Preview

Patient-Oriented Medicine and Pharmacy

Advanced search

Stress response during exercise, gut-brain axis, and gut microbiota in athletes: a review of the literature

https://doi.org/10.37489/2949-1924-0012

Abstract

Fatigue, mood disturbances, lack of performance, and gastrointestinal disturbances are common among athletes during training and competition. Psychosocial and physical demands during intense exercise can initiate a stress response that activates the sympathoadrenal and hypothalamic-pituitary-adrenal axes, resulting in the release of stress and catabolic hormones, inflammatory cytokines, and microbial molecules. The gut is home to trillions of microorganisms that play fundamental roles in many aspects of human biology, including metabolism, neuroendocrine, and immune function. The microbiome and its influence on host behavior, the gut barrier, and immunity is a critical aspect of the gut-brain axis. Data have been obtained showing a high correlation between physical and emotional stress during exercise and changes in the composition of the gastrointestinal microbiota. Modifications to the composition of the microbiota in professional athletes can improve training efficiency, improve athletic performance and shorten the recovery period after intense physical exertion.

About the Authors

V. A. Margazin
Yaroslavl State Pedagogical University named after K. D. Ushinsky
Russian Federation

Margazin Vladimir A. — M. D., D. Sc. (Medicine), Honored Doctor of the Russian Federation, Professor of the department. RSCI Author ID: 702664.

Yaroslavl


Competing Interests:

The authors declare no conflict of interest



M. A. Gansburgskiy
Yaroslavl State Medical University
Russian Federation

Gansburgskiy Mikhail A. — M. D., Ph. D. (Medicine), Associate Professor of the department of Physical Education and Sports. RSCI Author ID: 294904

Yaroslavl


Competing Interests:

The authors declare no conflict of interest



A. V. Koromyslov
Yaroslavl State Pedagogical University named after K. D. Ushinsky
Russian Federation

Koromyslov Alexander V. — M. D., Ph. D. (Medicine), associate Professor of the Department of Medical and Biological Sport Fundamentals. RSCI Author ID: 929133.

Yaroslavl


Competing Interests:

The authors declare no conflict of interest



References

1. Galley JD, Nelson MC, Yu Z, et al. Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol. 2014;14:189. doi: 10.1186/1471-2180-14-189

2. Clark A, Mach N. Exercise-induced stress behavior, gutmicrobiota brain axis and diet: a systematic review for athletes. J. Int. Soc. Sports Nutr. 2016;13:43. doi: 10.1186/s12970-016-0155-6

3. Morgan JA, Corrigan F, Baune BT. Effects of physical exercise on central nervous system functions: A review of brain region specific adaptations. J. Mol. Psychiatry. 2015;3:3. doi: 10.1186/s40303-015-0010-8

4. Margazin VA, Gansburgskiy MA, Koromyslov AV, Lebedev AV. Pathogenesis of symptoms of the gastrointestinal tract in athletes with various types of physical activity: a review of the literature. Lechebnaya fizkul'tura i sportivnaya meditsina. 2018;146(2):32–42. (In Russ.).

5. Lin TW, Chen SJ, Huang TY, et al. Different types of exercise induce differential effects on neuronal adaptations and memory performance. Neurobiol. Learn. Mem. 2012;97:140–7. doi: 10.1016/j.nlm.2011.10.006

6. Purvis D, Gonsalves S, Deuster PA. Physiological and psychological fatigue in extreme conditions: Overtraining and elite athletes. PM R. 2010;2:442– 50. doi: 10.1016/j.pmrj.2010.03.025

7. Mackinnon LT. Overtraining effects on immunity and performance in athletes. Immun. Cell Biol. 2000; 78:502–9. doi: 10.1111/j.1440–1711.2000.t01-7-.x

8. Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 2009;10:397–409. doi: 10.1038/nrn2647

9. Martins AS, Crescenzi A, Stern JE, et al. Hypertension and exercise training differentially affect oxytocin and oxytocin receptor expression in the brain. Hypertension. 2005;46:1004–9. doi: 10.1161/01.HYP.0000175812.03322.59

