Tobacco smoke exposure as a risk factor for human papillomavirus infections in women 18-26 years old in the United States

Autoři: Philip Kum-Nji aff001;  Linda Meloy aff001;  Lori Keyser-Marcus aff002
Působiště autorů: Children’s Hospital of Richmond at the Virginia Commonwealth University School of Medicine, Richmond, Virginia, United States of America aff001;  Department of Psychiatry, Virginia Commonwealth University, Richmond, Virginia, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article



Although tobacco smoke has been associated with many infections, little is known of its association with human papillomavirus (HPV) infections among young adult women. The aim of the study was to explore the association of tobacco smoke exposure on HPV infections in young adult women in the United States. It was hypothesized that tobacco smoke exposure (both active and passive) as objectively measured by cotinine levels was associated with increased HPV infection in a national sample of 18 and 26 year-old women in the United States.

Study methods and findings

The NHANES 2007–2012 dataset was used in the analyses. A national representative sample of women 18 to 26 year old (N = 1,414) was included in the study. Infection with any HPV was determined by PCR while tobacco smoke exposure was determined by measuring serum cotinine levels. Women with cotinine levels <0.05 ng/mL were considered unexposed and those with levels > = 0.05 were considered as exposed. Exposed women were further categorized as passive smokers (cotinine levels 0.05-<10 ng/mL, while active smokers were those with cotinine levels = > 10ng/mL). Data were analyzed by descriptive statistics and multiple logistic regression analysis. Exposed women (passive smokers with cotinine levels > = 0.05ng/mL-10ng/mL) were almost 2 times (64% vs 35%) more likely to be infected with any HPV type than their unexposed counterparts (cotinine levels <0.05ng/mL). Also women who were active smokers (cotinine levels > = 10 ng/mL) were more than twice more likely (75%) to be infected with the virus than the unexposed counterparts. The relationship held true even after controlling for various socio-demographics. Indeed in the multiple regression analyses controlling for the various confounders, compared to their unexposed counterparts, women exposed to second hand smoke were more than twice more likely to have HPV infections (OR: 2.45; 95% C.I = 1.34–4.48). When compared to their unexposed counterparts, actively smoking women were more than 3.5 times more likely to be infected with HPV (OR = 3.56; 95% CI 1.23–10.30).

Finally, a strong dose-response relationship was further demonstrated with increasing risk of HPV with each quartile of cotinine levels even after controlling for various confounders. The risk of HPV was lowest in the lowest quartile (Referent OR = 1) and increased steadily with each quartile of cotinine levels until the risk was highest among women with cotinine levels in the 4th quartile (OR = 4.16; 95% C.I. = 1.36–12.67).


Both passive and active tobacco smoking were strongly associated with any HPV infection in 18 to 26 year old young women with a significant dose-response relationship. Future studies should explore the effect of tobacco smoke exposure among younger women less than 18 years of age.

Klíčová slova:

Dose prediction methods – Human papillomavirus infection – Regression analysis – Respiratory infections – Sexually transmitted diseases – Smoking habits – Smoking related disorders – Young adults


1. Satterwhite CL, Torrone E, Meites E, Dunne EF, Mahajan R, Ocfemia MC, et al. Sexually transmitted infections among US women and men: prevalence and incidence estimates, 2008. Sex Transm Dis. 2013 Mar;40(3):187–93. doi: 10.1097/OLQ.0b013e318286bb53 23403598 Review.

2. Dunne EF, Markowitz LE, Saraiya M, Stokley S, Middleman A, Unger ER, et al. Centers for Disease Control and Prevention (CDC). CDC grand rounds: Reducing the burden of HPV-associated cancer and disease. MMWR Morb Mortal Wkly Rep. 2014 Jan 31;63(4):69–72. 24476977

3. Wiley D, Masongsong E. Human papillomavirus: the burden of infection. Obstet Gynecol Surv. 2006 Jun;61(6 Suppl 1):S3–14. Review. doi: 10.1097/01.ogx.0000221010.82943.8c 16729902

4. Winer RL, Hughes JP, Feng Q, Xi LF, Lee SK, O’Reilly SF, et al. Prevalence and risk factors for oncogenic human papillomavirus infections in high-risk mid-adult women. Sex Transm Dis. 2012 Nov;39(11):848–56. doi: 10.1097/OLQ.0b013e3182641f1c 23064533 Erratum in: Sex Transm Dis. 2013 Nov;40(11):898.

