A phase I clinical trial of a PER.C6® cell grown influenza H7 virus vaccine

Vaccine

Volumn 27, Issue 13, 2009, Pages 1889-1897

  Cox, Rebecca J ^a   Madhun, Abdullah S ^a   Hauge, Solveig ^a   Sjursen, Haakon ^b   Major, Diane ^c   Kuhne, Mirjam ^d   Höschler, Katja ^d   Saville, Melanie ^e   Vogel, Frederick R ^e   Barclay, Wendy ^f   Donatelli, Isabella ^g   Zambon, Maria ^d   Wood, John ^c   Haaheim, Lars R ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^c NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^d PUBLIC HEALTH ENGLAND   (United Kingdom)

^e SANOFI PASTEUR   (France)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

^g ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Human; Influenza H7; Vaccine

Indexed keywords

ALUMINUM HYDROXIDE; AVIAN INFLUENZA H7N1 VACCINE; AVIAN INFLUENZA VACCINE; INTERLEUKIN 2; UNCLASSIFIED DRUG; VIRUS HEMAGGLUTININ;

ADULT; ANTIBODY RESPONSE; ARTHRALGIA; ARTICLE; AVIAN INFLUENZA; AVIAN INFLUENZA VIRUS H7N1; CELL SECRETION; CELL STRAIN; CELL STRAIN PER C 6; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIARRHEA; DRUG DOSE ESCALATION; DRUG FORMULATION; DRUG SAFETY; DRUG TOLERABILITY; ECCHYMOSIS; FEMALE; HEADACHE; HEMAGGLUTINATION INHIBITION; HUMAN; HUMAN EXPERIMENT; IMMUNOGENICITY; INFLUENZA VIRUS; INJECTION SITE EDEMA; INJECTION SITE ERYTHEMA; INJECTION SITE PAIN; MALAISE; MALE; MYALGIA; NORMAL HUMAN; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; RESPIRATORY TRACT DISEASE; SHIVERING; SIDE EFFECT; SWEATING; VACCINE PRODUCTION; VIRUS NEUTRALIZATION;

ADJUVANTS, IMMUNOLOGIC; ADULT; ALUMINUM HYDROXIDE; ANTIBODIES, VIRAL; ANTIBODY FORMATION; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INFLUENZA A VIRUS; INFLUENZA VACCINES; INFLUENZA, HUMAN; INTERLEUKIN-2; MALE; NEUTRALIZATION TESTS; VACCINES, ATTENUATED; YOUNG ADULT;

EID: 61349200100     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.01.116     Document Type: Article

References (68)

1. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., and Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 56 March (1) (1992) 152-179
2. World Health Organization. Cumulative Number of Confirmed Human Cases of Avian Influenza A/(H5N1) Reported to WHO. 2009 [cited 2009]; Available from: .
3. HPA Press Statement. Confirmation of Avian Influenza H7N2 Infection. 2007 [cited 2007 25 May]; Available from: .
4. Tweed S.A., Skowronski D.M., David S.T., Larder A., Petric M., Lees W., et al. Human illness from avian influenza H7N3, British Columbia. Emerg Infect Dis 10 December (12) (2004) 2196-2199
5. Fouchier R.A., Schneeberger P.M., Rozendaal F.W., Broekman J.M., Kemink S.A., Munster V., et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci USA 101 February (5) (2004) 1356-1361
6. Kurtz J., Manvell R.J., and Banks J. Avian influenza virus isolated from a woman with conjunctivitis. Lancet 348 September (9031) (1996) 901-902
7. Banks J., Speidel E., and Alexander D.J. Characterisation of an avian influenza A virus isolated from a human-is an intermediate host necessary for the emergence of pandemic influenza viruses?. Arch Virol 143 4 (1998) 781-787
8. Koopmans M., Wilbrink B., Conyn M., Natrop G., van der Nat H., Vennema H., et al. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363 February (9409) (2004) 587-593
9. Belser J.A., Blixt O., Chen L.M., Pappas C., Maines T.R., Van Hoeven N., et al. Contemporary North American influenza H7 viruses possess human receptor specificity: implications for virus transmissibility. Proc Natl Acad Sci USA 105 May (21) (2008) 7558-7563
10. Treanor J.J., Campbell J.D., Zangwill K.M., Rowe T., and Wolff M. Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. N Engl J Med 354 March (13) (2006) 1343-1351
11. Hehme N., Engelmann H., Kunzel W., Neumeier E., and Sanger R. Pandemic preparedness: lessons learnt from H2N2 and H9N2 candidate vaccines. Med Microbiol Immunol (Berl) 191 December (3-4) (2002) 203-208
12. Nicholson K.G., Colegate A.E., Podda A., Stephenson I., Wood J., Ypma E., et al. Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomised trial of two potential vaccines against H5N1 influenza. Lancet 357 June (9272) (2001) 1937-1943
13. Wood J.M., and Robertson J.S. Reference viruses for seasonal and pandemic influenza vaccine preparation. Influenza Other Respir Viruses 1 (2007) 5-9
14. Legastelois I., Garcia-Sastre A., Palese P., Tumpey T.M., Maines T.R., Katz J.M., et al. Preparation of genetically engineered A/H5N1 and A/H7N1 pandemic vaccine viruses by reverse genetics in a mixture of Vero and chicken embryo cells. Influenza Other Respir Viruses 1 3 (2007) 95-104
15. Pappas C., Matsuoka Y., Swayne D.E., and Donis R.O. Development and evaluation of an influenza virus subtype H7N2 vaccine candidate for pandemic preparedness. Clin Vaccine Immunol 14 November (11) (2007) 1425-1432
16. Jadhao S.J., Achenbach J., Swayne D.E., