Acquisition, prevalence and clearance of type-specific human papillomavirus infections in young sexually active Indian women: A community-based multicentric cohort study

Richard Muwonge, Partha Basu, Tarik Gheit, Devasena Anantharaman, Yogesh Verma, Neerja Bhatla, Smita Joshi, Pulikottil O Esmy, Usha Rani Reddy Poli, Anand Shah, Eric Zomawia, Surendra S Shastri, Sharmila Pimple, Priya R Prabhu, Sanjay Hingmire, Aruna Chiwate, Catherine Sauvaget, Eric Lucas, Sylla G Malvi, Maqsood Siddiqi, Subha Sankaran, Thiraviam Pillai Rameshwari Ammal Kannan, Rintu Varghese, Uma Divate, Shachi Vashist, Gauravi Mishra, Radhika Jadhav, Massimo Tommasino, M Radhakrishna Pillai, Rengaswamy Sankaranarayanan, Kasturi Jayant, Indian HPV vaccine study group, Richard Muwonge, Partha Basu, Tarik Gheit, Devasena Anantharaman, Yogesh Verma, Neerja Bhatla, Smita Joshi, Pulikottil O Esmy, Usha Rani Reddy Poli, Anand Shah, Eric Zomawia, Surendra S Shastri, Sharmila Pimple, Priya R Prabhu, Sanjay Hingmire, Aruna Chiwate, Catherine Sauvaget, Eric Lucas, Sylla G Malvi, Maqsood Siddiqi, Subha Sankaran, Thiraviam Pillai Rameshwari Ammal Kannan, Rintu Varghese, Uma Divate, Shachi Vashist, Gauravi Mishra, Radhika Jadhav, Massimo Tommasino, M Radhakrishna Pillai, Rengaswamy Sankaranarayanan, Kasturi Jayant, Indian HPV vaccine study group

Abstract

In context of the ongoing multi-centric HPV vaccine study in India, unvaccinated married women (N = 1484) aged 18-23 years were recruited in 2012-2015 as age-matched controls to the vaccinated women and followed up yearly. We assess type-specific prevalence, natural history and potential determinants of human papillomavirus (HPV) infection in these unvaccinated women. Cervical samples were collected yearly for at least four consecutive years. A Multiplex Type-Specific E7-Based polymerase chain reaction assay was used to detect 21 HPV types. HPV prevalence was 36.4% during 6 years. Most common HPV types were 16 (6.5%) and 31 (6.1%). Highest persistence were observed for HPV 35 (62.5%) and 52 (25%). New HPV acquisition rate was 5.6/1000 person-months of observation (PMO), highest for HPV 16 (1.1/1000 PMO). Type-specific clearance rates ranged between 2.9-5.5/100 PMO. HPV 16 and/or 18 infections were 41% (95% CI 4-63%) lower among women with 2-<3 years between marriage and first cervical sample collection compared to those with <2 years. HPV prevalence and acquisition rates in young Indian women were lower than their Western counterparts. HPV 16 infections being most common shows the importance and potential impact of HPV vaccination in India. Women with 2-3 years exposure had reduced risk possibly due to higher infections clearance.

Conflict of interest statement

The corresponding authors, on behalf of all authors, declares the following potential competing interests: Neerja Bhatla has received research funding through her institute from GlaxoSmithKline and Merck. Smita Joshi has received funds from GlaxoSmithKline through the Jehangir Clinical Development Center to do an HPV vaccine study. Partha Basu has received research funding from GlaxoSmithKline through Chittaranjan National Cancer Institute, India during his previous position at the institute. This does not alter our adherence to PLOS ONE policies on sharing data and materials. The other authors declare no competing interests.

Figures

Fig 1. Kaplan-Meier curves of cumulative probability…
Fig 1. Kaplan-Meier curves of cumulative probability of HPV infection among women negative for a specific type on their first cervical cell sample collection.
Fig 2. Kaplan-Meier curves of the proportion…
Fig 2. Kaplan-Meier curves of the proportion women who had type-specific HPV clearance.
Fig 3. Cervical cancer incidence reported by…
Fig 3. Cervical cancer incidence reported by population-based cancer registries at the Indian study sites and rank of cervical cancer by incidence among all cancers in females (Data source: National Cancer Registry Programme, India).

