2,222
Views
19
CrossRef citations to date
0
Altmetric
Review

Current issues facing the introduction of human papillomavirus vaccine in China and future prospects

ORCID Icon, , , , & ORCID Icon
Pages 1533-1540 | Received 21 Nov 2018, Accepted 17 Apr 2019, Published online: 16 Jul 2019

References

  • Gallagher KE, LaMontagne DS, Watson-Jones D. Status of HPV vaccine introduction and barriers to country uptake. Vaccine. 2018;36(32):4761–67. doi:10.1016/j.vaccine.2018.02.003.
  • Wang T, Wu M-H, Wu Y-M, Zhang W-Y. A population-based study of invasive cervical cancer patients in Beijing: 1993–2008. Chin Med J. 2015;128(24):3298–304. doi:10.4103/0366-6999.171420.
  • ICO/IARC Information Centre on HPV and Cancer. China Human Papillomavirus and Related Cancers, Fact Sheet 2017 July 27 [accessed 2014 8 Oct 21]. http://www.hpvcentre.net/statistics/reports/CHN_FS.pdf
  • Song B, Ding C, Chen W, Sun H, Zhang M. Incidence and mortality of cervical cancer in China, 2013. Chinese Journal Cancer Research. 2017;29(6):471–76. doi:10.21147/j.issn.1000-9604.2017.06.01.
  • Zhao FH, Lewkowitz AK, Hu SY, Chen F, Li LY, Zhang QM, Wu RF, Li CQ, Wei LH, Xu AD, et al. Prevalence of human papillomavirus and cervical intraepithelial neoplasia in China: A pooled analysis of 17 population‐based studies. International Journal of Cancer. 2012;131(12):2929–38. doi:10.1002/ijc.27571.
  • Drolet M, É B, Boily MC, Ali H, Baandrup L, Bauer H, Beddows S, Brisson J, Brotherton JM, Cummings T, et al. Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis. 2015;15(5):565–80. doi:10.1016/S1473-3099(14)71073-4.
  • Lehtinen M, Lagheden C, Luostarinen T, Eriksson T, Apter D, Harjula K, Kuortti M, Natunen K, Palmroth J, Petäjä T et al. Ten-year follow-up of human papillomavirus vaccine efficacy against the most stringent cervical neoplasia end-point-registry-based follow-up of three cohorts from randomized trials. BMJ Open. 2017 Aug 18;7(8):e015867. doi:10.1136/bmjopen-2017-015867.
  • Kjaer SK, Nygard M, Dillner J, Marshall JB, Radley D, Li M, Munk C, Hansen BT, Sigurdardottir LG, Hortlund M, et al. A 12-year follow up on the long-term effectiveness of the quadrivalent human papillomavirus vaccine in 4 Nordic countries. Clinical Infectious Diseases. 2018;66(3):339–45. doi:10.1093/cid/cix797.
  • Wei L, Xie X, Liu J, Zhao Y, Chen W, Zhao C, Wang S, Liao X, Shou Q, Qiu Y, et al. Efficacy of quadrivalent human papillomavirus vaccine against persistent infection and genital disease in Chinese women: A randomized, placebo-controlled trial with 78-month follow-up. Vaccine. 2018;S0264-410X(18):31116–2. doi:10.1016/j.vaccine.2018.08.009).
  • Ferris DG, Samakoses R, Block SL, Lazcano-Ponce E, Restrepo JA, Mehlsen J, Chatterjee A, Iversen OE, Joshi A, Chu JL, et al. 4-Valent Human Papillomavirus (4vHPV) Vaccine in Preadolescents and Adolescents After 10 Years. Pediatrics. 2017;140(6):e20163947. doi:10.1542/peds.2017-0685.
  • Arbyn M, Xu L, Simoens C, Martin‐Hirsch PP. Prophylactic vaccination against human papillomaviruses to prevent cervical cancer and its precursors. Cochrane Database of Systematic Reviews. 2018;(5):CD009069.
