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

Human Vaccines

Volumn 7, Issue 12, 2011, Pages 1359-1373

  Einstein, Mark H ^a   Baron, Mira ^b   Levin, Myron J ^c   Chatterjee, Archana ^d   Fox, Bradley ^e   Scholar, Sofia ^f   Rosen, Jeffrey ^g   Chakhtoura, Nahida ^h   Lebacq, Marie ⁱ   Van Der Most, Robbert ⁱ   Moris, Philippe ⁱ   Giannini, Sandra L ⁱ   Schuind, Anne ^j   Datta, Sanjoy K ⁱ   Descamps, Dominique ⁱ  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b Rapid Medical Research   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Liberty Family Practice   (United States)

^f Walla Walla Clinic   (United States)

^g Clinical Research of South Florida   (United States)

^h UNIVERSITY OF MIAMI   (United States)

ⁱ GLAXOSMITHKLINE BIOLOGICALS   (Belgium)

^j GLAXOSMITHKLINE   (United States)

more..

Author keywords

Cervarix ; Cervical cancer; Cross protection; Gardasil ; HPV 31; HPV 45; Human papillomavirus; Immunogenicity

Indexed keywords

WART VIRUS VACCINE;

ADULT; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; COMPARATIVE EFFECTIVENESS; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSS REACTION; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 31; HUMAN PAPILLOMAVIRUS TYPE 45; HUMAN PAPILLOMAVIRUS TYPE 6; IMMUNE RESPONSE; IMMUNOGENICITY; INFECTION PREVENTION; MEMORY CELL; NORMAL HUMAN; PAPILLOMAVIRUS INFECTION; SEROLOGY; TUMOR VIRUS;

ADOLESCENT; ADULT; ALPHAPAPILLOMAVIRUS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; HUMAN PAPILLOMAVIRUS 31; HUMANS; MIDDLE AGED; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; TREATMENT OUTCOME; VACCINATION; YOUNG ADULT;

EID: 84855169688     PISSN: 15548600     EISSN: 15548619     Source Type: Journal    
DOI: 10.4161/hv.7.12.18282     Document Type: Article

