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The impact of smoking on HPV infection and the development of anogenital warts

Abstract

Purpose

The worldwide prevalence of human papillomavirus (HPV) infection is estimated at 9–13 %. Persistent infection can lead to the development of malignant and nonmalignant diseases. Low-risk HPV types are mostly associated with benign lesions such as anogenital warts. In the present systematic review, we examined the impact of smoking on HPV infection and the development of anogenital warts, respectively.

Methods

A systematic literature search was performed using MEDLINE database for peer-reviewed articles published from January 01, 1985 to November 30, 2013. Pooled rates of HPV prevalence were compared using the χ 2 test.

Results

In both genders, smoking is associated with higher incidence and prevalence rates for HPV infection, whereas the latter responds to a dose-effect relationship. The overall HPV prevalence for smoking patients was 48.2 versus 37. 5 % for nonsmoking patients (p < 0.001) (odds ratio (OR) = 1.5, 95 % confidence interval (CI) 1.4–1.7). Smoking does also increase persistence rates for high-risk HPV infection, while this correlation is debatable for low-risk HPV. The incidence and recurrence rates of anogenital warts are significantly increased in smokers.

Conclusions

Most current data demonstrate an association between smoking, increased anogenital HPV infection, and development of anogenital warts. These data add to the long list of reasons for making smoking cessation a keystone of patient health.

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References

  1. WHO Vaccines against human papilloma virus. http://www.who.int/vaccines/en/hpvrd.shtml. Accessed April 01, 2014

  2. Forcier M, Musacchio N (2010) An overview of human papillomavirus infection for the dermatologist: disease, diagnosis, management, and prevention. Dermatol Ther 23(5):458–476. doi:10.1111/j.1529-8019.2010.01350.x

    PubMed  Google Scholar 

  3. Markowitz LE, Dunne EF, Saraiya M, Lawson HW, Chesson H, Unger ER (2007) Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recommendations and reports: Morbidity and mortality weekly report Recommendations and reports / Centers for Disease Control 56 (Rr-2):1-24

  4. Hathaway JK (2012) HPV: diagnosis, prevention, and treatment. Clin Obstet Gynecol 55(3):671–680. doi:10.1097/GRF.0b013e31825caa36

    PubMed  Google Scholar 

  5. Fleischer AB Jr, Parrish CA, Glenn R, Feldman SR (2001) Condylomata acuminata (genital warts): patient demographics and treating physicians. Sex Transm Dis 28(11):643–647

    PubMed  Google Scholar 

  6. Stanley M (2007) Prophylactic HPV vaccines: prospects for eliminating ano-genital cancer. Br J Cancer 96(9):1320–1323. doi:10.1038/sj.bjc.6603695

    CAS  PubMed Central  PubMed  Google Scholar 

  7. Gross G, Pfister H (2004) Role of human papillomavirus in penile cancer, penile intraepithelial squamous cell neoplasias and in genital warts. Med Microbiol Immunol 193(1):35–44. doi:10.1007/s00430-003-0181-2

    CAS  PubMed  Google Scholar 

  8. Tay EH, Garland S, Tang G, Nolan T, Huang LM, Orloski L, Lu S, Barr E (2008) Clinical trial experience with prophylactic HPV 6/11/16/18 VLP vaccine in young women from the Asia-Pacific region. Int J Gynaecol Obstet Off Organ Int Fed Gynaecol Obstet 102(3):275–283. doi:10.1016/j.ijgo.2008.03.021

    CAS  Google Scholar 

  9. Patel H, Wagner M, Singhal P, Kothari S (2013) Systematic review of the incidence and prevalence of genital warts. BMC Infect Dis 13:39. doi:10.1186/1471-2334-13-39

    PubMed Central  PubMed  Google Scholar 

  10. Scheinfeld N, Lehman DS (2006) An evidence-based review of medical and surgical treatments of genital warts. Dermatol Online J 12(3):5

    PubMed  Google Scholar 

  11. Wiley DJ, Douglas J, Beutner K, Cox T, Fife K, Moscicki AB, Fukumoto L (2002) External genital warts: diagnosis, treatment, and prevention. Clin Infect Dis Off Publ Infect Dis Soc Am 35(Suppl 2):S210–S224. doi:10.1086/342109

    CAS  Google Scholar 

  12. Kodner CM, Nasraty S (2004) Management of genital warts. Am Fam Physician 70(12):2335–2342

    PubMed  Google Scholar 

  13. Wen LM, Estcourt CS, Simpson JM, Mindel A (1999) Risk factors for the acquisition of genital warts: are condoms protective? Sex Transm Infect 75(5):312–316

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Vaccarella S, Herrero R, Snijders PJ, Dai M, Thomas JO, Hieu NT, Ferreccio C, Matos E, Posso H, de Sanjose S, Shin HR, Sukvirach S, Lazcano-Ponce E, Munoz N, Meijer CJ, Franceschi S (2008) Smoking and human papillomavirus infection: pooled analysis of the International Agency for Research on Cancer HPV Prevalence Surveys. Int J Epidemiol 37(3):536–546. doi:10.1093/ije/dyn033