  • Palmer T, Wallace L, Pollock KG, Cuschieri K, Robertson C, Kavanagh K, Cruickshank M. Prevalence of cervical disease at age 20 after immunisation with bivalent HPV vaccine at age 12-13 in Scotland: retrospective population study. bmj. 2019 Apr;3(365):l1161. doi:10.1136/bmj.l1161.
  • Scavone C, Di Mauro C, Brusco S, Bertini M, Di Mauro G, Rafaniello C, Sportiello L, Rossi F, Capuano A. Surveillance of adverse events following immunization related to human papillomavirus vaccines: 12 years of vaccinovigilance in Southern Italy. Expert Opin Drug Saf. 2019. doi:10.1080/14740338.2019.1598969.
  • Kane MA, Sherris J, Coursaget P, Aguado T, Cutts F. HPV vaccine use in the developing world. Vaccine. 2006;24:S132–9. doi:10.1016/j.vaccine.2006.05.128.
  • Yin Y. HPV vaccination in China needs to be more cost-effective. The Lancet. 2017;390(10104):1735–36. doi:10.1016/S0140-6736(17)32606-5.
  • Levin CE, Sharma M, Olson Z, Verguet S, Shi J-F, Wang S-M, Qiao Y-L, Jamison DT, Kim JJ. An extended cost-effectiveness analysis of publicly financed HPV vaccination to prevent cervical cancer in China. Vaccine. 2015;33(24):2830–41. doi:10.1016/j.vaccine.2015.02.052.
  • Li S, Hu T, Lv W, Zhou H, Li X, Yang R, Jia Y, Huang K, Chen Z, Wang S, et al. Changes in prevalence and clinical characteristics of cervical cancer in the People‘s Republic of China: a study of 10,012 cases from a nationwide working group. Oncologist. 2013;18(10):1101–07. doi:10.1634/theoncologist.2013-0123.
  • Times G. HPV vaccine market burst. 2018 March 19. [accessed 2018 Nov] http://www.globaltimes.cn/content/1094044.shtml
  • Times F. Chinese medical tourism exacerbates shortage of HPV vaccine. 2018. June 15 [accessed 2018 Nov] https://www.ft.com/content/d92ac2c2-6e1e-11e8-92d3-6c13e5c92914
  • Zhao F, Qiao Y. Cervical cancer prevention in China: a key to cancer control. The Lancet. 2019;393(10175):969–70. doi:10.1016/S0140-6736(18)32849-6.
  • Qiu J, Hu H, Zhou S, Liu Q. Vaccine scandal and crisis in public confidence in China. The Lancet. 2016;387(10036):2382. doi:10.1016/S0140-6736(16)30737-1.
  • The Lancet. Vaccine scandal and confidence crisis in China. Lancet (London, England). 2018;392(10145):360. doi:10.1016/S0140-6736(18)31695-7.
  • Dell DL, Chen H, Ahmad F, Stewart DE. Knowledge about human papillomavirus among adolescents. Obstetrics & Gynecology. 2000;96:653–56.
  • Sharpe PA, Brandt HM, McCree DH. Knowledge and beliefs about abnormal pap test results and HPV among women with high-risk HPV: results from in-depth interview. Women Health. 2005;42:107–33.
  • Wong LP. Young multiethnic women‘s attitudes toward the HPV vaccine and HPV vaccination. Int J Gynecology Obstetrics. 2008;103(2):1315. doi:10.1016/j.ijgo.2008.07.005.
  • Walsh CD, Gera A, Shah M, Sharma A, Powell JE, Wilson S. Public knowledge and attitudes towards Human Papilloma Virus (HPV) vaccination. BMC Public Health. 2008;8:368. doi:10.1186/1471-2458-8-368.
