Gastrointestinal Integrity, Gastrointestinal Symptoms, Systemic Endotoxin and Cytokine Profiles

Rhiannon M. J. Snipe
1   Department of Nutrition Dietetics & Food, Monash University, Notting Hill, Australia
,
Anthony Khoo
1   Department of Nutrition Dietetics & Food, Monash University, Notting Hill, Australia
,
Cecilia M. Kitic
2   School of Health Sciences, University of Tasmania, Launceston, Australia
,
Peter R. Gibson
3   Department of Gastroenterology, Monash University, Melbourne, Australia
,
Ricardo J. S. Costa
1   Department of Nutrition Dietetics & Food, Monash University, Notting Hill, Australia
› Author Affiliations
Further Information

Publication History



accepted 29 October 2017

Publication Date:
07 February 2018 (online)

Also available at
    Permissions and Reprints

Abstract

The study aimed to determine the effects of mild exertional heat stress on intestinal injury, permeability, gastrointestinal symptoms, and systemic endotoxin and cytokine responses. Ten endurance runners completed 2 h of running at 60% V̇O2max in warm (WARM: 30°C) and temperate (TEMP: 22°C) ambient conditions. Rectal temperature (Tre) and gastrointestinal symptoms were recorded every 10 min during exercise. Blood samples were collected pre- and post-exercise, and during recovery to determine plasma intestinal fatty acid-binding protein (I-FABP) and cortisol concentrations, and systemic endotoxin and inflammatory cytokine profiles. Urinary lactulose:L-rhamnose ratio (L/R) was used to measure small intestine permeability. Compared with TEMP, WARM significantly increased Tre from 50 min onwards (38.1±0.3°C vs. 38.4±0.5°C, respectively; p<0.01), gastrointestinal symptoms (p=0.017), post-exercise plasma cortisol (26% vs. 59%, respectively; p<0.001) and I-FABP (127% vs. 184%, respectively; p<0.001) concentrations. Circulatory anti-endotoxin antibodies increased post-exercise (p<0.001) on WARM (20%) and TEMP (28%). No differences were observed for plasma endotoxin concentration (6% vs. 5% increase, respectively) or small intestine permeability (L/R 0.026±0.010 and 0.025±0.015, respectively). Both pro- and anti-inflammatory cytokines increased post-exercise, with inflammatory response cytokines TNF-α (p=0.015) and IL-8 (p=0.044), and compensatory anti-inflammatory cytokines IL-10 (p=0.065), and IL-1ra higher on WARM than TEMP. Findings suggest that exposure to warm ambient conditions during prolonged submaximal running induces transient intestinal epithelial injury, increases gastrointestinal symptoms, and promotes greater perturbations to the systemic cytokine profile compared to running in temperate conditions.