10. Eisenstein M. Microbiome: Bacterial broadband. Nature. 2016;533:104–6. doi: 10.1038/533S104a

11. Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat. Rev. Gastroenterol. Hepatol. 2009;6:306–14. doi: 10.1038/nrgastro.2009.35

12. Lyte M, Vulchanova L, Brown DR. Stress at the intestinal surface: Catecholamines and mucosa-bacteria interactions. Cell Tissue Res. 2011; 343:23–32. doi: 10.1007/s00441-010-1050-0

13. Stilling RM, Dinan TG, Cryan JF. Microbial genes, brain & behaviour — epigenetic regulation of the gut-brain axis. Genes Brain Behav. 2014;13:69–86. doi: 10.1111/gbb.12109

14. Li J, Jia H, Cai X, et al. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 2014;32:834–41. doi: 10.1038/nbt.2942

15. Olbricht H, Twadell K, Sandel B, et al. Is There a Universal Endurance Microbiota? Microorganisms. 2022; Nov 9;10 (11):2213. doi: 10.3390/microorganisms10112213

16. Rajilic-Stojanovic M, de Vos WM. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiology Reviews. 2014;38:996–1047. doi: 10.1111/1574–6976.12075

17. Flint HJ, Bayer EA, Rincon MT, et al. Polysaccharide utilization by gut bacteria: Potential for new insights from genomic analysis. Nat. Rev. Microbiol. 2008;6:121–31. doi: 10.1038/nrmicro1817

18. Mach N, Berri M, Estelle J, et al. Early-life establishment of the swine gut microbiome and impact on host phenotypes. Environ. Microbiol. Rep. 2015;7:554–69. doi: 10.1111/1758–2229.12285

19. Mohr AE, Jäger R, Carpenter KC et al. The athletic gut microbiota. J. Int. Soc. Sports Nutr. 2020; May 12;17(1):24. doi: 10.1186/s12970-020-00353-w

20. Fontana F, Longhi G, Tarracchini C, et al. The human gut microbiome of athletes: metagenomic and metabolic insights. Microbiome. 2023; Feb 14;11(1):27. doi: 10.1186/s40168-023-01470-9

21. Nicholson JK, Holmes E, Kinross J, et al. Hostgut microbiota metabolic interactions. Science. 2012;336:1262–7. doi: 10.1126/science.1223813

22. Moloney RD, Desbonnet L, Clarke G, et al. The microbiome: Stress, health and disease. Mamm. Genome. 2014;25:49–74. doi: 10.1007/s00335-013-9488-5

23. Mach N and Fuster-Botella D. Endurance exercise and gut microbiota: A review. J. Sport Health Sci. 2017; Jun;6(2):179–97. doi: 10.1016/j.jshs.2016.05.001. Epub 2016 May 10.

24. Tarracchini Ch, Fontana F, Lugli GA et al. Investigation of the Ecological Link between Recurrent Microbial Human Gut Communities and Physical Activity. Microbiol. Spectr. 2022; Apr 27;10(2):e0042022. doi: 10.1128/spectrum.00420–22. Epub 2022 Apr 4.

25. Dziewiecka H, Buttar HS, Kasperska A, et al. Physical activity induced alterations of gut microbiota in humans: a systematic review. BMC Sports Sci. Med. Rehabil. 2022; Jul 7;14(1):122. doi: 10.1186/s13102-022-00513-2

26. Marttinen M, Ala-Jaakkola R, Laitila A, Lehtinen MJ. Gut Microbiota, Probiotics and Physical Performance in Athletes and Physically Active Individuals. Nutrients. 2020; Sep 25;12(10):2936. doi: 10.3390/nu12102936

27. Bragina TV, Yelizarova YeV, Sheveleva SA. Intestinal microbiota of athletes. Voprosy pitaniya. 2021;90 (4):36–52. (In Russ.).

