Biology of Sport
eISSN: 2083-1862
ISSN: 0860-021X
Biology of Sport
Current Issue Manuscripts accepted About the journal Editorial board Abstracting and indexing Archive Ethical standards and procedures Contact Instructions for authors Journal's Reviewers Special Information
Editorial System
Submit your Manuscript
SCImago Journal & Country Rank
3/2024
vol. 41
 
Share:
Share:
Original paper

Physical activity shifts gut microbiota structure in aged subjects with overweight/obesity and metabolic syndrome

Patricia Ruiz-Limón
1, 2
,
Jananee Muralidharan
2, 3
,
Ana M. Gomez-Perez
1, 2
,
Mora Murri
1, 2
,
Jesús Vioque
4, 5
,
Dolores Corella
2, 6
,
Montse Fitó
2, 7
,
Josep Vidal
8, 9
,
Jordi Salas-Salvadó
2, 3, 10
,
Laura Torres-Collado
4, 5
,
Oscar Coltell
11
,
Alessandro Atzeni
2, 3
,
Olga Castañer
2, 7
,
Mònica Bulló
2, 3
,
M. Rosa Bernal-López
12, 2
,
Isabel Moreno-Indias
1, 2
,
Francisco J. Tinahones
1, 2

1.
Department of Endocrinology and Nutrition, Virgen de la Victoria University Hospital, The Biomedical Research Institute of Malaga and Platform in Nanomedicine (IBIMA BIONAND Platform), University of Malaga, 29016 Malaga, Spain
2.
CIBER in Physiopathology of Obesity and Nutrition (CIBEROBN), Carlos III Health Institute, 28029 Madrid, Spain
3.
University of Rovira i Virgili, Department of Biochemistry and Biotechnology, Human Nutrition Unit, 43003 Reus, Spain
4.
Institute of Health and Biomedical Research of Alicante. University of Miguel Hernández (ISABIAL-UMH), 03010 Alicante, Spain
5.
CIBER Epidemiology and Public Health (CIBERESP), Carlos III Health Institute, 28029 Madrid, Spain
6.
Department of Preventive Medicine, University of Valencia, 46100 Valencia, Spain
7.
Cardiovascular Risk and Nutrition (Regicor Study Group), Hospital del Mar Research Institute (IMIM), 08003 Barcelona, Spain
8.
Endocrinology and Nutrition Department, Clinic Universitary Hospital, 08036 Barcelona, Spain
9.
August Pi i Sunyer Biomedical Research Institute (IDIBAPS), 08036 Barcelona, Spain
10.
Pere i Virgili Health Research Institute (IISPV). San Joan University Hospital, 43003 Reus, Spain
11.
Department of Computer Sciences. University Jaume I, Castellon, Spain
12.
Department of Internal Medicine of Regional University Hospital, Institute of Biomedical Research in Malaga (IBIMA), 29009 Málaga, Spain
Biol Sport. 2024; 41(3): 47–60
Online publish date: 2023/12/20
Article file
- 5_03583_Article.pdf  [3.32 MB]
Get citation
 
PlumX metrics:
 
1. Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, Franklin BA, Macera CA, Heath GW, Thompson PD, Bauman A. Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc. 2007 Aug; 39(8):1423–34.
2. Harvey JA, Chastin SFM, Skelton DA. Prevalence of sedentary behavior in older adults: a systematic review. Int J Environ Res Public Health. 2013 Dec; 10(12):6645–61.
3. Cárdenas Fuentes G, Bawaked RA, Martínez González MÁ, Corella D, Subirana Cachinero I, Salas-Salvadó J, Estruch R, Serra-Majem L, Ros E, Lapetra Peralta J, Fiol M, Rekondo J, Gómez-Gracia E, Tur Marí JA, Pinto Sala X, Babio N, Ortega C, Martínez JA, Schröder H. Association of physical activity with body mass index, waist circumference and incidence of obesity in older adults. Eur J Public Health. 2018 Oct; 28(5):944–50.
4. Salas-Salvadó J, Díaz-López A, Ruiz-Canela M, Basora J, Fitó M, Corella D, Serra-Majem L, Wärnberg J, Romaguera D, Estruch R, Vidal J, Alfredo Martínez J, Arós F, Vázquez C, Ros E, Vioque J, López-Miranda J, Bueno-Cavanillas A, Tur JA, Tinahones FJ, Martín V, Lapetra J, Pintó X, Daimiel L, Delgado-Rodríguez M, Matía P, Gómez-Gracia E, Díez-Espino J, Babio N, Castañer O, Sorlí J V., Fiol M, Zulet MÁ, Bulló M, Goday A, Martínez-González M. Effect of a Lifestyle Intervention Program With Energy-Restricted Mediterranean Diet and Exercise on Weight Loss and Cardiovascular Risk Factors: One-Year Results of the PREDIMED-Plus Trial. Diabetes Care [Internet]. 2019 May 1 [cited 2023 Jul 10]; 42(5):777–88. Available from: https://pubmed.ncbi.nlm .nih.gov/30389673/
5. Monda V, Villano I, Messina A, Valenzano A, Esposito T, Moscatelli F, Viggiano A, Cibelli G, Chieffi S, Monda M, Messina G. Exercise modifies the gut microbiota with positive health effects [Internet]. Vol. 2017, Oxidative Medicine and Cellular Longevity. Hindawi Limited; 2017 [cited 2021 Apr 16]. Available from: /pmc/articles/PMC 5357536/
6. Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, Kayser BD, Levenez F, Chilloux J, Hoyles L, Dumas ME, Rizkalla SW, Doré J, Cani PD, Clément K, Le Mouhaër S, Cotillard A, Kennedy SP, Pons N, Le Chatelier E, Almeida M, Quinquis B, Galleron N, Batto JM, Renault P, Zucker JD, Ehrlich SD, Blottière H, Leclerc M, Juste C, De Wouters T, Lepage P. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut. 2016 Mar 1; 65(3):426–36.
7. Aya V, Flórez A, Perez L, Ramírez JD. Association between physical activity and changes in intestinal microbiota composition: A systematic review. PLoS One [Internet]. 2021 Feb 1 [cited 2022 Feb 4]; 16(2):e0247039. Available from: https://journals.plos.org/ plosone/article?id = 10.1371/journal. pone.0247039
8. Shimizu Y. Gut microbiota in common elderly diseases affecting activities of daily living. World J Gastroenterol. 2018 Nov; 24(42):4750–8.
9. Zhong X, Powell C, Phillips CM, Millar SR, Carson BP, Dowd KP, Perry IJ, Kearney PM, Harrington JM, O’Toole PW, Donnelly AE. The Influence of Different Physical Activity Behaviours on the Gut Microbiota of Older Irish Adults. J Nutr Health Aging. 2021;
10. Sayón-Orea C, Razquin C, Bulló M, Corella D, Fitó M, Romaguera D, Vioque J, Alonso-Gómez ÁM, Wärnberg J, Martínez JA, Serra-Majem L, Estruch R, Tinahones FJ, Lapetra J, Pintó X, Tur JA, López-Miranda J, Bueno-Cavanillas A, Delgado-Rodríguez M, Matía-Martín P, Daimiel L, Sánchez VM, Vidal J, Vázquez C, Ros E, Ruiz-Canela M, Sorlí J V., Castañer O, Fiol M, Navarrete-Muñoz EM, Arós F, Gómez-Gracia E, Zulet MA, Sánchez-Villegas A, Casas R, Bernal-López R, Santos-Lozano JM, Corbella E, Bouzas C, García-Arellano A, Basora J, Asensio EM, Schröder H, Moñino M, García De La Hera M, Tojal-Sierra L, Toledo E, Díaz-López A, Goday A, Salas-Salvadó J, Martínez-González MA. Effect of a Nutritional and Behavioral Intervention on Energy-Reduced Mediterranean Diet Adherence Among Patients With Metabolic Syndrome: Interim Analysis of the PREDIMED-Plus Randomized Clinical Trial. JAMA [Internet]. 2019 Oct 10 [cited 2022 Nov 25]; 322(15):1486. Available from: /pmc/articles/PMC 6802271/