    PubMed  Google Scholar 

  15. Clarke M, Schiffman M, Wacholder S, Rodriguez AC, Hildesheim A, Quint W (2013) A prospective study of absolute risk and determinants of human papillomavirus incidence among young women in Costa Rica. BMC Infect Dis 13:308. doi:10.1186/1471-2334-13-308

    PubMed Central  PubMed  Google Scholar 

  16. Schabath MB, Villa LL, Lin HY, Fulp WJ, Lazcano-Ponce E, Salmeron J, Abrahamsen ME, Papenfuss MR, Quiterio M, Giuliano AR (2013) A prospective analysis of smoking and human papillomavirus infection among men in the HPV in Men Study. Int J Cancer J Int Cancer. doi:10.1002/ijc.28567

    Google Scholar 

  17. Almonte M, Silva Idos S, Asare A, Gilham C, Sargent A, Bailey A, Turner A, Desai M, Kitchener HC, Peto J (2011) Sexual behavior and HPV infection in British women, by postal questionnaires and telephone interviews. J Med Virol 83(7):1238–1246. doi:10.1002/jmv.22085

    PubMed  Google Scholar 

  18. Nielsen A, Iftner T, Munk C, Kjaer SK (2009) Acquisition of high-risk human papillomavirus infection in a population-based cohort of Danish women. Sex Transm Dis 36(10):609–615. doi:10.1097/OLQ.0b013e3181a96d0e

    PubMed Central  PubMed  Google Scholar 

  19. Sarian LO, Hammes LS, Longatto-Filho A, Guarisi R, Derchain SF, Roteli-Martins C, Naud P, Erzen M, Branca M, Tatti S, de Matos JC, Gontijo R, Maeda MY, Lima T, Costa S, Syrjanen S, Syrjanen K (2009) Increased risk of oncogenic human papillomavirus infections and incident high-grade cervical intraepithelial neoplasia among smokers: experience from the Latin American screening study. Sex Transm Dis 36(4):241–248. doi:10.1097/OLQ.0b013e3181935a7d

    PubMed  Google Scholar 

  20. Oh JK, Ju YH, Franceschi S, Quint W, Shin HR (2008) Acquisition of new infection and clearance of type-specific human papillomavirus infections in female students in Busan, South Korea: a follow-up study. BMC Infect Dis 8:13. doi:10.1186/1471-2334-8-13

    PubMed Central  PubMed  Google Scholar 

  21. Partridge JM, Hughes JP, Feng Q, Winer RL, Weaver BA, Xi LF, Stern ME, Lee SK, O'Reilly SF, Hawes SE, Kiviat NB, Koutsky LA (2007) Genital human papillomavirus infection in men: incidence and risk factors in a cohort of university students. J Infect Dis 196(8):1128–1136. doi:10.1086/521192

    PubMed  Google Scholar 

  22. Syrjanen K, Shabalova I, Petrovichev N, Kozachenko V, Zakharova T, Pajanidi J, Podistov J, Chemeris G, Sozaeva L, Lipova E, Tsidaeva I, Ivanchenko O, Pshepurko A, Zakharenko S, Nerovjna R, Kljukina L, Erokhina O, Branovskaja M, Nikitina M, Grunberga V, Grunberg A, Juschenko A, Santopietro R, Cintorino M, Tosi P, Syrjanen S (2007) Smoking is an independent risk factor for oncogenic human papillomavirus (HPV) infections but not for high-grade CIN. Eur J Epidemiol 22(10):723–735. doi:10.1007/s10654-007-9180-8

    PubMed  Google Scholar 

  23. Kjaer SK, Munk C, Winther JF, Jorgensen HO, Meijer CJ, van den Brule AJ (2005) Acquisition and persistence of human papillomavirus infection in younger men: a prospective follow-up study among Danish soldiers. Cancer Epidemiol Biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol 14(6):1528–1533. doi:10.1158/1055-9965.epi-04-0754

    Google Scholar 

  24. Minkoff H, Feldman JG, Strickler HD, Watts DH, Bacon MC, Levine A, Palefsky JM, Burk R, Cohen MH, Anastos K (2004) Relationship between smoking and human papillomavirus infections in HIV-infected and -uninfected women. J Infect Dis 189(10):1821–1828. doi:10.1086/383479

    PubMed  Google Scholar 

  25. Sellors JW, Karwalajtys TL, Kaczorowski J, Mahony JB, Lytwyn A, Chong S, Sparrow J, Lorincz A (2003) Incidence, clearance and predictors of human papillomavirus infection in women. CMAJ: Can Med Assoc J 168(4):421–425

    Google Scholar 

  26. Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB, Koutsky LA (2003) Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students. Am J Epidemiol 157(3):218–226

    PubMed  Google Scholar 

  27. Nyitray AG, Carvalho da Silva RJ, Baggio ML, Smith D, Abrahamsen M, Papenfuss M, Lin HY, Quiterio M, Salmeron J, Lazcano-Ponce E, Villa LL, Giuliano AR (2011) Six-month incidence, persistence, and factors associated with persistence of anal human papillomavirus in men: the HPV in men study. J Infect Dis 204(11):1711–1722. doi:10.1093/infdis/jir637

    PubMed Central  PubMed  Google Scholar 

  28. Goodman MT, Shvetsov YB, McDuffie K, Wilkens LR, Zhu X, Ning L, Killeen J, Kamemoto L, Hernandez BY (2008) Acquisition of anal human papillomavirus (HPV) infection in women: the Hawaii HPV cohort study. J Infect Dis 197(7):957–966. doi:10.1086/529207

    PubMed  Google Scholar 

  29. Moscicki AB, Hills N, Shiboski S, Powell K, Jay N, Hanson E, Miller S, Clayton L, Farhat S, Broering J, Darragh T, Palefsky J (2001) Risks for incident human papillomavirus infection and low-grade squamous intraepithelial lesion development in young females. JAMA: J Am Med Assoc 285(23):2995–3002

    CAS  Google Scholar 

  30. Kjaer SK, Breugelmans G, Munk C, Junge J, Watson M, Iftner T (2008) Population-based prevalence, type- and age-specific distribution of HPV in women before introduction of an HPV-vaccination program in Denmark. Int J Cancer 123(8):1864–1870. doi:10.1002/ijc.23712

    CAS  PubMed  Google Scholar 

  31. Shvetsov YB, Hernandez BY, McDuffie K, Wilkens LR, Zhu X, Ning L, Killeen J, Kamemoto L, Goodman MT (2009) Duration and clearance of anal human papillomavirus (HPV) infection among women: the Hawaii HPV cohort study. Clin Infect Dis: Off Publ Infect Dis Soc Am 48(5):536–546. doi:10.1086/596758

    Google Scholar 

  32. Schmeink CE, Melchers WJ, Siebers AG, Quint WG, Massuger LF, Bekkers RL (2011) Human papillomavirus persistence in young unscreened women, a prospective cohort study. PLoS One 6(11):e27937. doi:10.1371/journal.pone.0027937

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Maucort-Boulch D, Plummer M, Castle PE, Demuth F, Safaeian M, Wheeler CM, Schiffman M (2010) Predictors of human papillomavirus persistence among women with equivocal or mildly abnormal cytology. Int J Cancer 126(3):684–691. doi:10.1002/ijc.24752

    CAS  PubMed  Google Scholar 

  34. Koshiol J, Schroeder J, Jamieson DJ, Marshall SW, Duerr A, Heilig CM, Shah KV, Klein RS, Cu-Uvin S, Schuman P, Celentano D, Smith JS (2006) Smoking and time to clearance of human papillomavirus infection in HIV-seropositive and HIV-seronegative women. Am J Epidemiol 164(2):176–183. doi:10.1093/aje/kwj165

    PubMed  Google Scholar 

  35. Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD (1998) Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338(7):423–428. doi:10.1056/nejm199802123380703

    CAS  PubMed  Google Scholar 

  36. Louvanto K, Rintala MA, Syrjanen KJ, Grenman SE, Syrjanen SM (2010) Genotype-specific persistence of genital human papillomavirus (HPV) infections in women followed for 6 years in the Finnish Family HPV Study. J Infect Dis 202(3):436–444. doi:10.1086/653826

    PubMed  Google Scholar 

  37. Nielsen A, Kjaer SK, Munk C, Osler M, Iftner T (2010) Persistence of high-risk human papillomavirus infection in a population-based cohort of Danish women. J Med Virol 82(4):616–623. doi:10.1002/jmv.21750

    PubMed  Google Scholar 

  38. Phanuphak N, Teeratakulpisarn N, Pankam T, Kerr SJ, Barisri J, Deesua A, Rodbamrung P, Hongchookiat P, Chomchey N, Phanuphak P, Sohn AH, Ananworanich J, Palefsky JM (2013) Anal human papillomavirus infection among Thai men who have sex with men with and without HIV infection: prevalence, incidence, and persistence. J Acquir Immune Defic Syndr 63(4):472–479. doi:10.1097/QAI.0b013e3182918a5a

    PubMed  Google Scholar 

  39. Giuliano AR, Sedjo RL, Roe DJ, Harri R, Baldwi S, Papenfuss MR, Abrahamsen M, Inserra P (2002) Clearance of oncogenic human papillomavirus (HPV) infection: effect of smoking (United States). Cancer Causes Control: CCC 13(9):839–846

    PubMed  Google Scholar 

  40. Schabath MB, Villa LL, Lazcano-Ponce E, Salmeron J, Quiterio M, Giuliano AR (2012) Smoking and human papillomavirus (HPV) infection in the HPV in Men (HIM) study. Cancer Epidemiol Biomark Prev: Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol 21(1):102–110. doi:10.1158/1055-9965.epi-11-0591

    CAS  Google Scholar 

  41. Kliucinskas M, Nadisauskiene RJ, Minkauskiene M (2006) Prevalence and risk factors of HPV infection among high-risk rural and urban Lithuanian women. Gynecol Obstet Investig 62(3):173–180. doi:10.1159/000093572

    Google Scholar 

  42. Kataja V, Syrjanen S, Yliskoski M, Hippelinen M, Vayrynen M, Saarikoski S, Mantyjarvi R, Jokela V, Salonen JT, Syrjanen K (1993) Risk factors associated with cervical human papillomavirus infections: a case-control study. Am J Epidemiol 138(9):735–745