28. Hughes RL, Holscher HD. Fueling Gut Microbes: A Review of the Interaction between Diet, Exercise, and the Gut Microbiota in Athletes. Adv. Nutr. 2021; Dec 1;12(6):2190–215. doi: 10.1093/advances/nmab077

29. Herman JP. Neural control of chronic stress adaptation. Front. Behav. Neurosci. 2013;7:61. doi: 10.3389/fnbeh.2013.00061

30. Angeli A, Minetto M, Dovio A, et al. The overtraining syndrome in athletes: A stress-related disorder. J. Endocrinol. Invest. 2004;27:603–12. doi: 10.1007/BF03347487

31. Hill EE, Zack E, Battaglini C, et al. Exercise and circulating cortisol levels: The intensity threshold effect. J. Endocrinol. Invest. 2008;31:587–91. doi: 10.1007/BF03345606

32. Cronin O, Molloy MG, Shanahan F. Exercise, fitness, and the gut. Curr. Opin. Gastroenterol. 2016; 32:67–73. doi: 10.1097/MOG.0000000000000240

33. Carabotti M, Scirocco A, Maselli MA, et al. The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. 2015;28:203–9. PMID: 25830558; PMCID: PMC4367209.

34. Marchesi JR, Adams DH, Fava F, et al. The gut microbiota and host health: A new clinical frontier. Gut. 2016;65:330–9. doi: 10.1136/gutjnl-2015-309990

35. Holzer P, Farzi A. Neuropeptides and the microbiota-gut-brain axis. Adv. Exp. Med. Biol. 2014;817: 195–219. doi: 10.1007/978-1-4939-0897-4_9

36. Barrett E, Ross RP, O'Toole PW, et al. Gamma-aminobutyric acid production by culturable bacteria from the human intestine. J. Appl. Microbiol. 2012;113:411–27. doi: 10.1111/j.1365–2672.2012.05344.x

37. Hsu YC, Chen HI, Kuo YM, et al. Chronic treadmill running in normotensive rats resets the resting blood pressure to lower levels by upregulating the hypothalamic gabaergic system. J. Hypertens. 2011;29:2339–48. doi: 10.1097/HJH.0b013e32834c628f

38. Ramson R, Jurimae J, Jurimae T, et al. The effect of 4-week training period on plasma neuropeptide y, leptin and ghrelin responses in male rowers. Eur. J. Appl. Physiol. 2012;112:1873–80. doi: 10.1007/s00421-011-2166-y

39. Saunders PR, Santos J, Hanssen NP, et al. Physical and psychological stress in rats enhances colonic epithelial permeability via peripheral CRH. Dig. Dis. Sci. 2002;47:208–15. doi: 10.1023/A:1013204612762

40. Eisenhofer G, Aneman A, Friberg P, et al. Substantial production of dopamine in the human gastrointestinal tract. J. Clin. Endocrinol. Metab. 1997;82:3864–71. doi: 10.1210/jcem.82.11.4339

41. Heijnen S, Hommel B, Kibele A, et al. Neuromodulation of aerobic exercise-a review. Front Psychol. 2016; Jan 7;6:1890. doi: 10.3389/fpsyg.2015.01890.eCollection2015.

42. Foster J. Gut-brain communication: How the microbiome influences anxiety and depression. Europ. Neuro Psycho Pharmacol. 2015;25:14.

43. Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic- pituitary-adrenal system for stress response in mice. J. Physiol. 2004;558:263–75. doi: 10.1113/jphysiol.2004.063388

44. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat. Neurosci. 2004;7:841–6. doi: 10.1038/nn129

45. Bermon S, Petriz B, Kajeniene A, et al. The microbiota: An exercise immunology perspective. Exerc. Immunol. Rev. 2015;21:70–9. PMID: 25825908.

