Subscribe to RSS
DOI: 10.1055/s-0042-1742662
Screening for Early Detection of Cervical Cancer in Women Living with HIV in Mumbai, India - Retrospective Cohort Study from a Tertiary Cancer Center
Funding None.Abstract
Introduction Women living with human immunodeficiency virus (HIV) have an increased risk of persistent human papillomavirus infection (HPV) of developing cervical cancer precursors and are, therefore, considered at higher risk for cervical cancer. Despite the higher risk, screening for cervical cancer is extremely low among HIV-positive women in India.
Objectives Given the limited usefulness of cytology-based screening programs, the current study retrospectively evaluated the comparative performance of visual inspection with 5% acetic acid (VIA), conventional cytology, and human papillomavirus (HPV) testing among HIV-positive women attending the cancer screening clinic at the tertiary cancer center.
Materials and Methods Retrospective analysis of 291 HIV-positive women attending cervical cancer screening services in a tertiary cancer center in Mumbai was undertaken. All underwent simultaneous screening with VIA, Pap cytology, and HPV DNA testing, followed by diagnostic colposcopy and histopathology. Sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) to detect cervical intraepithelial neoplasia (CIN) 2/3 on histology were estimated.
Results The screen positivity rate for cervical cancer screening by VIA, high-risk HPV DNA, and Pap cytology was 35.7, 34.4, and 6.2% respectively. At the CIN2+ disease threshold, the sensitivity, specificity, PPV, and NPV estimates were 80.00% (59.30–93.17), 68.42% (62.46–73.96), 19.23% (15.46–23.67), 97.33% (94.30–98.77) for VIA; 80.00% (68.78–97.45), 70.68% (64.81–76.08), 22.00% (18.22–26.32), 98.43% (95.58–99.45) for HPV DNA; and 64.00% (42.52–82.03), 98.12% (95.67–99.39), 76.19% (56.13–88.89), 96.67% (94.50–98.00) for cytology (HSIL cutoff).
Conclusion The diagnostic performance of VIA and HPV DNA was comparable and better than cytology indicating that VIA as a cost-effective cervical cancer screening test can be incorporated within the services under sexually transmitted diseases /HIV testing and counseling centers within the country.
Acknowledgments
This manuscript has been read and approved by all the authors and represents honest work.
Publication History
Article published online:
27 February 2022
© 2022. Indian Society of Medical and Paediatric Oncology. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)
Thieme Medical and Scientific Publishers Pvt. Ltd.
A-12, 2nd Floor, Sector 2, Noida-201301 UP, India
-
References
- 1 Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68 (06) 394-424
- 2 Baseman JG, Koutsky LA. The epidemiology of human papillomavirus infections. J Clin Virol 2005; 32 (Suppl. 01) S16-S24
- 3 International Agency for Research on Cancer. Globocan India 2020. Accessed December 2, 2021 at: https://gco.iarc.fr/today/data/factsheets/populations/356-india-fact-sheets.pdf
- 4 Palefsky J. Human papillomavirus-related disease in people with HIV. Curr Opin HIV AIDS 2009; 4 (01) 52-56
- 5 Maiman M, Fruchter RG, Clark M, Arrastia CD, Matthews R, Gates EJ. Cervical cancer as an AIDS-defining illness. Obstet Gynecol 1997; 89 (01) 76-80
- 6 Denny L, Boa R, Williamson AL. et al. Human papillomavirus infection and cervical disease in human immunodeficiency virus-1-infected women. Obstet Gynecol 2008; 111 (06) 1380-1387
- 7 Liu G. et al. Prevalent HPV infection increases the risk of HIV acquisition in African women: advancing the argument for HPV immunization. AIDS 2022; 36 (02) 257-265
- 8 Averbach SH, Gravitt PE, Nowak RG. et al. The association between cervical human papillomavirus infection and HIV acquisition among women in Zimbabwe. AIDS 2010; 24 (07) 1035-1042