References (55)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010; 127:2893-917; PMID:21351269; DOI:10.1002/ijc.25516.
2. Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003; 348:518-27; PMID:12571259; DOI:10.1056/NEJMoa021641.
3. Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: A meta-analysis update. Int J Cancer 2007; 121:621-32; PMID:17405118; DOI:10.1002/ijc.22527.
4. de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, et al. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 2010; 11:1048-56; PMID:20952254; DOI:10.1016/S1470-2045(10)70230-8.
5. Barr E, Tamms G. Quadrivalent human papillomavirus vaccine. Clin Infect Dis 2007; 45:609-17; PMID:17682997; DOI:10.1086/520654.
6. Siddiqui MA, Perry CM. Human papillomavirus quadrivalent (types 6, 11, 16, 18) recombinant vaccine (Gardasil). Drugs 2006; 66:1263-71; PMID:16827602; DOI:10.2165/00003495-200666090-00008.
7. Vandepapeliere P, Barrasso R, Meijer CJ, Walboomers JM, Wettendorff M, Stanberry LR, et al. Randomized controlled trial of an adjuvanted human papillomavirus (HPV) type 6 L2E7 vaccine: infection of external anogenital warts with multiple HPV types and failure of therapeutic vaccination. J Infect Dis 2005; 192:2099-107; PMID:16288373; DOI:10.1086/498164.
8. Giannini SL, Hanon E, Moris P, Van Mechelen M, Morel S, Dessy F, et al. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine 2006; 24:5937-49; PMID:16828940; DOI:10.1016/j.vaccine.2006. 06.005.
9. Keam SJ, Harper DM. Human papillomavirus types 16 and 18 vaccine (recombinant, AS04 adjuvanted, adsorbed) [Cervarix]. Drugs 2008; 68:359- 72; PMID:18257611; DOI:10.2165/00003495-200868030-00007.
10. Caulfield MJ, Shi L, Wang S, Wang B, Tobery TW, Mach H, et al. Effect of alternative aluminum adjuvants on the absorption and immunogenicity of HPV16 L1 VLPs in mice. Hum Vaccin 2007; 3:139-45; PMID:17581283; DOI:10.4161/hv.3.4.4309.
11. Tovar JM, Bazaldua OV. New quadrivalent HPV vaccine developments. Postgrad Med 2008; 120:14-6; PMID:19020361; DOI:10.3810/pgm.2008.11.1929.
12. De Carvalho N, Teixeira J, Roteli-Martins CM, Naud P, De Borba P, Zahaf T, et al. Sustained efficacy and immunogenicity of the HPV-16/18 AS04-adjuvanted vaccine up to 7.3 years in young adult women. Vaccine 2010; 28:6247-55; PMID:20643092; DOI:10.1016/j. vaccine.2010.07.007.
13. FUTURE II Study Group. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 2007; 356:1915-27; PMID:17494925; DOI:10.1056/NEJMoa061741.
14. Harper DM, Franco EL, Wheeler C, Ferris DG, Jenkins D, Schuind A, et al. Efficacy 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; PMID:15541448; DOI:10.1016/S0140- 6736(04)17398-4.
15. Harper DM, Franco EL, Wheeler CM, Moscicki AB, Romanowski B, Roteli-Martins CM, et al. Sustained efficacy 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 controlled trial. Lancet 2006; 367:1247-55; PMID:16631880; DOI:10.1016/S0140-6736(06)68439-0.
16. Olsson SE, Villa LL, Costa RL, Petta CA, Andrade RP, Malm C, et al. Induction of immune memory following administration of a prophylactic quadrivalent human papillomavirus (HPV) types 6/11/16/18 L1 virus-like particle (VLP) vaccine. Vaccine 2007; 25:4931-9; PMID:17499406; DOI:10.1016/j.vaccine. 2007.03.049.
17. Paavonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter D, 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; PMID:19586656; DOI:10.1016/S0140-6736(09)61248-4.
18. Villa LL, Costa RL, Petta CA, Andrade RP, Ault KA, Giuliano AR, et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16 and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol 2005; 6:271-8; PMID:15863374; DOI:10.1016/S1470-2045(05)70101-7.
19. Villa LL, Costa RL, Petta CA, Andrade RP, Paavonen J, Iversen OE, et al. High sustained efficacy 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; PMID:17117182; DOI:10.1038/sj.bjc.6603469.
20. Brown DR, Kjaer SK, Sigurdsson K, Iversen OE, Hernandez-Avila M, Wheeler CM, 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; PMID:19236279; DOI:10.1086/597307.
21. Einstein MH, Baron M, Levin MJ, Chatterjee A, Edwards RP, Zepp F, et al. Comparison of the immunogenicity and safety of CervarixTM and Gardasil® human papillomavirus (HPV) cervical cancer vaccines in healthy women aged 18-45 years. Hum Vaccin 2009; 5:705-19; PMID:19684472; DOI:10.4161/hv.5.10.9518.
