We sought to evaluate prevalence, age-adjusted distribution, and impact of single and multiple high- and low-risk human papillomavirus (HPV) subtypes and their associations with cervical lesions.
Data were extracted from 11,224 women who underwent routine screening of HPV genotyping and liquid-based cytology co-testing. Fifteen high-risk (HR) and six low-risk (LR) HPV types were genotyped.
Overall HPV prevalence was 10.7 %, and young women (under 21 years old) harbored highest HPV infection rate (40.38 %). The rate declined in old women 9.49 % (age 30–49) and 6.89 % (age 50 and above). Normal cytology had lowest HPV (5.66 %) compared to low-grade (60.49 %), high-grade (71.96 %) squamous intraepithelial lesions (LSIL and HSIL) and squamous cell carcinoma SCC (86.9 %). LR HPV subtypes were absent in SCC and were consistently lower than HR HPV in LSIL (6.74 vs. 33.54 %) and HSIL (2.12 vs. 51.32 %). Multiple HPV infection was more frequent in young women under 30 years old (10 %) than older women (2 %) and in LSIL (20.2 %), HSIL (18.5 %) than SCC (4.4 %). HR HPV 52, 16, 18, and 58 were the most frequent subtypes in normal, LSIL, and HSIL. Greater or equal proportion of HPV 16, 18, 45, and 52 was found in SCC compared to normal cytology (SCC/normal ratios 4.8, 1.2, 1.6, and 1.7). While important in LSIL and HSIL, HPV58 was not detected in SCC.
Taken together, identification of these HPV types, especially HPV 16, 18, 45, and 52, and their associated cervical lesions may improve cervical cancer preventive strategies in Indonesia.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Safaeian M, Rodriguez AC (2014) Invited commentary: multiple human papillomavirus infections and type replacement—anticipating the future after human papillomavirus vaccination. Am J Epidemiol 180:1076–1081. doi:10.1093/aje/kwu265
Hausen zur h (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342–350. doi:10.1038/nrc798
Schiffman M, Wentzensen N (2013) Human papillomavirus infection and the multistage carcinogenesis of cervical cancer. Cancer Epidemiol Biomark Prev 22:553–560. doi:10.1158/1055-9965.EPI-12-1406
Trottier H (2006) Human papillomavirus infections with multiple types and risk of cervical neoplasia. Cancer Epidemiol Biomark Prev 15:1274–1280. doi:10.1158/1055-9965.EPI-06-0129
Dickson EL, Vogel RI, Geller MA, Downs LS Jr (2014) Cervical cytology and multiple type HPV infection: a study of 8182 women ages 31–65. Gynecol Oncol 133:405–408. doi:10.1016/j.ygyno.2014.03.552
Chagas BS, Comar M, Gurgel APAD et al (2015) Association study between cervical lesions and single or multiple vaccine-target and non-vaccine target human papillomavirus (HPV) types in women from northeastern Brazil. PLoS One 10:e0132570. doi:10.1371/journal.pone.0132570
Wentzensen N, Nason M, Schiffman M et al (2014) No evidence for synergy between human papillomavirus genotypes for the risk of high-grade squamous intraepithelial lesions in a large population-based study. J Infect Dis 209:855–864. doi:10.1093/infdis/jit577
Liu SS, Leung R, Chan K (2010) Evaluation of a newly developed GenoArray human papillomavirus (HPV) genotyping assay and comparison with the Roche Linear Array HPV genotyping assay. J Clin 48:758–764. doi:10.1128/JCM.00989-09
Yang Z, Cuzick J, Hunt WC, Wheeler CM (2014) Concurrence of multiple human papillomavirus infections in a large US population-based cohort. Am J Epidemiol 180:1066–1075. doi:10.1093/aje/kwu267
Goodman A (2015) HPV testing as a screen for cervical cancer. BMJ 350:h2372. doi:10.1136/bmj.h2372
Blatt AJ, Kennedy R, Luff RD et al (2015) Comparison of cervical cancer screening results among 256,648 women in multiple clinical practices. Cancer Cytopathol 123:282–288. doi:10.1002/cncy.21544
Hosaka M, Fujita H, Hanley SJ et al (2012) Incidence risk of cervical intraepithelial neoplasia 3 or more severe lesions is a function of human papillomavirus genotypes and severity of cytological and histological abnormalities in adult Japanese women. Int J Cancer 132:327–334. doi:10.1002/ijc.27680
