Evaluation of the immune response to human papillomavirus types 16, 18, 31, 45 and 58 in a group of Colombian women vaccinated with the quadrivalent vaccine

Authors

  • Alba Cómbita Instituto Nacional de Cancerología (INC)
  • Diego Duarte Instituto Nacional de Cancerología (INC)
  • Josefa Rodríguez Instituto Nacional de Cancerología (INC)
  • Mónica Molano Instituto Nacional de Cancerología (INC)
  • Lina Martínez Instituto Nacional de Cancerología (INC)
  • Pilar Romero Instituto Nacional de Cancerología (INC)
  • Lina Trujillo Instituto Nacional de Cancerología
  • Mauricio González Instituto Nacional de Cancerología
  • Joaquín Luna Instituto Nacional de Cancerología
  • Natascha Ortiz Instituto Nacional de Cancerología
  • Gustavo Hernández Instituto Nacional de Cancerología
  • Pierre Coursaget Université François-Rabelais
  • Antoine Touzé Université François-Rabelais

Keywords:

Papillomavirus Vaccines, Immunity, Seroprevalence

Abstract

Objective: To analyze whether the immune response to HPV-16, -18, -31, -45 and -58 capsids in women vaccinated with the quadrivalent vaccine induces cross-reactivity against other HPV virus-like particles (VLPs).
Methods: A total of 88 women aged between 18 and 27 years attending the HPV clinic at the Instituto Nacional de Cancerología were enrolled and vaccinated against HPV. Follow-up visits were scheduled at months 7, 12, and 24. Samples were collected for cytology, HPV-DNA typing,and detection of HPV antibodies. IgG antibodies were measured by ELISA using HPV-16, -18, -31,-45, and -58 VLPs. HPV-DNA detection was done by GP5+/GP6+PCR-ELISA and HPV typing was performed by Reverse Line-Blot assay.
Results: Pre-vaccination, the seroprevalence of HPV-16, -18, -31, -45, and -58 was 39%, 31.7%, 15.9%, 31.7%, and 23.2%, respectively. One month post-vaccination, the seroprevalence increased close to 100% for all types. At month 24, this response was maintained only for HPV-16 and -18. For HPV-31, -45 and -58, the seroprevalence decreased to below 50%. The prevalence of HPV DNA types 16, 18 and 58 before vaccination was little changed 1 month after vaccination. No new infections were observed at 24 months. For HPV-16 and -18 related types, no differences were observed before vaccination and at month 24. For other high-risk HPV types, the prevalence increased 18 months post-vaccination (15.5%) compared with pre-vaccination (9.8%).
Conclusion: Immune response to all HPV types increased after vaccination, but this increase was maintained only for HPV-16 and -18. These results suggest a possible cross-reactivity against HPV types 31, 45 and 58, but this cross-reactivity wanes with time

Author Biographies

Alba Cómbita, Instituto Nacional de Cancerología (INC)

Grupo de Investigación en Biología del Cáncer, Instituto Nacional de Cancerología (INC), Bogotá, D. C., Colombia
Departamento de Microbiología, Facultad de Medicina, Universidad Nacional de Colombia, Bogotá, D. C., Colombia

Diego Duarte, Instituto Nacional de Cancerología (INC)

Grupo de Investigación en Biología del Cáncer, Instituto Nacional de Cancerología (INC), Bogotá, D. C., Colombia

Josefa Rodríguez, Instituto Nacional de Cancerología (INC)

Grupo de Investigación en Biología del Cáncer, Instituto Nacional de Cancerología (INC), Bogotá, D. C., Colombia
Unidad de Inmunología, Facultad de Medicina, Universidad del Rosario, Bogotá, D. C., Colombia

Mónica Molano, Instituto Nacional de Cancerología (INC)

Grupo de Investigación en Biología del Cáncer, Instituto Nacional de Cancerología (INC), Bogotá, D. C., Colombia

Lina Martínez, Instituto Nacional de Cancerología (INC)

Grupo de Investigación en Biología del Cáncer, Instituto Nacional de Cancerología (INC), Bogotá, D. C., Colombia

Pilar Romero, Instituto Nacional de Cancerología (INC)

