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Association between cigarette smoking and the vaginal microbiota: a pilot study

BACKGROUND: Smoking has been identified in observational studies as a risk factor for bacterial vaginosis (BV), a condition defined in part by decimation of Lactobacillus spp. The anti-estrogenic effect of smoking and trace amounts of benzo[a]pyrene diol epoxide (BPDE) may predispose women to BV. BP...

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Autores principales: Brotman, Rebecca M, He, Xin, Gajer, Pawel, Fadrosh, Doug, Sharma, Eva, Mongodin, Emmanuel F, Ravel, Jacques, Glover, Elbert D, Rath, Jessica M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4161850/
https://www.ncbi.nlm.nih.gov/pubmed/25169082
http://dx.doi.org/10.1186/1471-2334-14-471
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author Brotman, Rebecca M
He, Xin
Gajer, Pawel
Fadrosh, Doug
Sharma, Eva
Mongodin, Emmanuel F
Ravel, Jacques
Glover, Elbert D
Rath, Jessica M
author_facet Brotman, Rebecca M
He, Xin
Gajer, Pawel
Fadrosh, Doug
Sharma, Eva
Mongodin, Emmanuel F
Ravel, Jacques
Glover, Elbert D
Rath, Jessica M
author_sort Brotman, Rebecca M
collection PubMed
description BACKGROUND: Smoking has been identified in observational studies as a risk factor for bacterial vaginosis (BV), a condition defined in part by decimation of Lactobacillus spp. The anti-estrogenic effect of smoking and trace amounts of benzo[a]pyrene diol epoxide (BPDE) may predispose women to BV. BPDE increases bacteriophage induction in Lactobacillus spp. and is found in the vaginal secretions of smokers. We compared the vaginal microbiota between smokers and non-smokers and followed microbiota changes in a smoking cessation pilot study. METHODS: In 2010–2011, 20 smokers and 20 non-smokers were recruited to a cross-sectional study (Phase A) and 9 smokers were enrolled and followed for a 12-week smoking cessation program (Phase B). Phase B included weekly behavioral counseling and nicotine patches to encourage smoking cessation. In both phases, participants self-collected mid-vaginal swabs (daily, Phase B) and completed behavioral surveys. Vaginal bacterial composition was characterized by pyrosequencing of barcoded 16S rRNA genes (V1-V3 regions). Vaginal smears were assigned Nugent Gram stain scores. Smoking status was evaluated (weekly, Phase B) using the semi-quantitative NicAlert® saliva cotinine test and carbon monoxide (CO) exhalation. RESULTS: In phase A, there was a significant trend for increasing saliva cotinine and CO exhalation with elevated Nugent scores (P value <0.005). Vaginal microbiota clustered into three community state types (CSTs); two dominated by Lactobacillus (L. iners, L. crispatus), and one lacking significant numbers of Lactobacillus spp. and characterized by anaerobes (termed CST-IV). Women who were observed in the low-Lactobacillus CST-IV state were 25-fold more likely to be smokers than those dominated by L. crispatus (aOR: 25.61, 95 % CI: 1.03-636.61). Four women completed Phase B. One of three who entered smoking cessation with high Nugent scores demonstrated a switch from CST-IV to a L.iners-dominated profile with a concomitant drop in Nugent scores which coincided with completion of nicotine patches. The other two women fluctuated between CST-IV and L. iners-dominated CSTs. The fourth woman had low Nugent scores with L. crispatus-dominated CSTs throughout. CONCLUSION: Smokers had a lower proportion of vaginal Lactobacillus spp. compared to non-smokers. Smoking cessation should be investigated as an adjunct to reducing recurrent BV. Larger studies are needed to confirm these findings. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2334-14-471) contains supplementary material, which is available to authorized users.
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spelling pubmed-41618502014-09-13 Association between cigarette smoking and the vaginal microbiota: a pilot study Brotman, Rebecca M He, Xin Gajer, Pawel Fadrosh, Doug Sharma, Eva Mongodin, Emmanuel F Ravel, Jacques Glover, Elbert D Rath, Jessica M BMC Infect Dis Research Article BACKGROUND: Smoking has been identified in observational studies as a risk factor for bacterial vaginosis (BV), a condition defined in part by decimation of Lactobacillus spp. The anti-estrogenic effect of smoking and trace amounts of benzo[a]pyrene diol epoxide (BPDE) may predispose women to BV. BPDE increases bacteriophage induction in Lactobacillus spp. and is found in the vaginal secretions of smokers. We compared the vaginal microbiota between smokers and non-smokers and followed microbiota changes in a smoking cessation pilot study. METHODS: In 2010–2011, 20 smokers and 20 non-smokers were recruited to a cross-sectional study (Phase A) and 9 smokers were enrolled and followed for a 12-week smoking cessation program (Phase B). Phase B included weekly behavioral counseling and nicotine patches to encourage smoking cessation. In both phases, participants self-collected mid-vaginal swabs (daily, Phase B) and completed behavioral surveys. Vaginal bacterial composition was characterized by pyrosequencing of barcoded 16S rRNA genes (V1-V3 regions). Vaginal smears were assigned Nugent Gram stain scores. Smoking status was evaluated (weekly, Phase B) using the semi-quantitative NicAlert® saliva cotinine test and carbon monoxide (CO) exhalation. RESULTS: In phase A, there was a significant trend for increasing saliva cotinine and CO exhalation with elevated Nugent scores (P value <0.005). Vaginal microbiota clustered into three community state types (CSTs); two dominated by Lactobacillus (L. iners, L. crispatus), and one lacking significant numbers of Lactobacillus spp. and characterized by anaerobes (termed CST-IV). Women who were observed in the low-Lactobacillus CST-IV state were 25-fold more likely to be smokers than those dominated by L. crispatus (aOR: 25.61, 95 % CI: 1.03-636.61). Four women completed Phase B. One of three who entered smoking cessation with high Nugent scores demonstrated a switch from CST-IV to a L.iners-dominated profile with a concomitant drop in Nugent scores which coincided with completion of nicotine patches. The other two women fluctuated between CST-IV and L. iners-dominated CSTs. The fourth woman had low Nugent scores with L. crispatus-dominated CSTs throughout. CONCLUSION: Smokers had a lower proportion of vaginal Lactobacillus spp. compared to non-smokers. Smoking cessation should be investigated as an adjunct to reducing recurrent BV. Larger studies are needed to confirm these findings. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2334-14-471) contains supplementary material, which is available to authorized users. BioMed Central 2014-08-28 /pmc/articles/PMC4161850/ /pubmed/25169082 http://dx.doi.org/10.1186/1471-2334-14-471 Text en © Brotman et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.
spellingShingle Research Article
Brotman, Rebecca M
He, Xin
Gajer, Pawel
Fadrosh, Doug
Sharma, Eva
Mongodin, Emmanuel F
Ravel, Jacques
Glover, Elbert D
Rath, Jessica M
Association between cigarette smoking and the vaginal microbiota: a pilot study
title Association between cigarette smoking and the vaginal microbiota: a pilot study
title_full Association between cigarette smoking and the vaginal microbiota: a pilot study
title_fullStr Association between cigarette smoking and the vaginal microbiota: a pilot study
title_full_unstemmed Association between cigarette smoking and the vaginal microbiota: a pilot study
title_short Association between cigarette smoking and the vaginal microbiota: a pilot study
title_sort association between cigarette smoking and the vaginal microbiota: a pilot study
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4161850/
https://www.ncbi.nlm.nih.gov/pubmed/25169082
http://dx.doi.org/10.1186/1471-2334-14-471
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