The DOI matches its Crossref record; 53 of the 53 references it cites were found in a registry or an index.
Exercise Attenuates PCB-Induced Changes in the Mouse Gut Microbiome
Open accessAbstract
Background: The gut microbiome, a dynamic bacterial community that interacts with the host, is integral to human health because it regulates energy metabolism and immune functions. The gut microbiome may also play a role in risks from environmental toxicants. Objectives: We investigated the effects of polychlorinated biphenyls (PCBs) and exercise on the composition and structure of the gut microbiome in mice. Methods: After mice exercised voluntarily for 5 weeks, they were treated by oral gavage with a mixture of environmentally relevant PCB congeners (PCB153, PCB138, and PCB180; total PCB dose, 150 µmol/kg) for 2 days. We then assessed the microbiome by determination of 16S rRNA using microarray analysis. Results: Oral exposure to PCBs significantly altered the abundance of the gut microbiome in mice primarily by decreasing the levels of Proteobacteria. The activity level of the mice correlated with a substantial shift in abundance, biodiversity, and composition of the microbiome. Importantly, exercise attenuated PCB-induced changes in the gut microbiome. Conclusions: Our results show that oral exposure to PCBs can induce substantial changes in the gut microbiome, which may then influence their systemic toxicity. These changes can be attenuated by behavioral factors, such as voluntary exercise.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“It is reasonable to think of exercise as being crucial to healthy interactions within the gut microbiota (Choi et al., 2013).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Choi et al., 2013
Experimental — accuracy not yet measuredIn the citing paper
“Exercise appears to be able to enrich microbiota diversity [20–25]”
From International Society of Sports Nutrition Position Stand: Probiotics (2019) · cites this paper as [22]
In the citing paper
“In particular, Choi et al. [73] reported that, in comparison to a sedentary control, mice with running wheel exercise had higher phylum Firmicutes but fewer phyla Tenericutes and Bacteroidetes, which attenuated changes in gut microbiota induced by oral exposure to the environmental toxin, polychlorinated biphenyls.”
From The athletic gut microbiota (2020) · cites this paper as [73]
In the citing paper
“Other than a positive correlation between exercise and Lactobacillus [73, 86, 87], there are no other taxa that consistently increase in relative abundance in regularly exercised mice or rats.”
From The athletic gut microbiota (2020) · cites this paper as [73]
In the citing paper
“Other animal studies demonstrated that daily wheel running exercise may improve some aspects of unhealthy states, such as diet-induced obesity, diabetes, and toxicity, by impacting the gut microbial composition in mice [73–75].”
From The athletic gut microbiota (2020) · cites this paper as [73]
In the citing paper
“Several other studies using murine-based models also demonstrated increased alpha diversity in animals that exercised vs. those that were sedentary [73, 74, 86, 87].”
From The athletic gut microbiota (2020) · cites this paper as [73]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
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
Frank, D. N., St. Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., & Pace, N. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706625104 · Cited by 4,611
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
Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine
Ley, R. E., Peterson, D. A., & Gordon, J. I. (2006) · Cell · doi:10.1016/j.cell.2006.02.017 · Cited by 3,358
Diagnosis of multiple cancer types by shrunken centroids of gene expression
Tibshirani, R. J., Hastie, T. J., Narasimhan, B., & Chu, G. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082099299 · Cited by 2,931
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
Colonic Health: Fermentation and Short Chain Fatty Acids
Wong, J. M. W., de Souza, R., Kendall, C. W. C., Emam, A., & Jenkins, D. J. A. (2006) · Journal of Clinical Gastroenterology · doi:10.1097/00004836-200603000-00015 · Cited by 2,739
Human gut microbiota in obesity and after gastric bypass
Zhang, H., DiBaise, J. K., Zuccolo, A., Kudrna, D., Braidotti, M., Yu, Y., Parameswaran, P., Crowell, M. D., Wing, R., Rittmann, B. E., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812600106 · Cited by 1,880
