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Distribution of human papillomavirus genotypes in western China and their association with cervical cancer and precancerous lesions

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Abstract

The aim of this study was to describe the distribution of human papillomavirus (HPV) genotypes among cervical cancers and pre-cancers in Shaanxi province of western China. A total of 17,341 women who were screened for cervical cancer from January 2014 to December 2016, using HPV genotyping and ThinPrep cytologic test were included. The prevalence and attribution of HPV genotypes were stratified by cervical lesion and age group. Of the subjects, 26.3% were infected with HPV, 28.0% of whom had multiple infections. The crude HPV prevalence increased from atypical squamous cells of undetermined significance/low-grade squamous intraepithelial lesions (ASCUS/LSIL, 64.3%) to high-grade squamous intraepithelial lesions (HSIL, 79.8%) and to invasive cervical cancer (ICC, 89.7%, P < 0.001). The three most prevalent genotypes were HPV 16 (8.0%), 58 (4.2%), and 52 (4.0%), and HPV 16, 31 and 33 were positively correlated with increased severity of cervical lesions. Additionally, the divalent vaccine genotypes HPV 16 and 18 accounted for 68.2% of ICC cases. Although 78.5% of ICC and 60.3% of HSIL cases were attributed to 9-valent vaccine genotypes, the other genotypes not covered by any vaccine still resulted in increases in coverage, with 1.5% for ICC, 5.3% for HSIL, and 13.5% for ASCUS/LSIL. HPV prevalence in western China was consistent with other regions of China. Early vaccination with 9-valent HPV vaccine is recommended in this locality for females younger than 26 years with no prior infection, while divalent the vaccine is more appropriate for women between 26 and 45 years, considering the efficacy, safety and cost-effectiveness of vaccines.

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Availability of data and material

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

The code used in this study will be made available by the authors, without undue reservation, to any qualified researcher.

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492

    Article  PubMed  Google Scholar 

  2. Guo F, Cofie LE, Berenson AB (2018) Cervical cancer incidence in young U.S. females after human papillomavirus vaccine introduction. Am J Prev Med 55(2):197–204. https://doi.org/10.1016/j.amepre.2018.03.013

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136(5):E359-386. https://doi.org/10.1002/ijc.29210

    Article  CAS  PubMed  Google Scholar 

  4. Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J (2016) Cancer statistics in China, 2015. CA Cancer J Clin 66(2):115–132. https://doi.org/10.3322/caac.21338

    Article  PubMed  Google Scholar 

  5. Pierce Campbell CM, Menezes LJ, Paskett ED, Giuliano AR (2012) Prevention of invasive cervical cancer in the United States: past, present, and future. Cancer Epidemiol Biomark Prev 21(9):1402–1408. https://doi.org/10.1158/1055-9965.EPI-11-1158

    Article  Google Scholar 

  6. Zeng Z, Yang H, Li Z, He X, Griffith CC, Chen X, Guo X, Zheng B, Wu S, Zhao C (2016) Prevalence and genotype distribution of HPV infection in China: analysis of 51,345 HPV genotyping results from China’s largest CAP Certified Laboratory. J Cancer 7(9):1037–1043. https://doi.org/10.7150/jca.14971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ, International Agency for Research on Cancer Multicenter Cervical Cancer Study G (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348(6):518–527. https://doi.org/10.1056/NEJMoa021641

    Article  PubMed  Google Scholar 

  8. zur Hausen H (2000) Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. J Natl Cancer Inst 92(9):690–698. https://doi.org/10.1093/jnci/92.9.690

    Article  CAS  PubMed  Google Scholar 

  9. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H (2004) Classification of papillomaviruses. Virology 324(1):17–27. https://doi.org/10.1016/j.virol.2004.03.033

    Article  CAS  PubMed  Google Scholar 

  10. de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, Vallejos CS, de Ruiz PA, Lima MA, Guimera N, Clavero O, Alejo M, Llombart-Bosch A, Cheng-Yang C, Tatti SA, Kasamatsu E, Iljazovic E, Odida M, Prado R, Seoud M, Grce M, Usubutun A, Jain A, Suarez GA, Lombardi LE, Banjo A, Menendez C, Domingo EJ, Velasco J, Nessa A, Chichareon SC, Qiao YL, Lerma E, Garland SM, Sasagawa T, Ferrera A, Hammouda D, Mariani L, Pelayo A, Steiner I, Oliva E, Meijer CJ, Al-Jassar WF, Cruz E, Wright TC, Puras A, Llave CL, Tzardi M, Agorastos T, Garcia-Barriola V, Clavel C, Ordi J, Andujar M, Castellsague X, Sanchez GI, Nowakowski AM, Bornstein J, Munoz N, Bosch FX, Retrospective International S, Group HPVTTS (2010) Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 11(11):1048–1056. https://doi.org/10.1016/S1470-2045(10)70230-8

