Type-specific Prevalence of Human Papillomavirus by Cervical Cytology among Women in Brasov, Romania

  • Moga, Marius Alexandru (Department of Gynecology, Transilvania University) ;
  • Irimie, Marius (Department of Dermatology, Transilvania University) ;
  • Oanta, Alexandru (Department of Dermatology, Transilvania University) ;
  • Pascu, Alina (Department of Pathophysiology, Transilvania University) ;
  • Burtea, Victoria (Department of Psychiatry, Transilvania University)
  • Published : 2014.08.30


The oncogenic role of human papillomavirus (HPV) in triggering cervical cancer, the second most common cancer in women worldwide, is well established. Romania ranks in first place in Europe in terms of the incidence of cervical cancer. Geographical widespread data on HPV type-distribution are essential for estimating the impact of HPV vaccines and cervical cancer screening programmes. In this study we aimed to identify the prevalence of HPV genotypes and to establish correlations with abnormal cervical cytology among the female population of Brasov County, Romania. A total of 1,000 women aged 17.3-57 years, attending routine cervical examination in the Obstetrics and Gynecology Hospital of Brasov, Romania, and undergoing both cytological examination and HPV genotyping were screened. Infection with 35 different HPV genotypes was detected in 39.6% of cytological specimens. Overall HPV infections were highest in young women under 25 years (p<0.0001), in which cervical cytological abnormalities also reached the highest prevalence. Patients infected by HPV-16 or HPV-18 showed the highest prevalence of cervical cytological abnormalities. Some 48.2% of women with abnormal cytology were infected with high-risk HPV types whereas less than 3% of them were infected only with low-risk HPV types. Our study showed that the prevalence of high-risk HPV infection among Romanian women is higher compared to other studies in other geographic areas. Thus, we consider that in areas where there is an increased prevalence of high-risk HPV infections, HPV genotyping should be performed in all women aged between 18 and 45 years, and Pap test should be performed every 6 months in women with high-risk HPV infection, even those with previous normal cervical cytology.