Guide for the Care and Use of Laboratory Animals (8th edn)
Albus, U. (2012) · Laboratory Animals · doi:10.1258/la.2012.150312 · Cited by 1,706
UniFrac – An online tool for comparing microbial community diversity in a phylogenetic context
Lozupone, C., Hamady, M., & Knight, R. D. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-371 · Cited by 1,454
Deep-Sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria
Hazen, T. C., Dubinsky, E. A., DeSantis, T. Z., Andersen, G. L., Piceno, Y. M., Singh, N., Jansson, J. K., Probst, A. J., Borglin, S. E., Fortney, J. L., et al. (2010) · Science · doi:10.1126/science.1195979 · Cited by 1,231
Human Intestinal Lumen and Mucosa-Associated Microbiota in Patients with Colorectal Cancer
Chen, W., Liu, F., Ling, Z., Tong, X., & Xiang, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039743 · Cited by 1,054
Bile Acid Is a Host Factor That Regulates the Composition of the Cecal Microbiota in Rats
Islam, K. B. M. S., Fukiya, S., Hagio, M., Fujii, N., Ishizuka, S., Ooka, T., Ogura, Y., Hayashi, T., & Yokota, A. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.07.046 · Cited by 918
Armougom, F., Henry, M., Vialettes, B., Raccah, D., & Raoult, D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007125 · Cited by 905
Santacruz, A., Collado, M. C., García-Valdés, L., Segura, M. T., Martín-Lagos, J. A., Anjos, T., Martí-Romero, M., Lopez, R. M., Florido, J., Campoy, C., et al. (2010) · British Journal of Nutrition · doi:10.1017/s0007114510000176 · Cited by 868
Gut microbiome, obesity, and metabolic dysfunction
Tilg, H., & Kaser, A. (2011) · Journal of Clinical Investigation · doi:10.1172/jci58109 · Cited by 860
Enterococci as probiotics and their implications in food safety
Franz, C. M. A. P., Huch, M., Abriouel, H., Holzapfel, W. H., & Gálvez, A. (2011) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2011.08.014 · Cited by 795
Goodman, A. L., Kallstrom, G., Faith, J. J., Reyes, A., Moore, A. M., Dantas, G. A., & Gordon, J. I. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102938108 · Cited by 781
Walker, A. W., Sanderson, J. D., Churcher, C. M., Parkes, G. C., Hudspith, B. N., Rayment, N. B., Brostoff, J., Parkhill, J., Dougan, G., & Petrovska, L. (2011) · BMC Microbiology · doi:10.1186/1471-2180-11-7 · Cited by 727
Gut microbiome-host interactions in health and disease
Kinross, J. K., Darzi, A. W., & Nicholson, J. K. (2011) · Genome Medicine · doi:10.1186/gm228 · Cited by 714
Understanding the role of gut microbiome–host metabolic signal disruption in health and disease
Holmes, E., Li, J. V., Athanasiou, T., Ashrafian, H., & Nicholson, J. K. (2011) · Trends in Microbiology · doi:10.1016/j.tim.2011.05.006 · Cited by 541
Colonization-induced host-gut microbial metabolic interaction
Claus, S. P., Ellero, S. L., Berger, B., Krause, L., Bruttin, A., Molina, J., Paris, A., Want, E. J., de Waziers, I., Cloarec, O., et al. (2011) · mBio · doi:10.1128/mbio.00271-10 · Cited by 414
Mechanism of growth inhibition by free bile acids in lactobacilli and bifidobacteria
Kurdi, P., Kawanishi, K., Mizutani, K., & Yokota, A. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.5.1979-1986.2006 · Cited by 364
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
LYTE, M., LI, W., OPITZ, N., GAYKEMA, R., & GOEHLER, L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.06.019 · Cited by 334
Human Colon Microbiota Transform Polycyclic Aromatic Hydrocarbons to Estrogenic Metabolites
de Wiele, T. V., Vanhaecke, L., Boeckaert, C., Peru, K. M., Headley, J. V., Verstraete, W., & Siciliano, S. D. (2004) · Environmental Health Perspectives · doi:10.1289/ehp.7259 · Cited by 248
Friedenreich, C. M., Norat, T., Steindorf, K., Boutron‐Ruault, M., Pischon, T., Mazuir, M., Clavel‐Chapelon, F., Linseisen, J., Boeing, H., Bergman, M. M., et al. (2006) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-06-0595 · Cited by 234
WORLD PCBs MAP: STORAGE AND EFFECTS IN MAN AND HIS BIOLOGIC ENVIRONMENT IN THE 1970s
Wassermann, M., WASSERMANN, D., Cucos, S., & Miller, H. J. (1979) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1979.tb13137.x · Cited by 218
Willems, R. J. L., Hanage, W. P., Bessen, D. E., & Feil, E. J. (2011) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2011.00284.x · Cited by 207
Do Interactions Between Gut Ecology and Environmental Chemicals Contribute to Obesity and Diabetes?