References

    1. Schiffman M, Clifford G, Buonaguro FM. Classification of weakly carcinogenic human papillomavirus types: addressing the limits of epidemiology at the borderline. Infect Agent Cancer. 2009;4:8 10.1186/1750-9378-4-8
    1. Trottier H, Franco EL. The epidemiology of genital human papillomavirus infection. Vaccine. 2006;24(Suppl 1):S1–15. 10.1016/j.vaccine.2005.09.054
    1. Koutsky LA, Holmes KK, Critchlow CW, Stevens CE, Paavonen J, Beckmann AM, et al. A cohort study of the risk of cervical intraepithelial neoplasia grade 2 or 3 in relation to papillomavirus infection. N Engl J Med. 1992; 327(18):1272–8. 10.1056/NEJM199210293271804
    1. Maucort-Boulch D, Franceschi S, Plummer M; IARC HPV Prevalence Surveys Study Group. International correlation between human papillomavirus prevalence and cervical cancer incidence. Cancer Epidemiol Biomarkers Prev. 2008; 17(3):717–20. 10.1158/1055-9965.EPI-07-2691
    1. Sharma M, Bruni L, Diaz M, Castellsagué X, de Sanjosé S, Bosch FX, et al. Using HPV prevalence to predict cervical cancer incidence. Int J Cancer. 2013; 132(8):1895–900. 10.1002/ijc.27835
    1. Sankaranarayanan R, Basu P, Kaur P, Bhaskar R, Singh GB, Denzongpa P, et al. Current status of human papillomavirus vaccination in India's cervical cancer prevention efforts. Lancet Oncol. 2019; 20(11):e637–e644. 10.1016/S1470-2045(19)30531-5
    1. Basu P, Muwonge R, Bhatla N, Nene BM, Joshi S, Esmy PO, et al. Two-dose recommendation for Human Papillomavirus vaccine can be extended up to 18 years—updated evidence from Indian follow-up cohort study. Papillomavirus Res. 2019; 7:75–81. 10.1016/j.pvr.2019.01.004
    1. Sankaranarayanan R, Prabhu PR, Pawlita M, Gheit T, Bhatla N, Muwonge R, et al. Immunogenicity and HPV infection after one, two, and three doses of quadrivalent HPV vaccine in girls in India: a multicentre prospective cohort study. Lancet Oncol. 2016; 17(1):67–77. 10.1016/S1470-2045(15)00414-3
    1. Eklund C, Forslund O, Wallin KL, Dillner J. Continuing global improvement in human papillomavirus DNA genotyping services: The 2013 and 2014 HPV LabNet international proficiency studies. J Clin Virol. 2018; 101:74–85. 10.1016/j.jcv.2018.01.016
    1. Plummer M, Schiffman M, Castle PE, Maucort-Boulch D, Wheeler CM; ALTS Group. A 2-year prospective study of human papillomavirus persistence among women with a cytological diagnosis of atypical squamous cells of undetermined significance or low-grade squamous intraepithelial lesion. J Infect Dis. 2007; 195(11):1582–9. 10.1086/516784
    1. Koshiol J, Lindsay L, Pimenta JM, Poole C, Jenkins D, Smith JS. Persistent human papillomavirus infection and cervical neoplasia: a systematic review and meta-analysis. Am J Epidemiol. 2008;168(2):123–37. 10.1093/aje/kwn036
    1. Giuliano AR, Harris R, Sedjo RL, Baldwin S, Roe D, Papenfuss MR, et al. Incidence, prevalence, and clearance of type-specific human papillomavirus infections: The Young Women's Health Study. J Infect Dis. 2002; 186(4):462–9. 10.1086/341782
    1. Castle PE, Schiffman M, Herrero R, Hildesheim A, Rodriguez AC, Bratti MC, et al. A prospective study of age trends in cervical human papillomavirus acquisition and persistence in Guanacaste, Costa Rica. J Infect Dis. 2005; 191(11):1808–16. 10.1086/428779
    1. Ramanakumar AV, Naud P, Roteli-Martins CM, de Carvalho NS, de Borba PC, Teixeira JC, et al. Incidence and duration of type-specific human papillomavirus infection in high-risk HPV-naïve women: results from the control arm of a phase II HPV-16/18 vaccine trial. BMJ Open. 2016; 6(8):e011371 10.1136/bmjopen-2016-011371
    1. Datta P, Bhatla N, Pandey RM, Dar L, Patro AR, Vasisht S, et al. Type-specific incidence and persistence of HPV infection among young women: a prospective study in North India. Asian Pac J Cancer Prev. 2012; 3(3):1019–24. 10.7314/apjcp.2012.13.3.1019
    1. Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch FX, de Sanjosé S. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis. 2010; 202(12):1789–99. 10.1086/657321
