Influence of some components of specialized products for athletes on the intestinal microbiome and related macroorganism indicators

Purpose: to analyze literature data on the influence of some components of specialized food products for athletes on the qualitative and quantitative composition of the intestinal microbiome and related indicators of the macroorganism.
Materials and methods: The selection of current scientific articles was carried out in open electronic databases: Web of Science, Scopus, PubMed. ncbi, Scientific Electronic Library of the Russian Federation (elibrary.ru), Russian State Library and others. The search depth is not limited.
Results. It has been shown that normalization of the diet, and therefore the nutritional status, deficient in some macro- (calcium, magnesium), microelements (iron, zinc), vitamins (A, B1, B2, B6, folates, B12, D), antioxidants, is possible not only with the help of dietary supplements containing these and other (L-carnitine, caffeine) substances, but to a significant extent this improvement is possible through the consumption of pro- and prebiotics, modulating and creating favorable conditions for maintaining the optimal composition of the intestinal microbiota and endogenous synthesis of various biologically active substances. The participation of microflora in maintaining the integrity of the functional activity of the gastrointestinal tract, ensuring an adequate immune response, maintaining acid-base balance and water-salt metabolism, and the synthesis of a number of biologically active substances has been established. Most studies have been conducted on animals.
Conclusion: optimization of athletes’ diets using specialized food products that have a modulating effect on microflora plays an important role in maintaining health and performance. The issue requires further study with the participation of volunteers.

1. Kerksick C.M., Wilborn C.D., Roberts M.D., Smith-Ryan A., Kleiner S.M., Jäger R., Collins R., Cooke M., Davis J.N., Galvan E., Greenwood M., Lowery L.M., Wildman R., Antonio J., Kreider R.B. ISSN exercise & sports nutrition review update: research & recommendations. J Int Soc Sports Nutr. 2018 Aug 1;15(1):38. https://doi.org/10.1186/s12970-018-0242-y.

2. Kobelkova I.V., Korosteleva M.M. The influence of basic nutrients on the composition of the intestinal microbiome and optimization of the adaptive potential of an athlete. Science and sport: modern trends. 2022. T. 10. No. 2. P. 15-26 https://doi.org/10.36028/2308-8826-2022-10-2-15-26

3. Kobelkova I.V., Korosteleva M.M., Mavliev F.A., Nabatov A.A., Nazarenko A.S., Nikityuk D.B. Introduction of specialized food products into the diet of athletes of the Russian national rowing team. Science and sport: modern trends. 2022. T. 10. No. 4. P. 6–15. https://doi.org/10.36028/2308-8826-2022-10-4-6-15

4. Maughan R.J., Burke L.M., Dvorak J., Larson-Meyer D.E., Peeling P., Phillips S.M., Rawson E.S., Walsh N.P., Garthe I., Geyer H., Meeusen R., van Loon L.J.C., Shirreffs S.M., Spriet L.L., Stuart M., Vernec A., Currell K., Ali V.M., Budgett R.G., Ljungqvist A., Mountjoy M., Pitsiladis Y.P., Soligard T., Erdener U., Engebretsen L. IOC consensus statement: dietary supplements and the high-performance athlete. Br J Sports Med. 2018 Apr;52(7):439-455. https://doi.org/10.1136/bjsports-2018-099027.

5. Methodological recommendations MP 2.3.1.0253-21 “Norms for physiological needs for energy and nutrients for various groups of the population of the Russian Federation” (approved by the Federal Service for Surveillance on Consumer Rights Protection and Human Well-Being on July 22, 2021)

6. Donati Zeppa S., Agostini D., Gervasi M., Annibalini G., Amatori S., Ferrini F., Sisti D., Piccoli G., Barbieri E., Sestili P., Stocchi V. Mutual Interactions among Exercise, Sport Supplements and Microbiota. Nutrients. 2019 Dec 20;12(1):17. https://doi.org/10.3390/nu12010017.