- 9 Stelzle D, Tanaka LF, Lee KK. et al. Estimates of the global burden of cervical cancer associated with HIV. Lancet Glob Health 2021; 9 (02) e161-e169
- 10 National AIDS Control Organization & ICMR-National Institute of Medical Statistics. (2020). India HIV Estimates 2019: Report. New Delhi: NACO, Ministry of Health and Family Welfare, Government of India. Accessed September 27, 2021 at: http://naco.gov.in/sites/default/files/Estimation%20Report%202019.pdf
- 11 Ferreira MP, Coghill AE, Chaves CB. et al. Outcomes of cervical cancer among HIV-infected and HIV-uninfected women treated at the Brazilian National Institute of Cancer. AIDS 2017; 31 (04) 523-531
- 12 Chaturvedi AK, Madeleine MM, Biggar RJ, Engels EA. Risk of human papillomavirus-associated cancers among persons with AIDS. J Natl Cancer Inst 2009; 101 (16) 1120-1130
- 13 Massad LS, Seaberg EC, Watts DH. et al. Long-term incidence of cervical cancer in women with human immunodeficiency virus. Cancer 2009; 115 (03) 524-530
- 14 Chambuso RS, Shadrack S, Lidenge SJ, Mwakibete N, Medeiros RM. Influence of HIV/AIDS on cervical cancer: a retrospective study from Tanzania. J Glob Oncol 2016; 3 (01) 72-78
- 15 Shastri SS, Mittra I, Mishra GA. et al. Effect of VIA screening by primary health workers: randomized controlled study in Mumbai, India. J Natl Cancer Inst 2014; 106 (03) dju009
- 16 Sankaranarayanan R, Esmy PO, Rajkumar R. et al. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: a cluster-randomised trial. Lancet 2007; 370 (9585): 398-406
- 17 Sankaranarayanan R, Nene BM, Shastri SS. et al. HPV screening for cervical cancer in rural India. N Engl J Med 2009; 360 (14) 1385-1394
- 18 Arbyn M, Sankaranarayanan R, Muwonge R. et al. Pooled analysis of the accuracy of five cervical cancer screening tests assessed in eleven studies in Africa and India. Int J Cancer 2008; 123 (01) 153-160
- 19 Sankaranarayanan R, Wesley RS. A practical manual on visual screening for cervical neoplasia. Lyon: International Agency for Research on Cancer, World Health Organization; 2003. IARC Technical Publication; No. 41. Available at A practical manual on visual screening for cervical neoplasia (iarc.fr). Accessed September 27, 2021
- 20 Nayar R, Wilbur DC. The Pap Test and Bethesda 2014. “The reports of my demise have been greatly exaggerated.” (after a quotation from Mark Twain). Acta Cytol 2015; 59 (02) 121-132
- 21 Darragh TM, Colgan TJ, Thomas Cox J. et al; Members of the LAST Project Work Groups. The lower anogenital squamous terminology standardization project for HPV-associated lesions: background and consensus recommendations from the college of American pathologists and the American society for colposcopy and cervical pathology. Int J Gynecol Pathol 2013; 32 (01) 76-115
- 22 Dinshaw KA, Tongaonkar HB, Shrivastava SK, Parikh PM, Maheshwari A. Evidence Based Management Guideline. Gynaecological Cancer. Vol III. Mumbai: Tata Memorial Hospital; 2004
- 23 Bornstein J, Bentley J, Bösze P. et al. 2011 colposcopic terminology of the International Federation for Cervical Pathology and Colposcopy. Obstet Gynecol 2012; 120 (01) 166-172
- 24 Clifford GM, Gonçalves MA, Franceschi S. HPV and HIV Study Group. Human papillomavirus types among women infected with HIV: a meta-analysis. AIDS 2006; 20 (18) 2337-2344
- 25 De Vuyst H, Lillo F, Broutet N, Smith JS. HIV, human papillomavirus, and cervical neoplasia and cancer in the era of highly active antiretroviral therapy. Eur J Cancer Prev 2008; 17 (06) 545-554
- 26 Teeraananchai S, Kerr SJ, Amin J, Ruxrungtham K, Law MG. Life expectancy of HIV-positive people after starting combination antiretroviral therapy: a meta-analysis. HIV Med 2017; 18 (04) 256-266
