Combined Physical Exercise and Diet: Regulation of Gut Microbiota to Prevent and Treat of Metabolic Disease: A Review
Abstract
:1. Introduction
2. Effect of Physical Exercise on Gut Microbiota
3. Effect of Diet on Gut Microbiota
3.1. Nutrients
3.1.1. Dietary Carbohydrates
3.1.2. Dietary Proteins
3.1.3. Dietary Fats
3.1.4. Other Dietary Components
3.2. Dietary Patterns
4. Gut Microbial Dysbiosis Linked to Metabolic Diseases
5. Combined Physical Exercise and Diet for Preventing Metabolic Diseases by Modulating Gut Microbiota
5.1. Evidence from Animal Studies
5.2. Evidence from Human Studies
5.3. Underlying Mechanisms
6. Conclusions and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Kramer, A. An overview of the beneficial effects of exercise on health and performance. Adv. Exp. Med. Biol. 2020, 1228, 3–22. [Google Scholar] [PubMed]
- Wu, N.N.; Tian, H.; Chen, P.; Wang, D.; Ren, J.; Zhang, Y. Physical exercise and selective autophagy: Benefit and risk on cardiovascular health. Cells 2019, 8, 1436. [Google Scholar] [CrossRef] [Green Version]
- Peeri, M.; Amiri, S. Protective effects of exercise in metabolic disorders are mediated by inhibition of mitochondrial-derived sterile inflammation. Med. Hypotheses 2015, 85, 707–709. [Google Scholar] [CrossRef] [PubMed]
- Jeong, J.; Park, H.; Kwon, S.; Jang, H.; Jun, J.; Kim, M.-W.; Lee, S.K.; Lee, K.; Lee, W.L. Effect of moderate exercise training and low-fat diet on peritoneal macrophage immunocompetence in high-fat diet-induced obese mice model. Phys. Act. Nutr. 2012, 16, 133–142. [Google Scholar] [CrossRef]
- Ejtahed, H.S.; Soroush, A.R.; Angoorani, P.; Larijani, B.; Hasani-Ranjbar, S. Gut microbiota as a target in the pathogenesis of metabolic disorders: A new approach to novel therapeutic agents. Horm. Metab. Res. 2016, 48, 349–358. [Google Scholar] [CrossRef] [Green Version]
- Mailing, L.J.; Allen, J.M.; Buford, T.W.; Fields, C.J.; Woods, J.A. Exercise and the gut microbiome: A review of the evidence, potential mechanisms, and implications for human health. Exerc. Sport Sci. Rev. 2019, 47, 75–85. [Google Scholar] [CrossRef]
- Chen, J.; Guo, Y.; Gui, Y.; Xu, D. Physical exercise, gut, gut microbiota, and atherosclerotic cardiovascular diseases. Lipids Health Dis. 2018, 17, 17. [Google Scholar] [CrossRef] [Green Version]
- Hughes, R.L. A review of the role of the gut microbiome in personalized sports nutrition. Front. Nutr. 2019, 6, 191. [Google Scholar] [CrossRef]
- Wolter, M.; Grant, E.T.; Boudaud, M.; Steimle, A.; Pereira, G.V.; Martens, E.C.; Desai, M.S. Leveraging diet to engineer the gut microbiome. Nat. Rev. Gastroenterol. Hepatol. 2021, 18, 885–902. [Google Scholar] [CrossRef]
- Cordero, A.; Masia, M.D.; Galve, E. Physical exercise and health. Rev. Esp. Cardiol. 2014, 67, 748–753. [Google Scholar] [CrossRef]
- Codella, R.; Luzi, L.; Terruzzi, I. Exercise has the guts: How physical activity may positively modulate gut microbiota in chronic and immune-based diseases. Dig. Liver Dis. 2018, 50, 331–341. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, Q.; Jiang, S.; Du, G. Effects of exercise frequency on the gut microbiota in elderly individuals. Microbiologyopen 2020, 9, e1053. [Google Scholar] [CrossRef] [PubMed]
- Clarke, S.F.; Murphy, E.F.; O’Sullivan, O.; Lucey, A.J.; Humphreys, M.; Hogan, A.; Hayes, P.; O’Reilly, M.; Jeffery, I.B.; Wood-Martin, R.; et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 2014, 63, 1913–1920. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bressa, C.; Bailen-Andrino, M.; Perez-Santiago, J.; Gonzalez-Soltero, R.; Perez, M.; Montalvo-Lominchar, M.G.; Mate-Munoz, J.L.; Dominguez, R.; Moreno, D.; Larrosa, M. Differences in gut microbiota profile between women with active lifestyle and sedentary women. PLoS ONE 2017, 12, e0171352. [Google Scholar] [CrossRef] [Green Version]