22. Einstein MH, Baron M, Levin M, Chatterjee A, Fox B, Scholar S, et al. Comparative immunogenicity and safety of Cervarix® and Gardasil® human papillomavirus (HPV) vaccines: Follow-up from Month 12-24 in a Phase III study of healthy women ages 18-45 years. Hum Vaccin 2011; 7; In press.
23. th International Papillomavirus Conference, Montreal, Canada, July 3-8, 2010.
24. Paavonen J, Jenkins D, Bosch FX, Naud P, Salmeron J, Wheeler CM, et al. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet 2007; 369:2161-70; PMID:17602732; DOI:10.1016/S0140-6736(07)60946-5.
25. Bosch FX, Burchell AN, Schiffman M, Giuliano AR, de Sanjose S, Bruni L, et al. Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine 2008; 26:1-16; PMID:18847553; DOI:10.1016/j.vaccine. 2008.05.064.
26. Tokoyoda K, Zehentmeier S, Chang H, Radbruch A. Organization and maintenance of immunological memory by stroma niches. Eur J Immunol 2009; 39:2095-9; PMID:19637201; DOI:10.1002/eji.200939500.
27. Smith JF, Brownlow M, Brown M, Kowalski R, Esser MT, Ruiz W, et al. Antibodies from women immunized with Gardasil cross-neutralize HPV 45 pseudovirions. Hum Vaccin 2007; 3:109-15; PMID:17611417; DOI:10.4161/hv.3.4. 4058.
28. Kemp TJ, Hildesheim A, Safaeian M, Dauner JG, Pan Y, Porras C, et al. HPV16/18 L1 VLP vaccine induces cross-neutralizing antibodies that may mediate cross-protection. Vaccine 2011; 29:2011-4; PMID:21241731; DOI:10.1016/j.vaccine. 2011.01.001.
29. Moscicki AB, Wheeler C, Romanowski B, Hedrick J, Gall S, Ferris D, et al. Anamnestic response elicited by a fourth dose of the HPV-16/18 AS04-adjuvanted vaccine in young women. EUROGIN, Monte Carlo, Monaco, February 17-20, 2010.
30. Moscicki B, Wheeler C, Romanowski B, Hedrick J, Gall S, Ferris D, et al. Anamnestic response to nonvaccine types elicited by a fourth dose of the HPV-16/18 AS04-adjuvanted vaccine. EUROGIN, Monte Carlo, Monaco, February 17-20, 2010.
31. Krajden M, Cook D, Yu A, Chow R, Mei W, McNeil S, et al. Human Papillomavirus 16 (HPV 16) and HPV 18 Antibody Responses Measured by Pseudovirus Neutralization and Competitive Luminex Assays in a Two- versus Three-Dose HPV Vaccine Trial. Clin Vaccine Immunol 2011; 18:418-23; PMID:21248158; DOI:10.1128/CVI.00489-10.
32. Dessy F, Poncelet S, Xhenseval V, Méric S, Dubin G, et al. Comparative evaluation of the immunogenicity of two prophylactic HPV cervical cancer vaccines by Merck's competitive Luminex immunoassay (cLIA) and GSK's binding ELISA. EUROGIN, Monte Carlo, Monaco, February 17-20, 2010.
33. Langley JM, Frenette L, Ferguson L, Riff D, Sheldon E, Risi G, et al. Safety and cross-reactive immunogenicity of candidate AS03-adjuvanted prepandemic H5N1 influenza vaccines: a randomized controlled phase 1/2 trial in adults. J Infect Dis 2010; 201:1644-53; PMID:20423222; DOI:10.1086/652701.
34. Leroux-Roels I, Borkowski A, Vanwolleghem T, Drame M, Clement F, Hons E, et al. Antigen sparing and cross-reactive immunity with an adjuvanted rH5N1 prototype pandemic influenza vaccine: a randomised controlled trial. Lancet 2007; 370:580-9; PMID:17707753; DOI:10.1016/S0140-6736(07)61297-5.
35. Moris P, van der Most R, Leroux-Roels I, Clement F, Drame M, Hanon E, et al. H5N1 influenza vaccine formulated with AS03 A induces strong cross-reactive and polyfunctional CD4 T-cell responses. J Clin Immunol 2011; 31:443-54; PMID:21174144; DOI:10.1007/s10875-010-9490-6.
36. Didierlaurent AM, Morel S, Lockman L, Giannini SL, Bisteau M, Carlsen H, et al. AS04, an aluminum salt- and TLR4 agonist-based adjuvant system, induces a transient localized innate immune response leading to enhanced adaptive immunity. J Immunol 2009; 183:6186-97; PMID:19864596; DOI:10.4049/jimmunol. 0901474.
37. Baldridge JR, McGowan P, Evans JT, Cluff C, Mossman S, Johnson D, et al. Taking a Toll on human disease: Toll-like receptor 4 agonists as vaccine adjuvants and monotherapeutic agents. Expert Opin Biol Ther 2004; 4:1129-38; PMID:15268679; DOI:10.1517/14712598.4.7.1129.
