Skip to main content

Advertisement

Log in

Tobacco smoking and chewing as risk factors for multiple human papillomavirus infections and cervical squamous intraepithelial lesions in two countries (Côte d’Ivoire and Finland) with different tobacco exposure

  • Original Paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Our objective was to compare the association between tobacco smoking and chewing and the risk of multiple human papillomavirus (HPV) infections and cervical squamous intraepithelial lesions (SILs) in two populations with different tobacco exposure. We studied 2,162 women from Côte d’Ivoire, West Africa, and 419 women from Finland, Northern Europe, with baseline data on cervical screening, HPV DNA status and smoking and chewing habits. The proportion of women who smoked and/or chewed tobacco was higher in Finland (36.8%) than in Côte d’Ivoire (3.7%), where tobacco chewing (2.6%) was more common than tobacco smoking (1.4%). Having multiple HPV infections was common in HPV16 and/or 18-infected women (60.4% in Finland and 47.2% in Côte d’Ivoire). There was no increased risk of multiple HPV infections among tobacco consumers. We found that women ≥30 years of age exposed to tobacco through smoking in Finland (OR: 2.2, 95% CI: 0.5–8.7) and chewing in Côte d’Ivoire (OR: 5.5, 95% CI: 2.1–14) had a moderately or highly increased risk of high-grade SIL, respectively. In the latter, the risk was statistically significant. Our findings emphasize the need for health initiatives targeted to prevent tobacco smoking or chewing among women especially in less industrialized countries.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. World Health Organisation (2003) World cancer report. IARC Press, Lyon, France

    Google Scholar 

  2. Ferlay J, Bray F, Pisani P, Parkin DM (2004) GLOBOCAN 2002: cancer incidence, mortality and prevalence worldwide. IARC cancer-base No. 5 version 2.0. IARC Press, Lyon

    Google Scholar 

  3. Parkin DM, Whelan SL, Ferlay J, Thomas DB, Teppo L (2002) Cancer incidence in five continents, vol 155. IARC Scientific publications, IARC Press, Lyon

    Google Scholar 

  4. Lehtinen M, Luukkaala T, Wallin KL, Paavonen J, Thoresen S, Dillner J et al (2001) Human papillomavirus type 16 infection and risk for subsequent development of cervical neoplasia—a systematic review. J Clin Virol 19:537–539

    Google Scholar 

  5. Munoz N, Bosch XF, de Sanjose S, Herrero R, Castellsague X, Shah KV et al (2003) Epidemiological classification of human papillomavirus types associated with cervical cancer. New Engl J Med 348:518–527

    Article  PubMed  Google Scholar 

  6. Kjellberg L, Hallmans G, Ahren AM, Johansson R, Bergman F, Wadell G et al (2000) Smoking, diet, pregnancy and oral contraceptive use as risk factors for cervical intra-epithelial neoplasia in relation to human papillomavirus infection. Br J Cancer 82:1332–1338

    Article  PubMed  CAS  Google Scholar 

  7. Winkelstein JW (1977) Smoking and cervical cancer of the uterine cervix: hypothesis. Am J Epidemiol 106:257–259

    PubMed  Google Scholar 

  8. Haverkos HW, Soon G, Steckley SL, Pickworth W (2003) Cigarette smoking and cervical cancer Part I: a meta-analysis. Biomed Pharmacother 57:67–77

    Article  PubMed  Google Scholar 

  9. Plummer M, Herrero R, Franceschi S, Meijer CJ, Snijders P, Bosch FX et al (2003) Smoking and cervical cancer: pooled analysis of the IARC multi-centric case–control study. Cancer Causes Control 14:805–814

    Article  PubMed  Google Scholar 

  10. McIntyre-Seltman K, Castle PE, Guido R, Schiffman M, Wheeler CM, ALTS Group (2005) Smoking is a risk factor for cervical intraepithelial neoplasia grade 3 among oncogenic human papillomavirus DNA-positive women with equivocal or mildly abnormal cytology. Cancer Epidemiol Biomarkers Prev 14:1165–1170

    Article  PubMed  CAS  Google Scholar 

  11. La Ruche G, Ramon R, Mensah-Ado I, Bergeron C, Diomandé M, Sylla-Koko F et al (1998) Squamous intraepithelial lesions of the cervix, invasive cervical carcinoma, and immunosuppression induced by human immunodeficiency virus in Africa Dyscer-CI Group. Cancer 82:2401–2408

    Article  PubMed  CAS  Google Scholar 

  12. Thomas JO, Herrero R, Omigbodun AA, Ojemakinde K, Ajayi IO et al (2004) Prevalence of papillomavirus infection in women in Ibadan, Nigeria: a population-based study. Br J Cancer 90:638–645

    Article  PubMed  CAS  Google Scholar 

  13. Liu J, Rose B, Huang X, Liao G, Carter J, Wu X et al (2004) Comparative analysis of characteristics of women with cervical cancer in high- versus low-incidence regions. Gynecol Oncol 94:803–810

