期刊论文详细信息
BMC Infectious Diseases
Association between cigarette smoking and the vaginal microbiota: a pilot study
Jessica M Rath6  Elbert D Glover1  Jacques Ravel3  Emmanuel F Mongodin3  Eva Sharma4  Doug Fadrosh5  Pawel Gajer5  Xin He2  Rebecca M Brotman7 
[1]Department of Behavioral and Community Health, University of Maryland School of Public Health, College Park, MD, USA
[2]Department of Epidemiology and Biostatistics, University of Maryland School of Public Health, College Park, MD, USA
[3]Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, USA
[4]Westat, Rockville, MD, USA
[5]Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, USA
[6]American Legacy Foundation, Washington, DC, USA
[7]Department of Epidemiology and Public Health, University of Maryland School of Medicine, 801 West Baltimore Street, Room Number 633, Baltimore, MD 21201, USA
关键词: Bacterial vaginosis;    16S rRNA gene analysis;    Cigarette;    Smoking cessation;    Vaginal microbiota;   
Others  :  1125713
DOI  :  10.1186/1471-2334-14-471
 received in 2014-03-10, accepted in 2014-08-18,  发布年份 2014
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【 摘 要 】

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.

【 授权许可】

   
2014 Brotman et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Larsson PG, Platz-Christensen JJ, Sundstrom E: Is bacterial vaginosis a sexually transmitted disease? Int J STD AIDS 1991, 2(5):362-364.
  • [2]Hellberg D, Nilsson S, Mardh PA: Bacterial vaginosis and smoking. Int J STD AIDS 2000, 11(9):603-606.
  • [3]Hay PE, Lamont RF, Taylor-Robinson D, Morgan DJ, Ison C, Pearson J: Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. BMJ 1994, 308(6924):295-298.
  • [4]Nelson DB, Bellamy S, Odibo A, Nachamkin I, Ness RB, Allen-Taylor L: Vaginal symptoms and bacterial vaginosis (BV): how useful is self-report? Development of a screening tool for predicting BV status. Epidemiol Infect 2007, 135(8):1369-1375.
  • [5]Larsson PG, Fahraeus L, Carlsson B, Jakobsson T, Forsum U: Predisposing factors for bacterial vaginosis, treatment efficacy and pregnancy outcome among term deliveries; results from a preterm delivery study. BMC Womens Health 2007, 7:20. BioMed Central Full Text
  • [6]Miller GC, McDermott R, McCulloch B, Fairley CK, Muller R: Predictors of the prevalence of bacterial STI among young disadvantaged Indigenous people in north Queensland. Australia Sex Transm Infect 2003, 79(4):332-335.
  • [7]Cherpes TL, Hillier SL, Meyn LA, Busch JL, Krohn MA: A delicate balance: risk factors for acquisition of bacterial vaginosis include sexual activity, absence of hydrogen peroxide-producing lactobacilli, black race, and positive herpes simplex virus type 2 serology. Sex Transm Dis 2008, 35(1):78-83.
  • [8]Peters N, Van Leeuwen AM, Pieters WJ, Hollema H, Quint WG, Burger MP: Bacterial vaginosis is not important in the etiology of cervical neoplasia: a survey on women with dyskaryotic smears. Sex Transm Dis 1995, 22(5):296-302.
  • [9]Bailey JV, Farquhar C, Owen C: Bacterial vaginosis in lesbians and bisexual women. Sex Transm Dis 2004, 31(11):691-694.
  • [10]Smart S, Singal A, Mindel A: Social and sexual risk factors for bacterial vaginosis. Sex Transm Infect 2004, 80(1):58-62.
  • [11]Thorsen P, Vogel I, Molsted K, Jacobsson B, Arpi M, Møller BR, Jeune B: Risk factors for bacterial vaginosis in pregnancy: a population-based study on Danish women. Acta Obstet Gynecol Scand 2006, 85(8):906-911.
  • [12]Bradshaw CS, Walker SM, Vodstrcil LA, Bilardi JE, Law M, Hocking JS, Fethers KA, Fehler G, Petersen S, Tabrizi SN, Chen MY, Garland SM, Fairley CK: The influence of behaviours and relationships on the vaginal microbiota of women and their female partners: The WOW Health Study. J Infect Dis 2013, 209(10):1562-1572.
  • [13]Bradshaw CS, Morton AN, Garland SM, Morris MB, Moss LM, Fairley CK: Higher-risk behavioral practices associated with bacterial vaginosis compared with vaginal candidiasis. Obstet Gynecol 2005, 106(1):105-114.