    CAS  PubMed  Google Scholar 

  43. Hoang HT, Ishizaki A, Nguyen CH, Tran VT, Matsushita K, Saikawa K, Hosaka N, Pham HV, Bi X, Ta VT, Van Pham T, Ichimura H (2013) Infection with high-risk HPV types among female sex workers in northern Vietnam. J Med Virol 85(2):288–294. doi:10.1002/jmv.23456

    PubMed  Google Scholar 

  44. Nielsen A, Munk C, Jorgensen H, Winther J, van den Brule A, Kjaer S (2013) Multiple-type human papillomavirus infection in younger uncircumcised men. Int J STD AIDS. doi:10.1177/0956462412472294

    PubMed  Google Scholar 

  45. Remschmidt C, Kaufmann AM, Hagemann I, Vartazarova E, Wichmann O, Delere Y (2013) Risk factors for cervical human papillomavirus infection and high-grade intraepithelial lesion in women aged 20 to 31 years in Germany. Int J Gynecol Cancer: Off J Int Gynecol Cancer Soc 23(3):519–526. doi:10.1097/IGC.0b013e318285a4b2

    Google Scholar 

  46. Brassard P, Jiang Y, Severini A, Goleski V, Santos M, Chatwood S, Lys C, Johnson G, Wong T, Kotaska A, Kandola K, Morrison H, Mao Y (2012) Factors associated with human papillomavirus infection among women in the Northwest Territories. Can J Public Health 103(4):e282–e287

    PubMed  Google Scholar 

  47. Bumbuliene Z, Alisauskas J (2012) Sexual behavior and high-risk human papillomavirus in 15- to 22-year-old Lithuanian women. Acta Obstet Gynecol Scand 91(4):511–513. doi:10.1111/j.1600-0412.2011.01334.x

    PubMed  Google Scholar 

  48. Monsonego J, Zerat L, Syrjanen K, Zerat JC, Smith JS, Halfon P (2012) Prevalence of type-specific human papillomavirus infection among women in France: implications for screening, vaccination, and a future generation of multivalent HPV vaccines. Vaccine 30(35):5215–5221. doi:10.1016/j.vaccine.2012.06.013

    PubMed  Google Scholar 

  49. Pista A, de Oliveira CF, Cunha MJ, Paixao MT, Real O (2012) Risk factors for human papillomavirus infection among women in Portugal: the CLEOPATRE Portugal Study. Int J Gynaecol Obstet: Off Organ Int Fed Gynaecol Obstet 118(2):112–116. doi:10.1016/j.ijgo.2012.03.028

    Google Scholar 

  50. Roset Bahmanyar E, Paavonen J, Naud P, Salmeron J, Chow SN, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR, Jaisamrarn U, Limson GA, Garland SM, Szarewski A, Romanowski B, Aoki F, Schwarz TF, Poppe WA, De Carvalho NS, Harper DM, Bosch FX, Raillard A, Descamps D, Struyf F, Lehtinen M, Dubin G (2012) Prevalence and risk factors for cervical HPV infection and abnormalities in young adult women at enrolment in the multinational PATRICIA trial. Gynecol Oncol 127(3):440–450. doi:10.1016/j.ygyno.2012.08.033

    PubMed  Google Scholar 

  51. Roura E, Iftner T, Vidart JA, Kjaer SK, Bosch FX, Munoz N, Palacios S, Rodriguez MS, Morillo C, Serradell L, Torcel-Pagnon L, Cortes J, Castellsague X (2012) Predictors of human papillomavirus infection in women undergoing routine cervical cancer screening in Spain: the CLEOPATRE study. BMC Infect Dis 12:145. doi:10.1186/1471-2334-12-145

    PubMed Central  PubMed  Google Scholar 

  52. Yetimalar H, Kasap B, Cukurova K, Yildiz A, Keklik A, Soylu F (2012) Cofactors in human papillomavirus infection and cervical carcinogenesis. Arch Gynecol Obstet 285(3):805–810. doi:10.1007/s00404-011-2034-3

    PubMed  Google Scholar 

  53. Badano I, Pedrozo RW, Ruiz Diaz LS, Galuppo JA, Picconi MA, Campos RH, Liotta DJ (2011) Human papillomavirus (HPV) detection and Papanicolaou cytology in low-resource women in Posadas city, Misiones, Argentina. Rev Argent Microbiol 43(4):263–267. doi:10.1590/s0325-75412011000400005

    PubMed  Google Scholar 

  54. Bell MC, Schmidt-Grimminger D, Jacobsen C, Chauhan SC, Maher DM, Buchwald DS (2011) Risk factors for HPV infection among American Indian and White women in the Northern Plains. Gynecol Oncol 121(3):532–536. doi:10.1016/j.ygyno.2011.02.032

    PubMed  Google Scholar 

  55. Ferrera A, Tabora N, Flores Y, Zelaya A, Massuger L, Melchers WJ (2011) Assessment of HPV infection among female university students in Honduras via Roche linear array. Int J Gynaecol Obstet: Off Organ Int Fed Gynaecol Obstet 113(2):96–99. doi:10.1016/j.ijgo.2010.11.016

