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Smoking Cessation Alters Intestinal Microbiota: Insights from Quantitative Investigations on Human Fecal Samples Using FISH
Abstract
BACKGROUND: There has been a dramatic increase in investigations on the potential mechanistic role of the intestinal microbiota in various diseases and factors modulating intestinal microbial composition. We recently reported on intestinal microbial shifts after smoking cessation in humans. In this study, we aimed to conduct further microbial analyses and verify our previous results obtained by pyrosequencing using a direct quantitative microbial approach. METHODS: Stool samples of healthy smoking human subjects undergoing controlled smoking cessation during a 9-week observational period were analyzed and compared with 2 control groups, ongoing smoking and nonsmoking subjects. Fluorescence in situ hybridization was applied to quantify specific bacterial groups. RESULTS: Intestinal microbiota composition was substantially altered after smoking cessation as characterized by an increase in key representatives from the phyla of Firmicutes (Clostridium coccoides, Eubacterium rectale, and Clostridium leptum subgroup) and Actinobacteria (HGC bacteria and Bifidobacteria) as well as a decrease in Bacteroidetes (Prevotella spp. and Bacteroides spp.) and Proteobacteria (β- and γ-subgroup of Proteobacteria). CONCLUSIONS: As determined by fluorescence in situ hybridization, an independent direct quantitative microbial approach, we could confirm that intestinal microbiota composition in humans is influenced by smoking. The characteristics of observed microbial shifts suggest a potential mechanistic association to alterations in body weight subsequent to smoking cessation. More importantly, regarding previously described microbial hallmarks of dysbiosis in inflammatory bowel diseases, a variety of observed microbial alterations after smoking cessation deserve further consideration in view of the divergent effect of smoking on the clinical course of Crohn's disease and ulcerative colitis.
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“Smoking reduces gut inflammation, decreases luminal epithelial permeability, and decreases the abundance of Enterobacteriaceae [189, 190].”
From The gut–brain axis in early Parkinson’s disease: from prodrome to prevention (2025) · cites this paper as [190]
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
Structure, function and diversity of the healthy human microbiome
The Human Microbiome Project Consortium (2012) · Nature · doi:10.1038/nature11234 · Cited by 11,726
A metagenome-wide association study of gut microbiota in type 2 diabetes
Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., et al. (2012) · Nature · doi:10.1038/nature11450 · Cited by 6,762
The gut microbiota as an environmental factor that regulates fat storage
Bäckhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F., & Gordon, J. I. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407076101 · Cited by 6,245
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
Gut metagenome in European women with normal, impaired and diabetic glucose control
Karlsson, F. H., Tremaroli, V., Nookaew, I., Bergström, G., Behre, C. J., Fagerberg, B., Nielsen, J., & Bäckhed, F. (2013) · Nature · doi:10.1038/nature12198 · Cited by 3,115
A Molecular View of Microbial Diversity and the Biosphere
Pace, N. R. (1997) · Science · doi:10.1126/science.276.5313.734 · Cited by 2,797
Dethlefsen, L., & Relman, D. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000087107 · Cited by 2,421
Dethlefsen, L., Huse, S., Sogin, M. L., & Relman, D. A. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060280 · Cited by 2,361
Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach
Manichanh, C., Rigottier-Gois, L., Bonnaud, E., Gloux, K., Pelletier, E., Frangeul, L., Nalin, R., Jarrin, C., Chardon, P., Marteau, P., et al. (2006) · Gut · doi:10.1136/gut.2005.073817 · Cited by 2,277
Amann, R., Krumholz, L. R., & Stahl, D. A. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.2.762-770.1990 · Cited by 2,207
Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis
von Wintzingerode, F., Göbel, U. B., & Stackebrandt, E. S. (1997) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.1997.tb00351.x · Cited by 2,085