Key words

heat - endurance - permeability - I-FABP - symptoms - gastrointestinal syndrome
 

  • References

  • 1 Armstrong LE, Casa DJ, Millard-Stafford M, Moran DS, Pyne SW, Roberts WO. American College of Sports Medicine position stand. Exertional heat illness during training and competition. Med Sci Sports Exerc 2007; 39: 556-572
    CrossrefPubMedGoogle Scholar
  • 2 Barberio MD, Elmer DJ, Laird RH, Lee KA, Gladden B, Pascoe DD. Systemic LPS and inflammatory response during consecutive days of exercise in heat. Int J Sports Med 2015; 36: 262-270
    Article in Thieme ConnectPubMedGoogle Scholar
  • 3 Bongers CC, Hopman MT, Eijsvogels TM. Cooling interventions for athletes: An overview of effectiveness, physiological mechanisms, and practical considerations. Temperature (Austin) 2017; 4: 60-78
    CrossrefPubMedGoogle Scholar
  • 4 Borg GA. Psychophysical bases of perceived exertion. Med Sci Sports Exerc 1982; 14: 377-381
    Google Scholar
  • 5 Caradonna L, Amati L, Magrone T, Pellegrino NM, Jirillo E, Caccavo D. Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: Biological and clinical significance. J Endotoxin Res 2000; 6: 205-214
    PubMedGoogle Scholar
  • 6 Casa DJ, DeMartini JK, Bergeron MF, Csillan D, Eichner ER, Lopez RM, Ferrara MS, Miller KC, O'Connor F, Sawka MN, Yeargin SW. National Athletic Trainers' Association Position Statement: Exertional Heat Illnesses. J Athl Train 2015; 50: 986-1000
    CrossrefPubMedGoogle Scholar
  • 7 Cohen DC, Winstanley A, Engledow A, Windsor AC, Skipworth JR. Marathon-induced ischemic colitis: Why running is not always good for you. Am J Emerg Med 2009; 27: e255-e257
    PubMedGoogle Scholar
  • 8 Costa RJ, Crockford MJ, Moore JP, Walsh NP. Heat acclimation responses of an ultra-endurance running group preparing for hot desert-based competition. Eur J Sport Sci 2014; 14: S131-S141
    CrossrefPubMedGoogle Scholar
  • 9 Costa RJ, Fortes MB, Richardson K, Bilzon JL, Walsh NP. The effects of postexercise feeding on saliva antimicrobial proteins. Int J Sport Nutr Exerc Metab 2012; 22: 184-191
    CrossrefPubMedGoogle Scholar
  • 10 Costa RJ, Oliver SJ, Laing SJ, Waiters R, Bilzon JL, Walsh NP. Influence of timing of postexercise carbohydrate-protein ingestion on selected immune indices. Int J Sport Nutr Exerc Metab 2009; 19: 366-384
    CrossrefPubMedGoogle Scholar
  • 11 Costa RJ, Snipe R, Camoes-Costa V, Scheer V, Murray A. The impact of gastrointestinal symptoms and dermatological injuries on nutritional intake and hydration status during ultramarathon events. Sports Med Open 2016; 2: 16
    PubMedGoogle Scholar
  • 12 Costa RJS, Miall A, Khoo A, Rauch C, Snipe R, Camões-Costa V, Gibson P. 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
    CrossrefPubMedGoogle Scholar
  • 13 Costa RJS, 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
    CrossrefPubMedGoogle Scholar
  • 14 Dill DB, Costill DL. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 1974; 37: 247-248
    CrossrefPubMedGoogle Scholar
  • 15 Gill SK, Allerton DM, Ansley-Robson P, Hemmings K, Cox M, Costa RJ. Does short-term high dose probiotic supplementation containing lactobacillus casei attenuate exertional-heat stress induced endotoxaemia and cytokinaemia?. Int J Sport Nutr Exerc Metab 2016; 26: 268-275
    CrossrefPubMedGoogle Scholar
  • 16 Gill SK, Hankey J, Wright A, Marczak S, Hemming K, Allerton DM, Ansley-Robson P, Costa RJ. The impact of a 24- h ultra-marathon on circulatory endotoxin and cytokine profile. Int J Sports Med 2015; 36: 688-695
    Article in Thieme ConnectPubMedGoogle Scholar
  • 17 Grootjans J, Lenaerts K, Buurman WA, Dejong CHC, Derikx JPM. Life and death at the mucosal-luminal interface: New perspectives on human intestinal ischemia-reperfusion. World J Gastroenterol 2016; 22: 2760-2770
    CrossrefPubMedGoogle Scholar
  • 18 Harriss DJ, Macsween A, Atkinson G. Standards for Ethics in Sport and Exercise Science Research: 2018 Update. Int J Sports Med 2017; 38: 1126-1131
    Article in Thieme ConnectPubMedGoogle Scholar
  • 19 Hoffman MD, Fogard K. Factors related to successful completion of a 161-km ultramarathon. Int J Sports Physiol Perform 2011; 6: 25-37
    CrossrefPubMedGoogle Scholar
  • 20 Hollies NRS, Goldman RF. Psychological scaling in comfort assessment. In: Hollies NRS, Goldman RF. eds Clothing comfort: Interaction of thermal, ventilation, construction, and assessment factors. Michigan, USA: Ann Arbor Science Publishers Inc; 1977: 107-120
    Google Scholar
  • 21 Horner KM, Schubert MM, Desbrow B, Byrne NM, King NA. Acute exercise and gastric emptying: A meta-analysis and implications for appetite control. Sports Med 2015; 45: 659-678
    CrossrefPubMedGoogle Scholar