    Article  CAS  PubMed  Google Scholar 

  11. Kavanagh K, Pollock KG, Cuschieri K, Palmer T, Cameron RL, Watt C, Bhatia R, Moore C, Cubie H, Cruickshank M, Robertson C (2017) Changes in the prevalence of human papillomavirus following a national bivalent human papillomavirus vaccination programme in Scotland: a 7-year cross-sectional study. Lancet Infect Dis 17(12):1293–1302. https://doi.org/10.1016/S1473-3099(17)30468-1

    Article  PubMed  Google Scholar 

  12. Castanon A, Landy R, Pesola F, Windridge P, Sasieni P (2018) Prediction of cervical cancer incidence in England, UK, up to 2040, under four scenarios: a modelling study. Lancet Public Health 3(1):e34–e43. https://doi.org/10.1016/S2468-2667(17)30222-0

    Article  PubMed  Google Scholar 

  13. Zhu C, Wang Y, Mao W, Zhang H, Ma J (2019) Prevalence and distribution of HPV types in genital warts in Xi’an, China: a prospective study. BMJ Open 9(5):e023897. https://doi.org/10.1136/bmjopen-2018-023897

    Article  PubMed  PubMed Central  Google Scholar 

  14. Low HC, Silver MI, Brown BJ, Leng CY, Blas MM, Gravitt PE, Woo YL (2015) Comparison of Hybribio GenoArray and Roche human papillomavirus (HPV) linear array for HPV genotyping in anal swab samples. J Clin Microbiol 53(2):550–556. https://doi.org/10.1128/JCM.02274-14

    Article  PubMed  PubMed Central  Google Scholar 

  15. Nayar R, Wilbur DC (2015) The Pap test and Bethesda 2014. Cancer Cytopathol 123(5):271–281. https://doi.org/10.1002/cncy.21521

    Article  PubMed  Google Scholar 

  16. Insinga RP, Liaw KL, Johnson LG, Madeleine MM (2008) A systematic review of the prevalence and attribution of human papillomavirus types among cervical, vaginal, and vulvar precancers and cancers in the United States. Cancer Epidemiol Biomark Prev 17(7):1611–1622. https://doi.org/10.1158/1055-9965.EPI-07-2922

    Article  CAS  Google Scholar 

  17. Newcombe RG (1998) Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 17(8):857–872. https://doi.org/10.1002/(sici)1097-0258(19980430)17:8%3c857::aid-sim777%3e3.0.co;2-e

    Article  CAS  PubMed  Google Scholar 

  18. Xu HH, Wang K, Feng XJ, Dong SS, Lin A, Zheng LZ, Yan WH (2018) Prevalence of human papillomavirus genotypes and relative risk of cervical cancer in China: a systematic review and meta-analysis. Oncotarget 9(20):15386–15397. https://doi.org/10.18632/oncotarget.24169

    Article  PubMed  PubMed Central  Google Scholar 

  19. Xu HH, Lin A, Chen YH, Dong SS, Shi WW, Yu JZ, Yan WH (2017) Prevalence characteristics of cervical human papillomavirus (HPV) genotypes in the Taizhou area, China: a cross-sectional study of 37 967 women from the general population. BMJ Open 7(6):e014135. https://doi.org/10.1136/bmjopen-2016-014135

    Article  PubMed  PubMed Central  Google Scholar 

  20. Yao L, Yuan M, Yuan J, Zhou P, Mei L, Cheng J (2018) Analysis of cervical human papillomavirus infection in 2300 women in Urumqi, China. Medicine (Baltimore) 97(45):e13206. https://doi.org/10.1097/MD.0000000000013206

    Article  Google Scholar 

  21. Zhang L, Bi Q, Deng H, Xu J, Chen J, Zhang M, Mu X (2017) Human papillomavirus infections among women with cervical lesions and cervical cancer in Eastern China: genotype-specific prevalence and attribution. Bmc Infect Dis 17(1):107. https://doi.org/10.1186/s12879-017-2223-1

    Article  PubMed  PubMed Central  Google Scholar 

  22. Li M, Du X, Lu M, Zhang W, Sun Z, Li L, Ye M, Fan W, Jiang S, Liu A, Wang M, Meng Y, Li Y (2019) Prevalence characteristics of single and multiple HPV infections in women with cervical cancer and precancerous lesions in Beijing. China. J Med Virol 91(3):473–481. https://doi.org/10.1002/jmv.25331

    Article  CAS  PubMed  Google Scholar 

  23. Kjaer SK, Munk C, Junge J, Iftner T (2014) Carcinogenic HPV prevalence and age-specific type distribution in 40,382 women with normal cervical cytology, ASCUS/LSIL, HSIL, or cervical cancer: what is the potential for prevention? Cancer Causes Control 25(2):179–189. https://doi.org/10.1007/s10552-013-0320-z

    Article  PubMed  Google Scholar 

  24. Smelov V, Elfstrom KM, Johansson AL, Eklund C, Naucler P, Arnheim-Dahlstrom L, Dillner J (2015) Long-term HPV type-specific risks of high-grade cervical intraepithelial lesions: a 14-year follow-up of a randomized primary HPV screening trial. Int J Cancer 136(5):1171–1180. https://doi.org/10.1002/ijc.29085