  • Cartmell KB, Young-Pierce J, McGue S, Alberg AJ, Luque JS, Zubizarreta M, Brandt HM. Barriers, facilitators, and potential strategies for increasing HPV vaccination: A statewide assessment to inform action. Papillomavirus Research. 2018;5:21–31. doi:10.1016/j.pvr.2017.11.003.
  • Coles VA, Patel AS, Allen FL, Keeping ST, Carroll SM. The association of human papillomavirus vaccination with sexual behaviours and human papillomavirus knowledge: a systematic review. Int J STD AIDS. 2015;26(11):777–88. doi:10.1177/0956462414554629.
  • Zhuang QY, Wong RX, Chen WM, Guo XX. Knowledge, attitudes and practices regarding human papillomavirus vaccination among young women attending a tertiary institution in Singapore. Singapore Med J. 2016 Jun;57(6):329. doi:10.11622/smedj.2016108.
  • Zhao M, Qu S, Zhao L, Campy KS, Wang S. Parental perceptions of human papillomavirus vaccination in Central China: the Moderating Role of Socioeconomic Factors. Human Vaccines & Immunotherapeutics. 2018;1–9: doi: 10.1080/21645515.2018.1547605.
  • He J, He L. Knowledge of HPV and acceptability of HPV vaccine among women in western China: a cross-sectional survey. BMC Women‘S Health. 2018;18(1):130. doi:10.1186/s12905-018-0619-8.
  • Yuanyue L, Baloch Z, Shanshan L, Yasmeen N, Xiaomei W, Khan JM, Cervical Cancer XX, Infection HP. Vaccine-Related Knowledge: awareness in Chinese Women. Cancer Control. 2018;25(1):1073274818799306. doi:10.1177/1073274818799306.
  • Baloch Z, Yasmeen N, Li Y, Zhang W, Lu H, Wu X, Xia X, Yang S. Knowledge and awareness of cervical cancer, human papillomavirus (HPV), and HPV vaccine among HPV-infected chinese women. Med Sci Monit. 2017;23:4269–77. PMID: 28867818.
  • Restivo V, Costantino C, Fazio TF, Casuccio N, D’Angelo C, Vitale F, Casuccio A. Factors Associated with HPV Vaccine Refusal among Young Adult Women after Ten Years of Vaccine Implementation. Int J Environ Res Public Health. 2018;15(4):770. doi:10.3390/ijerph15061188.
  • Wong LP. Knowledge of and attitudes toward the HPV vaccine among multi‐ethnic women from urban/university and rural areas. Int J Gynecology Obstetrics. 2011;112(2):146–47. doi:10.1016/j.ijgo.2010.09.006.
  • Daley EM, Vamos CA, Zimet GD, Rosberger Z, Thompson EL, Merrell L. The feminization of HPV: reversing gender biases in US human papillomavirus vaccine policy. Am J Public Health. 2016;106:983–84. doi:10.2105/AJPH.2016.303122.
  • Wigle J, Coast E, Watson-Jones D. Human papillomavirus (HPV) vaccine implementation in low and middle-income countries (LMICs): health system experiences and prospects. Vaccine. 2013;31(37):3811–17. doi:10.1016/j.vaccine.2013.06.016.
  • Abliz G, Zh L P, Liu SL. Detection of human papillomavirus DNA in cervical cancer tissues from Xinjiang Hotan Uyghur women. Sichuan J Cancer Control. 2001;14:77–81.
  • Li HQ, Jin SQ, Xu HX, Thomas DB. The decline in the mortality rates of cervical cancer and a plausible explanation in Shandong, China. Int J Epidemiol. 2000;29:398–404.
  • Hussain S, Bharadwaj M, Nasare V, Kumari M, Sharma S, Hedau S, Das BC. Human papillomavirus infection among young adolescents in India: impact of vaccination. J Med Virol. 2012;84(2):298–305. doi:10.1002/jmv.22261.