    Article  PubMed  Google Scholar 

  14. Franco E, Villa L, Rohan T, Ferenczy A, Petzl-Erler M, Matlashewski G (1999) Design and methods of Ludwig-McGill longitudinal study of the natural history of human papillomavirus infection and cervical neoplasia in Brazil Ludwig-McGill study group. Rev Panam Salud Publica 6:223–233

    Article  PubMed  CAS  Google Scholar 

  15. Trottier H, Mahmud S, Costa MC, Sobrinho JP, Duarte-Franco E, Rohan TE et al (2006) Human papillomavirus infections with multiple types and risk of cervical neoplasia. Cancer Epidemiol Biomarkers Prev 15:1274–1280

    Article  PubMed  CAS  Google Scholar 

  16. Sasagawa T, Basha W, Yamazaki H, Inoue M (2001) High-risk and multiple human papillomavirus infections associated with cervical abnormalities in Japanese women. Cancer Epidemiol Biomarkers Prev 10:45–52

    PubMed  CAS  Google Scholar 

  17. Simen-Kapeu A, Kataja V, Yliskoski M, Syrjänen K, Dillner J, Koskela P et al (2008) Smoking impairs human papillomavirus (HPV) type 16 and 18 capsids antibody response following natural HPV infection. Scand J Infect Dis 40:745–751

    Article  PubMed  CAS  Google Scholar 

  18. Kataja V, Syrjänen S, Mäntyjärvi R, Yliskoski M, Saarikoski S, Syrjänen K (1992) Prognostic factors in cervical human papillomavirus infections. Sex Transm Dis 19:154–160

    Article  PubMed  CAS  Google Scholar 

  19. La Ruche G, Mensah-Ado I, Bergeron C, Welffens-Ekra C, Dabis F (1999) Cervical screening in Africa: discordant diagnosis in a double independent reading DYSCER-CI Group. J Clin Epidemiol 52:953–958

    Article  PubMed  CAS  Google Scholar 

  20. La Ruche G, You B, Mensah-Ado I, Bergeron C, Montcho C, Ramon R et al (1998) Human papillomavirus and human immunodeficiency virus infections: relation with cervical dysplasia-neoplasia in African women. Int J Cancer 76:480–486

    Article  PubMed  CAS  Google Scholar 

  21. Syrjänen S, Syrjänen K (1986) An improved in situ hybridization protocol for detection of human papillomavirus (HPV) DNA sequences in paraffin-embedded biopsies. J Virol Meth 14:293–304

    Article  Google Scholar 

  22. Jarvis MJ, Tunstall-Pedoe H, Feyerabend C, Vesey C, Saloojee Y (1987) Comparison of test used to distinguish smokers from non-smokers. Am J Public Health 77:1435–1438

    Article  PubMed  CAS  Google Scholar 

  23. National Infectious Diseases Register (NIDR) (2007) National Public Health Institute (KTL), Finland

  24. Takuma F, Nobuo M, Miyuki SCT, Nobumaru H, Schinichi N, Makio M et al (2005) Comparison between in situ hybridization and real-time PCR technique as a means of detecting the integrated form of human papillomavirus 16 in cervical neoplasia. Diagn Mol Pathol 14:103–108

    Article  Google Scholar 

  25. Dabié MM, Hlupié L, Babié D, Jukié S, Seiwerth S (2004) Comparison of polymerase chain reaction and catalyzed signal amplification in situ hybridization methods for human papillomavirus detection in paraffin-embedded cervical preneoplastic and neoplastic lesions. Arch Med Res 35:511–516

    Article  CAS  Google Scholar 

  26. Biedermman K, Dandachi N, Trattner M, Vogl G, Doppelmayr H, Moré E et al (2004) Comparison of real-time PCR signal-amplified in situ hybridization and conventional PCR for detection and quantification of human papillomavirus in archival cervical cancer tissue. J Clin Microbiol 42:3758–3765

    Article  CAS  Google Scholar 

  27. Leminen A, Paavonen J, Vesterinen E, Wahlström T, Rantala I, Lehtinen M (1992) Human papillomavirus types 16 and 18 in adenocarcinoma of the uterine cervix. Am J Clin Pathol 95:647–652

    Google Scholar 

  28. Rajkumar T, Franceschi S, Vaccarella S, Gajalakshmi V, Sharmila A, Snijders PJ et al (2003) Role of paan chewing and dietary habits in cervical carcinoma in Chennai, India. Br J Cancer 88:1388–1393

    Article  PubMed  CAS  Google Scholar 

  29. Muwonge R, Ramadas K, Sankila R, Thara S, Thomas G, Vinoda J et al (2007) Role of tobacco smoking, chewing and alcohol drinking in the risk of oral cancer in Trivandrum, India: a nested case–control design using incident cancer cases. Oral Oncol 44:446–454