    Google Scholar 

  56. Garland SM, Brotherton JM, Condon JR, McIntyre PB, Stevens MP, Smith DW, Tabrizi SN (2011) Human papillomavirus prevalence among indigenous and non-indigenous Australian women prior to a national HPV vaccination program. BMC Med 9:104. doi:10.1186/1741-7015-9-104

    PubMed Central  PubMed  Google Scholar 

  57. Kasap B, Yetimalar H, Keklik A, Yildiz A, Cukurova K, Soylu F (2011) Prevalence and risk factors for human papillomavirus DNA in cervical cytology. Eur J Obstet Gynecol Reprod Biol 159(1):168–171. doi:10.1016/j.ejogrb.2011.06.021

    CAS  PubMed  Google Scholar 

  58. Montalvo MT, Lobato I, Villanueva H, Borquez C, Navarrete D, Abarca J, Calaf GM (2011) Prevalence of human papillomavirus in university young women. Oncol Lett 2(4):701–706. doi:10.3892/ol.2011.290

    PubMed Central  PubMed  Google Scholar 

  59. Shikova E, Todorova I, Ganchev G, Kouseva-Dragneva V, Kalascheva-Zaimova P (2011) Prevalence of human papillomavirus infection among female sex workers in Bulgaria. Int J STD AIDS 22(5):278–280. doi:10.1258/ijsa.2009.009362

    CAS  PubMed  Google Scholar 

  60. Cercato MC, Mariani L, Vocaturo A, Carrone A, Terrenato I, Morano G, Benevolo M, Rollo F, Germelli C, Paolini F, Venuti A (2010) Predictors of human papilloma virus (HPV) infection in Italian women. J Med Virol 82(11):1921–1927. doi:10.1002/jmv.21887

    CAS  PubMed  Google Scholar 

  61. Iftner T, Eberle S, Iftner A, Holz B, Banik N, Quint W, Straube AN (2010) Prevalence of low-risk and high-risk types of human papillomavirus and other risk factors for HPV infection in Germany within different age groups in women up to 30 years of age: an epidemiological observational study. J Med Virol 82(11):1928–1939. doi:10.1002/jmv.21910

    PubMed  Google Scholar 

  62. Ripabelli G, Grasso GM, Del Riccio I, Tamburro M, Sammarco ML (2010) Prevalence and genotype identification of human papillomavirus in women undergoing voluntary cervical cancer screening in Molise, central Italy. Cancer Epidemiol 34(2):162–167. doi:10.1016/j.canep.2009.12.010

    PubMed  Google Scholar 

  63. Chan PK, Ho WC, Wong MC, Chang AR, Chor JS, Yu MY (2009) Epidemiologic risk profile of infection with different groups of human papillomaviruses. J Med Virol 81(9):1635–1644. doi:10.1002/jmv.21575

    PubMed  Google Scholar 

  64. Nielson CM, Harris RB, Flores R, Abrahamsen M, Papenfuss MR, Dunne EF, Markowitz LE, Giuliano AR (2009) Multiple-type human papillomavirus infection in male anogenital sites: prevalence and associated factors. Cancer Epidemiol Biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol 18(4):1077–1083. doi:10.1158/1055-9965.epi-08-0447

    Google Scholar 

  65. Silva KC, Rosa ML, Moyse N, Afonso LA, Oliveira LH, Cavalcanti SM (2009) Risk factors associated with human papillomavirus infection in two populations from Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 104(6):885–891

    PubMed  Google Scholar 

  66. Valles X, Murga GB, Hernandez G, Sabido M, Chuy A, Lloveras B, Alameda F, de San JS, Bosch FX, Pedroza I, Castellsague X, Casabona J (2009) High prevalence of human papillomavirus infection in the female population of Guatemala. Int J Cancer 125(5):1161–1167. doi:10.1002/ijc.24444

    CAS  PubMed  Google Scholar 

  67. Gonzalez C, Canals J, Ortiz M, Munoz L, Torres M, Garcia-Saiz A, Del Amo J (2008) Prevalence and determinants of high-risk human papillomavirus (HPV) infection and cervical cytological abnormalities in imprisoned women. Epidemiol Infect 136(2):215–221. doi:10.1017/s0950268807008382

    CAS  PubMed Central  PubMed  Google Scholar 

  68. Lindau ST, Drum ML, Gaumer E, Surawska H, Jordan JA (2008) Prevalence of high-risk human papillomavirus among older women. Obstet Gynecol 112(5):979–989. doi:10.1097/AOG.0b013e31818b0df2

    PubMed Central  PubMed  Google Scholar 

  69. Nielson CM, Harris RB, Dunne EF, Abrahamsen M, Papenfuss MR, Flores R, Markowitz LE, Giuliano AR (2007) Risk factors for anogenital human papillomavirus infection in men. J Infect Dis 196(8):1137–1145. doi:10.1086/521632

    PubMed  Google Scholar 

  70. del Amo J, Gonzalez C, Losana J, Clavo P, Munoz L, Ballesteros J, Garcia-Saiz A, Belza MJ, Ortiz M, Menendez B, del Romero J, Bolumar F (2005) Influence of age and geographical origin in the prevalence of high risk human papillomavirus in migrant female sex workers in Spain. Sex Transm Infect 81(1):79–84. doi:10.1136/sti.2003.008060

