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Clearance of oncogenic human papillomavirus (HPV) infection: effect of smoking (United States)

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Abstract

Objective: The purpose of this investigation was to assess the association between smoking and clearance of oncogenic human papillomavirus (HPV) infection. Methods: A prospective cohort study of 346 women aged 18–35 years was conducted. HPV testing was conducted with the Hybrid Capture II (HC II) system and polymerase chain reaction (PCR) with genotyping using the reverse line blot method. At each visit tobacco exposure, reproductive, and sexual histories were assessed. Probability of clearing an oncogenic HPV infection and duration of oncogenic HPV infections by smoking status was assessed. Results: Regardless of method used, HC II or PCR, ever smokers maintained an HPV infection significantly longer (median duration of 8.5 months vs 10.7 months, never vs ever smokers), and had a lower probability of clearing an oncogenic infection compared with women who never smoked. Smoking duration was significantly associated with HPV clearance, and a dose response was observed. Older age (> 13 years) at smoking initiation was significantly associated with a reduced probability of clearing an oncogenic HPV infection. Conclusion: This is the first study to demonstrate that smoking promotes early cervical carcinogenic events by increasing duration of oncogenic HPV infections and decreasing probability of clearing oncogenic infections.

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References

  1. Palefsky JM, Holly EA (1995) Molecular virology and epidemiology of human papillomavirus and cervical cancer. Cancer Epidemiol Biomarkers Prev 4: 415–428.

    Google Scholar 

  2. Ho GY, Burk RD, Klein S, et al. (1995) Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia. J Natl Cancer Inst 87: 1365–1371.

    Google Scholar 

  3. Koutsky LA, Holmes KH, Critchlow CW, et al. (1992) A cohort study of the risk of cervical intraepithelial neoplasia grade 2 or 3 in relation to papillomavirus infection. N Engl JMed 327: 1272–1278.

    Google Scholar 

  4. Schiffman MH (1995) New epidemiology of human papillomavirus infection and cervical neoplasia. J Natl Cancer Inst 87: 1345–1347.

    Google Scholar 

  5. Winkelstein W (1986) Cigarette smoking and cancer of the uterine cervix. In: Hoffman D, Harris CC, eds. Mechanisms in Tobacco Carcinogenesis. Banbury report 23. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, pp. 329–341.

    Google Scholar 

  6. Winkelstein W (1990) Smoking and cervical cancer-current status: a review. Am J Epidemiol 131: 945–957.

    Google Scholar 

  7. Hellberg D, Nilsson S, Haley NJ, Hoffman D, Wynder E (1988) Smoking and cervical intraepithelial neoplasia: nicotine and cotinine in serum and cervical mucus in smokers and non-smokers. Am J Obstet Gynecol 158: 910–913.

    Google Scholar 

  8. Sasson IM, Haley NJ, Hoffman D, Wynder EL, Hellberg D (1985) Cigarette smoking and neoplasia of the uterine cervix: smoke constituents in cervical mucus. N Engl J Med 312: 315–316.

    Google Scholar 

  9. Holly EA, Petrakis NL, Friend NF, Sarles DL, Lee RE, Flander LB (1986) Mutagenic mucus in the cervix of smokers. J Natl Cancer Inst 76: 983–986.

    Google Scholar 

  10. Barton SE, Jenkins D, Cuzick J, Maddox PH, Edwards R, Singer A (1988) Effect of cigarette smoking on cervical epithelial immunity: a mechanism for neoplastic change? Lancet 2: 652–654.

    Google Scholar 

  11. Hildesheim A, Schiffman MH, Gravitt PE, et al. (1994) Persistence of type-specific human papillomavirus infection among cytologically normal women. J Infect Dis 169: 235–240. Effect of smoking on HPV clearance 845

    Google Scholar 

  12. Ho GYF, Bierman R, Beardsley L, Chang CJ, Burk RD (1998) Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338: 423–428.