5. Kum-Nji P, Meloy L, Herrod HG. Environmental tobacco smoke exposure: prevalence and mechanisms of causation of infections in children. Pediatrics. 2006 May;117(5):1745–54. doi: 10.1542/peds.2005-1886 16651333

6. Kelsey KT, Nelson HH, Kim S, Pawlita M, Langevin SM, Eliot M, et al. Human papillomavirus serology and tobacco smoking in a community control group. BMC Infect Dis. 2015 Jan 9;15:8. doi: 10.1186/s12879-014-0737-3 25572638

7. Sadate-Ngatchou P, Carter JJ, Hawes SE, Feng Q, Lasof T, Stern JE, et al. Determinants of High-Risk Human Papillomavirus Seroprevalence and DNA Prevalence in Mid-Adult Women. Sex Transm Dis. 2016 Mar;43(3):192–8. doi: 10.1097/OLQ.0000000000000409 26859807

8. CDC. National Health And Nutrition Examination Survey:

9. Watts RR, Langone JJ, Knight GJ, Lewtas J. Cotinine analytical workshopbreport: consideration of analytical methods for determining cotinine in human body fluids as a measure of passive exposure to tobacco smoke. Environ Health Perspect. 1990 Mar;84:173–82. doi: 10.1289/ehp.9084173 2190812

10. Gravitt PE, Peyton CL, Alessi TQ, Wheeler CM, Coutlee F, Hildesheim A, et al. Improved Amplification of Genital Human Papillomaviruses. J Clin Microbiol 2000; 38: 357–361. 10618116

11. CDC. National Health And Nutrition Examination Survey: (retrieved on 11/03/2016)

12. IBM Corp. Released 2012. IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.

13. Prokopczyk B, Cox JE, Hoffmann D, Waggoner SE. Identification of tobacco-specific carcinogen in the cervical mucus of smokers and nonsmokers. J Natl Cancer Inst. 1997 Jun 18;89(12):868–73. doi: 10.1093/jnci/89.12.868 9196253

14. McCann MF, Irwin DE, Walton LA, Hulka BS, Morton JL, Axelrad CM. Nicotine and cotinine in the cervical mucus of smokers, passive smokers, and nonsmokers. Cancer Epidemiol Biomarkers Prev. 1992 Jan-Feb;1(2):125–9. 1306094

15. 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 Jan 31;312(5):315–6.

16. Alam S, Conway MJ, Chen HS, Meyers C. The cigarette smoke carcinogen benzo[a]pyrene enhances human papillomavirus synthesis. J Virol. 2008 Jan;82(2):1053–8. Epub 2007 Nov 7. doi: 10.1128/JVI.01813-07 17989183.

17. Scott DA, Palmer RM. The influence of tobacco smoking on adhesion molecule profiles. Tob Induc Dis. 2002 Jan 15;1(1):7–25. doi: 10.1186/1617-9625-1-1-7 19570245

18. Simen-Kapeu A, Kataja V, Yliskoski M, Syrjänen K, Dillner J, Koskela P, et al. Smoking impairs human papillomavirus (HPV) type 16 and 18 capsids antibody response following natural HPV infection. Scand J Infect Dis. 2008;40(9):745–51. doi: 10.1080/00365540801995360 19086247

19. Kalra R, Singh SP, Savage SM, Finch GL, Sopori ML. Effects of cigarette smoke on immune response: chrnic exposure to cigarette smoke impairs antigen-mediated signaling in T cells and depletes IP3-sensitive Ca(2+) stores. J Pharmacol Exp Ther. 2000 Apr;293(1):166–71. 10734166

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2019 Číslo 10
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