Physical activity differentially affects the cecal microbiota of ovariectomized female rats selectively bred for high and low aerobic capacity
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The gut microbiota is considered a relevant factor in obesity and associated metabolic diseases, for which postmenopausal women are particularly at risk. Increasing physical activity has been recognized as an efficacious approach to prevent or treat obesity, yet the impact of physical activity on the microbiota remains under-investigated. We examined the impacts of voluntary exercise on host metabolism and gut microbiota in ovariectomized (OVX) high capacity (HCR) and low capacity running (LCR) rats. HCR and LCR rats (age = 27 wk) were OVX and fed a high-fat diet (45% kcal fat) ad libitum and housed in cages equipped with (exercise, EX) or without (sedentary, SED) running wheels for 11 wk (n = 7-8/group). We hypothesized that increased physical activity would hinder weight gain, increase metabolic health and shift the microbiota of LCR rats, resulting in populations more similar to that of HCR rats. Animals were compared for characteristic metabolic parameters including body composition, lipid profile and energy expenditure; whereas cecal digesta were collected for DNA extraction. 16S rRNA gene-based amplicon Illumina MiSeq sequencing was performed, followed by analysis using QIIME 1.8.0 to assess cecal microbiota. Voluntary exercise decreased body and fat mass, and normalized fasting NEFA concentrations of LCR rats, despite only running one-third the distance of HCR rats. Exercise, however, increased food intake, weight gain and fat mass of HCR rats. Exercise clustered the gut microbial community of LCR rats, which separated them from the other groups. Assessments of specific taxa revealed significant (p<0.05) line by exercise interactions including shifts in the abundances of Firmicutes, Proteobacteria, and Cyanobacteria. Relative abundance of Christensenellaceae family was higher (p = 0.026) in HCR than LCR rats, and positively correlated (p<0.05) with food intake, body weight and running distance. These findings demonstrate that exercise differentially impacts host metabolism and gut microbial communities of female HCR and LCR rats without ovarian function.
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Exercise decreased Proteobacteria in rats with high aerobic capacity.
“In agreement with our findings, exercise decreased Proteobacteria in rats with high aerobic capacity (Liu et al., 2015).”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Liu et al., 2015
In rats, unidentified Desulfovibrionaceae decreased in response to voluntary exercise.
“and in rats the latter decreased in response to voluntary exercise (Liu et al., 2015).”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Liu et al., 2015
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QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887 · see citing works
An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444 · see citing works
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., & Andersen, G. L. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.03006-05 · Cited by 10,891 · see citing works
Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Lozupone, C., Turnbaugh, P. J., Fierer, N., & Knight, R. D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000080107 · Cited by 9,633 · see citing works
Human gut microbes associated with obesity
Ley, R. E., Turnbaugh, P. J., Klein, S., & Gordon, J. I. (2006) · Nature · doi:10.1038/4441022a · Cited by 8,785 · see citing works
Prevalence of Childhood and Adult Obesity in the United States, 2011-2012
Ogden, C. L., Carroll, M. D., Kit, B. K., & Flegal, K. M. (2014) · JAMA · doi:10.1001/jama.2014.732 · Cited by 8,072 · see citing works
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823 · see citing works
Official Methods of Analysis of the Association of Official Analytical Chemists
(1971) · Journal of Pharmaceutical Sciences · doi:10.1002/jps.2600600253 · Cited by 6,406 · see citing works
Official Methods of Analysis of the Association of Official Analytical Chemists
(1971) · Soil Science Society of America Journal · doi:10.2136/sssaj1971.03615995003500050003x · Cited by 6,367 · see citing works
Obesity alters gut microbial ecology
Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., & Gordon, J. I. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504978102 · Cited by 6,176 · see citing works
Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010.