    Google Scholar 

  13. Giuliano AR, Harris R, Sedjo RL, et al. (2002) Incidence and clearance of type-specific HPV infections: The Young Women's Health Study. J Infect Dis 186: (in press).

  14. Cox TJ, Lorincz AT, Schiffman MH, Sherman ME, Cullen A, Kurman RJ (1995) Human papillomavirus testing by Hybrid Capture appears to be useful in triaging women with a cytologic diagnosis of atypical squamous cells of undetermined significance. Am J Obstet Gynecol 172: 946–954.

    Google Scholar 

  15. Hall S, Lorincz A, Shah F, et al. (1996) Human papillomavirus DNA detection in cervical specimens by Hybrid Capture: correlation with cytologic and histologic diagnoses of squamous intraepithelial lesions of the cervix. Gynecol Oncol 62: 353–359.

    Google Scholar 

  16. Vernon SD, Unger ER, Williams D (2000) Comparison of human papillomavirus detection and typing by cycle sequencing, line blotting, and Hybrid Capture. J Clin Microbiol. 38: 651–655.

    Google Scholar 

  17. Gravitt P, Peyton C, Alessi T, et al. (2000) Improved amplification of genital human papillomaviruses. J Clin Microbiol 38: 357–361S.

    Google Scholar 

  18. Gravitt PE, Payton CL, Apple RJ, Wheeler CM (1998) Genotyping of 27 human papillomavirus types by using L1 consensus PCR products by a single-hybridization, reverse line blot detection method. J Clin Microbiol 36: 3020–3027.

    Google Scholar 

  19. Layde PM (1989) Smoking and cervical cancer: cause or coincidence? JAMA 261: 1631–1633.

    Google Scholar 

  20. Simons AM, Phillips DH, Coleman DV (1993) Damage to DNA in cervical epithelium related to smoking tobacco. BMJ 306: 1444–1448.

    Google Scholar 

  21. Becker TM, Wheeler CM, McGiuough NS, et al. (1994) Cigarette smoking and other risk factors for cervical dysplasia in Southwestern Hispanic and non-Hispanic white women. Cancer Epidemiol Biomarkers Prev 3: 113–119.

    Google Scholar 

  22. Lacey JV Jr, Frisch M, Brinton LA, et al. (2001) Associations between smoking and adenocarcinomas and squamous cell carcinomas of the uterine cervix (United States). Cancer Causes Control 12: 153–161.

    Google Scholar 

  23. Gram IT, Austin H, Stalsberg H (1992) Cigarette smoking and the incidence of cervical intraepithelial neoplasia, Grade III, and cancer of the cervix uteri. Am J Epidemiol 135: 341–346.

    Google Scholar 

  24. Burger MP, Hollema H, Gouww AS, Pieters WJ, Quint WG (1993) Cigarette smoking and human papillomavirus. BMJ 306: 749–752.

    Google Scholar 

  25. Dahling JR, Sherman KJ, Hislop TG, Maden C, Mandelsohn MT, Beckman AM, Weiss NS (1992) Cigarette smoking and the risk of anogenital cancer. Am J Epidemiol 135: 180–189.

    Google Scholar 

  26. Deacon JM, Evans CD, Yule R, et al. (2000) Sexual behaviour and smoking as determinants of cervical HPV infection and of CIN3 among those infected: a case-control study nested within the Manchester cohort. Br J Cancer 88: 1565–1572.

    Google Scholar 

  27. Kjaer SK, Van den Brucle AJC, Bock JE, et al. (1996) Human papillomavirus-the most significant risk determinant of cervical intraepithelial neoplasia. Int J Cancer 65: 601–606.

    Google Scholar 

  28. Kjaer SK, Engholm G, Dahl C, Bock JE (1996) Case-control study of risk factors for cervical squamous cell neoplasia in Denmark. IV: Role of smoking habits. Eur J Cancer Prev 5: 359–365.