    PubMed Central  PubMed  Google Scholar 

  71. Beby-Defaux A, Bourgoin A, Ragot S, Battandier D, Lemasson JM, Renaud O, Bouguermouh S, Vienne Md Mde L, Agius G (2004) Human papillomavirus infection of the cervix uteri in women attending a Health Examination Center of the French social security. J Med Virol 73(2):262–268. doi:10.1002/jmv.20085

    CAS  PubMed  Google Scholar 

  72. Shin HR, Franceschi S, Vaccarella S, Roh JW, Ju YH, Oh JK, Kong HJ, Rha SH, Jung SI, Kim JI, Jung KY, van Doorn LJ, Quint W (2004) Prevalence and determinants of genital infection with papillomavirus, in female and male university students in Busan, South Korea. J Infect Dis 190(3):468–476. doi:10.1086/421279

    PubMed  Google Scholar 

  73. Chan PK, Chang AR, Cheung JL, Chan DP, Xu LY, Tang NL, Cheng AF (2002) Determinants of cervical human papillomavirus infection: differences between high- and low-oncogenic risk types. J Infect Dis 185(1):28–35. doi:10.1086/338010

    PubMed  Google Scholar 

  74. Lazcano-Ponce E, Herrero R, Munoz N, Hernandez-Avila M, Salmeron J, Leyva A, Meijer CJ, Walboomers JM (2001) High prevalence of human papillomavirus infection in Mexican males: comparative study of penile-urethral swabs and urine samples. Sex Transm Dis 28(5):277–280

    CAS  PubMed  Google Scholar 

  75. Nyari T, Cseh I, Woodward M, Szollosi J, Bak M, Deak J (2001) Screening for human papillomavirus infection in asymptomatic women in Hungary. Hum Reprod (Oxford, England) 16(10):2235–2237

    CAS  Google Scholar 

  76. Sellors JW, Mahony JB, Kaczorowski J, Lytwyn A, Bangura H, Chong S, Lorincz A, Dalby DM, Janjusevic V, Keller JL (2000) Prevalence and predictors of human papillomavirus infection in women in Ontario, Canada. Survey of HPV in Ontario Women (SHOW) Group. CMAJ: Can Med Assoc J 163(5):503–508

    CAS  Google Scholar 

  77. Marrazzo JM, Koutsky LA, Stine KL, Kuypers JM, Grubert TA, Galloway DA, Kiviat NB, Handsfield HH (1998) Genital human papillomavirus infection in women who have sex with women. J Infect Dis 178(6):1604–1609

    CAS  PubMed  Google Scholar 

  78. Burk RD, Ho GY, Beardsley L, Lempa M, Peters M, Bierman R (1996) Sexual behavior and partner characteristics are the predominant risk factors for genital human papillomavirus infection in young women. J Infect Dis 174(4):679–689

    CAS  PubMed  Google Scholar 

  79. Davidson M, Schnitzer PG, Bulkow LR, Parkinson AJ, Schloss ML, Fitzgerald MA, Knight JA, Murphy CM, Kiviat NB, Toomey KE et al (1994) The prevalence of cervical infection with human papillomaviruses and cervical dysplasia in Alaska Native women. J Infect Dis 169(4):792–800

    CAS  PubMed  Google Scholar 

  80. Palefsky JM, Shiboski S, Moss A (1994) Risk factors for anal human papillomavirus infection and anal cytologic abnormalities in HIV-positive and HIV-negative homosexual men. J Acquir Immune Defic Syndr 7(6):599–606

    CAS  PubMed  Google Scholar 

  81. Bauer HM, Hildesheim A, Schiffman MH, Glass AG, Rush BB, Scott DR, Cadell DM, Kurman RJ, Manos MM (1993) Determinants of genital human papillomavirus infection in low-risk women in Portland, Oregon. Sex Transm Dis 20(5):274–278

    CAS  PubMed  Google Scholar 

  82. Ley C, Bauer HM, Reingold A, Schiffman MH, Chambers JC, Tashiro CJ, Manos MM (1991) Determinants of genital human papillomavirus infection in young women. J Natl Cancer Inst 83(14):997–1003

    CAS  PubMed  Google Scholar 

  83. Rohan T, Mann V, McLaughlin J, Harnish DG, Yu H, Smith D, Davis R, Shier RM, Rawls W (1991) PCR-detected genital papillomavirus infection: prevalence and association with risk factors for cervical cancer. Int J Cancer 49(6):856–860

    CAS  PubMed  Google Scholar 

  84. Feldman JG, Chirgwin K, Dehovitz JA, Minkoff H (1997) The association of smoking and risk of condyloma acuminatum in women. Obstet Gynecol 89(3):346–350. doi:10.1016/s0029-7844(97)00011-2

