Different responses of the oral, nasal and lung microbiomes to cigarette smoke

Abstract

To examine the role of smoking on the bacterial community composition of the upper and the lower respiratory tract, a monocentric, controlled prospective study was performed, including healthy smokers, ex-smokers and never-smokers. Smokers were further grouped according to their smoking history. Bacterial diversity was analysed using a molecular barcoding approach based on directly extracted DNA. Our study shows for the first time distinct bacterial response patterns in the upper and lower respiratory tract to cigarette smoking leading to a higher abundance of opportunistic pathogens. The clinical significance of these dysbioses for health needs to be further explored.

Trial registration: ClinicalTrials.gov NCT03562442.

Keywords: tobacco and the lung.

Conflict of interest statement

Competing interests: None declared.

© Author(s) (or their employer(s)) 2022. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

Figures

Figure 1

Influence of cigarette smoke on the nasal microbiota. (A) Upper panel: Correlation array of smoking factors with nasal cavity (n=46) genera across smoking parameters and transformed sequencing data (centred log-ratio transformation) to remove constrains introduced by the compositionality of the data. The size of the circles shows the significance of the correlation (bigger circle corresponds to a lower p value). The colour of the circle indicates the Pearson correlation between 1 (blue, positive correlation) and −1 (red, negative correlation) between taxa (horizontal) and smoking parameters (vertical). Lower panel: Pearson correlation of bacterial taxa with smoking-related parameters. Dots represent samples. The line corresponds to the fitted linearmodel. CIs of the model are shown in square brackets and by the light blue area. (B) Boxplots show median relative abundances of zero-radius operational taxonomic units of Staphylococcus epidermidis among smoking groups. Smoking status: never-smokers (n=10), ex-smokers (n=6) and smokers (n=30); smoking history: heavy long-term smokers (long-term: n=9), heavy smokers (short-term: n=9) and mild/occasional smokers (mild: n=12). Significant differences in relative abundance were determined using pairwise Mann-Whitney U test (p<0.05, FDR corrected) and are indicated by horizontal brackets with *(p<0.05). CPD, cigarettes per day; Max-CPD, maximum cigarettes per day.

Figure 2

Influence of cigarette smoke on the oropharyngeal microbiota. (A) Upper panel: correlation array of smoking factors with oropharynx (n=54) genera across smoking parameters and transformed sequencing data (centred log-ratio transformation) to remove constrains introduced by the compositionality of the data. The size of the circles shows the significance of the correlation (bigger circle corresponds to a lower p value). The colour of the circle indicates the Pearson correlation between 1 (blue, positive correlation) and –1 (negative correlation) between taxa (horizontal) and smoking parameters (vertical). Lower panel: Pearson correlation of bacterial taxa with smoking-related parameters. Dots represent samples. The line corresponds to the fitted linear model. CIs of the model are shown in square brackets and by the light blue area. (B) Boxplots showing significantly different median relative abundances of zero-radius operational taxonomic units related to different taxa among smoking groups. Smoking status: never-smokers (n=14), smokers (n=34) and ex-smokers (n=6) of paired samples. Significant differences in relative abundance were determined using pairwise Mann-Whitney U test (p

Figure 3

Influence of cigarette smoke on the lung microbiota. (A) Upper panel: correlation array of smoking factors with lungs (n=52) genera across smoking parameters and transformed sequencing data (centred log-ratio transformation) to remove constrains introduced by the compositionality of the data. The size of the circles shows the significance of the correlation (bigger circle corresponds to a lower p value). The colour of the circle indicates the Pearson correlation between 1 (blue, positive correlation) and –1 (red, negative correlation) between taxa (horizontal) and smoking parameters (vertical). Lower panel: Pearson correlation of bacterial taxa with smoking-related parameters. Dots represent samples. The line corresponds to the fitted linear model. CIs of the model are shown in square brackets and by the light blue area. The correlation coefficient (upper row), the false discovery rate-corrected p value (middle row) and the number of observations (lower row) are shown in the corners of the plots. (B) Boxplots showing significantly different median relative abundances of the three most abundant phyla between oropharyngeal and lung samples of never-smokers and smokers. Brackets with * indicate significant (p