  • Toh ZQ, Licciardi PV, Russell FM, Garland SM, Batmunkh T, Mulholland EK. Cervical cancer prevention through HPV vaccination in low-and middle-income countries in Asia. Asian Pacific Journal of Cancer Prevention: APJCP. 2017;18(9):2339. doi:10.22034/APJCP.2017.18.1.23.
  • LaMontagne DS, Barge S, Le N T, Mugisha E, Penny ME, Gandhi S, Janmohamed A, Kumakech E, Mosqueira NR, Nguyen NQ, et al. Human papillomavirus vaccine delivery strategies that achieved high coverage in low-and middle-income countries. Bull World Health Organ. 2011;89:821–30. doi:10.2471/BLT.11.089862.
  • Kasting ML, Shapiro GK, Rosberger Z, Kahn JA, Zimet GD. Tempest in a teapot: A systematic review of HPV vaccination and risk compensation research. Hum Vaccin Immunother. 2016;12(6):1435–50. doi:10.1080/21645515.2016.1141158.
  • Aranda S, Berkley S, Cowal S, Dybul M, Evans T, Iversen K, Moeti M, Osotimehin B, Peterson S, Piot P, et al. Ending cervical cancer: A call to action. Int J Gynecology Obstetrics. 2017;138:4–6. doi:10.1002/ijgo.12182.
  • Colombara DV, Wang S-M. The impact of HPV vaccination delays in China: lessons from HBV control programs. Vaccine. 2013;31(38):4057–59. doi:10.1016/j.vaccine.2013.06.031.
  • Raffle AE. Challenges of implementing human papillomavirus (HPV) vaccination policy. BMJ : British Medical Journal. 2007;335(7616):375–77. doi:10.1136/bmj.39273.458322.BE.
  • Canfell K, Shi JF, Lew JB, Walker R, Zhao FH, Simonella L, Chen JF, Legood R, Smith MA, Nickson C, et al. Prevention of cervical cancer in rural China: evaluation of HPV vaccination and primary HPV screening strategies. Vaccine. 2011;29(13):2487–94. doi:10.1016/j.vaccine.2010.12.085.
  • Baeten S, Van Ourti T, Van Doorslaer E. Rising inequalities in income and health in China: who is left behind?. J Health Econ. 2013;32(6):1214–29. doi:10.1016/j.jhealeco.2013.10.002.
  • Zou X, Chow EP, Zhao P, Xu Y, Ling L, Zhang L. Rural-to-urban migrants are at high risk of sexually transmitted and viral hepatitis infections in China: a systematic review and meta-analysis. BMC Infect Dis. 2014;14(1):490. doi:10.1186/1471-2334-14-490.
  • Wu RF, Dai M, Qiao YL, Clifford GM, Liu ZH, Arslan A, Li N, Shi JF, Snijders PJ, Meijer CJ, et al. Human papillomavirus infection in women in Shenzhen City, People‘s Republic of China, a population typical of recent Chinese urbanisation. International Journal of Cancer. 2007;121(6):1306–11. doi:10.1002/ijc.22726.
  • Li C, Wu M, Wang J, Zhang S, Zhu L, Pan J, Zhang WN. A population-based study on the risks of cervical lesion and human papillomavirus infection among women in Beijing, People‘s Republic of China. Cancer Epidemiology and Prevention Biomarkers. 2010;19(10):2655–64.
  • Luxembourg A, Bautista O, Moeller E, Ritter M, Chen J. Design of a large outcome trial for a multivalent human papillomavirus L1 virus-like particle vaccine. Contemp Clin Trials. 2015;42:18–25. doi:10.1016/j.cct.2015.02.009.
  • de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, et al. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 2010;11(11):1048–56. doi:10.1016/S1470-2045(10)70230-8.
  • Mennini FS, Bonanni P, Bianic F, de Waure C, Baio G, Plazzotta G, Uhart M, Rinaldi A, Largeron N. Cost-effectiveness analysis of the nine-valent HPV vaccine in Italy. Cost Eff Resour Alloc. 2017;15:11. eCollection 2017. doi:10.1186/s12962-017-0073-8.
