The DOI matches its Crossref record; 66 of the 66 references it cites were found in a registry or an index.
Exercise and gut immune function: evidence of alterations in colon immune cell homeostasis and microbiome characteristics with exercise training
Abstract
There is robust evidence that habitual physical activity is anti‐inflammatory and protective against developing chronic inflammatory disease. Much less is known about the effects of habitual moderate exercise in the gut, the compartment that has the greatest immunological responsibility and interactions with the intestinal microbiota. The link between the two has become evident, as recent studies have linked intestinal dysbiosis, or the disproportionate balance of beneficial to pathogenic microbes, with increased inflammatory disease susceptibility. Limited animal and human research findings imply that exercise may have a beneficial role in preventing and ameliorating such diseases by having an effect on gut immune function and, recently, microbiome characteristics. Emerging data from our laboratory show that different forms of exercise training differentially impact the severity of intestinal inflammation during an inflammatory insult (for example, ulcerative colitis) and may be jointly related to gut immune cell homeostasis and microbiota–immune interactions. The evidence we review and present will provide data in support of rigorous investigations concerning the effects of habitual exercise on gut health and disease.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“These preliminary studies indicate that exercise influences the composition of the gut microbiota community.”
From The athletic gut microbiota (2020) · cites this paper as [71]
Citations
Cites
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
Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity
Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J. P., Druart, C., Bindels, L. B., Guiot, Y., Derrien, M., Muccioli, G. G., Delzenne, N. M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219451110 · Cited by 4,511
The Neuroendocrinology of Stress: A Never Ending Story
Lightman, S. L. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01711.x · Cited by 3,588
Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43
Maslowski, K. M., Vieira, A. T., Ng, A., Kranich, J., Sierro, F., Yu, D., Schilter, H. C., Rolph, M. S., Mackay, F., Artis, D., et al. (2009) · Nature · doi:10.1038/nature08530 · Cited by 3,241
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
Vrieze, A., Van Nood, E., Holleman, F., Salojärvi, J., Kootte, R. S., Bartelsman, J. F. W. M., Dallinga–Thie, G. M., Ackermans, M. T., Serlie, M. J., Oozeer, R., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.06.031 · Cited by 2,913
Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota
Atarashi, K., Tanoue, T., Oshima, K., Suda, W., Nagano, Y., Nishikawa, H., Fukuda, S., Saito, T., Narushima, S., Hase, K., et al. (2013) · Nature · doi:10.1038/nature12331 · Cited by 2,872
Cytokines in inflammatory bowel disease
Neurath, M. F. (2014) · Nature Reviews Immunology · doi:10.1038/nri3661 · Cited by 2,706
Louis, P., & Flint, H. J. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01514.x · Cited by 2,179
Dao, M. C., Everard, A., Aron-Wisnewsky, J., Sokolovska, N., Prifti, E., Verger, E. O., Kayser, B. D., Levenez, F., Chilloux, J., Hoyles, L., et al. (2016) · Gut · doi:10.1136/gutjnl-2014-308778 · Cited by 1,931
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748
Gut Dysbiosis Is Linked to Hypertension
Yang, T., Santisteban, M. M., Rodriguez, V., Li, E., Ahmari, N., Carvajal, J. M., Zadeh, M., Gong, M., Qi, Y., Zubcevic, J., et al. (2015) · Hypertension · doi:10.1161/hypertensionaha.115.05315 · Cited by 1,478
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
Png, C. W., Lindén, S. K., Gilshenan, K. S., Zoetendal, E. G., McSweeney, C. S., Sly, L. I., McGuckin, M. A., & Florin, T. H. J. (2010) · American Journal of Gastroenterology · doi:10.1038/ajg.2010.281 · Cited by 1,364
Position statement. Part one: Immune function and exercise.
