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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Dysbiosis is prompted by various factors, including host diet, inflammatory responses, systemic disruptions, and habits such as alcohol intake, smoking tobacco and consuming alcohol.
“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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“For example, an altered microbiota composition was noted in studies of 62 swabs from the tonsillar pillars [3], 200 subgingival samples [4], 30 marginal and subgingival plaque and gingival crevicular fluid samples [5], and oral wash samples comparing 13–41 current smokers with 77–194 never smokers in 4 groups [6] and…”
MethodThe oral microbiota – a mechanistic role for systemic diseases
Jia, G., Zhi, A., Lai, P. F. H., Wang, G., Xia, Y., Xiong, Z., Zhang, H., Che, N., & Ai, L. (2018) · BDJ · doi:10.1038/sj.bdj.2018.217 · Cited by 183 · see citing works
Amer, A., Galvin, S., Healy, C. M., & Moran, G. P. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02391 · Cited by 182 · see citing works
“Fusobacterium spp. have also been associated with cancers of the esophagus and were shown by PCR to be significantly enriched in esophageal cancer samples compared to normal esophageal mucosa (Yamamura et al., 2016).”
BackgroundFu, Y., Lyu, J., & Wang, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1277102 · Cited by 175 · see citing works
Betel nut chewing, oral premalignant lesions, and the oral microbiome
Hernandez, B. Y., Zhu, X., Goodman, M. T., Gatewood, R. R., Mendiola, P., Quinata, K. M. G., & Paulino, Y. C. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172196 · Cited by 174 · see citing works
Progress in Oral Microbiome Related to Oral and Systemic Diseases: An Update
Lee, Y.-H., Chung, S., Auh, Q., Hong, S.-J., Lee, Y.-A., Jung, J.-H., Lee, G.-J., Park, H., Shin, S.-I., & Hong, J.-Y. (2021) · Diagnostics · doi:10.3390/diagnostics11071283 · Cited by 144 · see citing works
“[46] reported that the relative abundance of the phylum Proteobacteria was lower in current smokers than in never-smokers, with no difference between former and never-smokers.”
BackgroundOral Dysbiotic Communities and Their Implications in Systemic Diseases
Sudhakara, P., Gupta, A., Bhardwaj, A., & Wilson, A. (2018) · Dental journal · doi:10.3390/dj6020010 · Cited by 150 · see citing works
“Other major 232 factors causing oral dysbiosis include poor oral hygiene, dietary habits, smoking, gingival 233 inflammation, genetic difference and dysfunction of salivary glands such as activity of salivary 234 proteins [73-75].”
BackgroundA tale of two risks: smoking, diabetes and the subgingival microbiome
Ganesan, S. M., Joshi, V., Fellows, M. L., Dabdoub, S. M., Nagaraja, H. N., OʼDonnell, B., Deshpande, N. R., & Kumar, P. (2017) · The ISME Journal · doi:10.1038/ismej.2017.73 · Cited by 164 · see citing works
“The effects of smoking on the oral microbiome have been extensively studied in recent years and several investigations have established that the oral microbiome shifts in response to this environmental press (Fullmer et al., 2009; Delima et al., 2010; Shchipkova et al., 2010a; Kumar, 2012; Wu et al., 2016).”
BackgroundRampelli, S., Soverini, M., D’Amico, F., Barone, M., Tavella, T., Monti, D., Capri, M., Astolfi, A., Brigidi, P., Biagi, E., et al. (2020) · mSystems · doi:10.1128/msystems.00124-20 · Cited by 161 · see citing works
Oral microbiota in human health and disease: A perspective
Santacroce, L., Passarelli, P. C., Azzolino, D., Bottalico, L., Charitos, I. A., Cazzolla, A. P., Colella, M., Topi, S., Godoy, F. G., & D’Addona, A. (2023) · Experimental Biology and Medicine · doi:10.1177/15353702231187645 · Cited by 168 · see citing works
Leptotrichia species in human infections II
Eribe, E. R. K., & Olsen, I. (2017) · Journal of Oral Microbiology · doi:10.1080/20002297.2017.1368848 · Cited by 158 · see citing works
“[57] reported recovery of Leptotrichia species, together with Veillonella parvula and Peptostreptococcus species in low amounts in cigarette smokers’ mouthwash (Table 2) [57,90,91].”