Metabolic Syndrome and Altered Gut Microbiota in Mice Lacking Toll-Like Receptor 5
Vijay-Kumar, M., Aitken, J. D., Carvalho, F. A., Cullender, T. C., Mwangi, S., Srinivasan, S., Sitaraman, S. V., Knight, R., Ley, R. E., & Gewirtz, A. T. (2010) · Science · doi:10.1126/science.1179721 · Cited by 2,068
The Long-Term Stability of the Human Gut Microbiota
Faith, J. J., Guruge, J. L., Charbonneau, M., Subramanian, S., Seedorf, H., Goodman, A. L., Clemente, J. C., Knight, R., Heath, A. C., Leibel, R. L., et al. (2013) · Science · doi:10.1126/science.1237439 · Cited by 2,058
Manz, W., Amann, R., Ludwig, W., Wagner, M., & SCHLEIFER, K. H. (1992) · Systematic and Applied Microbiology · doi:10.1016/s0723-2020(11)80121-9 · Cited by 2,044
Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination
Berer, K., Mues, M., Koutrolos, M., Rasbi, Z. A., Boziki, M., Johner, C., Wekerle, H., & Krishnamoorthy, G. (2011) · Nature · doi:10.1038/nature10554 · Cited by 1,251
Wallner, G., Amann, R., & Beisker, W. (1993) · Cytometry · doi:10.1002/cyto.990140205 · Cited by 1,227
Human oral, gut, and plaque microbiota in patients with atherosclerosis
Koren, O., Spor, A., Felin, J., Fåk, F., Stombaugh, J., Tremaroli, V., Behre, C. J., Knight, R., Fagerberg, B., Ley, R. E., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1011383107 · Cited by 1,196
Manz, W., Amann, R., Ludwig, W., Vancanneyt, M., & SCHLEIFER, K. H. (1996) · Microbiology · doi:10.1099/13500872-142-5-1097 · Cited by 1,176
Dysbiosis of the faecal microbiota in patients with Crohn’s disease and their unaffected relatives
Joossens, M., Huys, G., Cnockaert, M., De Preter, V., Verbeke, K., Rutgeerts, P., Vandamme, P., & Vermeire, S. (2011) · Gut · doi:10.1136/gut.2010.223263 · Cited by 1,063
Franks, A. H., Harmsen, H. J. M., Raangs, G. C., Jansen, G. J., Schut, F., & Welling, G. W. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.9.3336-3345.1998 · Cited by 1,056
Willing, B. P., Dicksved, J., Halfvarson, J., Andersson, A. F., Lucio, M., Zheng, Z., Järnerot, G., Tysk, C., Jansson, J. K., & Engstrand, L. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.08.049 · Cited by 1,032
Kassinen, A., Krogius-Kurikka, L., Mäkivuokko, H., Rinttilä, T., Paulin, L., Corander, J., Malinen, E., Apajalahti, J., & Palva, A. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.04.005 · Cited by 1,002
Langendijk-Genevaux, P. S., Schut, F., Jansen, G. J., Raangs, G. C., Kamphuis, G. R., Wilkinson, M. H. F., & Welling, G. W. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.8.3069-3075.1995 · Cited by 974
Smoking and Inflammatory Bowel Disease: A Meta-analysis
Mahid, S. S., Minor, K. S., Soto, R. E., Hornung, C. A., & Galandiuk, S. (2006) · Mayo Clinic Proceedings · doi:10.4065/81.11.1462 · Cited by 830
Amann, R., & Fuchs, B. M. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1888 · Cited by 804
Fluorescence in situ hybridization (FISH) for direct visualization of microorganisms
Moter, A., & Göbel, U. B. (2000) · Journal of Microbiological Methods · doi:10.1016/s0167-7012(00)00152-4 · Cited by 786
Intestinal microbiota in patients with nonalcoholic fatty liver disease
Mouzaki, M., Comelli, E. M., Arendt, B. M., Bonengel, J., Fung, S. K., Fischer, S. E., McGilvray, I. D., & Allard, J. P. (2013) · Hepatology · doi:10.1002/hep.26319 · Cited by 749
Roller, C., Wagner, M., Amann, R., Ludwig, W., & SCHLEIFER, K. H. (1994) · Microbiology · doi:10.1099/00221287-140-10-2849 · Cited by 535
Quantification of Bacterial Groups within Human Fecal Flora by Oligonucleotide Probe Hybridization
Sghir, A., Gramet, G., Suau, A., Rochet, V., Pochart, P., & Dore, J. M. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.5.2263-2266.2000 · Cited by 530
Disordered Microbial Communities in the Upper Respiratory Tract of Cigarette Smokers
Charlson, E. S., Chen, J., Custers-Allen, R., Bittinger, K., Li, H., Sinha, R., Hwang, J., Bushman, F. D., & Collman, R. G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015216 · Cited by 437
Smoking Cessation Induces Profound Changes in the Composition of the Intestinal Microbiota in Humans
Biedermann, L., Zeitz, J., Mwinyi, J., Sutter-Minder, E., Rehman, A., Ott, S. J., Steurer-Stey, C. A., Frei, A. L., Frei, P., Scharl, M. M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059260 · Cited by 424