Human papillomavirus;cervical cancer;genotyping;Brasov;Romania


  1. Aral SO, Holmes KK (1999). Social and behavioral determinants of epidemiology of STDs: industrialized and developing countries. In: Holmes KK, Mardh P-A, Sparling PF, et al., editors. Sexually Transmitted Diseases. New York: McGraw- Hill; p. 39-76.
  2. Barzon L, Giorgi C, Buonaguro FM, Palu G (2008). Guidelines of the Italian Society for Virology on HPV testing and vaccination for cervical cancer prevention. Infect Agents Cancer, 3, 14.
  3. Bello BD, Spinillo A, Alberizzi P, et al (2009). Cervical infections by multiple human papillomavirus (HPV) genotypes: prevalence and impact on the risk of precancerous epithelial lesions. J Med Virol, 81, 703-12.
  4. Bosch FX, Manos MM, Munoz N, et al (1995). International biological study on cervical cancer (ibscc) study group. prevalence of human papillomavirus in cervical cancer: a worldwide perspective. J Natl Cancer Inst, 87, 796-802.
  5. Bouvard V, Baan R, Straif K, et al (2009). A review of human carcinogens - Part B: biological agents. Lancet Oncol, 10, 321-2.
  6. Brown DR, Shew ML, Qadadri B, et al (2005). A longitudinal study of genital human papillomavirus infection in a cohort of closely followed adolescent women. J Infect Dis, 191, 182-92.
  7. Castellsague X, Menendez C, Loscertales MP, et al (2001). Human papillomavirus genotypes in rural Mozambique. Lancet, 358, 1429-30.
  8. Clifford GM, Gallus S, Herrero R, et al (2005). Worldwide distribution of human papillomavirus types in cytologically normal women in the International Agency for Research on Cancer HPV prevalence surveys: a pooled analysis. Lancet, 366, 991-8.
  9. Clifford GM, Smith JS, Plummer M, Munoz N, Franceschi S (2003). Human papillomavirus types in invasive cervical cancer worldwide: A metaanalysis. Br J Cancer, 88, 63-73.
  10. Datta P, Bhatla N, Pandey RM, et al (2012). Type-specific incidence and persistence of HPV infection among young women: a prospective study in North India. Asian Pac J Cancer Prev, 13, 1019-24.
  11. Davey DD, Neal MH, Wilbur DC, et al (2004). Bethesda 2001 implementation and reporting rates: 2003 practices of participants in the college of american pathologists interlaboratory comparison program in cervicovaginal cytology. Arch Pathol Lab Med, 128, 1224-9.
  12. De Sanjose S, Quint WC, Alemany L, et al (2010). Human papillomavirus genotype attribution in invasive cervical cancer: a retrospecttive cross-sectional worldwide study. Lancet Oncol, 11, 1048-56.
  13. Fife KH, Cramer HM, Schroeder JM, Brown DR (2001). Detection of multiple human papillomavirus types in the lower genital tract correlates with cervical dysplasia. J Med Virol, 64, 550-9.
  14. Forslund O, Antonsson A, Edlund K, et al (2002). Populationbased type-specific prevalence of high-risk human papillomavirus infection in middle-aged Swedish women. J Med Virol, 66, 535-41.
  15. Franceschi S, Herrero R, Clifford GM, et al (2006). Variations in the age-specific curves of human papillomavirus prevalence in women worldwide. Int J Cancer, 119, 2677-84.
  16. GLOBOCAN 2008 (IARC), Section of Cancer Information ( Accesed 12 March 2014.
  17. Halfon P, Sandri MT, Raimondo A, et al (2013). Comparison of the performance of carcinogenic HPV typing of the Roche Linear Array and Qiagen $LiquiChip^{(R)}$ HPV assays. BMC Infect Dis, 13, 499.
  18. Hamzi Abdul Raub S, Isa NM, Zailani HA, et al (2014). Distribution of HPV genotypes in cervical cancer in multiethnic Malaysia. Asian Pac J Cancer Prev, 15, 651-6.
  19. Herrero R, Hildesheim A, Bratti C, et al (2000). Populationbased study of human papillomavirus infection and cervical neoplasia in rural Costa Rica. J Natl Cancer Inst, 92, 464-74.
  20. Ho GY, Bierman R, Beardesley L, et al (1998). Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med, 338, 423-8.
  21. IARC monographs on the evaluation of carcinogenic risks to humans: A review of human carcinogens: part B. Biological agents. 100th edition. Lyon, France: International Agency for Research on Cancer; 2011: 261-319. .
  22. Lee EH, Um TH. Chi HS, et al (2012). Prevalence and distribution of human papillomavirus infection in Korean women as determined by restriction fragment mass polymorphism assay. J Korean Med Sci, 27, 1091-7.
  23. Mandelblatt JS, Lawrence WF, Womack SM, et al. (2002). Benefits and costs of using HPV testing to screen for cervical cancer. JAMA, 287, 2372-81.
  24. Masia G, Mazzoleni AP, Contu G, et al (2009). Epidemiology and genotype distribution of human papillomavirus (HPV) in women of Sardinia (Italy). Vaccine, 27, 11-16.
  25. Meijer CJ, Snijders PJ, Castle PE (2006). Clinical utility of HPV genotyping. Gynecol Oncol, 103, 12-17.
  26. Munoz N, Mendez F, Posso H, et al (2004). Incidence, duration, and determinants of cervical human papillomavirus infection in a cohort of Colombian women with normal cytological results. J Infect Dis, 190, 2077-87.
  27. Natphopsuk S, Settheetham-Ishida W, Pientong C, et al (2013). Human papillomavirus genotypes and cervical cancer in northeast Thailand. Asian Pac J Cancer Prev, 14, 6961-4.
  28. Nessa A, Nahar KN, Begum SA, et al. (2013). Comparison between visual inspection of cervix and cytology based screening procedures in Bangladesh. Asian Pac J Cancer Prev, 14, 7607-11.
  29. Othman N, Othman NH (2014). Detection of human papillomavirus DNA in routine cervical scraping samples: use for a national cervical cancer screening program in a developing nation. Asian Pac J Cancer Prev, 15, 2245-9.
  30. Pandey S, Mishra M, Chandrawati (2012). Human papillomavirus screening in north Indian women. Asian Pac J Cancer Prev, 13, 2643-6.
  31. Schlecht NF, Kulaga S, Robitaille J, et al (2001). Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA, 286, 3106-14.
  32. Sengul D, Altinay S, Oksuz H, Demirturk H, Korkmazer E (2014). Population-based cervical screening outcomes in Turkey over a period of approximately nine and a half years with emphasis on results for women aged 30-34. Asian Pac J Cancer Prev, 15, 2069-74.
  33. Siriaunkgul S, Settakorn J, Sukpan K, et al (2014). HPV detection and genotyping in vulvar squamous cell carcinoma in northern Thailand. Asian Pac J Cancer Prev, 15, 3773-8.
  34. Smith JS, Lindsay L, Hoots B, et al (2007). Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer, 121, 621-32.
  35. Smith JS, Melendy A, Rana RK, Pimenta JM (2008). Agespecific prevalence of infection with human papillomavirus in females: a global review. J Adolesc Health, 43, 5-25.
  36. Snijders PJ, Steenberg RD, Heideman DA, Meijer CJ (2006). HPV-mediated cervical carcinogenesis: concepts and clinical implications. J Pathol 208, 152-64.
  37. Stanley M (2006). Immune responses to human papillomavirus. Vaccine, 24, 16-22.
  38. Trottier H, Franco EL (2006). The epidemiology of genital human papillomavirus infection. Vaccine, 24, 4-15.
  39. Veena S, Premraj S, Narotam S, Pracheta, Ritu P (2012). Study of epidemiology of HPV infection in the uterine cervix of women in Delhi /NCR regions, India. Int J Drug Development and Research, 4, 311-5.
  40. Wang SM, Zhang SK, Pan XF, et al (2014). Human papillomavirus vaccine awareness, acceptability, and decision-making factors among chinese college students. Asian Pac J Cancer Prev, 15, 3239-45.
  41. Wang YY, Li L, Wei S, et al (2013). Human papillomavirus (HPV) infection in women participating in cervical cancer screening from 2006 to 2010 in Shenzhen City, South China. Asian Pac J Cancer Prev, 14, 7483-7.
  42. Weinstock H, Berman S, Caces Jr W (2004). Sexually transmitted diseases among American youth: incidence and prevalence estimates, 2000. Perspect Sex Reprod Health, 36, 6-10.

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