7. Roberts J.D., Suckling C.A., Peedle G.Y., Murphy J.A., Dawkins T.G., Roberts M.G. An Exploratory Investigation of Endotoxin Levels in Novice Long Distance Triathletes, and the Effects of a Multi-Strain Probiotic/Prebiotic, Antioxidant Intervention. Nutrients. 2016 Nov 17;8(11):733. https://doi.org/10.3390/nu8110733

8. Jacouton E., Mach N., Cadiou J., Lapaque N., Clement K., Dore J., van Hylckama Vlieg J.E., Smokvina T., Blottiere H.M. Lactobacillus rhamnosus CNCMI-4317 Modulates Fiaf/Angptl4 in Intestinal Epithelial Cells and Circulating Level in Mice. PLoS ONE. 2015;10:e0138880. https://doi.org/10.1371/journal.pone.0138880

9. Chen Y.M., Wei L., Chiu Y.S., Hsu Y.J., Tsai T.Y., Wang M.F., Huang C.C. Lactobacillus plantarum TWK10 Supplementation Improves Exercise Performance and Increases Muscle Mass in Mice. Nutrients. 2016;8:205. https://doi.org/10.3390/nu8040205

10. Huang W.C., Hsu Y.J., Li H., Kan N.W., Chen Y.M., Lin J.S., Hsu T.K., Tsai T.Y., Chiu Y.S., Huang C.C. Effect of Lactobacillus Plantarum TWK10 on Improving Endurance Performance in Humans. Chin. J. Physiol. 2018;61:163–170. https://doi.org/10.4077/CJP.2018.BAH587

11. Soares A.D.N., Wanner S.P., Morais E.S.S., Hudson A.S.R., Martins F.S., Cardoso V.N. Supplementation with Saccharomyces boulardii Increases the Maximal Oxygen Consumption and Maximal Aerobic Speed Attained by Rats Subjected to an Incremental-Speed Exercise. Nutrients.2019;11:2352. doi:10.3390/nu11102352

12. Rao A.V., Bested A.C., Beaulne T.M., Katzman M.A., Iorio C., Berardi J.M., Logan A.C. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog. 2009;1:6. https://doi.org/10.1186/1757-4749-1-6

13. West N.P., Pyne D.B., Cripps A.W., Hopkins W.G., Eskesen D.C., Jairath A., Christophersen C.T., Conlon M.A., Fricker P.A. Lactobacillus fermentum (PCC(R)) supplementation and gastrointestinal and respiratory-tract illness symptoms: a randomised control trial in athletes. Nutr J. 2011;10:30. https://doi.org/10.1186/1475-2891-10-30

14. Michalickova D., Minic R., Dikic N., Andjelkovic M., Kostic-Vucicevic M., Stojmenovic T., Nikolic I., Djordjevic B. Lactobacillus helveticus Lafti L10 supplementation reduces respiratory infection duration in a cohort of elite athletes: a randomized, double-blind, placebo-controlled trial. Appl Physiol Nutr Metab. 2016;41:782–789. https://doi.org/10.1139/apnm-2015-0541

15. Strozzi G.P., Mogna L. Quantification of folic acid in human feces after administration of Bifidobacterium probiotic strains. J Clin Gastroenterol. 2008 Sep;42 Suppl 3 Pt 2:S179-84. https://doi.org/10.1097/MCG.0b013e31818087d8

16. Solopova A., Bottacini F., Venturi Degli Esposti E., Amaretti A., Raimondi S., Rossi M., van Sinderen D. Riboflavin Biosynthesis and Overproduction by a Derivative of the Human Gut Commensal Bifidobacterium longum subsp. infantis ATCC 15697. Front Microbiol. 2020 Sep 15;11:573335. https://doi.org/10.3389/fmicb.2020.573335.

17. Bashir M., Prietl B., Tauschmann M., Mautner S.I., Kump P.K., Treiber G., Wurm P., Gorkiewicz G., Hogenauer C., Pieber T.R. Effects of high doses of vitamin D3 on mucosa-associated gut microbiome vary between regions of the human gastrointestinal tract. Eur. J. Nutr. 2016;55:1479–1489. https://doi.org/10.1007/s00394-015-0966-2

18. Choi Y., Lee S., Kim S., Lee J., Ha J., Oh H., Lee Y., Kim Y., Yoon Y. Vitamin E (α-tocopherol) consumption influences gut microbiota composition. Int J Food Sci Nutr. 2020 Mar;71(2):221-225. https://doi.org/10.1080/09637486.2019.1639637

