Correlation of Cervical Squamous Intraepithelial Lesions with Human Papillomavirus in Women Infected with the Human Immunodeficiency Virus

  • Gautam Kumar Vasnik
  • Gitanjali JainEmail author
  • Fatima Abbas Husainy
  • Vasu Bansal
Original Article



The human papillomavirus (HPV) is the major etiologic agent in the development of cervical cancer with known risk factors like immunosuppression. The natural history of HPV infection is altered in persons infected with the human immunodeficiency virus (HIV). The persistent HPV infection increases their risk of having cervical squamous intraepithelial lesions (SILs). This study emphasizes on prevalence of high-risk human papillomavirus (HR-HPV) and correlation with cervical smears cytology in HIV-positive women regardless of treatment.


A cross-sectional observational study was conducted at a tertiary care hospital over a period of 2 years. The study group is comprised of HIV seropositive women attending antiretroviral treatment center. CD4 cell counts were taken from the records available, and cervical samples were taken for cytological analysis and HR-HPV testing. Statistical analysis was done using the software Epi 6 Info, and p value was calculated by Chi-square test and Fisher’s exact 2-tailed test for associations of abnormal cytology and to determine risk factors for abnormal cytology.


The median age of the 100 participants was 33.34 years. Low-grade squamous intraepithelial neoplasms (LSILs), high-grade squamous intraepithelial neoplasms, atypical squamous cells of uncertain significance and atypical glandular cells were the precancerous lesions found. Prevalence of HR-HPV in HIV-positive women was found to be 35% among women with abnormal smears. A strong correlation between SILs and HR-HPV with p value of < 0.05 was found. A strong statistical correlation was also seen in between low CD4 count to that of detection of HR-HPV along with LSIL.


A strong correlation between cervical SILs and HR-HPV in our study suggests that routine screening of cervical cytology by PAP smear should include HPV subtype identification in HIV-positive women to pick up cases which are likely to progress to invasive carcinoma.


Cervical squamous intraepithelial lesions Human papillomavirus Human immunodeficiency virus 