Flegal, K., Carroll, M., Kit, B., & Ogden, C. (2012) · Journal of the American Medical Association (JAMA) · doi:10.1001/jama.2012.39 · Cited by 5,523 · see citing works
Exercise capacity and mortality among men referred for exercise testing
Myers, J., Prakash, M., Froelicher, V., Do, D., Partington, S., & Atwood, J. E. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa011858 · Cited by 4,114 · see citing works
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888 · see citing works
Human Genetics Shape the Gut Microbiome
Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., Beaumont, M., Van Treuren, W., Knight, R., Bell, J. T., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.053 · Cited by 3,164 · see citing works
Gut Microbiota in Human Adults with Type 2 Diabetes Differs from Non-Diabetic Adults
Larsen, N., Vogensen, F. K., van den Berg, F. W. J., Nielsen, D. S., Andreasen, A. S., Pedersen, B. K., Al-Soud, W. A., Sørensen, S. J., Hansen, L. H., & Jakobsen, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009085 · Cited by 2,952 · see citing works
Turnbaugh, P. J., Bäckhed, F., Fulton, L., & Gordon, J. I. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.02.015 · Cited by 2,915 · see citing works
Johansson, M., Larsson, J. M. H., & Hansson, G. C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006451107 · Cited by 1,459 · see citing works
Exercise and associated dietary extremes impact on gut microbial diversity
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. (2014) · Gut · doi:10.1136/gutjnl-2013-306541 · Cited by 1,439 · see citing works
Neufeld, K. M., Kang, N., Bienenstock, J., & Foster, J. A. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01620.x · Cited by 1,392 · see citing works
The core gut microbiome, energy balance and obesity
Turnbaugh, P. J., & Gordon, J. I. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.174136 · Cited by 993 · see citing works
Fitzgerald, K. R. (2013) · Journal of Vascular Nursing · doi:10.1016/j.jvn.2013.06.004 · Cited by 875 · see citing works
Sonnenburg, E. D., Zheng, H., Joglekar, P., Higginbottom, S. K., Firbank, S. J., Bolam, D. N., & Sonnenburg, J. L. (2010) · Cell · doi:10.1016/j.cell.2010.05.005 · Cited by 745 · see citing works
Cardiovascular risk factors emerge after artificial selection for low aerobic capacity.
Wisløff, U., Najjar, S. M., Ellingsen, Ø., Haram, P. M., Swoap, S., Al-Share, Q., Fernström, M., Rezaei, K., Lee, S. J., Koch, L. G., et al. (2005) · Science · doi:10.1126/science.1108177 · Cited by 657 · see citing works
Self-citationEvans, C. C., LePard, K. J., Kwak, J. W., Stancukas, M. C., Laskowski, S., Dougherty, J., Moulton, L., Glawe, A., Wang, Y., Leone, V., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092193 · Cited by 587 · see citing works
Exercise-Induced Splanchnic Hypoperfusion Results in Gut Dysfunction in Healthy Men
van Wijck, K., Lenaerts, K., van Loon, L. J. C., Peters, W. H. M., Buurman, W. A., & Dejong, C. H. C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022366 · Cited by 359 · cited 2× · see citing works
“High-intensity exercise redirects blood flow to the active tissues such as skeletal muscle and heart [33].”