Willis, J. R., González‐Torres, P., Pittis, A. A., Bejarano, L. A., Cozzuto, L., Andreu, N., Alloza-Trabado, M., Valentín, A., Księżopolska, E., Onywera, H., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0592-3 · Cited by 154 · see citing works
“[11, 12], diet [13–16], or hygiene habits [17–19].”
Jones, A. M., Vanhatalo, A., Seals, D. R., Rossman, M. J., Piknova, B., & Jonvik, K. L. (2021) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002470 · Cited by 156 · see citing works
Hsiao, J., Chang, C., Lee, W., Huang, C., Ou, C., Tsai, S., Chen, K.-C., Huang, J.-S., Wong, T.-Y., Lai, Y.-H., et al. (2018) · Carcinogenesis · doi:10.1093/carcin/bgy053 · Cited by 152 · see citing works
“showed that smoking was associated with depletion of bacteria genera that are associated with carbohydrate and energy metabolism and xenobiotic metabolism (60).”
BackgroundAcquisition and establishment of the oral microbiota
Kaan, A. M., Kahharova, D., & Zaura, E. (2021) · Periodontology 2000 · doi:10.1111/prd.12366 · Cited by 142 · see citing works
Apatzidou, D. A. (2022) · Periodontology 2000 · doi:10.1111/prd.12449 · Cited by 150 · see citing works
Kumar, A., Panda, M., Das, A. K., Rahman, T., Das, R., Das, K., Sarma, A., Kataki, A., & Chattopadhyay, I. (2020) · Archives of Microbiology · doi:10.1007/s00203-020-02011-w · Cited by 135 · see citing works
Karst rocky desertification progress: Soil calcium as a possible driving force
Tang, J. Y., Tang, X., Qin, Y., He, Q., Yi, Y., & Ji, Z. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.08.242 · Cited by 134 · see citing works
Stewart, C. J., Auchtung, T. A., Ajami, N. J., Velasquez, K. M., Smith, D. P., Garza, R. D. L., Salas, R., & Petrosino, J. F. (2018) · PeerJ · doi:10.7717/peerj.4693 · Cited by 126 · see citing works
“Indeed, smoking tobacco cigarettes has previously been shown to significantly alter the bacterial community in oral and lung samples (Charlson et al., 2010; Kozlowska et al., 2013; Mason et al., 2014; Wu et al., 2016).”
BackgroundInfluentialMicrobiomic differences in tumor and paired-normal tissue in head and neck squamous cell carcinomas
Wang, H., Funchain, P., Bebek, G., Altemus, J. B., Zhang, H., Niazi, F., Peterson, C., Lee, W. T., Burkey, B. B., & Eng, C. (2017) · Genome Medicine · doi:10.1186/s13073-017-0405-5 · Cited by 125 · see citing works
“However, recent studies have identified microbiomic shifts in the oral cavity associated with cigarette smoking, and in the gastrointestinal tract associated with alcohol consumption [15, 16].”
BackgroundBicknell, B. T., Liebert, A. D., Borody, T. J., Herkes, G., McLachlan, C. S., & Kiat, H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24119577 · Cited by 129 · see citing works
“Smoking has been shown to increase potential pathogens and decrease bene-ficial bacteria [178].”
Lim, Y., Fukuma, N. M., Totsika, M., Kenny, L., Morrison, M., & Punyadeera, C. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00267 · Cited by 119 · see citing works
“Studies have shown that smoking affects the oral microbiome; the oral microbiome panel will have to be tested on age-matched active smoking individuals in the future to avoid overrepresentation (Wu et al., 2016).”