    Google Scholar 

  29. Daling JR, Madeleine MM, McKnight B, et al. (1996) The relationship of human papillomavirus-related cervical tumors to cigarette smoking, oral contraceptive use, and prior herpes simplex virus type II infection. Cancer Epidemiol Biomarkers Prev 5: 541–548.

    Google Scholar 

  30. Sassagwa T, Dong Y, Saijoh K, Shin-ichirou S, Masaya T, Masaki I (1997) Human papillomavirus infection and risk determinants for squamous intraepithelial lesion and cervical cancer in Japan. Jpn J Cancer Res 88: 376–384.

    Google Scholar 

  31. Ho GYF, Kadish AS, Burk RD, et al. (1998) HPV 16 and cigarette smoking as risk factors for high grade cervical intraepithelial neoplasia. Int J Cancer 78: 281–285S.

    Google Scholar 

  32. Chichareon S, Herrero R, Munoz N, Bosch FX, et al. (1998) Risk factors for cervical cancer in Thailand: a case-control study. J Natl Cancer Inst 90: 50–57.

    Google Scholar 

  33. Ngelangel C, Munox N, Bosch FX, et al. (1998) Causes of cervical cancer in the Philippines: a case-control study. J Natl Cancer Inst 90: 43–49.

    Google Scholar 

  34. Olsen AO, Dillner J, Skrondal A, Magnus P(1998) Combined effect of smoking and human papillomavirus type 16 infection in cervical carcinogenesis. Epidemiololgy 9: 346–349.

    Google Scholar 

  35. Ylitalo N, Sorensen P, Josefsson A, et al. (1999) Smoking and oral contraceptives as risk factors for cervical carcinoma in situ. Int J Cancer 81: 357–365.

    Google Scholar 

  36. Kjellberg L, Hallmans G, Ahren A-M, et al. (2000) Smoking, diet, pregnancy, and oral contraceptive use as risk factors for cervical intraepithelial neoplasia in relation to human papillomavirus infection. Br J Cancer 82: 1332–1338.

    Google Scholar 

  37. Hildesheim A, Herrero R, Castle PE, et al. (2001) HPV co-factors related to the development of cervical cancer: results from a population-based study in Costa Rica. Br J Cancer 84: 1219–1226.

    Google Scholar 

  38. Ferson M, Edwards, A, Lind A, Milton GW, Hersey P(1979) Low natural killer cell activity and immunoglobulin levels associated with smoking in human subjects. Int J Cancer 23: 603–609.

    Google Scholar 

  39. Barton SE, Jenkins D, Cuzick J, Maddox PH, Edwards R, Singer A (1988) Effect of cigarette smoking on cervical epithelial immunity: a mechanism for neoplastic change? Lancet 2: 652–654.

    Google Scholar 

  40. Moscicki AB, Shiboski S, Broering J, et al. (1998) The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr 132: 277–284.

    Google Scholar 

  41. Schlecht NF, Kulaga S, Robitaille J, et al. (2001) Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA 286: 3106–3114.

    Google Scholar 

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Authors and Affiliations

  1. Arizona Cancer Center, University of Arizona, Tucson, AZ, USA

    Anna R. Giuliano, Rebecca L. Sedjo, Denise J. Roe, Robin Harris, Susie Baldwin, Mary R. Papenfuss, Martha Abrahamsen & Paula Inserra

  2. Arizona College of Public Health, University of Arizona, Tucson, AZ, USA

    Anna R. Giuliano, Denise J. Roe & Robin Harris

  3. Arizona Cancer Center, 1515 N. Campbell Avenue, Room 4977C, Tucson, AZ, 85724-5024, USA

    Anna R. Giuliano

  4. Department of Obstetrics and Gynecology, University of Arizona, Tucson, AZ, USA

    Susie Baldwin

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  1. Anna R. Giuliano
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Giuliano, A.R., Sedjo, R.L., Roe, D.J. et al. Clearance of oncogenic human papillomavirus (HPV) infection: effect of smoking (United States). Cancer Causes Control 13, 839–846 (2002). https://doi.org/10.1023/A:1020668232219

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