  • [14]Hillier SL, Holmes KK, Marrazzo JM: Bacterial Vaginosis. In Sex Transm Dis. 4th edition. New York: McGraw-Hill, Health Professions Division; 2008:737-768.
  • [15]Workowski KA, Berman S: Centers for Disease C, Prevention: Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep 2010, 59(RR-12):1-110.
  • [16]Bilardi JE, Walker S, Temple-Smith M, McNair R, Mooney-Somers J, Bellhouse C, Fairley CK, Chen MY, Bradshaw C: The Burden of Bacterial Vaginosis: Women's Experience of the Physical, Emotional, Sexual and Social Impact of Living with Recurrent Bacterial Vaginosis. PLoS One 2013, 8(9):e74378.
  • [17]Brotman RM, Klebanoff MA, Nansel TR, Yu KF, Andrews WW, Zhang J, Schwebke JR: Bacterial vaginosis assessed by gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. J Infect Dis 2010, 202(12):1907-1915.
  • [18]Sobel JD, Ferris D, Schwebke J, Nyirjesy P, Wiesenfeld HC, Peipert J, Soper D, Ohmit SE, Hillier SL: Suppressive antibacterial therapy with 0.75% metronidazole vaginal gel to prevent recurrent bacterial vaginosis. Am J Obstet Gynecol 2006, 194(5):1283-1289.
  • [19]Bradshaw CS, Morton AN, Hocking J, Garland SM, Morris MB, Moss LM, Horvath LB, Kuzevska I, Fairley CK: High recurrence rates of bacterial vaginosis over the course of 12 months after oral metronidazole therapy and factors associated with recurrence. J Infect Dis 2006, 193(11):1478-1486.
  • [20]Bagaitkar J, Demuth DR, Scott DA: Tobacco use increases susceptibility to bacterial infection. Tob Induc Dis 2008, 4:12. BioMed Central Full Text
  • [21]Hellberg D, Nilsson S, Haley NJ, Hoffman D, Wynder E: Smoking and cervical intraepithelial neoplasia: nicotine and cotinine in serum and cervical mucus in smokers and nonsmokers. Am J Obstet Gynecol 1988, 158(4):910-913.
  • [22]Sasson IM, Haley NJ, Hoffmann D, Wynder EL, Hellberg D, Nilsson S: Cigarette smoking and neoplasia of the uterine cervix: smoke constituents in cervical mucus. N Engl J Med 1985, 312(5):315-316.
  • [23]Schiffman MH, Haley NJ, Felton JS, Andrews AW, Kaslow RA, Lancaster WD, Kurman RJ, Brinton LA, Lannom LB, Hoffmann D: Biochemical epidemiology of cervical neoplasia: measuring cigarette smoke constituents in the cervix. Cancer Res 1987, 47(14):3886-3888.
  • [24]Westhoff C, Gentile G, Lee J, Zacur H, Helbig D: Predictors of ovarian steroid secretion in reproductive-age women. Am J Epidemiol 1996, 144(4):381-388.
  • [25]Hillier SL, Lau RJ: Vaginal microflora in postmenopausal women who have not received estrogen replacement therapy. Clin Infect Dis 1997, 25(Suppl 2):S123-S126.
  • [26]Hummelen R, Macklaim JM, Bisanz JE, Hammond JA, McMillan A, Vongsa R, Koenig D, Gloor GB, Reid G: Vaginal Microbiome and Epithelial Gene Array in Post-Menopausal Women with Moderate to Severe Dryness. PLoS One 2011, 6(11):e26602.
  • [27]Brotman RM, Shardell MD, Gajer P, Fadrosh D, Chang K, Silver MI, Viscidi RP, Burke AE, Ravel J, Gravitt PE: Association between the vaginal microbiota, menopause status, and signs of vulvovaginal atrophy. Menopause 2014, 21(5):450-458.
  • [28]Pavlova SI, Tao L: Induction of vaginal Lactobacillus phages by the cigarette smoke chemical benzo[a]pyrene diol epoxide. Mutat Res 2000, 466(1):57-62.
  • [29]Nugent R, Krohn M, Hillier S: Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation. J Clin Microbiol 1991, 29:297-301.
  • [30]Menard JP, Fenollar F, Raoult D, Boubli L, Bretelle F: Self-collected vaginal swabs for the quantitative real-time polymerase chain reaction assay of Atopobium vaginae and Gardnerella vaginalis and the diagnosis of bacterial vaginosis. EurJ Clin Microbiol Infect Dis 2012, 31(4):513-518.
  • [31]Forney LJ, Gajer P, Williams CJ, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Brotman RM, Davis CC, Ault K, Ravel J: Comparison of self-collected and physician-collected vaginal swabs for microbiome analysis. J Clin Microbiol 2010, 48(5):1741-1748.
