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Cigarette smoking and the oral microbiome in a large study of American adults
Open accessAbstract
Oral microbiome dysbiosis is associated with oral disease and potentially with systemic diseases; however, the determinants of these microbial imbalances are largely unknown. In a study of 1204 US adults, we assessed the relationship of cigarette smoking with the oral microbiome. 16S rRNA gene sequencing was performed on DNA from oral wash samples, sequences were clustered into operational taxonomic units (OTUs) using QIIME and metagenomic content was inferred using PICRUSt. Overall oral microbiome composition differed between current and non-current (former and never) smokers (P<0.001). Current smokers had lower relative abundance of the phylum Proteobacteria (4.6%) compared with never smokers (11.7%) (false discovery rate q=5.2 × 10−7), with no difference between former and never smokers; the depletion of Proteobacteria in current smokers was also observed at class, genus and OTU levels. Taxa not belonging to Proteobacteria were also associated with smoking: the genera Capnocytophaga, Peptostreptococcus and Leptotrichia were depleted, while Atopobium and Streptococcus were enriched, in current compared with never smokers. Functional analysis from inferred metagenomes showed that bacterial genera depleted by smoking were related to carbohydrate and energy metabolism, and to xenobiotic metabolism. Our findings demonstrate that smoking alters the oral microbiome, potentially leading to shifts in functional pathways with implications for smoking-related diseases.
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“Such dysbiosis is prompted by various factors, including host diet, inflammatory responses, systemic disruptions, and habits such as alcohol intake, smoking tobacco and consuming alcohol.50, 180, 181, 182, 183, 184, 185, 186”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [185]
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“34 perimenopausal 286 smoking 948 nonsmoking [21-65] years old”
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“A crucial factor in the inflammatory processes in the oral cavity is smoking [28–31].”
BackgroundThe Oral Microbiome and Lung Cancer Risk: An Analysis of 3 Prospective Cohort Studies
Vogtmann, E., Hua, X., Yu, G., Purandare, V., Hullings, A. G., Shao, D., Wan, Y., Li, S., Dagnall, C. L., Jones, K. M., et al. (2022) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djac149 · Cited by 88
Riverain-Gillet, É., Guet‐Revillet, H., Jaïs, J., Ungeheuer, M., Duchatelet, S., Delage, M., Lam, T., Hovnanian, A., Nassif, A., & Join‐Lambert, O. (2020) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2020.02.046 · Cited by 89
Recent Advances in Understanding the Structure and Function of the Human Microbiome
Mousa, W. K., Chehadeh, F., & Husband, S. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.825338 · Cited by 91
Martina, E., Campanati, A., Diotallevi, F., & Offidani, A. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020466 · Cited by 81
“reduction of Neisseria species in the oral cavity of smokers, with a theoretical improvement of ACH levels [100].”
BackgroundEnvironmental factors and periodontal microbiome
Buduneli, N. (2020) · Periodontology 2000 · doi:10.1111/prd.12355 · Cited by 83
Oral Microbiota: Microbial Biomarkers of Metabolic Syndrome Independent of Host Genetic Factors
Si, J., Lee, C., & Ko, G. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00516 · Cited by 80
“, 2008), diet (Bradshaw and Marsh, 1998), and smoke (Wu et al., 2016).”
BackgroundSalivary microbiome in non-oral disease: A summary of evidence and commentary
Acharya, A., Chan, Y., Kheur, S. M., Jin, L., Watt, R. M., & Mattheos, N. (2017) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2017.07.019 · Cited by 77
“In contrast, higher Leptotrichia has been associated with cancer in 2 studies (Torres et al., 2015; Xu et al., 2014).”