Grupo de Investigación en Biología del Cáncer, Instituto Nacional de Cancerología (INC), Bogotá, D. C., Colombia

Lina Trujillo, Instituto Nacional de Cancerología

Grupo de Ginecología, INC, Bogotá, D. C., Colombia

Mauricio González, Instituto Nacional de Cancerología

Grupo de Ginecología, INC, Bogotá, D. C., Colombia

Joaquín Luna, Instituto Nacional de Cancerología

Grupo de Ginecología, INC, Bogotá, D. C., Colombia

Natascha Ortiz, Instituto Nacional de Cancerología

Grupo de Investigaciones clínicas, INC, Bogotá, D. C., Colombia

Gustavo Hernández, Instituto Nacional de Cancerología

Grupo de Investigación en Epidemiología, INC, Bogotá, D. C., Colombia

Pierre Coursaget, Université François-Rabelais

Université François-Rabelais, UMR INRA 1282, Tours, France

Antoine Touzé, Université François-Rabelais

Université François-Rabelais, UMR INRA 1282, Tours, France

References

Walboomers JM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999;189:12-9.

https://doi.org/10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F

Harper DM, Franco EL, Wheeler C, et al. Eficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet. 2004;364:1757-65.

https://doi.org/10.1016/S0140-6736(04)17398-4

Tovar JM, Bazaldua OV. New quadrivalent HPV vaccine developments. Postgrad Med. 2008;120:14-6.

https://doi.org/10.3810/pgm.2008.11.1929

Villa L, Pérez G, Kjaer S, et al. Prophylactic efficacy of a quadrivalent human papillomavirus (HPV) vaccine in women with virological evidence of HPV infection. J Infect Dis. 2007; 196:1438-46.

https://doi.org/10.1086/522864

Future II Study Group. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med. 2007;356:1915-27.

https://doi.org/10.1056/NEJMoa061741

Ault KA. Effect of prophylactic human papillomavirus L1 virus-like-particle vaccine on risk of cervical intraepithelial neoplasia grade 2, grade 3, and adenocarcinoma in situ: a combined analysis of four randomised clinical trials. Lancet 2007;369:1861-8.

https://doi.org/10.1016/S0140-6736(07)60852-6

Garland SM, Hernández-Ávila M, Wheeler CM, et al. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med. 2007;356:1928-43.

https://doi.org/10.1056/NEJMoa061760

Harper DM, Franco EL, Wheeler CM, et al. Sustained eficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet 2006;367:1247-55.

https://doi.org/10.1016/S0140-6736(06)68439-0

Joura EA, Leodolter S, Hernández-Ávila M, et al. Eficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11,16, and 18) L1 virus-like-particle vaccine against high-grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet. 2007;369:1693-702.

https://doi.org/10.1016/S0140-6736(07)60777-6

Paavonen J, Naud P, Salmeron J, et al. Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet 2009;374:301-14.

https://doi.org/10.1016/S0140-6736(09)61248-4

Villa LL, Costa RL, Petta CA, et al. High sustained eficacy of a prophylactic quadrivalent human papillomavirus types 6/11/16/18 L1 virus-like particle vaccine through 5 years of follow-up. Br J Cancer. 2006;95:1459-66.

https://doi.org/10.1038/sj.bjc.6603469

Wheeler CM, Castellsague X, Garland SM, et al. Cross-protective eficacy of HPV-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by non-vaccine oncogenic HPV types: 4-year end-of-study analysis of the rando mised, double-blind PATRICIA trial. Lancet Oncol. 2012; 13:100-10.

https://doi.org/10.1016/S1470-2045(11)70287-X

Roteli-Martins CM, Naud P, De BP, et al. Sustained immunogenicity and efficacy of the HPV-16/18 AS04-adjuvanted vaccine: up to 8.4 years of follow-up. Hum Vaccin Immunother. 2012;8:390-7.

https://doi.org/10.4161/hv.18865

Joura EA, Kjaer SK, Wheeler CM, et al. HPV antibody levels and clinical eficacy following administration of a prophylactic quadrivalent HPV vaccine. Vaccine. 2008;26:6844-51.