  • [32]Nelson DB, Bellamy S, Gray TS, Nachamkin I: Self-collected versus provider-collected vaginal swabs for the diagnosis of bacterial vaginosis: an assessment of validity and reliability. J Clin Epidemiol 2003, 56(9):862-866.
  • [33]Bai G, Gajer P, Nandy M, Ma B, Yang H, Sakamoto J, Blanchard MH, Ravel J, Brotman RM: Comparison of storage conditions for human vaginal microbiome studies. PLoS One 2012, 7(5):e36934.
  • [34]Fiore MC, Bailey WC, Cohen SJ, Dorfman SF, Goldstein MG, Gritz ER, Heyman RB, Jaén CR, Kottke TE, Lando HA: Treating tobacco use and dependence: clinical practice guideline. 2000.
  • [35]Heffner JL DK, Jansern J, Nolting SL, Winders-Barrett S, Anthenelli RM: Guide to clearing the air (modified). Unpublished treatment manual. University of Cincinnati 2007.
  • [36]Henningfield JE, Shiffman S, Ferguson SG, Gritz ER: Tobacco dependence and withdrawal: science base, challenges and opportunities for pharmacotherapy. Pharmacol Ther 2009, 123(1):1-16.
  • [37]Montalto NJ, Wells WO: Validation of self-reported smoking status using saliva cotinine: a rapid semiquantitative dipstick method. Cancer Epidemiol Biomarkers Prev 2007, 16(9):1858-1862.
  • [38]Sandberg A, Sköld CM, Grunewald J, Eklund A, Wheelock ÅM: Assessing recent smoking status by measuring exhaled carbon monoxide levels. PLoS One 2011, 6(12):e28864.
  • [39]Marrone GF, Shakleya DM, Scheidweiler KB, Singleton EG, Huestis MA, Heishman SJ: Relative performance of common biochemical indicators in detecting cigarette smoking. Addiction (Abingdon, England) 2011, 106(7):1325-1334.
  • [40]Marrone GF, Paulpillai M, Evans RJ, Singleton EG, Heishman SJ: Breath carbon monoxide and semiquantitative saliva cotinine as biomarkers for smoking. Hum Psychopharmacol Clin Exp 2010, 25(1):80-83.
  • [41]Middleton ET, Morice AH: Breath carbon monoxide as an indication of smoking habit. Chest 2000, 117(3):758-763.
  • [42]Benowitz NL: Cotinine as a biomarker of environmental tobacco smoke exposure. Epidemiol Rev 1996, 18(2):188-204.
  • [43]Hurt RD, Dale LC, Offord KP, Lauger GG, Baskin LB, Lawson GM, Jiang NS, Hauri PJ: Serum nicotine and cotinine levels during nicotine-patch therapy. Clin Pharmacol Ther 1993, 54(1):98-106.
  • [44]Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, Brotman RM, Davis CC, Ault K, Peralta L, Forney LJ: Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011, 108(Suppl 1):4680-4687.
  • [45]Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ: Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 2008, 74(8):2461-2470.
  • [46]Ravel J, Brotman RM, Gajer P, Ma B, Nandy M, Fadrosh DW, Sakamoto J, Koenig SS, Fu L, Zhou X, Hickey RJ, Schwebke JR, Forney LJ: Daily temporal dynamics of vaginal microbiota before, during and after episodes of bacterial vaginosis. Microbiome 2013, 1(1):29. BioMed Central Full Text
  • [47]Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26(19):2460-2461.
  • [48]Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R: UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011, 27(16):2194-2200.
  • [49]Wang Q, Garrity GM, Tiedje JM, Cole JR: Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73(16):5261-5267.
  • [50]Gajer P, Brotman RM, Bai G, Sakamoto J, Schutte UM, Zhong X, Koenig SS, Fu L, Ma ZS, Zhou X, Abdo Z, Forney LJ, Ravel J: Temporal dynamics of the human vaginal microbiota. Sci Transl Med 2012, 4(132):132ra152.
  • [51]Macklaim JM, Gloor GB, Anukam KC, Cribby S, Reid G: At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc Natl Acad Sci U S A 2011, 108(Suppl 1):4688-4695.
  • [52]McMillan A, Macklaim JM, Burton JP, Reid G: Adhesion of Lactobacillus iners AB-1 to Human Fibronectin: A Key Mediator for Persistence in the Vagina? Reproduct Sci (Thousand Oaks, Calif) 2013, 20(7):791-796.