- Peng, L.; Li, Z.R.; Green, R.S.; Holzman, I.R.; Lin, J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J. Nutr. 2009, 139, 1619–1625. [Google Scholar] [CrossRef] [Green Version]
- Matsumoto, M.; Inoue, R.; Tsukahara, T.; Ushida, K.; Chiji, H.; Matsubara, N.; Hara, H. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci. Biotechnol. Biochem. 2008, 72, 572–576. [Google Scholar] [CrossRef]
- Canani, R.B.; Costanzo, M.D.; Leone, L.; Pedata, M.; Meli, R.; Calignano, A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroenterol. 2011, 17, 1519–1528. [Google Scholar] [CrossRef]
- Liu, T.W.; Park, Y.M.; Holscher, H.D.; Padilla, J.; Scroggins, R.J.; Welly, R.; Britton, S.L.; Koch, L.G.; Vieira-Potter, V.J.; Swanson, K.S. Physical activity differentially affects the cecal microbiota of ovariectomized female rats selectively bred for high and low aerobic capacity. PLoS ONE 2015, 10, e0136150. [Google Scholar] [CrossRef] [Green Version]
- Luo, B.; Xiang, D.; Nieman, D.C.; Chen, P. The effects of moderate exercise on chronic stress-induced intestinal barrier dysfunction and antimicrobial defense. Brain Behav. Immun. 2014, 39, 99–106. [Google Scholar] [CrossRef]
- de Oliveira, E.P.; Burini, R.C. The impact of physical exercise on the gastrointestinal tract. Curr. Opin. Clin. Nutr. Metab. Care 2009, 12, 533–538. [Google Scholar] [CrossRef]
- Karl, J.P.; Margolis, L.M.; Madslien, E.H.; Murphy, N.E.; Castellani, J.W.; Gundersen, Y.; Hoke, A.V.; Levangie, M.W.; Kumar, R.; Chakraborty, N.; et al. Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress. Am. J. Physiol. Gastrointest. Liver Physiol. 2017, 312, G559–G571. [Google Scholar] [CrossRef] [Green Version]
- Gutekunst, K.; Kruger, K.; August, C.; Diener, M.; Mooren, F.C. Acute exercises induce disorders of the gastrointestinal integrity in a murine model. Eur. J. Appl. Physiol. 2014, 114, 609–617. [Google Scholar] [CrossRef] [PubMed]
- Kumar, J.; Rani, K.; Datt, C. Molecular link between dietary fibre, gut microbiota and health. Mol. Biol. Rep. 2020, 47, 6229–6237. [Google Scholar] [CrossRef] [PubMed]
- Gentile, C.L.; Weir, T.L. The gut microbiota at the intersection of diet and human health. Science 2018, 362, 776–780. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sonnenburg, E.D.; Smits, S.A.; Tikhonov, M.; Higginbottom, S.K.; Wingreen, N.S.; Sonnenburg, J.L. Diet-induced extinctions in the gut microbiota compound over generations. Nature 2016, 529, 212–215. [Google Scholar] [CrossRef] [Green Version]
- Moszak, M.; Szulinska, M.; Bogdanski, P. You are what you eat-the relationship between diet, microbiota, and metabolic disorders-a review. Nutrients 2020, 12, 1096. [Google Scholar] [CrossRef] [Green Version]
- Sun, Y.; Zhang, Z.; Cheng, L.; Zhang, X.; Liu, Y.; Zhang, R.; Weng, P.; Wu, Z. Polysaccharides confer benefits in immune regulation and multiple sclerosis by interacting with gut microbiota. Food Res. Int. 2021, 149, 110675. [Google Scholar] [CrossRef] [PubMed]
- Li, M.; Yue, H.; Wang, Y.; Guo, C.; Du, Z.; Jin, C.; Ding, K. Intestinal microbes derived butyrate is related to the immunomodulatory activities of Dendrobium officinale polysaccharide. Int. J. Biol. Macromol. 2020, 149, 717–723. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.J.; Li, Q.M.; Zha, X.Q.; Luo, J.P. Dendrobium fimbriatum Hook polysaccharide ameliorates dextran-sodium-sulfate-induced colitis in mice via improving intestinal barrier function, modulating intestinal microbiota, and reducing oxidative stress and inflammatory responses. Food Funct. 2022, 13, 143–160. [Google Scholar] [CrossRef]