  • Brisson M, Laprise JF, Chesson HW, Drolet M, Malagón T, Boily MC, Markowitz LE. Health and Economic Impact of Switching from a 4-Valent to a 9-Valent HPV Vaccination Program in the United States. J Natl Cancer Inst. 2015;108:1.
  • China Daily. HPV 9-valent vaccine available in Hainan. 2018 May 30 [accessed 2018 Nov] http://www.chinadaily.com.cn/a/201805/30/WS5b0e907ba31001b82571d388.html
  • Serrano B, Alemany L, de Ruiz PA, Tous S, Lima MA, Bruni L, Jain A, Clifford GM, Qiao YL, Weiss T, et al. Potential impact of a 9-valent HPV vaccine in HPV-related cervical disease in 4 emerging countries (Brazil, Mexico, India and China). Cancer Epidemiol. 2014;38(6):748–56. doi:10.1016/j.canep.2014.09.003.
  • Lo KW, Wong YF, Chan MK, Li JC, Poon JS, Wang VW, Zhu SN, Zhang TM, He ZG, Wu QL, et al. Prevalence of human papillomavirus in cervical cancer: a multicenter study in China. International Journal of Cancer. 2002;100(3):327–31. doi:10.1002/ijc.10506.
  • Chen W, Zhang X, Molijn A, Jenkins D, Shi JF, Quint W, Schmidt JE, Wang P, Liu YL, Li LK, et al. Human papillomavirus type-distribution in cervical cancer in China: the importance of HPV 16 and 18. Cancer Causes & Control. 2009;20(9):1705–13. doi:10.1007/s10552-009-9422-z.
  • Singh S, Zhou Q, Yu Y, Xu X, Huang X, Zhao J, Han L, Wang K, Sun J, Li F. Distribution of HPV genotypes in Shanghai women. Int J Clin Exp Pathol. 2015;8:11901–08.
  • Xu HH, Wang K, Feng XJ, Dong SS, Lin A, Zheng LZ, Yan WH. Prevalence of human papillomavirus genotypes and relative risk of cervical cancer in China: a systematic review and meta-analysis. Oncotarget. 2018;9(20):15386–97. doi:10.18632/oncotarget.24169.
  • Dobson SR, McNeil S, Dionne M, Dawar M, Ogilvie G, Krajden M, Sauvageau C, Scheifele DW, Kollmann TR, Halperin SA, et al. Immunogenicity of 2 doses of HPV vaccine in younger adolescents vs 3 doses in young women: a randomized clinical trial. JAMA. 2013;309(17):1793–802. doi:10.1001/jama.2013.1625).
  • World Health Organization. Meeting of the strategic advisory group of experts on immunization, April 2014 – conclusions and recommendations. Wkly Epidemiol Rec 2014;89:221–36.
  • Bhatla N, Nene BM, Joshi S, Esmy PO, Poli UR, Joshi G, Verma Y, Zomawia E, Pimple S, Prabhu PR, et al. Are two doses of human papillomavirus vaccine sufficient for girls aged 15–18 years? Results from a cohort study in India. Papillomavirus Research. 2018;5:163–71. doi:10.1016/j.pvr.2018.03.008.
  • Sankaranarayanan R, Prabhu PR, Pawlita M, Gheit T, Bhatla N, Muwonge R, Nene BM, Esmy PO, Joshi S, Poli UR, 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. doi:10.1016/S1470-2045(15)00414-3.
  • Kreimer AR, Rodriguez AC, Hildesheim A, Herrero R, Porras C, Schiffman M, González P, Solomon D, Jiménez S, Schiller JT, et al. Proof-of-principle evaluation of the efficacy of fewer than three doses of a bivalent HPV16/18 vaccine. J Natl Cancer Inst. 2011;103(19):1444–51. doi:10.1093/jnci/djr319.