Koh, H., Blaser, M. J., & Li, H. (2017) · Microbiome · doi:10.1186/s40168-017-0262-x · Cited by 78
Self-citationMa, C., Chen, C., Jia, L., He, X., & Zhang, B. (2019) · AMB Express · doi:10.1186/s13568-019-0913-3 · Cited by 77
Sociodemographic variation in the oral microbiome
Renson, A., Jones, H. E., Beghini, F., Segata, N., Zolnik, C. P., Usyk, M., Moody, T. U., Thorpe, L. E., Burk, R. D., Waldron, L., et al. (2019) · Annals of Epidemiology · doi:10.1016/j.annepidem.2019.03.006 · Cited by 75
“In particular, evidence supports the existence of socioeconomic status disparities in smoking prevalence [49, 50], and effects of smoking on the oral microbiome [51, 52][CITATION PENDING – Beghini 2018 Companion Paper].”
BackgroundLi, D., Fang, Y., Lu, J. X., Sun, J., Zhao, X., Hou, N., & Xing, J. (2023) · Chemical Engineering Journal · doi:10.1016/j.cej.2023.141495 · Cited by 75
The Complicated Relationship of Short-Chain Fatty Acids and Oral Microbiome: A Narrative Review
Leonov, G. E., Varaeva, Y. R., Николаевна, Л. Е., & Starodubova, A. V. (2023) · Biomedicines · doi:10.3390/biomedicines11102749 · Cited by 78
Citizen-science reveals changes in the oral microbiome in Spain through age and lifestyle factors
Willis, J. R., Saus, E., Iraola‐Guzmán, S., Księżopolska, E., Cozzuto, L., Bejarano, L. A., Andreu, N., Alloza-Trabado, M., Blanco, A., Puig-Sola, A., et al. (2022) · npj Biofilms and Microbiomes · doi:10.1038/s41522-022-00279-y · Cited by 73
Barrett's esophagus is associated with a distinct oral microbiome
Snider, E. J., Compres, G., Freedberg, D. E., Giddins, M. J., Khiabanian, H., Lightdale, C. J., Nobel, Y. R., Toussaint, N. C., Uhlemann, A.-C., & Abrams, J. A. (2018) · Clinical and Translational Gastroenterology · doi:10.1038/s41424-018-0005-8 · Cited by 72
Zhao, X., Chen, J., Guo, M., Li, C., Hou, N., & Bai, S. (2022) · Chemical Engineering Journal · doi:10.1016/j.cej.2022.137460 · Cited by 73
Smoking and periodontal microorganisms
Hanioka, T., Morita, M., Yamamoto, T., Inagaki, K., Wang, P., Ito, H., Morozumi, T., Takeshita, T., Suzuki, N., Shigeishi, H., et al. (2019) · Japanese Dental Science Review · doi:10.1016/j.jdsr.2019.03.002 · Cited by 71
Smoking-induced microbial dysbiosis in health and disease
Shapiro, H., Goldenberg, K., Ratiner, K., & Elinav, E. (2022) · Clinical Science · doi:10.1042/cs20220175 · Cited by 77
Electronic Cigarette Use Promotes a Unique Periodontal Microbiome
Thomas, S. C., Xu, F., Pushalkar, S., Lin, Z., Thakor, N., Vardhan, M., Flaminio, Z., Khodadadi‐Jamayran, A., Vasconcelos, R., Akapo, A., et al. (2022) · mBio · doi:10.1128/mbio.00075-22 · Cited by 82
PLSDA-batch: a multivariate framework to correct for batch effects in microbiome data
Wang, Y., & Cao, K. L. (2023) · Briefings in Bioinformatics · doi:10.1093/bib/bbac622 · Cited by 68
Role of Oral Bacteria in the Development of Oral Squamous Cell Carcinoma
Li, Q., Hu, Y., Zhou, X., Liu, S., Han, Q., & Cheng, L. (2020) · Cancers · doi:10.3390/cancers12102797 · Cited by 71
“Alcohol dehydrogenase 2 (ALDH2) is the most effective enzyme in the detoxification of the alcohol metabolite acetaldehyde [110], and ALDH2 polymorphism may modify the association between alcohol use and periodontal pathogenic bacteria, and thus, affect the percentage of this kind of bacteria [109], while tobacco alter…”
BackgroundSymbiont community diversity is more variable in corals that respond poorly to stress
Howe‐Kerr, L. I., Bachelot, B., Wright, R. M., Kenkel, C. D., Bay, L. K., & Correa, A. M. S. (2020) · Global Change Biology · doi:10.1111/gcb.14999 · Cited by 67
“…these symbionts can now be added to the growing list of microbial communities, particularly those associated with various organ systems in primates (Chen et al., 2015; Halfvarson et al., 2017; Moeller et al., 2013; Wu et al., 2016) that exhibit increased stochasticity under environmental stressors.”