- Yan, T.; Wang, N.; Liu, B.; Wu, B.; Xiao, F.; He, B.; Jia, Y. Schisandra chinensis ameliorates depressive-like behaviors by regulating microbiota-gut-brain axis via its anti-inflammation activity. Phytother. Res. 2021, 35, 289–296. [Google Scholar] [CrossRef]
- Zhang, Q.; Yu, H.; Xiao, X.; Hu, L.; Xin, F.; Yu, X. Inulin-type fructan improves diabetic phenotype and gut microbiota profiles in rats. PeerJ. 2018, 6, e4446. [Google Scholar] [CrossRef] [PubMed]
- Makki, K.; Deehan, E.C.; Walter, J.; Backhed, F. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe 2018, 23, 705–715. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- World Health Organization. Protein and Amino Acid Requirements in Human Nutrition; World Health Organization: Geneva, Switzerland, 2007; pp. 1–265. [Google Scholar]
- Chen, X.; Song, P.; Fan, P.; He, T.; Jacobs, D.; Levesque, C.L.; Johnston, L.J.; Ji, L.; Ma, N.; Chen, Y.; et al. Moderate dietary protein restriction optimized gut microbiota and mucosal barrier in growing pig model. Front. Cell Infect. Microbiol. 2018, 8, 246. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mu, C.; Yang, Y.; Luo, Z.; Guan, L.; Zhu, W. The colonic microbiome and epithelial transcriptome are altered in rats fed a high-protein diet compared with a normal-protein diet. J. Nutr. 2016, 146, 474–483. [Google Scholar] [CrossRef] [Green Version]
- Johns, D.J.; Hartmann-Boyce, J.; Jebb, S.A.; Aveyard, P. Behavioural weight management review. Diet or exercise interventions vs combined behavioral weight management programs: A systematic review and meta-analysis of direct comparisons. J. Acad. Nutr. Diet 2014, 114, 1557–1568. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Koeth, R.A.; Wang, Z.; Levison, B.S.; Buffa, J.A.; Org, E.; Sheehy, B.T.; Britt, E.B.; Fu, X.; Wu, Y.; Li, L.; et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat. Med. 2013, 19, 576–585. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tang, W.H.; Hazen, S.L. The contributory role of gut microbiota in cardiovascular disease. J. Clin. Investig. 2014, 124, 4204–4211. [Google Scholar] [CrossRef] [Green Version]
- Karlund, A.; Gomez-Gallego, C.; Turpeinen, A.M.; Palo-Oja, O.M.; El-Nezami, H.; Kolehmainen, M. Protein supplements and their relation with nutrition, microbiota composition and health: Is more protein always better for sportspeople? Nutrients 2019, 11, 829. [Google Scholar] [CrossRef] [Green Version]
- Rodriguez, N.R.; DiMarco, N.M.; Langley, S.; American Dietetic Association; Dietitians of Canada; American College of Sports Medicine: Nutrition; Performance, A. Position of the American dietetic association, dietitians of Canada, and the American College of Sports Medicine: Nutrition and athletic performance. J. Am. Diet Assoc. 2009, 109, 509–527. [Google Scholar]
- Lagowska, K.; Kapczuk, K.; Friebe, Z.; Bajerska, J. Effects of dietary intervention in young female athletes with menstrual disorders. J. Int. Soc. Sports Nutr. 2014, 11, 21. [Google Scholar] [CrossRef] [Green Version]
- Coelho, O.G.L.; Candido, F.G.; Alfenas, R.C.G. Dietary fat and gut microbiota: Mechanisms involved in obesity control. Crit. Rev. Food Sci. Nutr. 2019, 59, 3045–3053. [Google Scholar] [CrossRef] [PubMed]