- 27 Joshi S, Sankaranarayanan R, Muwonge R, Kulkarni V, Somanathan T, Divate U. Screening of cervical neoplasia in HIV-infected women in India. AIDS 2013; 27 (04) 607-615
- 28 Chakravarty J, Chourasia A, Thakur M, Singh AK, Sundar S, Agrawal NR. Prevalence of human papillomavirus infection & cervical abnormalities in HIV-positive women in eastern India. Indian J Med Res 2016; 143 (01) 79-86
- 29 Gedefaw A, Astatkie A, Tessema GA. The prevalence of precancerous cervical cancer lesion among HIV-infected women in southern Ethiopia: a cross-sectional study. PLoS One 2013; 8 (12) e84519
- 30 Hopkins KL, Jaffer M, Hlongwane KE. et al. Assessing national cervical cancer screening guidelines: results from an HIV testing clinic also screening for cervical cancer and HPV in Soweto, South Africa. PLoS One 2021; 16 (07) e0255124
- 31 Memiah P, Mbuthia W, Kiiru G. et al. Prevalence and risk factors associated with precancerous cervical cancer lesions among HIV-infected women in resource-limited settings. Aids Res Treat 2012; 2012: 953743
- 32 Teixeira NC, Araújo AC, Correa CM. et al. Prevalence and risk factors for cervical intraepithelial neoplasia among HIV-infected women. Braz J Infect Dis 2012; 16 (02) 164-169
- 33 Zhang HY, Tiggelaar SM, Sahasrabuddhe VV. et al. HPV prevalence and cervical intraepithelial neoplasia among HIV-infected women in Yunnan Province, China: a pilot study. Asian Pac J Cancer Prev 2012; 13 (01) 91-96
- 34 Sahasrabuddhe VV, Bhosale RA, Kavatkar AN. et al. Comparison of visual inspection with acetic acid and cervical cytology to detect high-grade cervical neoplasia among HIV-infected women in India. Int J Cancer 2012; 130 (01) 234-240
- 35 Massad LS, Riester KA, Anastos KM. et al; Women's Interagency HIV Study Group. Prevalence and predictors of squamous cell abnormalities in Papanicolaou smears from women infected with HIV-1. J Acquir Immune Defic Syndr 1999; 21 (01) 33-41
- 36 Fruchter RG, Maiman M, Sedlis A, Bartley L, Camilien L, Arrastia CD. Multiple recurrences of cervical intraepithelial neoplasia in women with the human immunodeficiency virus. Obstet Gynecol 1996; 87 (03) 338-344
- 37 Frisch M, Biggar RJ, Goedert JJ. Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. J Natl Cancer Inst 2000; 92 (18) 1500-1510
- 38 Joshi SN, Gopalkrishna V, Kumar BK. 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 (04) 470-475
- 39 Sankaranarayanan R, Gaffikin L, Jacob M, Sellors J, Robles S. A critical assessment of screening methods for cervical neoplasia. Int J Gynaecol Obstet 2005; 89 (Suppl. 02) S4-S12
- 40 Denny L, Anorlu R. Cervical cancer in Africa. Cancer Epidemiol Biomarkers Prev 2012; 21 (09) 1434-1438
- 41 Akinwuntan AL, Adesina OA, Okolo CA. et al. Correlation of cervical cytology and visual inspection with acetic acid in HIV-positive women. J Obstet Gynaecol 2008; 28 (06) 638-641
- 42 Palefsky JM. Human papillomavirus-associated anal and cervical cancers in HIV-infected individuals: incidence and prevention in the antiretroviral therapy era. Curr Opin HIV AIDS 2017; 12 (01) 26-30
- 43 Mwanahamuntu MH, Sahasrabuddhe VV, Blevins M. et al. Utilization of cervical cancer screening services and trends in screening positivity rates in a ‘screen-and-treat’ program integrated with HIV/AIDS care in Zambia. PLoS One 2013; 8 (09) e74607
- 44 Meyerson BE, Sayegh MA, Davis A. et al. Cervical cancer screening in a sexually transmitted disease clinic: screening adoption experiences from a midwestern clinic. Am J Public Health 2015; 105 (2, Suppl 2) e8-e14
- 45 Datta SD, Saraiya M. Cervical cancer screening among women who attend sexually transmitted diseases (STD) clinics: background paper for 2010 STD Treatment Guidelines. Clin Infect Dis 2011; 53 (Suppl. 03) S153-S159