BackgroundRecent advances in modulating the microbiome
Quigley, E. M. M., & Gajula, P. (2020) · F1000Research · doi:10.12688/f1000research.20204.1 · Cited by 69
Salivary microbiome with gastroesophageal reflux disease and treatment
Kawar, N. I., Park, S. G., SCHWARTZ, J. L., Callahan, N. F., Obrez, A., Yang, B. J., Chen, Z., & Adami, G. R. (2021) · Scientific Reports · doi:10.1038/s41598-020-80170-y · Cited by 66
Li, W., & Ma, Z. S. (2020) · Scientific Reports · doi:10.1038/s41598-019-56561-1 · Cited by 66
The Oral Microbiome Bank of China
Xian, P., Zhou, X., Xu, X., Yuqing, L., Li, Y., Li, J., Su, X., Huang, S., Xu, J., & Liao, G. (2018) · International Journal of Oral Science · doi:10.1038/s41368-018-0018-x · Cited by 65
Radaic, A., Ganther, S., Kamarajan, P., Grandis, J. R., Yom, S. S., & Kapila, Y. L. (2021) · Periodontology 2000 · doi:10.1111/prd.12388 · Cited by 66
“89,90 Among the enriched bacteria, F. nucleatum is also able to damage host cell deoxyribonucleic acid (DNA).”
Wei, M., Xu, C., Chen, J., Zhu, C., Li, J., & Lv, G. (2017) · Atmospheric chemistry and physics · doi:10.5194/acp-17-5253-2017 · Cited by 65
“The PICRUSt can be used to predict the metabolic function pathway from corresponding bacteria and archaea and provide a community’s functional capabilities based on the 16S rRNA gene sequence (Langille et al., 2013; Corrigan et al., 2015; Wu et al., 2016).”
MethodDysbiosis of the buccal mucosa microbiome in primary Sjögren’s syndrome patients
van der Meulen, T. A., Harmsen, H. J. M., Bootsma, H., Liefers, S. C., Vila, A. V., Zhernakova, A., Fu, J., Wijmenga, C., Spijkervet, F. K. L., Kroese, F. G. M., et al. (2018) · Rheumatology · doi:10.1093/rheumatology/key215 · Cited by 68
“Under the Skin” and into the Gut: Social Epidemiology of the Microbiome
Dowd, J. B., & Renson, A. (2018) · Current Epidemiology Reports · doi:10.1007/s40471-018-0167-7 · Cited by 66
“Several human studies suggest that tobacco smoking also alters the oral microbiome, with structural changes consistent with increased anaerobiosis [89] along with proliferation of pathogens and decreased colonization resistance in oral biofilms [90].”
BackgroundThe effect of smoking on caries-related microorganisms
Wu, J., Li, M., & Huang, R. (2019) · Tobacco Induced Diseases · doi:10.18332/tid/105913 · Cited by 64
Self-citationWang, K., Huang, Y., Zhang, Z., Liao, J., Ding, Y., Fang, X., Liu, L., Luo, J., & Kong, J. (2019) · Medical Science Monitor · doi:10.12659/msm.915332 · Cited by 64
“Exposure to xenobiotics, such as carcinogens, insecticides, and drugs, and their deposition in pulmonary tissues were considered as initial factors for lung cancer development [36].”