Cuschieri KS (2005) Persistent high risk HPV infection associated with development of cervical neoplasia in a prospective population study. J Clin Pathol 58:946–950. doi:10.1136/jcp.2004.022863
Chen H-C, Schiffman M, Lin C-Y et al (2011) Persistence of type-specific human papillomavirus infection and increased long-term risk of cervical cancer. J Natl Cancer Inst 103:1387–1396. doi:10.1093/jnci/djr283
Bruni L, Barrionuevo-Rosas L, Albero G, Serrano B, Mena M, Gómez D, Muñoz J, Bosch FX, de Sanjosé S. ICO Information Centre on HPV and Cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in Indonesia. Summary Report 7 October 2016. Accessed 12 Oct 2016
Schellekens MC, Dijkman A, Aziz MF et al (2004) Prevalence of single and multiple HPV types in cervical carcinomas in Jakarta, Indonesia. Gynecol Oncol 93:49–53. doi:10.1016/j.ygyno.2003.12.015
Panigoro R, Susanto H, Novel SS et al (2013) HPV genotyping linear assay test comparison in cervical cancer patients: implications for HPV prevalence and molecular epidemiology in a limited-resource area in Bandung, Indonesia. Asian Pac J Cancer Prev 14:5843–5847. doi:10.7314/APJCP.2013.14.10.5843
Vet JNI, de Boer MA, van den Akker BEWM et al (2008) Prevalence of human papillomavirus in Indonesia: a population-based study in three regions. Br J Cancer 99:214–218. doi:10.1038/sj.bjc.6604417
Wheeler CM, Hunt WC, Cuzick J et al (2012) A population-based study of human papillomavirus genotype prevalence in the United States: baseline measures prior to mass human papillomavirus vaccination. Int J Cancer 132:198–207. doi:10.1002/ijc.27608
Clifford GM, Rana RK, Franceschi S et al (2005) Human papillomavirus genotype distribution in low-grade cervical lesions: comparison by geographic region and with cervical cancer. Cancer Epidemiol Biomark Prev 14:1157–1164. doi:10.1158/1055-9965.EPI-04-0812
Clifford GM, Smith JS, Aguado T, Franceschi S (2003) Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis. Br J Cancer 89:101–105. doi:10.1038/sj.bjc.6601024
Guan P, Howell-Jones R, Li N et al (2012) Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. Int J Cancer 131:2349–2359. doi:10.1002/ijc.27485
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 121:621–632. doi:10.1002/ijc.22527
Bao YP, Li N, Smith JS, Qiao YL (2008) Human papillomavirus type distribution in women from Asia: a meta-analysis. Int J Gynecol Cancer 18:71–79. doi:10.1111/j.1525-1438.2007.00959.x
Liu X-X, Fan X-L, Yu Y-P et al (2014) Human papillomavirus prevalence and type-distribution among women in Zhejiang Province, Southeast China: a cross-sectional study. BMC Infect Dis 14:708. doi:10.1186/s12879-014-0708-8
Wei H, Wang N, Zhang Y et al (2014) Distribution of various types of low-risk human papillomavirus according to cervical cytology and histology in northern Chinese women. Int J Gynaecol Obstet 126:28–32. doi:10.1016/j.ijgo.2014.01.020
Bruni L, Diaz M, Castellsagué X et al (2010) Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis 202:1789–1799. doi:10.1086/657321
Li N, Franceschi S, Howell-Jones R et al (2010) Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. Int J Cancer 128:927–935. doi:10.1002/ijc.25396
Katki HA, Schiffman M, Castle PE et al (2013) Benchmarking CIN3+ risk as the basis for incorporating HPV and Pap cotesting into cervical screening and management guidelines. J Lower Genit Tract Dis 17:S28–S35. doi:10.1097/LGT.0b013e318285423c
Funding was provided to Stem Cell and Cancer Institute by Kalbe Farma (Internal Research Grant). We thanked Sartika Sari, Gunawan, Apryanti Masniary, Lusiana Mutiara, Shirliey Foo, Audi Tri Harsono and Yudhi Nugraha S. Putra for their excellent technical assistance, also Dr. Yong Wee Wong (DNA Laboratories Sdn Bhd, Malaysia) for the technical collaborations.
About this article
Cite this article
Murdiyarso, L.S., Kartawinata, M., Jenie, I. et al. Single and multiple high-risk and low-risk Human Papillomavirus association with cervical lesions of 11,224 women in Jakarta. Cancer Causes Control 27, 1371–1379 (2016). https://doi.org/10.1007/s10552-016-0816-4
- Cervical cancer
- High-risk HPV
- Low-risk HPV