11. Molina L, Sarmiento M, Peñafiel J, Donaire D, Garcia-Aymerich J, Gomez M, Ble M, Ruiz S, Frances A, Schröder H, Marrugat J, Elosua R. Validation of the Regicor Short Physical Activity Questionnaire for the Adult Population. PLoS One. 2017 Jan; 12(1):e0168148.
12. Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett DR, Tudor-Locke C, Greer JL, Vezina J, Whitt-Glover MC, Leon AS. 2011 Compendium of Physical Activities: a second update of codes and MET values. Med Sci Sports Exerc. 2011 Aug; 43(8):1575–81.
13. Rosique-Esteban N, Díaz-López A, Martínez-González MA, Corella D, Goday A, Martínez JA, Romaguera D, Vioque J, Arós F, Garcia-Rios A, Tinahones F, Estruch R, Fernández-García JC, Lapetra J, Serra-Majem L, Pinto X, Tur JA, Bueno-Cavanillas A, Vidal J, Delgado-Rodríguez M, Daimiel L, Vázquez C, Rubio MÁ, Ros E, Salas-Salvadó J. Leisure-time physical activity, sedentary behaviors, sleep, and cardiometabolic risk factors at baseline in the PREDIMED-PLUS intervention trial: A cross-sectional analysis. PLoS One. 2017 Mar 1; 12(3).
14. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang K Bin, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik A V., Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019 Aug;37(8):852-857. doi: 10.1038/ s41587-019-0209-9
15. Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 2017 Jul; 45(W1):W180–8.
16. Watson MD, Cross BL, Grosicki GJ. Evidence for the Contribution of Gut Microbiota to Age-Related Anabolic Resistance. Nutrients. 2021 Feb 1; 13(2):1–21.
17. Ortiz-Alvarez L, Xu H, Martinez-Tellez B. Influence of Exercise on the Human Gut Microbiota of Healthy Adults: A Systematic Review. Clin Transl Gastroenterol. 2020 Feb 1; 11(2):e00126.
18. Keohane DM, Woods T, O’Connor P, Underwood S, Cronin O, Whiston R, O’Sullivan O, Cotter P, Shanahan F, Molloy MGM. Four men in a boat: Ultra-endurance exercise alters the gut microbiome. J Sci Med Sport. 2019 Sep 1; 22(9):1059–64.
19. Petriz BA, Castro AP, Almeida JA, Gomes CPC, Fernandes GR, Kruger RH, Pereira RW, Franco OL. Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats. BMC Genomics. 2014; 15(1):511.
20. Tavella T, Rampelli S, Guidarelli G, Bazzocchi A, Gasperini C, Pujos-Guillot E, Comte B, Barone M, Biagi E, Candela M, Nicoletti C, Kadi F, Battista G, Salvioli S, O’Toole PW, Franceschi C, Brigidi P, Turroni S, Santoro A. Elevated gut microbiome abundance of Christensenellaceae, Porphyromonadaceae and Rikenellaceae is associated with reduced visceral adipose tissue and healthier metabolic profile in Italian elderly. Gut Microbes. 2021; 13(1):1–19.
21. Garcia-Mantrana I, Selma-Royo M, Alcantara C, Collado MC. Shifts on gut microbiota associated to mediterranean diet adherence and specific dietary intakes on general adult population. Front Microbiol. 2018 May 7; 9(MAY).
22. Bressa C, Bailén-Andrino M, Pérez-Santiago J, González-Soltero R, Pérez M, Montalvo-Lominchar MG, Maté-Muñoz JL, Domínguez R, Moreno D, Larrosa M. Differences in gut microbiota profile between women with active lifestyle and sedentary women. Dasgupta S, editor. PLoS One. 2017 Feb 10; 12(2):e0171352.
23. Crovesy L, Masterson D, Rosado EL. Profile of the gut microbiota of adults with obesity: a systematic review. European Journal of Clinical Nutrition 2020 74:9. 2020 Mar 30; 74(9):1251–62.
24. Gupta RS, Bhandari V, Naushad HS. Molecular Signatures for the PVC Clade (Planctomycetes, Verrucomicrobia, Chlamydiae, and Lentisphaerae) of Bacteria Provide Insights into Their Evolutionary Relationships. Front Microbiol [Internet]. 2012 [cited 2023 Jul 10]; 3(SEP). Available from: https://pubmed.ncbi.nlm.nih.gov /23060863/
25. Shen X, Carlström M, Borniquel S, Jädert C, Kevil CG, Lundberg JO. Microbial regulation of host hydrogen sulfide bioavailability and metabolism. Free Radic Biol Med. 2013 Jul; 60:195–200.
26. Liang R, Zhang S, Peng X, Yang W, Xu Y, Wu P, Chen J, Cai Y, Zhou J. Characteristics of the gut microbiota in professional martial arts athletes: A comparison between different competition levels. PLoS One [Internet]. 2019 Dec 1 [cited 2023 Jul 10]; 14(12). Available from: https://pubmed .ncbi.nlm.nih.gov/31881037/