    CAS  PubMed  Google Scholar 

  85. Simen-Kapeu A, La Ruche G, Kataja V, Yliskoski M, Bergeron C, Horo A, Syrjanen K, Saarikoski S, Lehtinen M, Dabis F, Sasco AJ (2009) Tobacco smoking and chewing as risk factors for multiple human papillomavirus infections and cervical squamous intraepithelial lesions in two countries (Cote d'Ivoire and Finland) with different tobacco exposure. Cancer Causes Control: CCC 20(2):163–170. doi:10.1007/s10552-008-9230-x

    PubMed  Google Scholar 

  86. Werden J, Schnatz PF, Mandavilli S, Allen G, Murphy JL, Greene JF, Egan JF, Sorosky JI (2008) Prevalence of the human papillomavirus in an inner-city indigent population with previously normal Pap tests. Journal Lower Genit Tract Dis 12(4):287–292. doi:10.1097/LGT.0b013e31817e307b

    Google Scholar 

  87. Hajjaj AA, Senok AC, Al-Mahmeed AE, Issa AA, Arzese AR, Botta GA (2006) Human papillomavirus infection among women attending health facilities in the Kingdom of Bahrain. Saudi Med J 27(4):487–491

    PubMed  Google Scholar 

  88. O'Keefe EJ, Gardner A, Currie MJ, Garland S, Tabrizi S, Bowden FJ (2006) Prevalence of genital human papillomavirus DNA in a sample of senior school-aged women in the Australian Capital Territory. Sex Health 3(2):91–94

    PubMed  Google Scholar 

  89. de Sanjose S, Almirall R, Lloveras B, Font R, Diaz M, Munoz N, Catala I, Meijer CJ, Snijders PJ, Herrero R, Bosch FX (2003) Cervical human papillomavirus infection in the female population in Barcelona, Spain. Sex Transm Dis 30(10):788–793. doi:10.1097/01.olq.0000080177.82204.e0

    PubMed  Google Scholar 

  90. Franceschi S, Castellsague X, Dal Maso L, Smith JS, Plummer M, Ngelangel C, Chichareon S, Eluf-Neto J, Shah KV, Snijders PJ, Meijer CJ, Bosch FX, Munoz N (2002) Prevalence and determinants of human papillomavirus genital infection in men. Br J Cancer 86(5):705–711. doi:10.1038/sj.bjc.6600194

    CAS  PubMed Central  PubMed  Google Scholar 

  91. Svare EI, Kjaer SK, Worm AM, Osterlind A, Meijer CJ, van den Brule AJ (2002) Risk factors for genital HPV DNA in men resemble those found in women: a study of male attendees at a Danish STD clinic. Sex Transm Infect 78(3):215–218

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Muckerman DR (1994) Subclinical human papillomavirus infection in a high-risk population. J Am Osteopath Assoc 94(7):545–550, 555-547

    CAS  PubMed  Google Scholar 

  93. Hildesheim A, Gravitt P, Schiffman MH, Kurman RJ, Barnes W, Jones S, Tchabo JG, Brinton LA, Copeland C, Epp J et al (1993) Determinants of genital human papillomavirus infection in low-income women in Washington, D.C. Sex Transm Dis 20(5):279–285

    CAS  PubMed  Google Scholar 

  94. Wheeler CM, Parmenter CA, Hunt WC, Becker TM, Greer CE, Hildesheim A, Manos MM (1993) Determinants of genital human papillomavirus infection among cytologically normal women attending the University of New Mexico student health center. Sex Transm Dis 20(5):286–289

    CAS  PubMed  Google Scholar 

  95. Kemp EA, Hakenewerth AM, Laurent SL, Gravitt PE, Stoerker J (1992) Human papillomavirus prevalence in pregnancy. Obstet Gynecol 79(5 ( Pt 1)):649–656

    CAS  PubMed  Google Scholar 

  96. Meekin GE, Sparrow MJ, Fenwicke RJ, Tobias M (1992) Prevalence of genital human papillomavirus infection in Wellington women. Genitourin Med 68(4):228–232

    CAS  PubMed Central  PubMed  Google Scholar 

  97. Melbye M, Palefsky J, Gonzales J, Ryder LP, Nielsen H, Bergmann O, Pindborg J, Biggar RJ (1990) Immune status as a determinant of human papillomavirus detection and its association with anal epithelial abnormalities. Int J Cancer 46(2):203–206

    CAS  PubMed  Google Scholar 

  98. Moscicki AB, Palefsky J, Gonzales J, Schoolnik GK (1990) Human papillomavirus infection in sexually active adolescent females: prevalence and risk factors. Pediatr Res 28(5):507–513. doi:10.1203/00006450-199011000-00018

    CAS  PubMed  Google Scholar 

  99. Sherman JF, Mount SL, Evans MF, Skelly J, Simmons-Arnold L, Eltabbakh GH (2008) Smoking increases the risk of high-grade vaginal intraepithelial neoplasia in women with oncogenic human papillomavirus. Gynecol Oncol 110(3):396–401. doi:10.1016/j.ygyno.2008.05.015

    CAS  PubMed  Google Scholar 

  100. Munk C, Svare EI, Poll P, Bock JE, Kjaer SK (1997) History of genital warts in 10,838 women 20 to 29 years of age from the general population. Risk factors and association with Papanicolaou smear history. Sexually transmitted diseases 24(10):567–572