38. Tiberio L, Fletcher L, Eldridge JH, Duncan DD. Host factors impacting the innate response in humans to the candidate adjuvants RC529 and monophosphoryl lipid A. Vaccine 2004; 22:1515-23; PMID:15063577; DOI:10.1016/j.vaccine.2003.10. 019.
39. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. Classification of papillomaviruses. Virology 2004; 324:17-27; PMID:15183049; DOI:10.1016/j.virol.2004.03.033.
40. Nakagawa S, Yoshikawa H, Yasugi T, Kimura M, Kawana K, Matsumoto K, et al. Ubiquitous presence of E6 and E7 transcripts in human papillomavirus- positive cervical carcinomas regardless of its type. J Med Virol 2000; 62:251-8; PMID:11002256; DOI:10.1002/1096-9071(200010)62:2〈251::AIDJMV18〉 3.0.CO;2-V.
41. Deschuyteneer M, Elouahabi A, Plainchamp D, Plisnier M, Soete D, Corazza Y, et al. Molecular and structural characterization of the L1 virus-like particles that are used as vaccine antigens in CervarixTM, the AS04-adjuvanted HPV-16 and -18 cervical cancer vaccine. Hum Vaccin 2010; 6:407-19; PMID:20953154; DOI:10.4161/hv.6.5.11023.
42. Bishop B, Dasgupta J, Klein M, Garcea RL, Christensen ND, Zhao R, et al. Crystal structures of four types of human papillomavirus L1 capsid proteins: understanding the specificity of neutralizing monoclonal antibodies. J Biol Chem 2007; 282:31803-11; PMID:17804402; DOI:10.1074/jbc.M706380200.
43. Combita 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. J Virol 2002; 76:6480-6; PMID:12050360; DOI:10.1128/JVI.76.13.6480-6.2002.
44. Day PM, Kines RC, Thompson CD, Jagu S, Roden RB, Lowy DR, et al. In vivo mechanisms of vaccine-induced protection against HPV infection. Cell Host Microbe 2010; 8:260-70; PMID:20833377; DOI:10.1016/j.chom.2010.08.003.
45. Brendle SA, Culp TD, Broutian TR, Christensen ND. Binding and neutralization characteristics of a panel of monoclonal antibodies to human papillomavirus 58. J Gen Virol 2010; 91:1834-9; PMID:20181746; DOI:10.1099/vir.0.017228-0.
46. Giannini S, Lockman L, Christensen ND, Brendle SA, Balogh KK, Mossman S. HPV L1 VLP-based vaccines formulated with AS04 induce cross-protection against infection and disease in the rabbit HPV quasivirion challenge method. International Papillomavirus Conference, Montreal, Canada 2010; 193.
47. Schiller JT, Day PM, Kines RC. Current understanding of the mechanism of HPV infection. Gynecol Oncol 2010; 118:12-7; PMID:20494219; DOI:10.1016/j. ygyno.2010.04.004.
48. Fahey LM, Raff AB, Da Silva DM, Kast WM. A major role for the minor capsid protein of human papillomavirus type 16 in immune escape. J Immunol 2009; 183:6151-6; PMID:19864613; DOI:10.4049/jimmunol.0902145.
49. Fausch SC, Fahey LM, Da Silva DM, Kast WM. Human papillomavirus can escape immune recognition through Langerhans cell phosphoinositide- 3-kinase activation. J Immunol 2005; 174:7172-8; PMID:15905561.
50. Horowitz A, Behrens RH, Okell L, Fooks AR, Riley EM. NK cells as effectors of acquired immune responses: effector CD4+ T cell-dependent activation of NK cells following vaccination. J Immunol 2010; 185:2808-18; PMID:20679529; DOI:10.4049/jimmunol. 1000844.
51. Kenter GG, Welters MJ, Valentijn AR, Lowik MJ, Berends-van der Meer DM, Vloon AP, et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med 2009; 361:1838-47; PMID:19890126; DOI:10.1056/NEJMoa0810097.
52. Coleman N, Birley HD, Renton AM, Hanna NF, Ryait BK, Byrne M, et al. Immunological events in regressing genital warts. Am J Clin Pathol 1994; 102:768-74; PMID:7801889.
53. Dessy FJ, Giannini SL, Bougelet CA, Kemp TJ, David MP, Poncelet SM, et al. Correlation between direct ELISA, single-epitope based inhibition ELISA and pseudovirion-based neutralization assay for measuring anti-HPV-16 and anti-HPV-18 antibody response after vaccination with the AS04-adjuvanted HPV-16/18 cervical cancer vaccine. Hum Vaccin 2008; 4:425-34; PMID:18948732; DOI:10.4161/hv.4.6.6912.
54. Schiffman M, Wentzensen N. From human papillomavirus to cervical cancer. Obstet Gynecol 2010; 116:177-85; PMID:20567185; DOI:10.1097/AOG. 0b013e3181e4629f.
55. Schiffman M, Herrero R, DeSalle R, Hildesheim A, Wacholder S, Rodriguez AC, et al. The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005; 337:76-84; PMID:15914222; DOI:10.1016/j.virol.2005.04. 002.