https://doi.org/10.1016/j.vaccine.2008.09.073

Suzich JA, Ghim SJ, Palmer-Hill FJ, et al. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proc Natl Acad Sci USA. 1995;92:11553-7.

https://doi.org/10.1073/pnas.92.25.11553

Christensen ND, Reed CA, Cladel NM, Hall K, Leiserowitz GS. Monoclonal antibodies to HPV-6 L1 virus-like particles identify conformational and linear neutralizing epitopes on HPV-11 in addition to type-specific epitopes on HPV-6 28. Virology. 1996; 224:477-86.

https://doi.org/10.1006/viro.1996.0554

Cómbita AL, Touze A, Bousarghin L, Christensen ND, Coursaget P. Identification of two cross-neutralizing linear epitopes within the L1 major capsid protein of human papillomaviruses 6. J Virol. 2002;76:6480-6.

https://doi.org/10.1128/JVI.76.13.6480-6486.2002

Fleury MJ, Touze A, Álvarez E, et al. Identification of typespecific and cross-reactive neutralizing conformational epitopes on the major capsid protein of human papillomavirus type 3. Arch Virol. 2006;151:1511-23.

https://doi.org/10.1007/s00705-006-0734-y

Smith JF, Brownlow M, Brown M, et al. Antibodies from women immunized with Gardasil cross-neutralize HPV 45 pseudovirions. Hum Vaccin. 2007;3:109-15.

https://doi.org/10.4161/hv.3.4.4058

Yeager MD, Aste-Amezaga M, Brown DR, et al. Neutralization of human papillomavirus (HPV) pseudovirions: a novel and eficient approach to detect and characterize HPV neutralizing antibodies. Virology. 2000;278:570-7.

https://doi.org/10.1006/viro.2000.0674

Brown DR, Kjaer SK, Sigurdsson K, et al. The impact of quadrivalent human papillomavirus (HPV; types 6, 11, 16, and 18) L1 virus-like particle vaccine on infection and disease due to oncogenic nonvaccine HPV types in generally HPV-naive women aged 16-26 years. J Infect Dis. 2009;199:926-35.

https://doi.org/10.1086/597307

Ault KA. Human papillomavirus vaccines and the potential for cross-protection between related HPV types. Gynecol Oncol. 2007;107:S31-S33.

https://doi.org/10.1016/j.ygyno.2007.08.059

Draper E, Bissett SL, Howell-Jones R, et al. Neutralization of non-vaccine human papillomavirus pseudoviruses from the A7 and A9 species groups by bivalent HPV vaccine sera. Vaccine. 2011;29:8585-90.

https://doi.org/10.1016/j.vaccine.2011.09.021

Kemp TJ, Hildesheim A, Safaeian M, et al. HPV16/18 L1 VLP vaccine induces cross-neutralizing antibodies that may mediate cross-protection. Vaccine. 2011;29:2011-4.

https://doi.org/10.1016/j.vaccine.2011.01.001

Clifford GM, Gallus S, Herrero R, et al. Worldwide distribution of human papillomavirus types in cytologically normal women in the International Agency for Research on Cancer HPV prevalence surveys: a pooled analysis. Lancet. 2005;366:991-8.

https://doi.org/10.1016/S0140-6736(05)67069-9

Sanjosé de S, Díaz M, Castellsague X, et al. Worldwide prevalence and genotype distribution of cervical human papilloma virus DNA in women with normal cytology: a metaanalysis. Lancet Infect Dis. 2007;7:453-9.

https://doi.org/10.1016/S1473-3099(07)70158-5

Lazcano-Ponce E, Herrero R, Muñoz N, et al. Epidemiology of HPV infection among Mexican women with normal cervical cytology. Int J Cancer. 2001;91:412-20.

https://doi.org/10.1002/1097-0215(20010201)91:3<412::AID-IJC1071>3.0.CO;2-M

Molano M, Posso H, Weiderpass E, et al. Prevalence and determinants of HPV infection among Colombian women with normal cytology. Br J Cancer. 2002;87:324-33.