Snedeker, S. M., & Hay, A. G. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1104204 · Cited by 186
Weisglas‐Kuperus, N. (2004) · Toxicology Letters · doi:10.1016/j.toxlet.2003.12.039 · Cited by 139
Liebert, C. A., Wireman, J., Smith, T., & Summers, A. O. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.3.1066-1076.1997 · Cited by 135
Microbiome and immunological interactions
Kelly, D., & Mulder, I. E. (2012) · Nutrition Reviews · doi:10.1111/j.1753-4887.2012.00498.x · Cited by 131
Perturbation Dynamics of the Rumen Microbiota in Response to Exogenous Butyrate
Li, R. W., Wu, S., Baldwin, R. L., Li, W., & Li, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029392 · Cited by 114
Pinyayev, T. S., Kohan, M. J., Herbin-Davis, K., Creed, J. T., & Thomas, D. J. (2011) · Chemical Research in Toxicology · doi:10.1021/tx200040w · Cited by 111
Meissner, M., Lombardo, E., Havinga, R., Tietge, U. J. F., Kuipers, F., & Groen, A. K. (2011) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2011.06.040 · Cited by 99
Correa, P. A., Lin, L.-S., Just, C. L., Hu, D., Hornbuckle, K. C., Schnoor, J. L., & Aken, B. V. (2009) · Environment International · doi:10.1016/j.envint.2009.07.015 · Cited by 92
Choi, Y. J., Seelbach, M. J., Pu, H., Eum, S. Y., Chen, L., Zhang, B., Hennig, B., & Toborek, M. J. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.0901751 · Cited by 91
Self-citationPetrić, I. S., Bru, D., Udiković‐Kolić, N., Hršak, D., Philippot, L., & Martin-Laurent, F. A. (2011) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2011.08.036 · Cited by 71
Does a Physically Active Lifestyle Improve Symptoms in Women With Irritable Bowel Syndrome?
Lustyk, M. K. B., Jarrett, M. E., Bennett, J. C., & Heitkemper, M. M. (2001) · Gastroenterology Nursing · doi:10.1097/00001610-200105000-00007 · Cited by 61
Jensen, A. A. (1989) · Elsevier eBooks · doi:10.1016/b978-0-444-81029-8.50016-3 · Cited by 57
Physical Activity Benefits and Risks on the Gastrointestinal System
Martin, D. (2011) · Southern Medical Journal · doi:10.1097/smj.0b013e318236c263 · Cited by 53
Ashley, J. T. F., Secor, D. H., Zlokovitz, E. R., Wales, S. Q., & Baker, J. E. (2000) · Environmental Science & Technology · doi:10.1021/es990833t · Cited by 46
Choi, J. J., Choi, Y. J., Chen, L., Zhang, B., Eum, S. Y., Abreu, M. T., & Toborek, M. J. (2012) · Toxicology · doi:10.1016/j.tox.2012.08.001 · Cited by 40
Self-citationHagio, M., Matsumoto, M., Yajima, T., Hara, H., & Ishizuka, S. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00777.2009 · Cited by 40
Effect of Moderate Exercise on IgA Levels and Lymphocyte Count in Mouse Intestine
Viloria, M., Lara‐Padilla, E., Campos‐Rodríguez, R., Jarillo‐Luna, A., Reyna-Garfias, H., López‐Sánchez, P., Rivera‐Aguilar, V., Salas‐Casas, A., de la Rosa, F. J. B., & Garcı́a-Latorre, E. (2011) · Immunological Investigations · doi:10.3109/08820139.2011.575425 · Cited by 40
A Study in Balance: How Microbiomes Are Changing the Shape of Environmental Health
Betts, K. S. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.119-a340 · Cited by 37
Aroclor 1254 exposure reduces disease resistance and innate immune responses in fasted Arctic charr
Maule, A. G., Jørgensen, E. H., Vijayan, M. M., & Killie, J.-E. A. (2004) · Environmental Toxicology and Chemistry · doi:10.1897/03-700.1 · Cited by 36
Nelson, T. A., Holmes, S., Alekseyenko, A. V., Shenoy, M. M., DeSantis, T. Z., Wu, C. H., Andersen, G. L., Winston, J. H., Sonnenburg, J. L., Pasricha, P. J., et al. (2010) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01637.x · Cited by 33