- de Wit, N.; Derrien, M.; Bosch-Vermeulen, H.; Oosterink, E.; Keshtkar, S.; Duval, C.; de Vogel-van den Bosch, J.; Kleerebezem, M.; Muller, M.; van der Meer, R. Saturated fat stimulates obesity and hepatic steatosis and affects gut microbiota composition by an enhanced overflow of dietary fat to the distal intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 303, G589–G599. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.; Cui, Y.; Zhu, S.; Feng, F.; Zheng, X. Characterization and antimicrobial activity of a pharmaceutical microemulsion. Int. J. Pharm. 2010, 395, 154–160. [Google Scholar] [CrossRef]
- Parolini, C.; Bjorndal, B.; Busnelli, M.; Manzini, S.; Ganzetti, G.S.; Dellera, F.; Ramsvik, M.; Bruheim, I.; Berge, R.K.; Chiesa, G. Effect of dietary components from antarctic krill on atherosclerosis in apoE-deficient mice. Mol. Nutr. Food Res. 2017, 61, 10. [Google Scholar] [CrossRef]
- Usuda, H.; Okamoto, T.; Wada, K. Leaky gut: Effect of dietary fiber and fats on microbiome and intestinal barrier. Int. J. Mol. Sci. 2021, 22, 7613. [Google Scholar] [CrossRef] [PubMed]
- Boroni Moreira, A.P.; de Cassia Goncalves Alfenas, R. The influence of endotoxemia on the molecular mechanisms of insulin resistance. Nutr. Hosp. 2012, 27, 382–390. [Google Scholar] [PubMed]
- Yang, Q.; Liang, Q.; Balakrishnan, B.; Belobrajdic, D.P.; Feng, Q.J.; Zhang, W. Role of dietary nutrients in the modulation of gut microbiota: A narrative review. Nutrients 2020, 12, 381. [Google Scholar] [CrossRef] [Green Version]
- Grober, U.; Schmidt, J.; Kisters, K. Magnesium in prevention and therapy. Nutrients 2015, 7, 8199–8226. [Google Scholar] [CrossRef] [Green Version]
- Pachikian, B.D.; Neyrinck, A.M.; Deldicque, L.; De Backer, F.C.; Catry, E.; Dewulf, E.M.; Sohet, F.M.; Bindels, L.B.; Everard, A.; Francaux, M.; et al. Changes in intestinal bifidobacteria levels are associated with the inflammatory response in magnesium-deficient mice. J. Nutr. 2010, 140, 509–514. [Google Scholar] [CrossRef] [Green Version]
- Tomas-Barberan, F.A.; Selma, M.V.; Espin, J.C. Interactions of gut microbiota with dietary polyphenols and consequences to human health. Curr. Opin. Clin. Nutr. Metab. Care 2016, 19, 471–476. [Google Scholar] [CrossRef]
- Aron-Wisnewsky, J.; Warmbrunn, M.V.; Nieuwdorp, M.; Clement, K. Nonalcoholic fatty liver disease: Modulating gut microbiota to improve severity? Gastroenterology 2020, 158, 1881–1898. [Google Scholar] [CrossRef] [PubMed]
- Zinocker, M.K.; Lindseth, I.A. The Western diet-microbiome-host interaction and its role in metabolic disease. Nutrients 2018, 10, 365. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garcia-Montero, C.; Fraile-Martinez, O.; Gomez-Lahoz, A.M.; Pekarek, L.; Castellanos, A.J.; Noguerales-Fraguas, F.; Coca, S.; Guijarro, L.G.; Garcia-Honduvilla, N.; Asunsolo, A.; et al. Nutritional components in Western diet versus Mediterranean diet at the gut microbiota-immune system interplay. Implications for health and disease. Nutrients 2021, 13, 699. [Google Scholar] [CrossRef] [PubMed]
- Martinez-Gonzalez, M.A.; Salas-Salvado, J.; Estruch, R.; Corella, D.; Fito, M.; Ros, E.; Predimed, I. Benefits of the Mediterranean diet: Insights from the PREDIMED study. Prog. Cardiovasc. Dis. 2015, 58, 50–60. [Google Scholar] [CrossRef] [Green Version]
- Haro, C.; Garcia-Carpintero, S.; Alcala-Diaz, J.F.; Gomez-Delgado, F.; Delgado-Lista, J.; Perez-Martinez, P.; Rangel Zuniga, O.A.; Quintana-Navarro, G.M.; Landa, B.B.; Clemente, J.C.; et al. The gut microbial community in metabolic syndrome patients is modified by diet. J. Nutr. Biochem. 2016, 27, 27–31. [Google Scholar] [CrossRef]
- Kong, C.; Yan, X.; Liu, Y.; Huang, L.; Zhu, Y.; He, J.; Gao, R.; Kalady, M.F.; Goel, A.; Qin, H.; et al. Ketogenic diet alleviates colitis by reduction of colonic group 3 innate lymphoid cells through altering gut microbiome. Signal Transduct. Target Ther. 2021, 6, 154. [Google Scholar] [CrossRef]