BackgroundAerobic performance in brothers, dizygotic and monozygotic twins
BOUCHARD, C., LESAGE, R., LORTIE, G., SIMONEAU, J.-A., HAMEL, P., BOULAY, M. R., PERUSSE, L., THERIAULT, G., & LEBLANC, C. (1986) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198612000-00006 · Cited by 336 · see citing works
Potential benefits and hazards of physical activity and exercise on the gastrointestinal tract
Peters, H. P. F., de Vries, W. R., Henegouwen, G. P. V. B., & Akkermans, L. M. A. (2001) · Gut · doi:10.1136/gut.48.3.435 · Cited by 336 · see citing works
Habitual Physical Activity Is Associated With Intrahepatic Fat Content in Humans
Perseghin, G., Lattuada, G., De Cobelli, F., Ragogna, F., Ntali, G., Esposito, A., Belloni, E., Canu, T., Terruzzi, I., Scifo, P., et al. (2007) · Diabetes Care · doi:10.2337/dc06-2032 · Cited by 320 · see citing works
Differential susceptibility to obesity between male, female and ovariectomized female mice
Hong, J., Stubbins, R., Smith, R. R., Harvey, A. E., & Núñez, N. P. (2009) · Nutrition Journal · doi:10.1186/1475-2891-8-11 · Cited by 315 · see citing works
Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats
Petriz, B. A., Castro, A. P., Almeida, J. A., Gomes, C. P., Fernandes, G. R., Kruger, R. H., Pereira, R. W., & Franco, O. L. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-511 · Cited by 293 · see citing works
Intrinsic Aerobic Capacity Sets a Divide for Aging and Longevity
Koch, L. G., Kemi, O. J., Qi, N., Leng, S. X., Bijma, P., Gilligan, L. J., Wilkinson, J. E., Wisløff, H., Høydal, M. A., Rolim, N. P. L., et al. (2011) · Circulation Research · doi:10.1161/circresaha.111.253807 · Cited by 187 · see citing works
Self-citationThyfault, J. P., Rector, R. S., Uptergrove, G. M., Borengasser, S. J., Morris, E. M., Wei, Y., Laye, M. J., Burant, C., Qi, N., Ridenhour, S. E., et al. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.169060 · Cited by 173 · see citing works
Self-citationExercise regulation of intestinal tight junction proteins
Zuhl, M., Schneider, S., Lanphere, K., Conn, C., Dokladny, K., & Moseley, P. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2012-091585 · Cited by 167 · see citing works
Splanchnic vasoconstriction in hyperthermic man--role of falling blood pressure
Rowell, L. B., Detry, J.-M. R., PROFANT, G. R., & WYSS, C. R. (1971) · Journal of Applied Physiology · doi:10.1152/jappl.1971.31.6.864 · Cited by 113 · see citing works
Vieira Potter, V. J., Strissel, K. J., Xie, C., Chang, E., Bennett, G., Defuria, J., Obin, M. S., & Greenberg, A. S. (2012) · Endocrinology · doi:10.1210/en.2011-2006 · Cited by 99 · see citing works
Self-citationEffects of physical activity on intestinal gas transit and evacuation in healthy subjects
Dainese, R., Serra, J., Azpiroz, F., & Malagelada, J. (2004) · The American Journal of Medicine · doi:10.1016/j.amjmed.2003.12.018 · Cited by 96 · see citing works
Effects of the menopausal transition on energy expenditure: a MONET Group Study
Duval, K., homme, D. P., RABASA-LHORET, R. P. R., Strychar, I. M., Brochu, M., Lavoie, J.-M., & Doucet, É. (2013) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2013.33 · Cited by 88 · see citing works
Selection for aerobic capacity affects corticosterone, monoamines and wheel-running activity
Waters, R. P., Renner, K. J., Pringle, R. B., Summers, C. H., Britton, S. L., Koch, L. G., & Swallow, J. G. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.01.013 · Cited by 70 · see citing works
Self-citationOestrogen Receptors Enhance Dopamine Neurone Survival in Rat Midbrain
Johnson, M., Ho, C. C., Day, A. E., Walker, Q. D., Francis, R., & Kuhn, C. M. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01964.x · Cited by 65 · see citing works
Nickelson, K. J., Stromsdorfer, K. L., Pickering, R. T., Liu, T., Ortinau, L. C., Keating, A. F., & Perfield, J. W. (2012) · Experimental Diabetes Research · doi:10.1155/2012/859395 · Cited by 64 · see citing works
Self-citationVieira‐Potter, V. J., Padilla, J., Park, Y., Welly, R. J., Scroggins, R. J., Britton, S. L., Koch, L. G., Jenkins, N. T., Crissey, J. M., Zidon, T. M., et al. (2015) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00401.2014 · Cited by 57 · see citing works