    Article  CAS  PubMed  Google Scholar 

  25. 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(1):101–105. https://doi.org/10.1038/sj.bjc.6601024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cuschieri K, Ronco G, Lorincz A, Smith L, Ogilvie G, Mirabello L, Carozzi F, Cubie H, Wentzensen N, Snijders P, Arbyn M, Monsonego J, Franceschi S (2018) Eurogin roadmap 2017: Triage strategies for the management of HPV-positive women in cervical screening programs. Int J Cancer 143(4):735–745. https://doi.org/10.1002/ijc.31261

    Article  CAS  PubMed  Google Scholar 

  27. Castellsague X (2008) Natural history and epidemiology of HPV infection and cervical cancer. Gynecol Oncol 110(3 Suppl 2):S4-7. https://doi.org/10.1016/j.ygyno.2008.07.045

    Article  PubMed  Google Scholar 

  28. Woodman CB, Collins SI, Young LS (2007) The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer 7(1):11–22. https://doi.org/10.1038/nrc2050

    Article  CAS  PubMed  Google Scholar 

  29. Greer CE, Wheeler CM, Ladner MB, Beutner K, Coyne MY, Liang H, Langenberg A, Yen TS, Ralston R (1995) Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus-like particles in patients with genital warts. J Clin Microbiol 33(8):2058–2063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Serrano B, Alemany L, Tous S, Bruni L, Clifford GM, Weiss T, Bosch FX, de Sanjose S (2012) Potential impact of a nine-valent vaccine in human papillomavirus related cervical disease. Infect Agent Cancer 7(1):38. https://doi.org/10.1186/1750-9378-7-38

    Article  PubMed  PubMed Central  Google Scholar 

  31. Li X, Zheng R, Li X, Shan H, Wu Q, Wang Y, Chen W (2017) Trends of incidence rate and age at diagnosis for cervical cancer in China, from 2000 to 2014. Chin J Cancer Res 29(6):477–486. https://doi.org/10.21147/j.issn.1000-9604.2017.06.02

    Article  PubMed  PubMed Central  Google Scholar 

  32. Martinez-Lavin M (2019) HPV vaccine: adverse event signals were minimised or ignored. BMJ 366:l4508. https://doi.org/10.1136/bmj.l4508

    Article  PubMed  Google Scholar 

  33. Martinez-Lavin M, Amezcua-Guerra L (2017) Serious adverse events after HPV vaccination: a critical review of randomized trials and post-marketing case series. Clin Rheumatol 36(10):2169–2178. https://doi.org/10.1007/s10067-017-3768-5

    Article  PubMed  Google Scholar 

  34. Laprise JF, Chesson HW, Markowitz LE, Drolet M, Martin D, Benard E, Brisson M (2020) Effectiveness and cost-effectiveness of human papillomavirus vaccination through age 45 years in the United States. Ann Intern Med 172(1):22–29. https://doi.org/10.7326/M19-1182

    Article  PubMed  Google Scholar 

  35. Wright TC Jr, Huh WK, Monk BJ, Smith JS, Ault K, Herzog TJ (2008) Age considerations when vaccinating against HPV. Gynecol Oncol 109(2 Suppl):S40-47. https://doi.org/10.1016/j.ygyno.2008.02.002

    Article  PubMed  Google Scholar 

  36. Burger EA, Kim JJ, Sy S, Castle PE (2017) Age of acquiring causal human papillomavirus (HPV) infections: leveraging simulation models to explore the natural history of HPV-induced cervical cancer. Clin Infect Dis 65(6):893–899. https://doi.org/10.1093/cid/cix475

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by the Clinical Research Award of First Affiliated Hospital of Xi’an Jiaotong University, China [XJTU1AF-CRF-2015-009, XJTU1AF-CRF-2016-011].

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Authors and Affiliations

Authors

Contributions

Jiao Li: conceptualization, methodology, investigation, data curation, writing – reviewing and editing, project administration, funding acquisition. Juan-Juan Gao: conceptualization, methodology, formal analysis, data curation, writing – original draft, writing – reviewing and editing. Na Li: methodology, investigation, data curation. Ya-Wen Wang: conceptualization, methodology, writing – reviewing and editing, supervision, funding acquisition

Corresponding author

Correspondence to Ya-Wen Wang.

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The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This study was approved by the Institutional Review Board of the First Affiliated Hospital of Xi’an Jiaotong University (XJTU1AF2016LSL-043).

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Not applicable in this research, which is based on retrospective data.

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Handling Editor: Carolina Scagnolari.

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Li, J., Gao, JJ., Li, N. et al. Distribution of human papillomavirus genotypes in western China and their association with cervical cancer and precancerous lesions. Arch Virol 166, 853–862 (2021). https://doi.org/10.1007/s00705-021-04960-z

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  • DOI: https://doi.org/10.1007/s00705-021-04960-z

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