- Nowosad, K.; Sujka, M. Effect of various types of intermittent fasting (IF) on weight loss and improvement of diabetic parameters in human. Curr. Nutr. Rep. 2021, 10, 146–154. [Google Scholar] [CrossRef]
- Zhang, M.; Zhao, D.; Zhou, G.; Li, C. Dietary pattern, gut microbiota, and Alzheimer’s disease. J. Agric. Food. Chem. 2020, 68, 12800–12809. [Google Scholar] [CrossRef]
- Cignarella, F.; Cantoni, C.; Ghezzi, L.; Salter, A.; Dorsett, Y.; Chen, L.; Phillips, D.; Weinstock, G.M.; Fontana, L.; Cross, A.H.; et al. Intermittent fasting confers protection in CNS autoimmunity by altering the gut microbiota. Cell Metab. 2018, 27, 1222–1235.e6. [Google Scholar] [CrossRef] [Green Version]
- Christ, A.; Lauterbach, M.; Latz, E. Western diet and the immune system: An inflammatory connection. Immunity 2019, 51, 794–811. [Google Scholar] [CrossRef]
- Hatori, M.; Vollmers, C.; Zarrinpar, A.; DiTacchio, L.; Bushong, E.A.; Gill, S.; Leblanc, M.; Chaix, A.; Joens, M.; Fitzpatrick, J.A.; et al. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab. 2012, 15, 848–860. [Google Scholar] [CrossRef] [PubMed]
- Hargreaves, S.M.; Raposo, A.; Saraiva, A.; Zandonadi, R.P. Vegetarian diet: An overview through the perspective of quality of life domains. Int. J. Environ. Res. Public Health 2021, 18, 4067. [Google Scholar] [CrossRef] [PubMed]
- Rinninella, E.; Cintoni, M.; Raoul, P.; Lopetuso, L.R.; Scaldaferri, F.; Pulcini, G.; Miggiano, G.A.D.; Gasbarrini, A.; Mele, M.C. Food components and dietary habits: Keys for a healthy gut microbiota composition. Nutrients 2019, 11, 2393. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Backhed, F.; Ding, H.; Wang, T.; Hooper, L.V.; Koh, G.Y.; Nagy, A.; Semenkovich, C.F.; Gordon, J.I. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 2004, 101, 15718–15723. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Turnbaugh, P.J.; Ley, R.E.; Mahowald, M.A.; Magrini, V.; Mardis, E.R.; Gordon, J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444, 1027–1031. [Google Scholar] [CrossRef]
- Turnbaugh, P.J.; Baeckhed, F.; Fulton, L.; Gordon, J.I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008, 3, 213–223. [Google Scholar] [CrossRef] [Green Version]
- Kasai, C.; Sugimoto, K.; Moritani, I.; Tanaka, J.; Oya, Y.; Inoue, H.; Tameda, M.; Shiraki, K.; Ito, M.; Takei, Y.; et al. Comparison of the gut microbiota composition between obese and non-obese individuals in a Japanese population, as analyzed by terminal restriction fragment length polymorphism and next-generation sequencing. BMC Gastroenterol. 2015, 15, 100. [Google Scholar] [CrossRef] [Green Version]
- Bervoets, L.; Van Hoorenbeeck, K.; Kortleven, I.; Van Noten, C.; Hens, N.; Vael, C.; Goossens, H.; Desager, K.N.; Vankerckhoven, V. Differences in gut microbiota composition between obese and lean children: A cross-sectional study. Gut Pathog. 2013, 5, 10. [Google Scholar] [CrossRef] [Green Version]
- Liu, R.; Hong, J.; Xu, X.; Feng, Q.; Zhang, D.; Gu, Y.; Shi, J.; Zhao, S.; Liu, W.; Wang, X.; et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat. Med. 2017, 23, 859–868. [Google Scholar] [CrossRef]
- Wang, X.K.; Xu, X.Q.; Xia, Y. Further analysis reveals new gut microbiome markers of type 2 diabetes mellitus. Anton. Leeuw. Int. J. G. 2017, 110, 445–453. [Google Scholar] [CrossRef]
- Larsen, N.; Vogensen, F.K.; van den Berg, F.W.J.; Nielsen, D.S.; Andreasen, A.S.; Pedersen, B.K.; Abu Al-Soud, W.; Sorensen, S.J.; Hansen, L.H.; Jakobsen, M. Gut microbiota in Hhuman adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 2010, 5, e9085. [Google Scholar] [CrossRef] [PubMed]