Self-citationBody mass index following natural menopause and hysterectomy with and without bilateral oophorectomy
Gibson, C. J., Thurston, R. C., Khoudary, S. R. E., Sutton-Tyrrell, K., & Matthews, K. A. (2012) · International Journal of Obesity · doi:10.1038/ijo.2012.164 · Cited by 51 · see citing works
Naples, S. P., Borengasser, S. J., Rector, R. S., Uptergrove, G. M., Morris, E. M., Mikus, C. R., Koch, L. G., Britton, S. L., Ibdah, J. A., & Thyfault, J. P. (2010) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h09-139 · Cited by 49 · see citing works
Self-citationGenetic Analysis of a Rat Model of Aerobic Capacity and Metabolic Fitness
Ren, Y.-Y., Overmyer, K. A., Qi, N., Treutelaar, M. K., Heckenkamp, L., Kalahar, M., Koch, L. G., Britton, S. L., Burant, C., & Li, J. Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077588 · Cited by 47 · see citing works
Self-citationTraining Room Management of Medical Conditions: Sports Gastroenterology
CASEY, E. K., Mistry, D. J., & MacKnight, J. M. (2005) · Clinics in Sports Medicine · doi:10.1016/j.csm.2005.05.002 · Cited by 38 · see citing works
Development of Animal Models to Test the Fundamental Basis of Gene–Environment Interactions
Koch, L. G., & Britton, S. L. (2008) · Obesity · doi:10.1038/oby.2008.513 · Cited by 33 · see citing works
Self-citation
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- [19]Vieira-Potter VJ, Padilla J, Park YM, Welly RJ, Scroggins RJ, Britton SL, et al Female Rats Selectively Bred for High Intrinsic Aerobic Fitness Are Protected from Ovariectomy-Associated Metabolic Dysfunction. American journal of physiology Regulatory, integrative and comparative physiology. 2015:ajpregu 00401 2014 10.1152/ajpregu.00401.2014. 25608751 PMC4360065 · DOI
- [23]McInnes P, Cutting M. Core microbiome sampling protocol A HMP Protocol # 07–001. Manual of Procedures–Human Microbiome Project 2010; 11: 1– 109.
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Mailing, L. J., Allen, J. M., Buford, T. W., Fields, C. J., & Woods, J. A. (2019) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000183 · Cited by 521 · see citing works
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Munukka, E., Ahtiainen, J. P., Puigbó, P., Jalkanen, S., Pahkala, K., Keskitalo, A., Kujala, U. M., Pietilä, S., Hollmén, M., Elo, L., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02323 · Cited by 237 · see citing works
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Yazici, C., Wolf, P. G., Kim, H., Cross, T.-W. L., Vermillion, K., Carroll, T., Augustus, G. J., Mutlu, E., Tussing-Humphreys, L., Braunschweig, C., et al. (2017) · Gut · doi:10.1136/gutjnl-2016-313321 · Cited by 215 · see citing works
Codella, R., Luzi, L., & Terruzzi, I. (2018) · Digestive and Liver Disease · doi:10.1016/j.dld.2017.11.016 · Cited by 158 · see citing works
Cook, M. D., Allen, J. M., Pence, B. D., Wallig, M. A., Gaskins, H. R., White, B. A., & Woods, J. A. (2016) · Immunology & Cell Biology · doi:10.1038/icb.2015.108 · Cited by 140 · see citing works
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Liu, H., Hou, C., Li, N., Zhang, X., Zhang, G., Yang, F., Zeng, X., Liu, Z., & Qiao, S. (2019) · The FASEB Journal · doi:10.1096/fj.201801221rr · Cited by 130 · see citing works
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Zeppa, S. D., Agostini, D., Gervasi, M., Annibalini, G., Amatori, S., Ferrini, F., Sisti, D., Piccoli, G., Barbieri, E., Sestili, P., et al. (2019) · Nutrients · doi:10.3390/nu12010017 · Cited by 122 · see citing works
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Chen, X., Zhang, Z., Hu, Y., Cui, J., Zhi, X., Li, X.-Q., Jiang, H., Wang, Y., Gu, Z.-R., Qiu, Z., et al. (2019) · Aging and Disease · doi:10.14336/ad.2019.0613 · Cited by 68 · see citing works
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Self-citationLong, C., Zhou, X., Xia, F., & Zhou, B. (2024) · Biology · doi:10.3390/biology13040243 · Cited by 43 · see citing works
Exercise and gut microbiota: clinical implications for the feasibility of Tai Chi
Hamasaki, H. (2017) · Journal of Chinese Integrative Medicine · doi:10.1016/s2095-4964(17)60342-x · Cited by 43 · see citing works
Gut Microbiota at the Crossroad of Hepatic Oxidative Stress and MASLD