Walsh, N. P., Gleeson, M., Shephard, R. J., Gleeson, M., Woods, J. A., Bishop, N. C., Fleshner, M., Green, C., Pedersen, B. K., Hoffman‐Goetz, L., et al. (2011) · PubMed · Cited by 1,252
Self-citationPhylogenetic Relationships of Butyrate-Producing Bacteria from the Human Gut
Barcenilla, A., Pryde, S. E., Martin, J. C., Duncan, S. H., Stewart, C. S., Henderson, C., & Flint, H. J. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.4.1654-1661.2000 · Cited by 996
Karczewski, J., Troost, F. J., Konings, I., Dekker, J., Kleerebezem, M., Brummer, R.-J. M., & Wells, J. M. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00327.2009 · Cited by 676
Evans, 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
Epithelial crosstalk at the microbiota–mucosal interface
Wells, J. M., Rossi, O., Meijerink, M., & van Baarlen, P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000092107 · Cited by 574
Interactions Between the Host Innate Immune System and Microbes in Inflammatory Bowel Disease
Abraham, C., & Medzhitov, R. M. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.02.012 · Cited by 555
Microbiota disbiosis is associated with colorectal cancer
Gao, Z., Guo, B., Gao, R., Zhu, Q., & Qin, H. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00020 · Cited by 537
Miele, E., Pascarella, F., Giannetti, E., Quaglietta, L., Baldassano, R. N., & Staiano, A. (2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2008.118 · Cited by 517
Niedzielin, K., Kordecki, H., & Birkenfeld, B. (2001) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-200110000-00004 · Cited by 506
Queipo-Ortuño, M. I., Seoane, L. M., Murri, M., Pardo, M., Gomez-Zumaquero, J. M., Cardona, F., Casanueva, F., & Tinahones, F. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065465 · Cited by 497
Cummings, J. H., & Macfarlane, G. T. (1997) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607197021006357 · Cited by 443
Position statement. Part two: Maintaining immune health.
Walsh, N. P., Gleeson, M., Pyne, D. B., Nieman, D. C., Dhabhar, F. S., Shephard, R. J., Oliver, S. J., Bermon, S., & Kajėnienė, A. (2011) · PubMed · Cited by 365
MATSUMOTO, M., INOUE, R., TSUKAHARA, T., USHIDA, K., CHIJI, H., MATSUBARA, N., & HARA, H. (2008) · Bioscience, Biotechnology, and Biochemistry · doi:10.1271/bbb.70474 · Cited by 352
Kang, S. S., Jeraldo, P., Kurti, A., Miller, M. E. B., Cook, M. D., Whitlock, K. G., Goldenfeld, N. D., Woods, J. A., White, B. A., Chia, N., et al. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-36 · Cited by 331
Self-citationExercise Attenuates PCB-Induced Changes in the Mouse Gut Microbiome
Choi, J. J., Eum, S. Y., Rampersaud, E., Daunert, S., Abreu, M. T., & Toborek, M. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.1306534 · Cited by 298
van Wijck, K., Lenaerts, K., Grootjans, J., Wijnands, K. A. P., Poeze, M., van Loon, L. J. C., Dejong, C. H. C., & Buurman, W. A. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00066.2012 · Cited by 285
Role of intestinal bacteria in nutrient metabolism
Cummings, J. H., & Macfarlane, G. T. (1997) · Clinical Nutrition · doi:10.1016/s0261-5614(97)80252-x · Cited by 284
Huang, Y. J., & Boushey, H. A. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2014.11.011 · Cited by 280
Voluntary and forced exercise differentially alters the gut microbiome in C57BL/6J mice
Allen, J. M., Berg Miller, M. E., Pence, B. D., Whitlock, K., Nehra, V., Gaskins, H. R., White, B. A., Fryer, J. D., & Woods, J. A. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01077.2014 · Cited by 266
Self-citationExercise training modifies gut microbiota in normal and diabetic mice
Lambert, J. E., Myslicki, J. P., Bomhof, M. R., Belke, D. D., Shearer, J., & Reimer, R. A. (2015) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2014-0452 · Cited by 214
Carroll, I. M., Andrus, J. M., Bruno-Bárcena, J. M., Klaenhammer, T. R., Hassan, H. M., & Threadgill, D. S. (2007) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00132.2007 · Cited by 208
Zakostelska, Z. J., Kverka, M., Kostovcikova, K., Rossmann, P., Mrázek, J., Kopečný, J., Hornová, M., Šrůtková, D., Hudcovic, T., Rídl, J., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027961 · Cited by 207
Mika, A., Van Treuren, W., González, A., Herrera, J. J., Knight, R., & Fleshner, M. (2015) · PLOS ONE · doi:10.1371/journal.pone.0125889 · Cited by 197
Vieira‐Potter, V. J., Valentine, R. J., Wilund, K. R., Antao, N. N., Baynard, T., & Woods, J. A. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00054.2009 · Cited by 194
Self-citationTailford, L. E., Owen, C. D., Walshaw, J., Crost, E. H., Hardy-Goddard, J., Le Gall, G., de Vos, W. M., Taylor, G. L., & Juge, N. (2015) · Nature Communications · doi:10.1038/ncomms8624 · Cited by 183
Musso, G., Gambino, R., & Cassader, M. (2010) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e3283347ebb · Cited by 183
Prospective study of physical activity and the risk of symptomatic diverticular disease in men.