- Thaiss, C.A.; Levy, M.; Grosheva, I.; Zheng, D.P.; Soffer, E.; Blacher, E.; Braverman, S.; Tengeler, A.C.; Barak, O.; Elazar, M.; et al. Hyperglycemia drives intestinal barrier dysfunction and risk for enteric infection. Science 2018, 359, 1376–1383. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jensen, A.B.; Sorensen, T.I.A.; Pedersen, O.; Jess, T.; Brunak, S.; Allin, K.H. Increase in clinically recorded type 2 diabetes after colectomy. Elife 2018, 7, e37420. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.; Wang, X.; Feng, W.; Liu, Q.; Zhou, S.; Liu, Q.; Cai, L. The gut microbiota and its interactions with cardiovascular disease. Microb. Biotechnol. 2020, 13, 637–656. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Koren, O.; Spor, A.; Felin, J.; Fak, F.; Stombaugh, J.; Tremaroli, V.; Behre, C.J.; Knight, R.; Fagerberg, B.; Ley, R.E.; et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc. Natl. Acad. Sci. USA 2011, 108 (Suppl. 1), 4592–4598. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jie, Z.Y.; Xia, H.H.; Zhong, S.L.; Feng, Q.; Li, S.H.; Liang, S.S.; Zhong, H.Z.; Liu, Z.P.; Gao, Y.; Zhao, H.; et al. The gut microbiome in atherosclerotic cardiovascular disease. Nat. Commun. 2017, 8, 845. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Emoto, T.; Yamashita, T.; Kobayashi, T.; Sasaki, N.; Hirota, Y.; Hayashi, T.; So, A.; Kasahara, K.; Yodoi, K.; Matsumoto, T.; et al. Characterization of gut microbiota profiles in coronary artery disease patients using data mining analysis of terminal restriction fragment length polymorphism: Gut microbiota could be a diagnostic marker of coronary artery disease. Heart Vessels 2017, 32, 39–46. [Google Scholar] [CrossRef]
- Witkowski, M.; Weeks, T.L.; Hazen, S.L. Gut microbiota and cardiovascular disease. Circ. Res. 2020, 127, 553–570. [Google Scholar] [CrossRef]
- Rauchhaus, M.; Doehner, W.; Francis, D.P.; Davos, C.; Kemp, M.; Liebenthal, C.; Niebauer, J.; Hooper, J.; Volk, H.D.; Coats, A.J.; et al. Plasma cytokine parameters and mortality in patients with chronic heart failure. Circulation 2000, 102, 3060–3067. [Google Scholar] [CrossRef] [Green Version]
- Yang, G.; Wei, J.; Liu, P.; Zhang, Q.; Tian, Y.; Hou, G.; Meng, L.; Xin, Y.; Jiang, X. Role of the gut microbiota in type 2 diabetes and related diseases. Metabolism 2021, 117, 154712. [Google Scholar] [CrossRef]
- Jiang, W.; Wu, N.; Wang, X.; Chi, Y.; Zhang, Y.; Qiu, X.; Hu, Y.; Li, J.; Liu, Y. Dysbiosis gut microbiota associated with inflammation and impaired mucosal immune function in intestine of humans with non-alcoholic fatty liver disease. Sci. Rep. 2015, 5, 8096. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raman, M.; Ahmed, I.; Gillevet, P.M.; Probert, C.S.; Ratcliffe, N.M.; Smith, S.; Greenwood, R.; Sikaroodi, M.; Lam, V.; Crotty, P.; et al. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin. Gastroenterol. Hepatol. 2013, 11, 868–875.e1–3. [Google Scholar] [CrossRef] [PubMed]
- Del Chierico, F.; Nobili, V.; Vernocchi, P.; Russo, A.; De Stefanis, C.; Gnani, D.; Furlanello, C.; Zandona, A.; Paci, P.; Capuani, G.; et al. Gut microbiota profiling of pediatric nonalcoholic fatty liver disease and obese patients unveiled by an integrated meta-omics-based approach. Hepatology 2017, 65, 451–464. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sohail, M.U.; Yassine, H.M.; Sohail, A.; Thani, A.A.A. Impact of physical exercise on gut microbiome, inflammation, and the pathobiology of metabolic disorders. Rev. Diabet. Stud. 2019, 15, 35–48. [Google Scholar] [CrossRef] [Green Version]