19. Xuan Zhu, Shasha Xiang, Xiao Feng, Huanhuan Wang, Shiyi Tian, Yuanyuan Xu, Lihua Shi, Lu Yang, Mian Li, Yubiao Shen, Jie Chen, Yuewen Chen, and Jianzhong Han. Impact of Cyanocobalamin and Methylcobalamin on Inflammatory Bowel Disease and the Intestinal Microbiota Composition Journal of Agricultural and Food Chemistry 2019 67 (3), 916-926 Https://doi.org/10.1021/acs.jafc.8b05730Rudzki

20. Ditscheid B., Keller S. & Jahreis G. Faecal steroid excretion in humans is affected by calcium supplementation and shows gender-specific differences. Eur J Nutr (2009) 48, 22–30.

21. Starke I.C., Pieper, R. Neumann K., et al. The impact of high dietary zinc oxide on the development of the intestinal microbiota in weaned piglets. FEMS Microbiol. Ecol. 2014. 87:416–427.

22. Murakami S., Goto Y., Ito K., Hayasaka S., Kurihara S., Soga T., Tomita M., Fukuda S. The Consumption of Bicarbonate-Rich Mineral Water Improves Glycemic Control. Evid. Based Complement. Altern. Med. 2015;2015:824395. https://doi.org/10.1155/2015/824395

23. Watson H., Mitra S., Croden F.C., Taylor M., Wood H.M., Perry S.L., Spencer J.A., Quirke P., Toogood G.J., Lawton C.L., et al. A randomised trial of the effect of omega-3 polyunsaturated fatty acid supplements on the human intestinal microbiota. Gut. 2018;67:1974–1983. https://doi.org/10.1136/gutjnl-2017-314968

24. Etxeb erria U., Arias N., Boque N., Macarulla M.T., Portillo M.P., Martinez J.A., Milagro F.I. Reshaping faecal gut microbiota composition by the intake of trans-resveratrol and quercetin in high-fat sucrose diet-fed rats. J. Nutr. Biochem. 2015;26:651–660. https://doi.org/10.1016/j.jnutbio.2015.01.002

25. Anhe F.F., Roy D., Pilon G., Dudonne S., Matamoros S., Varin T.V., Garofalo C., Moine Q., Desjardins Y., Levy E., et al. A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut. 2015;64:872–883. https://doi.org/10.1136/gutjnl-2014-307142

26. Li Z., Henning S.M., Lee R.P., Lu Q.Y., Summanen P.H., Thames G., Corbett K., Downes J., Tseng C.H., Finegold S.M., et al. Pomegranate extract induces ellagitannin metabolite formation and changes stool microbiota in healthy volunteers. Food Funct. 2015;6:2487–2495. https://doi.org/10.1039/C5FO00669D

27. Jaquet M., Rochat I., Moulin J., Cavin C., Bibiloni R. Impact of coffee consumption on the gut microbiota: A human volunteer study. Int. J. Food Microbiol. 2009;130:117–121. https://doi.org/10.1016/j.ijfoodmicro.2009.01.011.

28. Janssens P.L., Penders J., Hursel R., Budding A.E., Savelkoul P.H., Westerterp-Plantenga M.S. Long-Term Green Tea Supplementation Does Not Change the Human Gut Microbiota. PLoS ONE. 2016;11:e0153134. https://doi.org/10.1371/journal.pone.0153134

29. “Formulary of medicines, biologically active food additives and medical products of the FMBA of Russia, used for medical and biological support of athletes of sports teams of the Russian Federation” (1052-formulyar-2023 (sportfmba.ru)) (1052-formulyar-2023 (sportfmba.ru))

30. World Anti-Doping Code, 2021 https://www.wada-ama.org/sites/default/files/resources/files/2021_vsemirnyy_antidopingovyy_kodeks.pdf

31. Official website of RUSADA https://rusada.ru/substances/bad/

32. Jäger R., Mohr A.E., Carpenter K.C., et al. International Society of Sports Nutrition Position Stand: Probiotics. J Int Soc Sports Nutr. 2019;16(1):62. doi:10.1186/s12970-019-0329-0

33. Coqueiro A.Y., de Oliveira Garcia A.B., Rogero M.M., Tirapegui J. /Probiotic supplementation in sports and physical exercise: does it present any ergogenic effect? //Nutr Health. 2017. 23.: P. 239–249. https://doi.org/10.1177/0260106017721000

34. Tuohy K.M., Probert H.M., Smejkal C.W., Gibson G.R. Using probiotics and prebiotics to improve gut health. Drug Discov Today. 2003 Aug 1;8(15):692–700. https://doi.org/10.1016/s1359-6446(03)02746-6.