Termite, F., Archilei, S., D’Ambrosio, F., Petrucci, L., Viceconti, N., Iaccarino, R., Liguori, A., Gasbarrini, A., & Miele, L. (2025) · Antioxidants · doi:10.3390/antiox14010056 · Cited by 46 · see citing works
Dietary fiber during gestation improves lactational feed intake of sows by modulating gut microbiota
Li, S., Zheng, J., He, J., Liu, H., Huang, Y., Huang, L., Wang, K., Zhao, X., Feng, B., Che, L., et al. (2023) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-023-00870-z · Cited by 40 · see citing works
Microbiome and NAFLD: potential influence of aerobic fitness and lifestyle modification
Panasevich, M. R., Peppler, W. T., Oerther, D. B., Wright, D. C., & Rector, R. S. (2017) · Physiological Genomics · doi:10.1152/physiolgenomics.00012.2017 · Cited by 35 · see citing works
Hassib, L., de Oliveira, C. L., Rouvier, G. A., Kanashiro, A., Guimarães, F. S., & Ferreira, F. R. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2226282 · Cited by 33 · see citing works
Exercise training-induced changes in the gut microbiota of Standardbred racehorses
Janabi, A. H. D., Biddle, A. S., Klein, D. J., & McKeever, K. H. (2016) · Comparative Exercise Physiology · doi:10.3920/cep160015 · Cited by 31 · see citing works
IL‐10 suppresses TNF‐α‐induced expression of human aromatase gene in mammary adipose tissue
Martínez‐Chacón, G., Brown, K. A., Docanto, M. M., Kumar, H., Salminen, S., Saarinen, N., & Mäkelä, S. (2018) · The FASEB Journal · doi:10.1096/fj.201700938rrr · Cited by 31 · see citing works
Gaukroger, C. H., Edwards, S. A., Walshaw, J., Nelson, A., Adams, I. P., Stewart, C. J., & Kyriazakis, I. (2020) · animal · doi:10.1016/j.animal.2020.100135 · Cited by 30 · see citing works
Lee, J. R., Muckerman, J. E., Wright, A. M., Davis, D. J., Childs, T. E., Gillespie, C. H., Vieira‐Potter, V. J., Booth, F. W., Ericsson, A. C., & Will, M. J. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.07.018 · Cited by 28 · see citing works
Self-citationTung, Y., Hsu, Y.-J., Liao, C.-C., Ho, S.-T., Huang, C., & Huang, W.-C. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01201 · Cited by 27 · see citing works
Xia, T., Yao, Y., Wang, C., Dong, M., Wu, Y., Li, D., Xie, M., Ni, Q., Zhang, M., & Xu, H. (2020) · Global Ecology and Conservation · doi:10.1016/j.gecco.2020.e01409 · Cited by 27 · see citing works
Hamm, A. K., Manter, D. K., Kirkwood, J. S., Wolfe, L. M., Cox‐York, K. A., & Weir, T. L. (2019) · Nutrients · doi:10.3390/nu11123004 · Cited by 27 · see citing works
Neves, V. G. D. O., de Oliveira, D. T., Oliveira, D. C., Perucci, L. O., dos Santos, T. A. P., Fernandes, I. D. C., de Sousa, G. G., Barboza, N. R., & Guerra‐Sá, R. (2020) · Food Science & Nutrition · doi:10.1002/fsn3.1842 · Cited by 24 · see citing works
Rosa, J. M., Pazini, F. L., Camargo, A., Wolin, I. A. V., Olescowicz, G., Eslabão, L. B., Bruña–Romero, O., Duarte, E. C. W., & Rodrigues, A. L. S. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112791 · Cited by 23 · see citing works
The effects of acute strenuous exercise on the faecal microbiota in Standardbred racehorses
Janabi, A. H. D., Biddle, A. S., Klein, D. J., & McKeever, K. H. (2017) · Comparative Exercise Physiology · doi:10.3920/cep160030 · Cited by 21 · see citing works
Lu, Z., Shen, H., & Shen, Z. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01079 · Cited by 19 · see citing works
Akbuğa-Schön, T., Suzuki, T. A., Jakob, D., Vu, D. L., Waters, J. L., & Ley, R. E. (2023) · mBio · doi:10.1128/mbio.02836-23 · Cited by 17 · see citing works
Hoseini, R., Rahim, H. A., Saifalddin, D. L., Kareem, D. A., & Fatah, A. M. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-07492-1 · Cited by 19 · see citing works
Exercise, Nutrition and Gut Microbiota: Possible Links and Consequences
Costa, A. (2017) · International Journal of Sports and Exercise Medicine · doi:10.23937/2469-5718/1510069 · Cited by 17 · see citing works
Pekkala, S., Lensu, S., Nokia, M., Vanhatalo, S., Koch, L. G., Britton, S. L., & Kainulainen, H. (2017) · Physiological Genomics · doi:10.1152/physiolgenomics.00081.2017 · Cited by 16 · see citing works
Self-citationCould Physical Exercise Help Modulate the Gut Microbiota in Chronic Kidney Disease?