- Denou, E.; Marcinko, K.; Surette, M.G.; Steinberg, G.R.; Schertzer, J.D. High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity. Am. J. Physiol. Endocrinol. Metab. 2016, 310, E982–E993. [Google Scholar] [CrossRef] [Green Version]
- Cho, J.A.; Park, S.H.; Cho, J.; Kim, J.O.; Yoon, J.H.; Park, E. Exercise and curcumin in combination improves cognitive function and attenuates ER stress in diabetic rats. Nutrients 2020, 12, 1309. [Google Scholar] [CrossRef]
- Ortega-Santos, C.P.; Al-Nakkash, L.; Whisner, C.M. Exercise and/or genistein treatment impact gut microbiota and inflammation after 12 weeks on a high-fat, high-sugar diet in C57BL/6 mice. Nutrients 2020, 12, 3410. [Google Scholar] [CrossRef]
- Wu, T.; Gao, X.; Chen, M.; van Dam, R.M. Long-term effectiveness of diet-plus-exercise interventions vs. diet-only interventions for weight loss: A meta-analysis. Obes. Rev. 2009, 10, 313–323. [Google Scholar] [CrossRef]
- Foster-Schubert, K.E.; Alfano, C.M.; Duggan, C.R.; Xiao, L.; Campbell, K.L.; Kong, A.; Bain, C.E.; Wang, C.Y.; Blackburn, G.L.; McTiernan, A. Effect of diet and exercise, alone or combined, on weight and body composition in overweight-to-obese postmenopausal women. Obesity 2012, 20, 1628–1638. [Google Scholar] [CrossRef] [Green Version]
- Liu, W.Y.; Lu, D.J.; Du, X.M.; Sun, J.Q.; Ge, J.; Wang, R.W.; Wang, R.; Zou, J.; Xu, C.; Ren, J.; et al. Effect of aerobic exercise and low carbohydrate diet on pre-diabetic non-alcoholic fatty liver disease in postmenopausal women and middle aged men--the role of gut microbiota composition: Study protocol for the AELC randomized controlled trial. BMC Public Health 2014, 14, 48. [Google Scholar] [CrossRef] [Green Version]
- Sun, S.; Kong, Z.; Shi, Q.; Zhang, H.; Lei, O.K.; Nie, J. Carbohydrate restriction with or without exercise training improves blood pressure and insulin sensitivity in overweight women. Healthcare 2021, 9, 637. [Google Scholar] [CrossRef] [PubMed]
- Sun, S.; Lei, O.K.; Nie, J.; Shi, Q.; Xu, Y.; Kong, Z. Effects of low-carbohydrate diet and exercise training on gut microbiota. Front. Nutr. 2022, 9, 884550. [Google Scholar] [CrossRef] [PubMed]
- Cheng, R.; Wang, L.; Le, S.; Yang, Y.; Zhao, C.; Zhang, X.; Yang, X.; Xu, T.; Xu, L.; Wiklund, P.; et al. A randomized controlled trial for response of microbiome network to exercise and diet intervention in patients with nonalcoholic fatty liver disease. Nat. Commun. 2022, 13, 2555. [Google Scholar] [CrossRef] [PubMed]
- Wilson, R.L.; Kang, D.W.; Christopher, C.N.; Crane, T.E.; Dieli-Conwright, C.M. Fasting and exercise in oncology: Potential synergism of combined interventions. Nutrients 2021, 13, 3421. [Google Scholar] [CrossRef]
- Hansen, D.; De Strijcker, D.; Calders, P. Impact of endurance exercise training in the fasted state on muscle biochemistry and metabolism in healthy subjects: Can these effects be of particular clinical benefit to type 2 diabetes mellitus and insulin-resistant patients? Sports Med. 2017, 47, 415–428. [Google Scholar] [CrossRef]
- Julio-Pieper, M.; Bravo, J.A.; Aliaga, E.; Gotteland, M. Review article: Intestinal barrier dysfunction and central nervous system disorders--a controversial association. Aliment. Pharmacol. Ther. 2014, 40, 1187–1201. [Google Scholar] [CrossRef]
- Campbell, S.C.; Wisniewski, P.J., 2nd. Exercise is a novel promoter of intestinal health and microbial diversity. Exerc. Sport Sci. Rev. 2017, 45, 41–47. [Google Scholar] [CrossRef]
- Campbell, S.C.; Wisniewski, P.J.; Noji, M.; McGuinness, L.R.; Haggblom, M.M.; Lightfoot, S.A.; Joseph, L.B.; Kerkhof, L.J. The effect of diet and exercise on intestinal integrity and microbial diversity in mice. PLoS ONE 2016, 11, e0150502. [Google Scholar] [CrossRef] [Green Version]