BackgroundRevealing oral microbiota composition and functionality associated with heavy cigarette smoking
Bataineh, M. T. A., Dash, N. R., Elkhazendar, M., Alnusairat, D. M. H., Darwish, I. M. I., Al‐Hajjaj, M. S., & Hamid, Q. A. (2020) · Journal of Translational Medicine · doi:10.1186/s12967-020-02579-3 · Cited by 63
Tumor-Associated Microbiome: Where Do We Stand?
Oliva, M., Mulet-Margalef, N., Ochoa-de-Olza, M., Napoli, S., Mas-Lloret, J., Laquente, B., Alemany, L., Duell, E. J., Nuciforo, P. G., & Moreno, V. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031446 · Cited by 63
“These compartments are constantly exposed to external aggressions such as smoking, alcohol consumption, or infections, which can alter their microbiome composition [62,63].”
BackgroundOld age and other factors associated with salivary microbiome variation
SCHWARTZ, J. L., Peña, N., Kawar, N. I., Zhang, A., Callahan, N. F., Robles, S. J., Griebel, A., & Adami, G. R. (2021) · BMC Oral Health · doi:10.1186/s12903-021-01828-1 · Cited by 69
“This was expected as these conditions were already known to alter the salivary microbiome [19, 32].”
BackgroundOral Microbiome: Getting to Know and Befriend Neighbors, a Biological Approach
Bacali, C., Vulturar, R., Buduru, S. D., Cozma, A., Fodor, A., Chiş, A., LUCACIU, O. P., Damian, L. O., & Moldovan, M. (2022) · Biomedicines · doi:10.3390/biomedicines10030671 · Cited by 63
Microbiota in the apical root canal system of tooth with apical periodontitis
Qian, W., Ma, T., Ye, M., Li, Z., Liu, Y., & Hao, P. (2019) · BMC Genomics · doi:10.1186/s12864-019-5474-y · Cited by 62
Komatsu, K., Shiba, T., Takeuchi, Y., Watanabe, T., Koyanagi, T., Nemoto, T., Shimogishi, M., Shibasaki, M., Katagiri, S., Kasugai, S., et al. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.596490 · Cited by 63
Metadata
- Authors
- Wu, J., Peters, B. A., Dominianni, C., Zhang, Y., Pei, Z., Yang, L., Ma, Y., Purdue, M. P., Jacobs, E. J., Gapstur, S. M., Li, H., Alekseyenko, A. V., Hayes, R. B., & Ahn, J.
- Affiliations
- NYU Langone Health (US)
- VA NY Harbor Healthcare System (US)
- Ontario Institute for Cancer Research (CA)
- American Cancer Society (US)
- Medical University of South Carolina (US)
- Corresponding author
- Ahn, Jiyoung
- ORCID
- Venue
- The ISME Journal
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-03-25
- Volume
- 10
- Issue
- 10
- Pages
- 2435-2446
- ISSN
- 1751-7362 (ISSN-L)
- 1751-7370
- PMC
- PMC5030690
- OpenAlex
- W2324897069
- Cited by
- 572
- References
- 57
- Citations by year
- 2026: 43 · 2025: 46 · 2024: 66 · 2023: 59 · 2022: 57 · 2021: 83 · 2020: 67 · 2019: 44 · 2018: 52 · 2017: 50 · 2016: 4
- FWCI
- 74.61
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The ISME Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Cancer Society
- U.S. Department of Veterans Affairs
- National Institutes of Health
- National Cancer Institute (U01CA170948, R01CA159036, R21CA183887, R03CA159414, U01CA182370, R01CA164964, P30CA016087)
- Topics
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › General Dentistry › Oral Health Pathology and Treatment
- Keywords
- cigarette smoking, oral microbiota, dysbiosis, Proteobacteria, Capnocytophaga, Peptostreptococcus, Leptotrichia, Streptococcus, Atopobium, xenobiotic metabolism, carbohydrate metabolism, energy metabolism, smoking-related diseases
- MeSH terms
- Adult, Bacteria, Female, Humans, Male, Mouth, RNA, Ribosomal, 16S, Smoking, United States, Metagenome, Young Adult, Metagenomics, Microbiota, Dysbiosis
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