Smoking and microbiome in oral, airway, gut and some systemic diseases

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Abstract

The human microbiome harbors a diverse array of microbes which establishes a mutually beneficial relation with the host in healthy conditions, however, the dynamic homeostasis is influenced by both host and environmental factors. Smoking contributes to modifications of the oral, lung and gut microbiome, leading to various diseases, such as periodontitis, asthma, chronic obstructive pulmonary disease, Crohn’s disease, ulcerative colitis and cancers. However, the exact causal relationship between smoking and microbiome alteration remains to be further explored.

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Most cited references 131

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While originally characterized as a collection of related syndromes, cystic fibrosis (CF) is now recognized as a single disease whose diverse symptoms stem from the wide tissue distribution of the gene product that is defective in CF, the ion channel and regulator, cystic fibrosis transmembrane conductance regulator (CFTR). Defective CFTR protein impacts the function of the pancreas and alters the consistency of mucosal secretions. The latter of these effects probably plays an important role in the defective resistance of CF patients to many pathogens. As the modalities of CF research have changed over the decades from empirical histological studies to include biophysical measurements of CFTR function, the clinical management of this disease has similarly evolved to effectively address the ever-changing spectrum of CF-related infectious diseases. These factors have led to the successful management of many CF-related infections with the notable exception of chronic lung infection with the gram-negative bacterium Pseudomonas aeruginosa. The virulence of P. aeruginosa stems from multiple bacterial attributes, including antibiotic resistance, the ability to utilize quorum-sensing signals to form biofilms, the destructive potential of a multitude of its microbial toxins, and the ability to acquire a mucoid phenotype, which renders this microbe resistant to both the innate and acquired immunologic defenses of the host.

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Cigarette smoking and the oral microbiome in a large study of American adults.

Jing Wu, Brandilyn A. Peters, Christine Dominianni … (2016)

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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Author and article information

Contributors

Chunrong Huang: huangchr5@mail2.sysu.edu.cn

Guochao Shi: shiguochao@hotmail.com

Journal

Journal ID (nlm-ta): J Transl Med

Journal ID (iso-abbrev): J Transl Med

Title: Journal of Translational Medicine

Publisher: BioMed Central (London )

ISSN (Electronic): 1479-5876

Publication date (Electronic): 15 July 2019

Publication date PMC-release: 15 July 2019

Publication date Collection: 2019

Volume: 17

Electronic Location Identifier: 225

Affiliations

[1 ]ISNI 0000 0004 0368 8293, GRID grid.16821.3c, Department of Pulmonary and Critical Care Medicine, Ruijin Hospital, , Shanghai Jiao Tong University School of Medicine, ; 197, Rui Jin Er Road, Shanghai, 200025 People’s Republic of China

[2 ]ISNI 0000 0004 0368 8293, GRID grid.16821.3c, Institute of Respiratory Diseases, , Shanghai Jiao Tong University School of Medicine, ; 197, Rui Jin Er Road, Shanghai, 200025 People’s Republic of China

Article

Publisher ID: 1971

DOI: 10.1186/s12967-019-1971-7

PMC ID: 6632217

PubMed ID: 31307469

SO-VID: 528700b1-084b-4d78-8d34-a6177f80f84f

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 17 March 2019

Date accepted : 5 July 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 81770025

Award Recipient : Guochao Shi

Custom metadata

ScienceOpen disciplines: Medicine

Keywords: microbiome,oral,lung,gut,disease

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ScienceOpen disciplines: Medicine

Keywords: microbiome, oral, lung, gut, disease

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Smoking and microbiome in oral, airway, gut and some systemic diseases

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Abstract

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Most cited references 131

Lung infections associated with cystic fibrosis.

Tobacco smoke and involuntary smoking.

Cigarette smoking and the oral microbiome in a large study of American adults.

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Cited by 101

Most referenced authors 3,932