  • [53]Verstraelen H, Verhelst R, Claeys G, De BE, Temmerman M, Vaneechoutte M: Longitudinal analysis of the vaginal microflora in pregnancy suggests that L. crispatus promotes the stability of the normal vaginal microflora and that L. gasseri and/or L. iners are more conducive to the occurrence of abnormal vaginal microflora. BMC Microbiol 2009, 9:116. BioMed Central Full Text
  • [54]Witkin SS, Mendes-Soares H, Linhares IM, Jayaram A, Ledger WJ, Forney LJ: Influence of vaginal bacteria and D- and L-lactic acid isomers on vaginal extracellular matrix metalloproteinase inducer: implications for protection against upper genital tract infections. mBio 2013, 4(4):e00460-13.
  • [55]Fredricks DN: Molecular methods to describe the spectrum and dynamics of the vaginal microbiota. Anaerobe 2011, 17(4):191-195.
  • [56]Mitchell C, Manhart LE, Thomas K, Fiedler T, Fredricks DN, Marrazzo J: Behavioral predictors of colonization with Lactobacillus crispatus or Lactobacillus jensenii after treatment for bacterial vaginosis: a cohort study. Infect Dis Obstet Gynecol 2012, 2012:706540.
  • [57]Ma B, Brotman RM, Gajer P, Fadrosh D, Mahurkar A, White O, Terplan M, Bavoil P, Forney LJ, Ravel J: Association between Chlamydia trachomatis genital infections and the vaginal microbiome. In The International Society for Sexually Transmitted Disease Research, 20th Biennial Congress: July 14–17, 2013 2013. Vienna, Austria: ᅟ; 2013.
  • [58]Rigotti NA, Thorndike AN, Regan S, McKool K, Pasternak RC, Chang Y, Swartz S, Torres-Finnerty N, Emmons KM, Singer DE: Bupropion for smokers hospitalized with acute cardiovascular disease. Am J Med 2006, 119(12):1080-1087.
  • [59]Hurt RD, Sachs DP, Glover ED, Offord KP, Johnston JA, Dale LC, Khayrallah MA, Schroeder DR, Glover PN, Sullivan CR, Croghan IT, Sullivan PM: A comparison of sustained-release bupropion and placebo for smoking cessation. N Engl J Med 1997, 337(17):1195-1202.
  • [60]Eisenberg MJ, Grandi SM, Gervais A, O'Loughlin J, Paradis G, Rinfret S, Sarrafzadegan N, Sharma S, Lauzon C, Yadav R, Pilote L, ZESCA Investigators: Bupropion for smoking cessation in patients hospitalized with acute myocardial infarction: a randomized, placebo-controlled trial. J Am Coll Cardiol 2013, 61(5):524-532.
  • [61]DeZee KJ, Wink JS, Cowan CM: Internet Versus In-Person Counseling for Patients Taking Varenicline for Smoking Cessation. Mil Med 2013, 178(4):401-405.
  • [62]Srinivasan S, Liu C, Mitchell CM, Fiedler TL, Thomas KK, Agnew KJ, Marrazzo JM, Fredricks DN: Temporal Variability of Human Vaginal Bacteria and Relationship with Bacterial Vaginosis. PLoS One 2010, 5(4):e10197.
  • [63]Keane FE, Ison CA, Taylor-Robinson D: A longitudinal study of the vaginal flora over a menstrual cycle. Int J STD AIDS 1997, 8(8):489-494.
  • [64]Rubinstein ML, Shiffman S, Rait MA, Benowitz NL: Race, gender, and nicotine metabolism in adolescent smokers. Nicotine Tob Res 2013, 15(7):1311-1315.
  • [65]Pérez-Stable EJ, Herrera B, Jacob P, Benowitz NL: Nicotine metabolism and intake in black and white smokers. JAMA 1998, 280(2):152-156.
  • [66]Caraballo RS, Giovino GA, Pechacek TF, Mowery PD, Richter PA, Strauss WJ, Sharp DJ, Eriksen MP, Pirkle JL, Maurer KR: Racial and ethnic differences in serum cotinine levels of cigarette smokers: Third National Health and Nutrition Examination Survey, 1988–1991. JAMA 1998, 280(2):135-139.
  • [67]Vodstrcil LA, Hocking JS, Law M, Walker S, Tabrizi SN, Fairley CK, Bradshaw CS: Hormonal contraception is associated with a reduced risk of bacterial vaginosis: a systematic review and meta-analysis. PLoS One 2013, 8(9):e73055.
  • [68]Bulletins-Gynecology ACoP: ACOG practice bulletin. No. 73: Use of hormonal contraception in women with coexisting medical conditions. Obstet Gynecol 2006, 107:1453-1472.
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