  • Basu P, Bhatla N, Ngoma T, Sankaranarayanan R. Less than 3 doses of the HPV vaccine - Review of efficacy against virological and disease end points. Hum Vaccines Immunother 24. 2016;12(6):1394–402. doi:10.1080/21645515.2016.1146429.
  • Safaeian M, Sampson JN, Pan Y, Porras C, Kemp TJ, Herrero R, Quint W, van Doorn LJ, Schussler J, Lowy DR, et al. Durability of protection afforded by fewer doses of the HPV16/18 vaccine: the CVT trial. JNCI: Journal of the National Cancer Institute. 2018;110(2). doi:10.1093/jnci/djx158
  • Sankaranarayanan R, Joshi S, Muwonge R, Esmy PO, Basu P, Prabhu P, Bhatla N, Nene BM, Shaw J, Poli URR, et al. Indian HPV vaccine study group. Can a single dose of human papillomavirus (HPV) vaccine prevent cervical cancer? Early findings from an Indian study. Vaccine. 2018;36(32Pt A):4783–91. doi:10.1016/j.vaccine.2018.02.087.
  • Kreimer AR, Herrero R, Sampson JN, Porras C, Lowy DR, Schiller JT, Schiffman M, Rodriguez AC, Chanock S, Jimenez S, et al. Evidence of single-dose protection by the bivalent HPV vaccine-Review of the Costa Rica HPV vaccine trial and future research studies. Vaccine. 2018;36:4774–82. doi:10.1016/j.vaccine.2017.12.078.
  • Brotherton JM, Malloy M, Budd AC, Saville M, Drennan KT, Gertig DM. Effectiveness of less than three doses of quadrivalent human papillomavirus vaccine against cervical intraepithelial neoplasia when administered using a standard doses pacing schedule: observational cohort of young women in Australia. Papillomavirus Res. 2015;1:59–73. doi:10.1016/j.pvr.2015.05.005.
  • Hariri S, Bennett NM, Niccolai LM, Schafer S, Park IU, Bloch KC, Unger ER, Whitney E, Julian P, Scahill MW, et al. Reduction in HPV 16/18- associated high grade cervical lesions following HPV vaccine introduction in the United States - 2008-2012. Vaccine. 2015;33(13):1608–13. doi:10.1016/j.vaccine.2015.01.084.
  • Crowe E, Pandeya N, Brotherton JM, Dobson AJ, Kisely S, Lambert SB, Whiteman DC. Effectiveness of quadrivalent human papillomavirus vaccine for the prevention of cervical abnormalities: case-control study nested within a population based screening programme in Australia. BMJ. 2014:348. doi:10.1136/bmj.g1458.
  • Herweijer E, Leval A, Ploner A, Eloranta S, Simard JF, Dillner J, Netterlid E, Sparén P, Arnheim-Dahlström L. Association of varying number of doses of quadrivalent human papillomavirus vaccine with incidence of condyloma. JAMA. 2014;311(6):597–603. doi:10.1001/jama.2014.95.
  • Lamb F, Herweijer E, Ploner A, Uhnoo I, Sundström K, Sparén P, Arnheim-Dahlström L. Timing of two versus three doses of quadrivalent HPV vaccine and associated effectiveness against condyloma in Sweden: a nationwide cohort study. BMJ Open. 2017;7(6):e015021. doi:10.1136/bmjopen-2016-015021.
  • Markowitz LE, Drolet M, Perez N, Jit M, Brisson M. Human papillomavirus vaccine effectiveness by number of doses: systematic review of data from national immunization programs. Vaccine. 2018;36(32 Pt A):4806–15. doi:10.1016/j.vaccine.2018.01.057.
  • Hanson CM, Eckert L, Bloem P, Cernuschi T. Gavi HPV Programs: application to Implementation. Vaccines (Basel). 2015;3(2):408–19. doi:10.3390/vaccines3020408.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.