BackgroundElectronic Cigarettes and Oral Health
Holliday, R., Chaffee, B. W., Jakubovics, N. S., Kist, R., & Preshaw, P. M. (2021) · Journal of Dental Research · doi:10.1177/00220345211002116 · Cited by 119 · see citing works
“For example, analysis of oral wash samples from 1,204 US adults identified depletion of Proteobacteria and enrichment for Firmicutes and Actinobacteria in smokers (Wu et al. 2016).”
BackgroundYang, J., Mu, X., Wang, Y., Zhu, D., Zhang, J., Liang, C., Chen, B., Wang, J., Zhao, C., Zuo, Z., et al. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00520 · Cited by 118 · see citing works
“However, cigarette smoking may lead to oral microbiome imbalance, thereby causing potential shifts in functional pathways, and having implications for smoking-related diseases (21).”
BackgroundAssessing the Variation within the Oral Microbiome of Healthy Adults
Nearing, J. T., DeClercq, V., Limbergen, J. V., & Langille, M. G. I. (2020) · mSphere · doi:10.1128/msphere.00451-20 · Cited by 112 · see citing works
“Various studies have focused on individual factors that may cause shifts in the oral microbiome, such as ethnicity (1, 23), alcohol consumption (24), smoking (25), obesity (26, 27), and dietary patterns (28).”
BackgroundAssociation Between Oral Microbiota and Cigarette Smoking in the Chinese Population
Jia, Y., Liao, Y., He, Y., Zheng, M., Tong, X., Xue, W., Zhang, J., Yuan, L., Zhang, W., & Jia, W. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.658203 · Cited by 116 · see citing works
The microbiome and oral cancer: More questions than answers
Healy, C. M., & Moran, G. P. (2018) · Oral Oncology · doi:10.1016/j.oraloncology.2018.12.003 · Cited by 107 · see citing works
Profiling the Salivary microbiome of the Qatari population
Murugesan, S., Ahmad, S. F. A., Singh, P., Saadaoui, M., Kumar, M., & Khodor, S. A. (2020) · Journal of Translational Medicine · doi:10.1186/s12967-020-02291-2 · Cited by 105 · see citing works
Zaura, E., Pappalardo, V. Y., Buijs, M. J., Volgenant, C. M. C., & Brandt, B. W. (2020) · Periodontology 2000 · doi:10.1111/prd.12359 · Cited by 105 · see citing works
Influence of cigarette smoking on the human duodenal mucosa-associated microbiota
Shanahan, E. R., Shah, A., Koloski, N. A., Walker, M. M., Talley, N. J., Morrison, M., & Holtmann, G. (2018) · Microbiome · doi:10.1186/s40168-018-0531-3 · Cited by 104 · see citing works
Sami, A., Elimairi, I., Stanton, C., Ross, R. P., & Ryan, C. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218061 · Cited by 105 · see citing works
“Furthermore, commensal bacteria such as Neisseria, in particular, seem to be lost amongst smokers [114,116], while an abundance of Fusobacteria, Mogibacterium and Tannerella occurs [117].”