Lapanje, A., Rupnik, M., & Drobne, D. (2007) · Environmental Toxicology and Chemistry · doi:10.1897/06-099r.1 · Cited by 25
Impact of nutrition on PCB toxicity
Májková, Z., Oesterling, E., Toborek, M. J., & Hennig, B. (2007) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2007.10.015 · Cited by 16
Self-citationAssessment of the Microbiota in Microdissected Tissues of Crohn's Disease Patients
Hertogh, G. D., Lemmens, B., Verhasselt, P., Hoogt, R. D., Sagaert, X., Joossens, M., Assche, G. V., Rutgeerts, P., Vermeire, S., & Aerssens, J. (2011) · International Journal of Inflammation · doi:10.1155/2012/505674 · Cited by 9
Colon Transit Time According to Physical Activity Level in Adults
Song, B., Kang, O.-C., Jo, Y., Oh, J.-W., & Kim, Y. (2012) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2012.18.1.64 · Cited by 8
Flagged first, then by citations
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286
Exercise alters gut microbiota composition and function in lean and obese humans
ALLEN, J. M., MAILING, L. J., NIEMIRO, G. M., MOORE, R., COOK, M. D., WHITE, B. A., HOLSCHER, H. D., & WOODS, J. A. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001495 · Cited by 820
The gut microbiota: a major player in the toxicity of environmental pollutants?
Claus, S. P., Guillou, H., & Ellero-Simatos, S. (2016) · npj Biofilms and Microbiomes · doi:10.1038/npjbiofilms.2016.3 · Cited by 678
Effects of environmental pollutants on gut microbiota
Jin, Y., Wu, S., Zeng, Z., & Fu, Z. (2017) · Environmental Pollution · doi:10.1016/j.envpol.2016.11.045 · Cited by 683
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
Metadata
- Authors
- Choi, J. J., Eum, S. Y., Rampersaud, E., Daunert, S., Abreu, M. T., & Toborek, M.
- Affiliations
- University of Miami (US)
- Department of Biochemistry and Molecular Biology,
- John P. Hussman Institute for Human Genomics, and
- Corresponding author
- Toborek, Michal
- Venue
- Environmental Health Perspectives
- Publisher
- American Chemical Society (ACS)
- Published
- 2013-04-26
- Volume
- 121
- Issue
- 6
- Pages
- 725-730
- ISSN
- 0091-6765 (ISSN-L)
- 1552-9924
- PMC
- PMC3672930
- OpenAlex
- W2028180178
- Cited by
- 298
- References
- 53
- Citations by year
- 2026: 10 · 2025: 16 · 2024: 19 · 2023: 28 · 2022: 19 · 2021: 23 · 2020: 32 · 2019: 36 · 2018: 31 · 2017: 28 · 2016: 19 · 2015: 22 · 2014: 9 · 2013: 6
- FWCI
- 8.37
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- creativecommons.org/licenses/by/4.0/ (vor, 1708 d)
- Locations
- Environmental Health Perspectives (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (DA027569)
- National Institute of Mental Health (MH072567, MH 63022, R01MH063022, R01MH072567)
- National Institute on Drug Abuse (R01DA027569, DA027569)
- National Cancer Institute (R01CA133257)
- National Institute of Environmental Health Sciences (P42 ES-07380, P42ES007380)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
- Physical Sciences › Environmental Science › Pollution › Microbial bioremediation and biosurfactants
- Keywords
- polychlorinated biphenyls, gut microbiota, voluntary exercise, environmental toxins, Proteobacteria, microbiome diversity, oral exposure, PCB congeners, mouse model
- MeSH terms
- Animals, Environmental Pollutants, Fatty Acids, Volatile, Humans, Intestines, Male, Mice, Inbred C57BL, Physical Conditioning, Animal, Polychlorinated Biphenyls, Cholic Acid, Mice, Metagenome
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