Esgalhado, M., Borges, N. A., & Mafra, D. (2016) · Future Microbiology · doi:10.2217/fmb.16.12 · Cited by 16 · see citing works
PQQ and quinoprotein research--the first decade.
Duine, J. A. (1989) · PubMed · Cited by 13 · see citing works
Li, Q., Chen, L., & Wang, R. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1652731 · Cited by 11 · see citing works
Dangoor, I., Stanić, D., Reshef, L., Pešić, V., & Gophna, U. (2021) · Microorganisms · doi:10.3390/microorganisms9091938 · Cited by 11 · see citing works
Moraes, M. M., Mendes, T. T., Borges, L., Marques, A. L., Núñez-Espinosa, C. A., Gonçalves, D. A. P., Simões, C. B., Vieira, T. S., Ladeira, R. V. P., Lourenço, T. G. B., et al. (2023) · Microorganisms · doi:10.3390/microorganisms11020339 · Cited by 10 · see citing works
de Brito, J. S., de Vargas, D. C. M., da Silva, G. S., Marinho, S. M., Borges, N. A., Cardozo, L., Fonseca, L. D. S., Ribeiro, M. M., Chermut, T. R., Moura, M., et al. (2021) · International Urology and Nephrology · doi:10.1007/s11255-021-02945-0 · Cited by 7 · see citing works
McNamara, M. P., Venable, E. M., Cadney, M. D., Castro, A. A., Schmill, M. P., Kazzazi, L., Carmody, R. N., & Garland, T. (2023) · Journal of Experimental Biology · doi:10.1242/jeb.245081 · Cited by 7 · see citing works
Leduc, R. Y. M., Rauw, G. A., Baker, G. B., & McDermid, H. E. (2017) · Europe PMC (PubMed Central) · Cited by 6 · see citing works
The Gut Microbiota: An Essential Component in Understanding Pediatric Obesity: A Narrative Review
Lupu, V. V., Nedelcu, A. H., Balas, R. B., Anton, C., Tarnita, I., Azoicai, A. N., Forna, L., Munteanu, D., Anton, S. C., Shawais, S. K., et al. (2026) · Nutrients · doi:10.3390/nu18060952 · Cited by 3 · see citing works
Parental cardiorespiratory fitness influences early life energetics and metabolic health
Sadler, D. G., Treas, L. D., Ross, T., Sikes, J. D., Britton, S. L., Koch, L. G., Piccolo, B. D., Børsheim, E., & Porter, C. C. (2023) · Physiological Genomics · doi:10.1152/physiolgenomics.00045.2023 · Cited by 3 · see citing works
Self-citationThe effect of physical activity on gut microbiota. A review
Barzak, B., Hankus, K., Parmar, S., & Woźniak, S. (2022) · Medical Journal of Cell Biology · doi:10.2478/acb-2022-0021 · Cited by 3 · see citing works
Sun, Y., Han, Z., Yao, X., Meng, J., Ren, W., Wang, C., Yuan, X.-X., Zeng, Y., Wang, Y.-F., Sun, Z.-W., et al. (2025) · Genes · doi:10.3390/genes16050504 · Cited by 2 · see citing works
Phoxim induces neurotoxicity and intestinal damage in Caenorhabditis elegans
Zhang, M., Zhao, X., Bai, H., Wang, Q., & Zou, W. (2025) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1657527 · Cited by 1 · see citing works
Rumão, M. S., Andrade, M. T., Costa, R. J., Santana, G. J., Cerqueira, J. P. C., Lima, G. S., Garcia, N. C., Heller, D., Espinosa, C. N., Arantes, R. M. E., et al. (2026) · International Journal of Microbiology · doi:10.1155/ijm/3405549 · Cited by 1 · see citing works
Exercise and Gut Microbiome: Trends and Advances in Research Methods