    CAS  PubMed  Google Scholar 

  101. Brisson J, Roy M, Fortier M, Bouchard C, Meisels A (1988) Condyloma and intraepithelial neoplasia of the uterine cervix: a case-control study. Am J Epidemiol 128(2):337–342

    CAS  PubMed  Google Scholar 

  102. Hansen BT, Hagerup-Jenssen M, Kjaer SK, Munk C, Tryggvadottir L, Sparen P, Liaw KL, Nygard M (2010) Association between smoking and genital warts: longitudinal analysis. Sex Transm Infect 86(4):258–262. doi:10.1136/sti.2009.038273

    PubMed  Google Scholar 

  103. Massad LS, Xie X, Darragh T, Minkoff H, Levine AM, Watts DH, Wright RL, D'Souza G, Colie C, Strickler HD (2011) Genital warts and vulvar intraepithelial neoplasia: natural history and effects of treatment and human immunodeficiency virus infection. Obstet Gynecol 118(4):831–839. doi:10.1097/AOG.0b013e31821a0f4d

    PubMed Central  PubMed  Google Scholar 

  104. Massad LS, Silverberg MJ, Springer G, Minkoff H, Hessol N, Palefsky JM, Strickler HD, Levine AM, Sacks HS, Moxley M, Heather Watts D (2004) Effect of antiretroviral therapy on the incidence of genital warts and vulvar neoplasia among women with the human immunodeficiency virus. Am J Obstet Gynecol 190(5):1241–1248. doi:10.1016/j.ajog.2003.12.037

    CAS  PubMed  Google Scholar 

  105. Luu HN, Amirian ES, Beasley RP, Piller L, Chan W, Scheurer ME (2012) Association between smoking and size of anal warts in HIV-infected women. Int J STD AIDS 23(11):792–798. doi:10.1258/ijsa.2012.011420

    CAS  PubMed  Google Scholar 

  106. Habel LA, Van Den Eeden SK, Sherman KJ, McKnight B, Stergachis A, Daling JR (1998) Risk factors for incident and recurrent condylomata acuminata among women. Popul-Based Stud Sex Transm Dis 25(6):285–292

    CAS  Google Scholar 

  107. Sopori M (2002) Effects of cigarette smoke on the immune system. Nat Rev Immunol 2(5):372–377. doi:10.1038/nri803

    CAS  PubMed  Google Scholar 

  108. Peters EJ, Morice R, Benner SE, Lippman S, Lukeman J, Lee JS, Ro JY, Hong WK (1993) Squamous metaplasia of the bronchial mucosa and its relationship to smoking. Chest 103(5):1429–1432

    CAS  PubMed  Google Scholar 

  109. Sekhon HS, Wright JL, Churg A (1994) Cigarette smoke causes rapid cell proliferation in small airways and associated pulmonary arteries. Am J Physiol 267(5 Pt 1):L557–L563

    CAS  PubMed  Google Scholar 

  110. Feng Z, Hu W, Hu Y, Tang MS (2006) Acrolein is a major cigarette-related lung cancer agent: Preferential binding at p53 mutational hotspots and inhibition of DNA repair. Proc Natl Acad Sci U S A 103(42):15404–15409. doi:10.1073/pnas.0607031103

    CAS  PubMed Central  PubMed  Google Scholar 

  111. Phillips DH, Hewer A, Scholefield JH, Skinner P (2004) Smoking-related DNA adducts in anal epithelium. Mutat Res 560(2):167–172. doi:10.1016/j.mrgentox.2004.02.014

    CAS  PubMed  Google Scholar 

  112. Herrero R, Brinton LA, Reeves WC, Brenes MM, Tenorio F, de Britton RC, Gaitan E, Garcia M, Rawls WE (1989) Invasive cervical cancer and smoking in Latin America. J Natl Cancer Inst 81(3):205–211

    CAS  PubMed  Google Scholar 

  113. Wiley DJ, Elashoff D, Masongsong EV, Harper DM, Gylys KH, Silverberg MJ, Cook RL, Johnson-Hill LM (2009) Smoking enhances risk for new external genital warts in men. Int J Environ Res Public Health 6(3):1215–1234. doi:10.3390/ijerph6031215

    PubMed Central  PubMed  Google Scholar 

  114. Kjaer SK, Tran TN, Sparen P, Tryggvadottir L, Munk C, Dasbach E, Liaw KL, Nygard J, Nygard M (2007) The burden of genital warts: a study of nearly 70,000 women from the general female population in the 4 Nordic countries. J Infect Dis 196(10):1447–1454. doi:10.1086/522863

    PubMed  Google Scholar 

  115. Daling JR, Sherman KJ, Weiss NS (1986) Risk factors for condyloma acuminatum in women. Sex Transm Dis 13(1):16–18

    CAS  PubMed  Google Scholar 

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Kaderli, R., Schnüriger, B. & Brügger, L.E. The impact of smoking on HPV infection and the development of anogenital warts. Int J Colorectal Dis 29, 899–908 (2014). https://doi.org/10.1007/s00384-014-1922-y

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Keywords

  • Smoking
  • Human papillomavirus
  • Anogenital warts