35. LeBlanc J. G. Burgess C., Sesma F., de Giori G.S., & van Sinderen, DIngestion of milk fermented by genetically modified Lactococcus lactis improves the riboflavin status of deficient rats //Journal of dairy science. 2005;88(10):3435–3442.

36. Mach N., Clark A. Micronutrient Deficiencies and the Human Gut Microbiota. Trends Microbiol. 2017 Aug;25(8):607-610. https://doi.org/10.1016/j.tim.2017.06.004

37. Cha H.R., et al. Downregulation of Th17 cells in the small intestine by disruption of gut flora in the absence of retinoic acid. Demonstrates how a single micronutrient, vitamin A, modulates host immune responses through its effects on the composition of the intestinal microbiota. J Immunol. 2010;184:6799–6806.

38. Ivanov I.I., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–498.

39. Gaboriau-Routhiau V., et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009;31:677–689.

40. Nicholas M. Fleischman, Debanu Das, Abhinav Kumar et al. Molecular characterization of novel pyridoxal-5′-phosphatedependent enzymes from the human microbiome /First published: 29 May 2014. https://doi.org/10.1002/pro.2493

41. Yamamoto E.A., Jørgensen T.N. Relationships between vitamin D, gut microbiome, and systemic autoimmunity. Frontiers in immunology. 2020:3141.

42. Bosman E.S. Bosman E.S., Albert A.Y., Lui H., Dutz J.P., & Vallance B.A. Skin exposure to narrow band ultraviolet (UVB) light modulates the human intestinal microbiome //Frontiers in Microbiology. 2019:2410.

43. Skrypnik K., Suliburska J. Association between the gut microbiota and mineral metabolism. J Sci Food Agric. 2018 May; 98(7):2449-2460. https://doi.org/10.1002/jsfa.8724

44. Gomes J.M., Costa J.A., Alfenas R.C. Could the beneficial effects of dietary calcium on obesity and diabetes control be mediated by changes in intestinal microbiota and integrity? Br J Nutr. 2015 Dec 14;114(11):1756–1765. https://doi.org/10.1017/S0007114515003608.

45. Weaver C.M. Diet, gut microbiome, and bone health. Curr Osteoporos Rep. 2015 Apr; 13(2):125-30. https://doi.org/10.1007/s11914-015-0257-0.

46. Hojberg O., Canibe N., Poulsen D., et al.Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned pigs. Appl. Environ. Microbiol. 2005. 71:2267-2277.

47. Reed S., Neuman H., Moscovich S., et al.2015. Chronic zinc deficiency alters chick gut microbiota composition and function. Nutrients7:9768-9784.

48. Schaible U.E., Kaufmann S.H. Iron and microbial infection. Nat Rev Microbiol. 2004;2:946–953.

49. Reddy B.S., Pleasants J.R., Wostmann B.S. Effect of intestinal microflora on iron and zinc metabolism, and on activities of metalloenzymes in rats. J Nutr. 1972;102:101–107.

50. Werner T., et al. Depletion of luminal iron alters the gut microbiota and prevents Crohn’s disease-like ileitis. Gut. 2011;60:325–333.

51. Uspensky Yu.P., Novikova V.P., & Baryshnikova N.V. (2022). Iron deficiency and intestinal microbiota//Medicine: theory and practice, 7(2), 3–14. t https://ojs3.gpmu.org/index.php/medtheory-and-practice/article/view/4148

52. Fielding R., Riede L., Lugo J.P., Bellamine A. l-Carnitine Supplementation in Recovery after Exercise. Nutrients. 2018;10:349. https://doi.org/10.3390/nu10030349