Self-citationExtensive Set of 16S rRNA-Based Probes for Detection of Bacteria in Human Feces
Harmsen, H. J. M., Raangs, G. C., He, T., Degener, J. E., & Welling, G. W. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.6.2982-2990.2002 · Cited by 401
Effects of cigarette smoking on the long-term course of Crohn's disease
Cosnes, J., Carbonnel, F., Beaugerie, L., Quintrec, Y. L., & Jp, G. (1996) · Gastroenterology · doi:10.1053/gast.1996.v110.pm8566589 · Cited by 389
Kang, S., Denman, S. E., Morrison, M., Yu, Z., Dore, J. M., Leclerc, M., & McSweeney, C. S. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21319 · Cited by 365
Highlighting new phylogenetic specificities of Crohn's disease microbiota
Mondot, S., Kang, S., Furet, J., de Cárcer, D. A., McSweeney, C., Morrison, M., Marteau, P., Doré, J., & Leclerc, M. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21436 · Cited by 283
A Molecular Analysis of Fecal and Mucosal Bacterial Communities in Irritable Bowel Syndrome
Codling, C., O’Mahony, L., Shanahan, F., Quigley, E. M. M., & Marchesi, J. R. (2010) · Digestive Diseases and Sciences · doi:10.1007/s10620-009-0934-x · Cited by 243
Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota
Noor, S. O., Ridgway, K., Scovell, L., Kemsley, E. K., Lund, E. K., Jamieson, C., Johnson, I. T., & Narbad, A. (2010) · BMC Gastroenterology · doi:10.1186/1471-230x-10-134 · Cited by 227
Early and Late Weight Gain following Smoking Cessation in the Lung Health Study
O’Hara, P., Connett, J. E., Lee, W. W., Nides, M. A., Murray, R. A., & Wise, R. A. (1998) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009706 · Cited by 227
Bibiloni, R., Mangold, M., Madsen, K. L., Fedorak, R. N., & Tannock, G. W. (2006) · Journal of Medical Microbiology · doi:10.1099/jmm.0.46498-0 · Cited by 226
Benjamin, J. L., Hedin, C. R. H., Koutsoumpas, A. L., Ng, S. C., McCarthy, N. E., Prescott, N. J., Pessôa‐Lopes, P., Mathew, C. G., Sanderson, J. D., Hart, A. L., et al. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21864 · Cited by 221
Impact of cessation of smoking on the course of ulcerative colitis
Beaugerie, L., Massot, N., Carbonnel, F., Cattan, S., Gendre, J., & Cosnes, J. (2001) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2001.03944.x · Cited by 212
Weight change following smoking cessation: The role of food intake and exercise
Rodin, J. (1987) · Addictive Behaviors · doi:10.1016/0306-4603(87)90045-1 · Cited by 134
Analysis of the Human Gut Microbiome and Association With Disease
Wu, G. D., & Lewis, J. D. (2013) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2013.03.038 · Cited by 113
Effects of light smoking consumption on the clinical course of Crohnʼs disease
Seksik, P., Nion–Larmurier, I., Sokol, H., Beaugerie, L., & Cosnes, J. (2008) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20828 · Cited by 97
Stamler, J. F., Rains-Clearman, D., Lenz-Litzow, K., Tillotson, J., & Grandits, G. (1997) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/65.1.374s · Cited by 39
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Metadata
- Authors
- Biedermann, L., Brülisauer, K., Zeitz, J., Frei, P., Scharl, M., Vavricka, S. R., Fried, M., Loessner, M. J., Rogler, G., & Schuppler, M.
- Affiliations
- University of Zurich (CH)
- ETH Zurich (CH)
- University Hospital Zurich (CH)
- ORCID
- Venue
- Inflammatory Bowel Diseases
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-09
- Volume
- 20
- Issue
- 9
- Pages
- 1496-1501
- ISSN
- 1078-0998 (ISSN-L)
- OpenAlex
- W2024172588
- Cited by
- 178
- References
- 47
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 19 · 2023: 16 · 2022: 13 · 2021: 19 · 2020: 24 · 2019: 15 · 2018: 16 · 2017: 17 · 2016: 11 · 2015: 13 · 2014: 1
- FWCI
- 5.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Inflammatory Bowel Diseases (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Smoking Behavior and Cessation
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- smoking cessation, gut microbiota
- MeSH terms
- DNA, Bacterial, Feces, Humans, Intestines, Colony Count, Microbial, Oligonucleotide Probes, Smoking Cessation, In Situ Hybridization, Fluorescence, Microbiota
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