Aldoori, W. H., Giovannucci, E. L., Rimm, E. B., Ascherio, A., Stampfer, M. J., Colditz, G. A., Wing, A. L., Trichopoulos, D., & Willett, W. C. (1995) · Gut · doi:10.1136/gut.36.2.276 · Cited by 183
Woods, J. A., Keylock, K. T., Lowder, T., Vieira‐Potter, V. J., Zelkovich, W., Dumich, S. A., Colantuano, K., Lyons, K. L., Leifheit, K. A., Cook, M. D., et al. (2009) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2009.02563.x · Cited by 179
Self-citationThe intestinal microbiota in health and disease
Young, V. B. (2011) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e32834d61e9 · Cited by 164
Probiotics as prevention and treatment for diarrhea
Guarino, A., Vecchio, A. L., & Canani, R. B. (2008) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e32831b4455 · Cited by 153
Cook, M. D., Martin, S. A., Williams, C., Whitlock, K., Wallig, M. A., Pence, B. D., & Woods, J. A. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2013.05.005 · Cited by 153
Self-citationSilva, S. D., Masselot, C. R., Ait-Belgnaoui, A., Mancuso, A., Mercade, M., Salvador–Cartier, C., Gillet, M., Ferrier, L., Loubière, P., Dague, É., et al. (2014) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00290.2013 · Cited by 147
Temporal stability of the mouse gut microbiota in relation to innate and adaptive immunity
Dimitriu, P. A., Boyce, G. K., Samarakoon, A., Hartmann, M., Johnson, P., & Mohn, W. W. (2012) · Environmental Microbiology Reports · doi:10.1111/j.1758-2229.2012.00393.x · Cited by 95
Hoffman‐Goetz, L., Pervaiz, N., Packer, N. H., & Guan, J. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.05.001 · Cited by 80
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. (2015) · PLOS ONE · doi:10.1371/journal.pone.0136150 · Cited by 78
Kotarsky, K., Sitnik, K., Stenstad, H., Kotarsky, H., Schmidtchen, A., Koslowski, M. J., Wehkamp, J., & Agace, W. W. (2009) · Mucosal Immunology · doi:10.1038/mi.2009.115 · Cited by 75
Treadmill exercise in mice increases intestinal lymphocyte loss via apoptosis
Hoffman‐Goetz, L., & Quadrilatero, J. (2003) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2003.01176.x · Cited by 75
Interactomics in the Human Intestine
Boesten, R. J., & de Vos, W. M. (2008) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31817dbd62 · Cited by 74
Chronic exercise increases macrophage-mediated tumor cytolysis in young and old mice
Lu, Q., Ceddia, M. A., Price, E. A., Ye, S.-M., & Woods, J. A. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.2.r482 · Cited by 72
Self-citationLowder, T., Padgett, D. A., & Woods, J. A. (2026) · PubMed · doi:10.22029/eir.2006.1625 · Cited by 70
Self-citationPacker, N. H., Hoffman‐Goetz, L., & Ward, G. (2010) · PubMed · Cited by 68
Hoffman‐Goetz, L., Pervaiz, N., & Guan, J. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.01.015 · Cited by 66
Falk, A., Olsson, C., Ahrné, S., Molin, G., Adawi, D., & Jeppsson, B. W. (2007) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365520701204238 · Cited by 65
Exercise-associated Intestinal Ischemia
Moses, F. M. (2005) · Current Sports Medicine Reports · doi:10.1097/01.csmr.0000306079.74945.ea · Cited by 63
Exercise Training Reduces Inflammatory Mediators in the Intestinal Tract of Healthy Older Adult Mice
Packer, N., & Hoffman‐Goetz, L. (2012) · Canadian Journal on Aging / La Revue canadienne du vieillissement · doi:10.1017/s0714980812000104 · Cited by 60
Physical Activity Benefits and Risks on the Gastrointestinal System
Martin, D. (2011) · Southern Medical Journal · doi:10.1097/smj.0b013e318236c263 · Cited by 53
Dysbiosis in the Pathogenesis of Pediatric Inflammatory Bowel Diseases
Comito, D., & Romano, C. (2012) · International Journal of Inflammation · doi:10.1155/2012/687143 · Cited by 49
Gastrointestinal bleeding and the athlete.