46. Gareau MG, Silva MA, Perdue MH. Pathophysiological mechanisms of stress-induced intestinal damage. Curr. Mol. Med. 2008;8:274–81. doi: 10.2174/156652408784533760

47. Rao R, Samak G. Role of glutamine in protection of intestinal epithelial tight junctions. J. Epithel. Biol. Pharmacol. 2012;5:47–54. doi: 10.2174/1875044301205010047

48. Brown WM, Davison GW, McClean CM, et al. A systematic review of the acute effects of exercise on immune and inflammatory indices in untrained adults. Sports Med. Open. 2015;1:35. doi: 10.1186/s40798-015-0032-x

49. Zuhl M, Schneider S, Lanphere K, et al. Exercise regulation of intestinal tight junction proteins. Br. J. Sports Med. 2014;48:980–6. doi: 10.1136/bjsports-2012–091585

50. Ferrier L. Significance of increased human colonic permeability in response to corticotrophin-releasing hormone (CRH). Gut. 2008;57:7–9. doi: 10.1136/gut.2007.129841

51. Wallon C, Yang PC, Keita AV, et al. Corticotropin-releasing hormone (CRH) regulates macromolecular permeability via mast cells in normal human colonic biopsies in vitro. Gut. 2008;57:50–8. doi: 10.1136/gut.2006.117549

52. Lamprecht M, Bogner S, Schippinger G, et al. Probiotic supplementation affects markers of intestinal barrier, oxidation, and inflammation in trained men; a randomized, double-blinded, placebo-controlled trial. J. Int. Soc. Sports Nutr. 2012;9:45. doi: 10.1186/1550-2783-9-45

53. Lambert GP. Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J. Anim. Sci. 2009;87:101–8. doi: 10.2527/jas.2008–1339

54. van Wijck K, Lenaerts K, Grootjans J, et al. Physiology and pathophysiology of splanchnic hypoperfusion and intestinal injury during exercise: Strategies for evaluation and prevention. Am. J. Physiol. Gastrointest. Liver Physiol. 2012;303:155–68. doi: 10.1152/ajpgi.00066.2012

55. 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):533–6. PMID: 3375945.

56. Gleeson M. Immune function in sport and exercise. J. Appl. Physiol. (1985) 2007;103:693–9. doi: 10.1152/japplphysiol.00008.2007

57. Neish AS. Mucosal immunity and the microbiome. Ann. Am. Thorac. Soc. 2014;11:28–32. doi: 10.1513/AnnalsATS.201306-161MG

58. Redondo N, Gheorghe A, Serrano R, et al. Hydragut study: Influence of hydration status on the gut microbiota and their impact on the immune system. The FASEB J. 2015;29:1.

59. Costa KA, Soares AD, Wanner SP, et al. L-arginine supplementation prevents increases in intestinal permeability and bacterial translocation in male Swiss mice subjected to physical exercise under environmental heat stress. J. Nutr. 2014;144:218–23. doi: 10.3945/jn.113.183186

60. Puddu A, Sanguineti R, Montecucco F, et al. Evidence for the gut microbiota short-chain fatty acids as key pathophysiological molecules improving diabetes. Mediators Inflamm. 2014;2014:162021. doi: 10.1155/2014/162021. Epub 2014 Aug 17.

61. den Besten G, van Eunen K, Groen AK, et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 2013;54:2325–40. doi: 10.1194/jlr.R036012

62. Canani RB, Costanzo MD, Leone L, et al. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroen- terol. 2011;17:1519–28. doi: 10.3748/wjg.v17.i12.1519

63. Matsumoto M, Inoue R, Tsukahara T, et al. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci. Biotechnol. Biochem. 2008;72:572–6. doi: 10.1271/bbb.70474


Review

For citations:


Margazin V.A., Gansburgskiy M.A., Koromyslov A.V. Stress response during exercise, gut-brain axis, and gut microbiota in athletes: a review of the literature. Patient-Oriented Medicine and Pharmacy. 2023;1(2):36-44. (In Russ.) https://doi.org/10.37489/2949-1924-0012

Views: 837


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2949-1924 (Online)

Адрес редакции и издательства:

ООО «Издательство ОКИ»
115522, Москва, Москворечье ул., 4-5-129

Генеральный директор Афанасьева Елена Владимировна

Тел. + 7 (916) 986-04-65; Email: eva88@list.ru