https://doi.org/10.1038/sj.bjc.6600442

de Roda Husman AM, Walboomers JM, van den Brule AJ, Meijer CJ, Snijders PJ. The use of general primers GP5 and GP6 elongated at their 3' ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol. 1995;76(Pt 4):1057-62.

https://doi.org/10.1099/0022-1317-76-4-1057

Molano M, Van den Brule A, Plummer M, et al. Determinants of clearance of human papillomavirus infections in Colombian women with normal cytology: a population-based, 5-year follow-up study. Am J Epidemiol. 2003;158:486-94.

https://doi.org/10.1093/aje/kwg171

van den Brule AJ, Pol R, Fransen-Daalmeijer N, Schouls LM, Meijer CJ, Snijders PJ. GP5+/6+ PCR followed by reverse line blot analysis enables rapid and high-throughput identification of human papillomavirus genotypes. J Clin Microbiol. 2002;40:779-87.

https://doi.org/10.1128/JCM.40.3.779-787.2002

Cómbita AL, Bravo MM, Touze A, Orozco O, Coursaget P. Serologic response to human oncogenic papillomavirus types 16, 18, 31, 33, 39, 58 and 59 virus-like particles in colombian women with invasive cervical cancer. Int J Cancer. 2002;97: 796-803.

https://doi.org/10.1002/ijc.10153

Einstein MH, Baron M, Levin MJ, et al. Comparison of the immunogenicity and safety of Cervarix and Gardasil human papillomavirus (HPV) cervical cancer vaccines in healthy women aged 18-45 years. Hum Vaccin. 2009;5:705-19.

https://doi.org/10.4161/hv.5.10.9518

Einstein MH, Baron M, Levin MJ, et al. Comparison of the immunogenicity of the human papillomavirus (HPV)-16/18 vaccine and the HPV-6/11/16/18 vaccine for oncogenic non-vaccine types HPV-31 and HPV-45 in healthy women aged 18-45 years. Hum Vaccin. 2011;7:1359-73.

https://doi.org/10.4161/hv.7.12.18282

Einstein MH, Baron M, Levin MJ, et al. Comparative immuno genicity and safety of human papillomavirus (HPV)-16/18 vaccine and HPV-6/11/16/18 vaccine: follow-up from months 12-24 in a Phase III randomized study of healthy women aged 18-45 years. Hum Vaccin. 2011;7:1343-58.

https://doi.org/10.4161/hv.7.12.18281

Romanowski B. Long term protection against cervical infection with the human papillomavirus: review of currently available vaccines. Hum Vaccin. 2011;7:161-9.

https://doi.org/10.4161/hv.7.2.13690

Romanowski B, de Borba PC, Naud PSm et al. Sustained efficacy and immunogenicity of the human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine: analysis of a randomised placebo-controlled trial up to 6.4 years. Lancet. 2009;374: 1975-85.

https://doi.org/10.1016/S0140-6736(09)61567-1

Schiller JT, Castellsague X, Villa LL, Hildesheim A. An update of prophylactic human papillomavirus L1 virus-like particle vaccine clinical trial results. Vaccine. 2008;26 (Suppl 10): K53-K61.

https://doi.org/10.1016/j.vaccine.2008.06.002

Kemp TJ, Safaeian M, Hildesheim A, et al. Kinetic and HPV infection effects on cross-type neutralizing antibody and avidity responses induced by Cervarix® . Vaccine. 2012;31: 165-70.

https://doi.org/10.1016/j.vaccine.2012.10.067

Wheeler CM, Kjaer SK, Sigurdsson K, et al. The impact of quadrivalent human papillomavirus (HPV; types 6, 11, 16, and 18) L1 virus-like particle vaccine on infection and disease due to oncogenic nonvaccine HPV types in sexually active women aged 16-26 years. J Infect Dis. 2009;199:936-44.

https://doi.org/10.1086/597309

How to Cite

[1]
Cómbita, A. et al. 2013. Evaluation of the immune response to human papillomavirus types 16, 18, 31, 45 and 58 in a group of Colombian women vaccinated with the quadrivalent vaccine. Revista Colombiana de Cancerología. 17, 3 (Sep. 2013), 103–110.

Downloads

Download data is not yet available.

Published

2013-09-01

Issue

Section

Research/original articles