Moses, F. M. (1993) · PubMed · Cited by 44
Boyle, T., Heyworth, J. S., Bull, F., McKerracher, S., Platell, C. F. E., & Fritschi, L. (2011) · Cancer Causes & Control · doi:10.1007/s10552-011-9841-5 · Cited by 44
Repeated exercise in mice alters expression of IL-10 and TNF-α in intestinal lymphocytes
Hoffman‐Goetz, L., Spagnuolo, P. A., & Guan, J. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.07.002 · Cited by 41
Physical activity, exercise, and immune function
Woods, J. A. (2005) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2005.04.007 · Cited by 31
Self-citationSpagnuolo, P. A., & Hoffman‐Goetz, L. (2009) · PubMed · Cited by 4
Cited by
Sorted by citations
Current understanding of the human microbiome
Gilbert, J. A., Blaser, M. J., Caporaso, J. G., Jansson, J. K., Lynch, S. V., & Knight, R. (2018) · Nature Medicine · doi:10.1038/nm.4517 · Cited by 2,609
The compelling link between physical activity and the body's defense system
Nieman, D. C., & Wentz, L. M. (2019) · Journal of Sport and Health Science · doi:10.1016/j.jshs.2018.09.009 · Cited by 1,340
Exercise Modifies the Gut Microbiota with Positive Health Effects
Monda, V., Villano, I., Messina, A., Valenzano, A., Esposito, T., Moscatelli, F., Viggiano, A., Cibelli, G., Chieffi, S., Monda, M., et al. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/3831972 · Cited by 654
Community characteristics of the gut microbiomes of competitive cyclists
Petersen, L. M., Bautista, E. J., Nguyen, H., Hanson, B. M., Chen, L., Lek, S. H., Sodergren, E., & Weinstock, G. M. (2017) · Microbiome · doi:10.1186/s40168-017-0320-4 · Cited by 377
Flandroy, L., Poutahidis, T., Berg, G., Clarke, G. A., Dao, M. C., Decaestecker, E., Furman, E., Haahtela, T., Massart, S., Plovier, H., et al. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.01.288 · Cited by 417
Metadata
- Authors
- Cook, M. D., Allen, J. M., Pence, B. D., Wallig, M. A., Gaskins, H. R., White, B. A., & Woods, J. A.
- Affiliations
- University of Illinois Chicago (US)
- University of Illinois Urbana-Champaign (US)
- Corresponding author
- Woods, Jeffrey A
- ORCID
- Venue
- Immunology & Cell Biology
- Publisher
- Wiley
- Published
- 2015-12-15
- Volume
- 94
- Issue
- 2
- Pages
- 158-163
- ISSN
- 0004-945X (ISSN-L)
- 0818-9641
- 1440-1711
- OpenAlex
- W2214051764
- Cited by
- 140
- References
- 66
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 12 · 2023: 16 · 2022: 12 · 2021: 14 · 2020: 20 · 2019: 17 · 2018: 11 · 2017: 13 · 2016: 7 · 2015: 1
- FWCI
- 1.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Immunology and Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American College of Sports Medicine
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Physiology (medical) › Exercise and Physiological Responses
- Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
- Keywords
- exercise training, gut microbiota, dysbiosis, intestinal inflammation, ulcerative colitis, microbiota-immune interactions, gut health
- MeSH terms
- Animals, Colitis, Colon, Exercise Therapy, Homeostasis, Humans, Intestines, Exercise, Immunity, Mucosal, Microbiota
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