BackgroundVariations in the oral microbiome are associated with depression in young adults
Wingfield, B., Lapsley, C. R., McDowell, A., Miliotis, G., McLafferty, M., O’Neill, S. M., Coleman, S., McGinnity, T. M., Bjourson, A. J., & Murray, E. K. (2021) · Scientific Reports · doi:10.1038/s41598-021-94498-6 · Cited by 103 · see citing works
Genetic influences on the human oral microbiome
Demmitt, B. A., Corley, R. P., Huibregtse, B. M., Keller, M. C., Hewitt, J. K., McQueen, M. B., Knight, R. D., McDermott, I., & Krauter, K. S. (2017) · BMC Genomics · doi:10.1186/s12864-017-4008-8 · Cited by 99 · see citing works
Wolf, A., Moissl‐Eichinger, C., Perras, A., Koskinen, K., Tomazic, P. V., & Thurnher, D. (2017) · Scientific Reports · doi:10.1038/s41598-017-06361-2 · Cited by 95 · see citing works
Explainable AI reveals changes in skin microbiome composition linked to phenotypic differences
Carrieri, A. P., Haiminen, N., Maudsley-Barton, S., Gardiner, L., Murphy, B., Mayes, A. E., Paterson, S., Grimshaw, S. G., Winn, M., Shand, C., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-83922-6 · Cited by 96 · see citing works
“34 perimenopausal 286 smoking 948 nonsmoking [21-65] years old”
BackgroundSalivary Microbiota for Gastric Cancer Prediction: An Exploratory Study
Huang, K., Gao, X., Wu, L., Yan, B., Wang, Z., Zhang, X., Peng, L., Yu, J.-F., Sun, G., & Yang, Y. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.640309 · Cited by 89 · see citing works
The Role of Interleukin 6 in Periodontitis and Its Complications
Mazurek−Mochol, M., Bonsmann, T., Mochol, M., Poniewierska-Baran, A., & Pawlik, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042146 · Cited by 89 · see citing works
“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 · see citing works
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 87 · see citing works
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 89 · see citing works
Martina, E., Campanati, A., Diotallevi, F., & Offidani, A. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020466 · Cited by 81 · see citing works
“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 80 · see citing works
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 79 · see citing works
“, 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 · see citing works
“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 77 · see citing works
Self-citationMa, C., Chen, C., Jia, L., He, X., & Zhang, B. (2019) · AMB Express · doi:10.1186/s13568-019-0913-3 · Cited by 76 · see citing works
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 76 · see citing works
“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 · see citing works
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 74 · see citing works
Citizen-science reveals changes in the oral microbiome in Spain through age and lifestyle factors
Willis, J., Saus, E., Iraola-Guzmán, S., Księżopolska, E., Cozzuto, L., Bejarano, L. A., Andreu-Somavilla, 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 68 · see citing works
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 · see citing works
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 72 · see citing works
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 · see citing works
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 70 · see citing works
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 70 · see citing works
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 · see citing works
Role of Oral Bacteria in the Development of Oral Squamous Cell Carcinoma
Li, Q., Hu, Y., Zhou, X.-D., Liu, S.-Y., Han, Q., & Cheng, L. (2020) · Cancers · doi:10.3390/cancers12102797 · Cited by 58 · see citing works
“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 · see citing works
“…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 68 · see citing works
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 · see citing works
Li, W., & Ma, Z. S. (2020) · Scientific Reports · doi:10.1038/s41598-019-56561-1 · Cited by 65 · see citing works
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 · see citing works
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 64 · see citing works
“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 · see citing works
“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) · Lara D. Veeken · doi:10.1093/rheumatology/key215 · Cited by 65 · see citing works
“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 65 · see citing works
“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].”
BackgroundBostanghadiri, N., Kouhzad, M., Taki, E., Elahi, Z., Khoshbayan, A., Navidifar, T., & Darban-Sarokhalil, D. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1431785 · Cited by 61 · see citing works
“Numerous toxicants from cigarette smoke can disrupt the oral cavity’s microbial diversity by antibiotic effects, oxygen reduction, or another way (Wu et al., 2016).”
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 · see citing works
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 · see citing works
“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 · see citing works
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 62 · see citing works
“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 66 · see citing works
“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., Cozma, A., Fodor, A., Chiș, A., Lucaciu, O., Damian, L., & Moldovan, M. (2022) · Biomedicines · doi:10.3390/biomedicines10030671 · Cited by 58 · see citing works
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 · see citing works
- 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 › Periodontics › 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
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 ›
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