Baek, K., Ahn, K., Ahn, Y. J., Xiang, Y.-Y., & Kim, J. (2022) · Exercise Science · doi:10.15857/ksep.2022.00479 · Cited by 1 · see citing works
Park, J., Yamamoto, Y., Hidaka, K., Wada-Takahashi, S., Takahashi, S., Morozumi, T., Kubota, N., Saita, M., Saruta, J., Sakaguchi, W., et al. (2023) · Medicina · doi:10.3390/medicina59040789 · Cited by 1 · see citing works
Allen, J. M. (2017) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Interaction of quinolone antibiotics with the human intestinal CACO-2 cell model
Kang, M. S. (2001) · Aston Publications Explorer (Aston University) · doi:10.48780/publications.aston.ac.uk.00012354
Wu, Y., Yao, Y., Dong, M., Xia, T., Li, D., Xie, M., Wu, J., Wen, A., Wang, Q., Zhu, G., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12038031
Wu, Y., Yao, Y., Dong, M., Xia, T., Li, D., Xie, M., Wu, J., Wen, A., Wang, Q., Zhu, G., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12038007
Wu, Y., Yao, Y., Dong, M., Xia, T., Li, D., Xie, M., Wu, J., Wen, A., Wang, Q., Zhu, G., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12038010
Wu, Y., Yao, Y., Dong, M., Xia, T., Li, D., Xie, M., Wu, J., Wen, A., Wang, Q., Zhu, G., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12038022
Duan, Y., Wang, L., Cui, H., Zilong, F. A. N. G., Lu, Y., & 孙中光 (2026) · Frontiers in Medicine · doi:10.3389/fmed.2026.1762454
- Authors
- 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.
- Affiliations
- University of Missouri (US)
- University of Illinois Urbana-Champaign (US)
- University of Michigan (US)
- Corresponding author
- Swanson, Kelly S.
- ORCID
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-08-24
- Volume
- 10
- Issue
- 8
- Pages
- e0136150
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4547806
- OpenAlex
- W1576927780
- Cited by
- 78
- References
- 46
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 1 · 2023: 8 · 2022: 5 · 2021: 3 · 2020: 14 · 2019: 9 · 2018: 7 · 2017: 12 · 2016: 8 · 2015: 1
- FWCI
- 4.05
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- University of Michigan
- National Institutes of Health (R24OD010950)
- University of Illinois at Urbana-Champaign
- College of Pharmacy, University of Michigan
- National Heart, Lung, and Blood Institute (K01HL125503)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK099034, P30DK020572)
- Office of Research Infrastructure Programs, National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- physical activity, voluntary exercise, cecal microbiota, gut microbiota, ovariectomy, postmenopausal women, cardiorespiratory fitness, high-fat diet, obesity, body composition, fat mass, energy expenditure, Christensenellaceae, Firmicutes, Proteobacteria, cyanobacteria, female rats
- MeSH terms
- Bacillota, Aerobiosis, Cyanobacteria, Animals, Cecum, Female, Humans, Motor Activity, Obesity, Ovariectomy, Ovary, Physical Conditioning, Animal, RNA, Ribosomal, 16S, Proteobacteria, Rats, Microbiota
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