    1. Bruni L, Albero G, Serrano B, Mena M, Gómez D, Muñoz J, et al. Human Papillomavirus and Related Diseases in the World. Summary Report 17 June 2019. Available from: . Access 07/04/2020.
    1. Aggarwal R, Gupta S, Nijhawan R, Suri V, Kaur A, Bhasin V, et al. Prevalence of high—risk human papillomavirus infections in women with benign cervical cytology: a hospital based study from North India. Indian J Cancer. 2006; 43(3):110–6. 10.4103/0019-509x.27932
    1. Vinodhini K, Shanmughapriya S, Sanmugham S, Senthikumar G, Das BC, Natarajaseenivasan K. Prevalence of high-risk HPV and associated risk factors in cases of cervical carcinoma in Tamil Nadu, India. Int J Gynaecol Obstet. 2012; 119(3):253–6. 10.1016/j.ijgo.2012.06.019
    1. Kerkar SC, Latta S, Salvi V, Mania-Pramanik J. Human Papillomavirus infection in asymptomatic population. Sex Reprod Healthc. 2011; 2(1):7–11. 10.1016/j.srhc.2010.11.001
    1. Varghese C. Prevalence and determinants of human papillomavirus (HPV) infection in Kerala, India. University of Tampere, Tampere, 2000. Available from: . Accessed 07/04/2020.
    1. Franceschi S, Rajkumar R, Snijders PJF, Arslan A, Mahe C, Plummer M. Papillomavirus infection in rural women in southern India. Br J Cancer. 2005; 92(3):601–6. 10.1038/sj.bjc.6602348
    1. Datta P, Bhatla N, Dar L, Patro AR, Gulati A, Kriplani A, et al. Prevalence of human papillomavirus infection among young women in North India. Cancer Epidemiol. 2010; 34(2):157–61. 10.1016/j.canep.2009.12.016
    1. Srivastava S, Gupta S, Roy JK. High prevalence of oncogenic HPV-16 in cervical smears of asymptomatic women of eastern Uttar Pradesh, India: a population-based study. J Biosci. 2012;37: 37(1):63–72. 10.1007/s12038-012-9181-y
    1. Sharma K, Kathait A, Jain A, Kujur K, Raghuwanshi S, Bharti AC, et al. Higher prevalence of human papillomavirus infection in adolescent and young adult girls belonging to different Indian tribes with varied socio-sexual lifestyle. PLoS One. 2015; 10(5):e0125693 10.1371/journal.pone.0125693
    1. Clifford GM, Vaccarella S, Franceschi S, Tenet V, Umulisa MC, Tshomo U, et al. Comparison of Two Widely Used Human Papillomavirus Detection and Genotyping Methods, GP5+/6+-Based PCR Followed by Reverse Line Blot Hybridization and Multiplex Type-Specific E7-Based PCR. J Clin Microbiol. 2016;54(8):2031–8. 10.1128/JCM.00618-16
    1. Comar M, Iannacone MR, Casalicchio G, McKay-Chopin S, Tommasino M, Gheit T. Comparison of hybrid capture II, linear array, and a bead-based multiplex genotyping assay for detection of human papillomavirus in women with negative pap test results and atypical squamous cells of undetermined significance. J Clin Microbiol. 2012;50(12):4041–6. 10.1128/JCM.02105-12
    1. Schmitt M, Dondog B, Waterboer T, Pawlita M, Tommasino M, Gheit T. Abundance of multiple high-risk human papillomavirus (HPV) infections found in cervical cells analyzed by use of an ultrasensitive HPV genotyping assay. J Clin Microbiol. 2010;48(1):143–9. 10.1128/JCM.00991-09
    1. International Institute for Population Sciences and ICF. National Family Health Survey (NFHS-4), 2015–16. Mumbai: IIPS, 2017.
    1. National Centre for Disease Informatics and Research, National Cancer Registry Programme, Indian Council of Medical Research. Three-Year Report of Population Based Cancer Registries 2012–2014. Incidence, Distribution, Trends in Incidence Rates and Projections of Burden of Cancer (Report of 27 PBCRs in India). Bengaluru, India March 2016.
    1. Bao YP, Li N, Smith JS, Qiao YL; ACCPAB members. Human papillomavirus type distribution in women from Asia: a meta-analysis. Int J Gynecol Cancer. 2008;18: 18(1):71–9. 10.1111/j.1525-1438.2007.00959.x
    1. Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB, Koutsky LA. Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students. Am J Epidemiol. 2003; 157(3):218–26. 10.1093/aje/kwf180
    1. Franco EL, Villa LL, Sobrinho JP, Prado JM, Rousseau MC, Désy M, et al. Epidemiology of acquisition and clearance of cervical human papillomavirus infection in women from a high-risk area for cervical cancer. J Infect Dis. 1999; 180(5):1415–23. 10.1086/315086

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