  • 22 Jeukendrup AE, Vet-Joop K, Sturk A, Stegen JH, Senden J, Saris WH, Wagenmakers AJ. Relationship between gastro-intestinal complaints and endotoxaemia, cytokine release and the acute-phase reaction during and after a long-distance triathlon in highly trained men. Clin Sci (Lond) 2000; 98: 47-55
    CrossrefPubMedGoogle Scholar
  • 23 Jones AM, Doust JH. A 1% treadmill grade most accurately reflects the energetic cost of outdoor running. J Sports Sci 1996; 14: 321-327
    CrossrefPubMedGoogle Scholar
  • 24 Kenney WL, Ho CW. Age alters regional distribution of blood flow during moderate-intensity exercise. J Appl Physiol (1985) 1995; 79: 1112-1119
    CrossrefPubMedGoogle Scholar
  • 25 Lang JA, Gisolfi CV, Lambert GP. Effect of exercise intensity on active and passive glucose absorption. Int J Sport Nutr Exerc Metab 2006; 16: 485-493
    CrossrefPubMedGoogle Scholar
  • 26 Leiper JB. Fate of ingested fluids: Factors affecting gastric emptying and intestinal absorption of beverages in humans. Nutr Rev 2015; 73 (Suppl. 02) 57-72
    CrossrefPubMedGoogle Scholar
  • 27 Miall A, Khoo A, Rauch C, Snipe RMJ, Camoes-Costa VL, Gibson PR, Costa RJS. Two weeks of repetitive gut-challenge reduce exercise-associated gastrointestinal symptoms and malabsorption. Scand J Med Sci Sports 2017; DOI: 10.1111/sms.12912.
    PubMedGoogle Scholar
  • 28 Morris G, Berk M, Galecki P, Maes M. The emerging role of autoimmunity in myalgic encephalomyelitis/chronic fatigue syndrome (ME/cfs). Mol Neurobiol 2014; 49: 741-756
    CrossrefPubMedGoogle Scholar
  • 29 Morrison SA, Cheung SS, Cotter JD. Bovine colostrum, training status, and gastrointestinal permeability during exercise in the heat: A placebo-controlled double-blind study. Appl Physiol Nutr Metab 2014; 39: 1070-1082
    CrossrefPubMedGoogle Scholar
  • 30 Moyen NE, Ellis CL, Ciccone AB, Thurston TS, Cochrane KC, Brown LE, Coburn JW, Judelson DA. Increasing relative humidity impacts low-intensity exercise in the heat. Aviat Space Environ Med 2014; 85: 112-119
    CrossrefPubMedGoogle Scholar
  • 31 Neufer PD, Young AJ, Sawka MN. Gastric emptying during exercise: Effects of heat stress and hypohydration. Eur J Appl Physiol Occup Physiol 1989; 58: 433-439
    CrossrefPubMedGoogle Scholar
  • 32 Pals KL, Chang RT, Ryan AJ, Gisolfi CV. Effect of running intensity on intestinal permeability. J Appl Physiol 1997; 82: 571-576
    CrossrefPubMedGoogle Scholar
  • 33 Pires W, Veneroso CE, Wanner SP, Pacheco DA, Vaz GC, Amorim FT, Tonoli C, Soares DD, Coimbra CC. Association between exercise-induced hyperthermia and intestinal permeability: A systematic review. Sports Med 2016; 47: 1389-1403
    PubMedGoogle Scholar
  • 34 Rav-Acha M, Hadad E, Epstein Y, Heled Y, Moran DS. Fatal exertional heat stroke: A case series. Am J Med Sci 2004; 328: 84-87
    CrossrefPubMedGoogle Scholar
  • 35 Selkirk GA, McLellan TM, Wright HE, Rhind SG. Mild endotoxemia, NF-kappaB translocation, and cytokine increase during exertional heat stress in trained and untrained individuals. Am J Physiol Regul Integr Comp Physiol 2008; 295: R611-R623
    CrossrefPubMedGoogle Scholar
  • 36 Shin HS, Ingram JR, McGill AT, Poppitt SD. Lipids, CHOs, proteins: Can all macronutrients put a 'brake' on eating?. Physiol Behav 2013; 120: 114-123
    CrossrefPubMedGoogle Scholar
  • 37 Shing CM, Peake JM, Lim CL, Briskey D, Walsh NP, Fortes MB, Ahuja KD, Vitetta L. Effects of probiotics supplementation on gastrointestinal permeability, inflammation and exercise performance in the heat. Eur J Appl Physiol 2014; 114: 93-103
    CrossrefPubMedGoogle Scholar
  • 38 Stacey MJ, Parsons IT, Woods DR, Taylor PN, Ross D. SJB Susceptibility to exertional heat illness and hospitalisation risk in UK military personnel. BMJ Open Sport Exerc Med 2015; 1: e000055
    CrossrefPubMedGoogle Scholar
  • 39 Stuempfle KJ, Hoffman MD. Gastrointestinal distress is common during a 161-km ultramarathon. J Sports Sci 2015; 33: 1814-1821
    CrossrefPubMedGoogle Scholar
  • 40 van Wijck K, Lenaerts K, van Loon LJC, Peters WHM, Buurman WA, Dejong CHC. Exercise-Induced splanchnic hypoperfusion results in gut dysfunction in healthy men. PLoS One 2011; 6: e22366
    Google Scholar
  • 41 van Wijck K, Pennings B, van Bijnen AA, Senden JM, Buurman WA, Dejong CH, van Loon LJ, Lenaerts K. Dietary protein digestion and absorption are impaired during acute postexercise recovery in young men. Am J Physiol Regul Integr Comp Physiol 2013; 304: R356-R361
    CrossrefPubMedGoogle Scholar
  • 42 Wendt D, van Loon LJ, Lichtenbelt WD. Thermoregulation during exercise in the heat: Strategies for maintaining health and performance. Sports Med 2007; 37: 669-682
    CrossrefPubMedGoogle Scholar
  • 43 Yeh Y, Law L, Lim C. Gastrointestinal response and endotoxemia during intense exercise in hot and cool environments. Eur J Appl Physiol 2013; 113: 1575-1583
    CrossrefPubMedGoogle Scholar