- Agus, A.; Clement, K.; Sokol, H. Gut microbiota-derived metabolites as central regulators in metabolic disorders. Gut 2021, 70, 1174–1182. [Google Scholar] [CrossRef]
- Lai, Z.L.; Tseng, C.H.; Ho, H.J.; Cheung, C.K.Y.; Lin, J.Y.; Chen, Y.J.; Cheng, F.C.; Hsu, Y.C.; Lin, J.T.; El-Omar, E.M.; et al. Fecal microbiota transplantation confers beneficial metabolic effects of diet and exercise on diet-induced obese mice. Sci. Rep. 2018, 8, 15625. [Google Scholar] [CrossRef]
Dietary Pattern | Characteristic | Changes of Gut Microbiota | Effect | Reference |
---|---|---|---|---|
WD | High consumption of saturated and trans fatty acids, refined grains, sugar, salt, alcohol and other harmful elements; Low content of complex dietary fiber. | Firmicutes/Bacteroidetes ratio↑ Alistipes↑ Bilophila↑ Bifidobacteria↓ | Systemic chronic inflammation and LPS translocation; Increase the risk of disease. | [61] |
MD | High intake of whole grains and vegetables; Use olive oil as the lipid supply; A regular but moderate consumption of fish and other meat, dairy products and red wine. | Bifidobacteria↑ Lactobacillus↑ Clostridium↑ Faecalibacterium↑ Oscillospira↑ Ruminococcus↓ Coprococcus↓ | Improve the gut barrier integrity; Protect against oxidative stress and inflammation; Reduce the total mortality and the risk of cardiovascular, metabolic and gastrointestinal diseases. | [56] |
KD | High-fat, adequate-protein, and low-carbohydrate. | Akkermansia↑ Parabacteroides↑ Escherichia↓ Shigella↓ | Nutritionally inadequate in fiber, necessary vitamins, minerals, and iron. | [57] |
IF | Manipulate meal time to improve body composition and overall health, including of time-restricted feeding, alternate day fasting, and religious fasting. | Akkermansia↑ Lactobacillus↑ Desulfovibrio↓ Turicibacter↓ | Improve gut epithelial integrity, the leaking LPS and blunted systemic inflammation; Improve metabolic profiles and reduce the risk of obesity, obesity-related conditions. | [62] |
VD | Reduce or restrict of animal-derived foods; High intake of plant-source foods. | Bacteroides/Prevotella ratio↑ Clostridium↑ Faecalibacterium↑ Bifidobacteria↓ | Reduce of caloric intake but nutritional deficiency of fatty acids, proteins, vitamins, and minerals; Prevent and better control of chronic diseases. | [63] |
GD | The exclusion of gluten-containing cereals like wheat, rye, barley and hybrids. | Bifidobacterium ↓ Lactobacillus↓ Enterobacteriaceae↑ Escherichia coli↑ | Appropriate for treatment of celiac disease, dermatitis herpetiformis and gluten ataxia. | [64] |
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Zhang, L.; Liu, Y.; Sun, Y.; Zhang, X. Combined Physical Exercise and Diet: Regulation of Gut Microbiota to Prevent and Treat of Metabolic Disease: A Review. Nutrients 2022, 14, 4774. https://doi.org/10.3390/nu14224774
Zhang L, Liu Y, Sun Y, Zhang X. Combined Physical Exercise and Diet: Regulation of Gut Microbiota to Prevent and Treat of Metabolic Disease: A Review. Nutrients. 2022; 14(22):4774. https://doi.org/10.3390/nu14224774
Chicago/Turabian StyleZhang, Li, Yuan Liu, Ying Sun, and Xin Zhang. 2022. "Combined Physical Exercise and Diet: Regulation of Gut Microbiota to Prevent and Treat of Metabolic Disease: A Review" Nutrients 14, no. 22: 4774. https://doi.org/10.3390/nu14224774
APA StyleZhang, L., Liu, Y., Sun, Y., & Zhang, X. (2022). Combined Physical Exercise and Diet: Regulation of Gut Microbiota to Prevent and Treat of Metabolic Disease: A Review. Nutrients, 14(22), 4774. https://doi.org/10.3390/nu14224774