Authors’ contribution

GKV conceived the study and was in charge of overall direction and planning and supervised the findings of this work and directed the author and co-authors. GJ wrote the manuscript in consultation with main and co-authors. FAH and VB contributed to case preparation and manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    World Health Organization: Cervical cancer (2018). Accessed 10 Nov 2018
  2. 2.
    Ellerbrock TV, Chiasson MA, Bush TJ, Sun XW, Sawo D, Brudney K, Wright TC Jr. Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA. 2000;283:1031–7.CrossRefGoogle Scholar
  3. 3.
    Jan N, Moscicki AB. Human papillomavirus infections in women with HIV disease: prevalence, risk, and management. AIDS. 2000;10:659–68.Google Scholar
  4. 4.
    World Health Organization: Human papillomavirus (HPV) and cervical cancer. 2016.
  5. 5.
    Sreedevi A, Javed R, Dinesh A. Epidemiology of cervical cancer with special focus on India. Int J Womens Health. 2015;7:405–14.PubMedPubMedCentralGoogle Scholar
  6. 6.
    Kanowitz S, Miller SB, Stone J, Hanson E. The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr. 1998;132(2):277–84.CrossRefGoogle Scholar
  7. 7.
    Strickler HD, Burk RD, Fazzari M, Nastos K, Minkoff H, Massad LS, Hall C, Bacon M, Levine AM, Watts DH, Silverberg MJ, Xue X, Schlecht NF, Melnick S, Palefsky JM. Natural history and possible reactivation of human papillomavirus in human immunodeficiency virus-positive women. J Natl Cancer Inst. 2005;97:577–86.CrossRefGoogle Scholar
  8. 8.
    Wright TC Jr, Ellerbrock TV, Chiasson MA, Van Devanter N, Sun XW. Cervical intraepithelial neoplasia in women infected with human immunodeficiency virus: prevalence, risk factors, and validity of Papanicolaou smears. New York Cervical Disease Study. Obstet Gynecol. 1994;84:591–7.PubMedGoogle Scholar
  9. 9.
    Minkoff H, Ahdieh L, Massad SL, Anastos K, Watts DH, Melnick S, et al. The effect of highly active antiretroviral therapy on cervical cytologic changes associated with oncogenic HPV among HIV-infected women. AIDS. 2001;15:2157–64.CrossRefGoogle Scholar
  10. 10.
    Enebe JT, Dim CC, Nnakenyi EF, Ezegwui HU, Ozumba BC. Effect of low CD4 cell count on cervical squamous intraepithelial lesions among HIV-positive women in Enugu, Southeastern Nigeria. J Clin Diagn Res. 2015;9(11):QC07–10.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Menon S, Luchters S, Rossi R, Callens S, Kishor M, Bogers J, Vanden Broeck D. Human papilloma virus correlates of high grade cervical dysplasia in HIV-infected women in Mombasa, Kenya: a cross-sectional analysis. Virol J. 2018;15(1):54.CrossRefGoogle Scholar
  12. 12.
    Harris TG, Burk RD, Palesky JM, Massad LS, Bang JY, Anastos K, Minkoff H, Hall CB, Bacon MC, Levine AM, Watts H, Silverberg MJ, Xue X, Melick SL, Strickler HD. Incidence of cervical intraepithelial lesions associated with HIV serostatus, CD4 cell counts and human papillomavirus test results. JAMA. 2005;293:1471–6.CrossRefGoogle Scholar
  13. 13.
    de Sanjose S, Palefsky J. Cervical and anal HIV infections in HIV positive women and men. Virus Res. 2002;89(2):201–11.CrossRefGoogle Scholar
  14. 14.
    Palefsky JM. Cervical human papillomavirus infection and cervical intraepithelial neoplasia in women positive for human immunodeficiency virus in the era of highly active antiretroviral therapy. Curr Opin Oncol. 2003;15:382–8.CrossRefGoogle Scholar
  15. 15.
    Heard I, Potard V, Costagliola D. Limited impact of immunosuppression and HAART on the incidence of cervical squamous intraepithelial lesions in HIV-positive women. Antivir Ther. 2006;11:1091–6.PubMedGoogle Scholar
  16. 16.
    Sankaranarayanan R, Esmy PO, Rajkumar R, Muwonge R, Swaminathan R, Shanthakumari S, et al. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: a cluster-randomised trial. Lancet. 2007;370:398–406.CrossRefGoogle Scholar
  17. 17.
    Dames DN, Ragin C, Griffith-Bowe A, Gomez P, Butler R. The prevalence of cervical cytology abnormalities and human papillomavirus in women infected with the human immunodeficiency virus. Infect Agents Cancer. 2009;4(Suppl 1):S8.CrossRefGoogle Scholar
  18. 18.
    Bagga R, Wanchu A, Rajwanshi A, Gupta KR, Prasad GRV, Gopalan S, Sachdeva RK, et al. Papanicolaou smear abnormalities in HIV-infected women in north India. Asia-Pac J Clin Oncol. 2005;1:77–80.CrossRefGoogle Scholar
  19. 19.
    Omar T, Schwartz S, Hanrahan C, Modisenyane T, Tshabangu N, Golub JE, et al. Progression and regression of premalignant cervical lesions in HIV-infected women from Soweto: a prospective cohort. AIDS. 2011;25(1):87–94.CrossRefGoogle Scholar
  20. 20.
    Carlucci M, Cimmino A, Fiore MG. The Pap test in HIV-positive women. Pathologica. 2001;93(6):651–3.PubMedGoogle Scholar
  21. 21.
    McKenzie KP, Rogers RK, Njoroge JW, John-Stewart G, Richardson BA, Mugo NR, et al. Cervical squamous intraepithelial lesions among HIV-positive women on antiretroviral therapy in Kenya. Curr HIV Res. 2011;9(3):180–5.CrossRefGoogle Scholar
  22. 22.
    Hameed M, Fernandes H, Skurnick J, Moore D, Kloser P, Heller D. Human papillomavirus typing in HIV-positive women. Infect Dis Obstet Gynecol. 2001;9:89–93.CrossRefGoogle Scholar
  23. 23.
    Zarcone R, Cardone G, Bellini P, Carfora E, Fortuna G, Raucci F. Incidence of HPV and CIN in HIV positive women. Minerva Ginecol. 1995;47(11):477–80.PubMedGoogle Scholar
  24. 24.
    Peedicayil A, Thiyagarajan K, Gnanamony M, Pulimood SA, Jeyaseelan V, Kannangai R, et al. Prevalence and risk factors for human papillomavirus and cervical intraepithelial neoplasia among HIV positive women at a tertiary level hospital in India. J Low Genit Tract Dis. 2009;13(3):159–64.CrossRefGoogle Scholar
  25. 25.
    Sarkar K, Pal R, Bal B, Saha B, Bhattacharya S, Sengupta S, Mazumdar PP, Chakraborti S. Oncogenic HPV among HIV infected female population in West Bengal, India. BMC Infect Dis. 2011;11:72.CrossRefGoogle Scholar
  26. 26.
    Joshi SN, Gopalkrishna V, Kumar BK, Dutta S, Nyaynirgune P, Thakar M, et al. Cervical squamous intra-epithelial changes and human papillomavirus infection in women infected with human immunodeficiency virus in Pune, India. J Med Virol. 2005;76(4):470–5.CrossRefGoogle Scholar
  27. 27.
    Mogtomo ML, Malieugoue LC, Djiepgang C, Wankam M, Moune A, Ngane AN. Incidence of cervical disease associated to HPV in human immunodeficiency infected women under highly active antiretroviral therapy. Infect Agent Cancer. 2009;4:9.CrossRefGoogle Scholar
  28. 28.
    Human Papillomavirus and Related Diseases Report (2018). Accessed 27 Oct 2018.
  29. 29.
    Mbulawa ZZ, Marais DJ, Johnson LF, Boulle A, Coetzee D, Williamson AL. Influence of human immunodeficiency virus and CD4 count on the prevalence of human papillomavirus in heterosexual couples. J Gen Virol. 2010;91(12):3023–31.CrossRefGoogle Scholar
  30. 30.
    Delmas MC, Larsen C, van Benthem B, Hamers FF, Bergeron C, Poveda JD, et al. Cervical squamous intraepithelial lesions in HIV-infected women: prevalence, incidence and regression. European Study Group on Natural History of HIV Infection in Women. AIDS. 2000;14:1775–84.CrossRefGoogle Scholar
  31. 31.
    Firnhaber C, Van Le H, Pettifor A, Schulze D, Michelow P, Sanne IM, et al. Association between cervical dysplasia and human papillomavirus in HIV seropositive women from Johannesburg South Africa. Cancer Causes Control. 2010;21(3):433–43.CrossRefGoogle Scholar

Copyright information

© Association of Gynecologic Oncologists of India 2019

Authors and Affiliations

  • Gautam Kumar Vasnik
    • 1
  • Gitanjali Jain
    • 2
    Email author
  • Fatima Abbas Husainy
    • 3
  • Vasu Bansal
    • 4
  1. 1.Department of PathologyMilitary HospitalNasirabadIndia
  2. 2.Department of PediatricsArmed Forces Medical CollegePuneIndia
  3. 3.Department of Obstetrics and Gynecology158 Base HospitalBagdograIndia
  4. 4.Armed Forces Medical CollegePuneIndia

Personalised recommendations