53. Koeth R.A., Lam-Galvez B.R., Kirsop J., Wang Z., Levison B.S., Gu X., Copeland M.F., Bartlett D., Cody D.B., Dai H.J., Culley M.K., Li X.S., Fu X., Wu Y., Li L., DiDonato J.A., Tang W.H.W, Garcia-Garcia J.C., Hazen S.L. l-Carnitine in omnivorous diets induces an atherogenic gut microbial pathway in humans. J Clin Invest. 2019 Jan 2;129(1):373-387. https://doi.org/10.1172/JCI94601

54. Coutinho-Wolino K.S., de F Cardozo L.F.M., de Oliveira Leal V., Mafra D., Stockler-Pinto M.B. Can diet modulate trimethylamine N-oxide (TMAO) production? What do we know so far? Eur J Nutr. 2021 Oct;60(7):3567–3584. https://doi.org/10.1007/s00394-021-02491-6.

55. González-Soltero R., Bailén M., de Lucas B., Ramírez-Goercke M.I., Pareja-Galeano H., Larrosa M. Role of Oral and Gut Microbiota in Dietary Nitrate Metabolism and Its Impact on Sports Performance. Nutrients. 2020 Nov 24;12(12):3611. https:// doi.org/10.3390/nu12123611

56. Guillochon M., Rowlands D.S. Solid, Gel, and Liquid Carbohydrate Format Effects on Gut Comfort and Performance. Int. J. Sport Nutr. Exerc. Metab. 2017;27:247–254. https://doi.org/10.1123/ijsnem.2016-0211

57. O’Brien W.J., Rowlands D.S. Fructose-maltodextrin ratio in a carbohydrate-electrolyte solution differentially affects exogenous carbohydrate oxidation rate, gut comfort, and performance. Am. J. Physiol. Gastrointest. Liver Physiol. 2011;300:G181–G189. https://doi.org/10.1152/ajpgi.00419.2010

58. Clark A., Mach N. Exercise-induced stress behavior, gutmicrobiota-brain axis and diet: a systematic review for athletes. J Int Soc Sports Nutr. 2016 Nov 24;13:43. https://doi.org/10.1186/s12970-016-0155-6

59. Burke L.M. Practical considerations for bicarbonate loading and sports performance. Nestle Nutr Inst Workshop Ser. 2013;75:15–26. https://doi.org/10.1159/000345814

60. D’Angelo S. Polyphenols: Potential Beneficial Effects of These Phytochemicals in Athletes. Curr Sports Med Rep. 2020 Jul;19(7):260–265. https://doi.org/10.1249/JSR.0000000000000729.

61. Ozdal T., Sela D.A., Xiao J., Boyacioglu D., Chen F., Capanoglu E. The Reciprocal Interactions between Polyphenols and Gut Microbiota and Effects on Bioaccessibility. Nutrients. 2016;8:78. https://doi.org/10.3390/nu8020078

62. Ma G., Chen Y. Polyphenol supplementation benefits human health via gut microbiota: A systematic review via metaanalysis. J. Funct. Foods. 2020;66:103829. https://doi.org/10.1016/j.jff.2020.103829

63. Sorrenti V., Fortinguerra S., Caudullo G., Buriani A. Deciphering the Role of Polyphenols in Sports Performance: From Nutritional Genomics to the Gut Microbiota toward Phytonutritional Epigenomics. Nutrients. 2020 Apr 29;12(5):1265. https://doi.org/10.3390/nu12051265

64. Wang P., Sang S. Metabolism and pharmacokinetics of resveratrol and pterostilbene. Biofactors. 2018;44:16–25. https://doi.org/10.1002/biof.1410

65. Chaplin A., Carpéné C., Mercader J. Resveratrol, Metabolic Syndrome, and Gut Microbiota. Nutrients. 2018 Nov 3;10(11):1651. https://doi.org/10.3390/nu10111651

66. Hu Y., Chen D., Zheng P., Yu J., He J., Mao X., Yu B. The Bidirectional Interactions between Resveratrol and Gut Microbiota: An Insight into Oxidative Stress and Inflammatory Bowel Disease Therapy. Biomed Res Int. 2019 Apr 24;2019:5403761. https://doi.org/10.1155/2019/5403761

67. Close G.L., Hamilton D.L., Philp A., Burke L.M., Morton J.P. New strategies in sport nutrition to increase exercise performance. Free Radic. Biol. Med. 2016;98:144–158. https://doi.org/10.1016/j.freeradbiomed.2016.01.016