27. Muralidharan J, Moreno-Indias I, Bulló M, Lopez JV, Corella D, Castañer O, Vidal J, Atzeni A, Fernandez-García JC, Torres-Collado L, Fernández-Carrión R, Fito M, Olbeyra R, Gomez-Perez AM, Galiè S, Bernal-López MR, Martinez-Gonzalez MA, Salas-Salvadó J, Tinahones FJ. Effect on gut microbiota of a 1-y lifestyle intervention with Mediterranean diet compared with energy-reduced Mediterranean diet and physical activity promotion: PREDIMED-Plus Study. Am J Clin Nutr. 2021 May 21;
28. Cancello R, Turroni S, Rampelli S, Cattaldo S, Candela M, Cattani L, Mai S, Vietti R, Scacchi M, Brigidi P, Invitti C. Effect of Short-Term Dietary Intervention and Probiotic Mix Supplementation on the Gut Microbiota of Elderly Obese Women. Nutrients [Internet]. 2019 Dec 1 [cited 2023 Jul 10]; 11(12). Available from: https://pubmed.ncbi.nlm.nih.gov /31835452/
29. Gomez-Arango LF, Barrett HL, Wilkinson SA, Callaway LK, McIntyre HD, Morrison M, Dekker Nitert M. Low dietary fiber intake increases Collinsella abundance in the gut microbiota of overweight and obese pregnant women. Gut Microbes. 2018 May 4; 9(3):189–201.
30. Kasai C, Sugimoto K, Moritani I, Tanaka J, Oya Y, Inoue H, Tameda M, Shiraki K, Ito M, Takei Y, Takase K. Comparison of human gut microbiota in control subjects and patients with colorectal carcinoma in adenoma: Terminal restriction fragment length polymorphism and next-generation sequencing analyses. Oncol Rep. 2016 Jan 1; 35(1):325–33.
31. Quiroga R, Nistal E, Estébanez B, Porras D, Juárez-Fernández M, Martínez-Flórez S, García-Mediavilla MV, de Paz JA, González-Gallego J, Sánchez-Campos S, Cuevas MJ. Exercise training modulates the gut microbiota profile and impairs inflammatory signaling pathways in obese children. Exp Mol Med. 2020 Jul 1; 52(7):1048–61.
32. Eren AM, Sogin ML, Morrison HG, Vineis JH, Fisher JC, Newton RJ, McLellan SL. A single genus in the gut microbiome reflects host preference and specificity. ISME J [Internet]. 2015 Jan 11 [cited 2023 Jul 10]; 9(1):90–100. Available from: https://pubmed.ncbi.nlm .nih.gov/24936765/
33. Huang WC, Hsu YJ, Huang CC, Liu HC, Lee MC. Exercise Training Combined with Bifidobacterium Longum OLP01 Supplementation Improves Exercise Physiological Adaption and Performance. Nutrients. 2020 Apr 1; 12(4).
34. Castellanos N, Diez GG, Antúnez-Almagro C, Bressa C, Bailén M, González-Soltero R, Pérez M, Larrosa M. Key bacteria in the gut microbiota network for the transition between sedentary and active lifestyle. Microorganisms. 2020 May 1; 8(5).
35. Palmas V, Pisanu S, Madau V, Casula E, Deledda A, Cusano R, Uva P, Vascellari S, Loviselli A, Manzin A, Velluzzi F. Gut microbiota markers associated with obesity and overweight in Italian adults. Sci Rep. 2021 Dec 1; 11(1).
36. Lim MY, You HJ, Yoon HS, Kwon B, Lee JY, Lee S, Song YM, Lee K, Sung J, Ko G. The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut. 2017 Jun 1; 66(6):1031–8.
37. Manore MM. Effect of physical activity on thiamine, riboflavin, and vitamin B-6 requirements. Am J Clin Nutr. 2000 Aug 1; 72(2):598S-606S.
38. Yoshii K, Hosomi K, Sawane K, Kunisawa J. Metabolism of dietary and microbial vitamin b family in the regulation of host immunity. Vol. 6, Frontiers in Nutrition. Frontiers Media S.A.; 2019. p. 48.
39. Yu D, Yang Y, Long J, Xu W, Cai Q, Wu J, Cai H, Zheng W, Shu XO. Long-term Diet Quality and Gut Microbiome Functionality: A Prospective, Shotgun Metagenomic Study among Urban Chinese Adults. Curr Dev Nutr. 2021 Apr 29; 5(4).
40. Liu Y, Wang Y, Ni Y, Cheung CKY, Lam KSL, Wang Y, Xia Z, Ye D, Guo J, Tse MA, Panagiotou G, Xu A. Gut Microbiome Fermentation Determines the Efficacy of Exercise for Diabetes Prevention. Cell Metab. 2020 Jan 7; 31(1):77-91.e5.
Copyright: Institute of Sport. This is an Open Access article distributed under the terms of the Creative Commons CC BY License (https://creativecommons.org/licenses/by/4.0/). This license enables reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
 
Quick links
© 2024 Termedia Sp. z o.o.
Developed by Bentus.