    Article  PubMed  CAS  Google Scholar 

  30. Hoffmann D, Djordjevic MV (1997) Chemical composition and carcinogenicity of smokeless tobacco. Adv Dent Res 11:322–329

    Article  PubMed  CAS  Google Scholar 

  31. Cogliano V, Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F (2004) Smokeless tobacco and tobacco-related nitrosamines. Lancet Oncol 5:708

    Article  PubMed  Google Scholar 

  32. International Agency for Research on Cancer (2005) Smokeless tobacco and some related nitrosamines. IARC monographs on the evaluation of carcinogenic risk to humans, vol 89. IARC Press, Lyon, France

    Google Scholar 

  33. Tolstrup J, Munk C, Lykke Thomsen B, Svare E, van Den Brule AJC, Grønæk M et al (2006) The role of smoking and alcohol intake in the development of high-grade squamous intraepithelial lesions among high–risk HPV-positive women. Acta Obstet Gynecol Scand 85:1114–1119

    Article  PubMed  Google Scholar 

  34. Krüger-kjær S, van Den Brule AJC, Svare EI, Engholm G, Sherman ME, Poll PA et al (1998) Different risk factor patterns for high-grade and low-grade intraepithelial lesions on the cervix among HPV-positive and HPV-negative young women. Int J Cancer 76:613–619

    Article  PubMed  Google Scholar 

  35. Vartiainen E, Seppälä T, Lillsunde P, Puska P (2002) Validation of self reported smoking by serum cotinine measurement in a community-based study. J Epidemiol Community Health 56:167–170

    Article  PubMed  CAS  Google Scholar 

  36. Deacon JM, Evans CD, Yule R, Desai M, Binns W, Taylor C 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 83:1565–1572

    Article  PubMed  CAS  Google Scholar 

  37. Rousseau MC, Abrahamowicz M, Villa LL, Costa MC, Rohan TE, Franco EL (2003) Predictors of cervical coinfection with multiple human papillomavirus types. Cancer Epidemiol Biomarkers Prev 12:1029–1037

    PubMed  Google Scholar 

  38. Syrjänen K, Shabalova I, Petrovichev N, Kozachenko V, Zakharova T, Pajanidi J (2007) Smoking is an independent risk factor for oncogenic human papillomavirus (HPV) infections but not for high-grade CIN. Eur J Epidemiol 22:723–735

    Article  PubMed  Google Scholar 

  39. Kataja V, Syrjänen S, Yliskoski M, Hippelïnen M, Väyrynen M, Saarikoski S et al (1993) Risk factors associated with cervical human papillomavirus Infections: a case–control study. Am J Epidemiol 138:735–745

    PubMed  CAS  Google Scholar 

  40. Simons AM, Múgica van Herckenrode C, Rodriguez JA, Maitland N, Anderson M, Phillips DH et al (1995) Demonstration of smoking-related DNA damage in cervical epithelium and correlation with human papillomavirus type 16, using exfoliated cervical cells. Br J Cancer 71:246–249

    PubMed  CAS  Google Scholar 

  41. Poppe WAJ, Ide PS, Drijkoningen M, Lauweryns JM, van Assche FA (1995) Tobacco smoking impairs the local immunosurveillance in the uterine cervix. Gynecol Obstet Invest 39:34–38

    Article  PubMed  CAS  Google Scholar 

  42. Arcavi L, Benowitz NL (2004) Cigarette smoking and infection. Arch Intern Med 164:2206–2216

    Article  PubMed  Google Scholar 

  43. La Ruche G, Leroy V, Mensah-Ado I, Ramon R, You B, Bergeron C et al (1999) Short-term follow up of cervical squamous intraepithelial lesions associated with HIV and human papillomavirus infections in Africa. Int J STD AIDS 10:363–368

    Article  PubMed  CAS  Google Scholar 

  44. IARC (2004) Tobacco smoke and involuntary smoking. IARC Monographs on the Evaluation of the carcinogenic risks to humans, vol 83. IARC Press, Lyon, France

    Google Scholar 

  45. Sukvirach S, Smith JS, Tunsakul S, Muñoz N, Kesararat V, Opasatian O et al (2003) Population-based human papillomavirus prevalence in Lampang and Songkla, Thailand. J Infect Dis 187:1246–1256

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

This study was supported by a grant from the Cancer Control using Population-based Registries and Biobanks (CCPRB) European Union Network. The study conducted in Cote d’Ivoire was supported by grants from the French Agence Nationale de Recherches sur le Sida (ANRS) and the French Ministry of Cooperation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aline Simen-Kapeu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Simen-Kapeu, A., La Ruche, G., Kataja, V. et al. Tobacco smoking and chewing as risk factors for multiple human papillomavirus infections and cervical squamous intraepithelial lesions in two countries (Côte d’Ivoire and Finland) with different tobacco exposure. Cancer Causes Control 20, 163–170 (2009). https://doi.org/10.1007/s10552-008-9230-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-008-9230-x

Keywords

Navigation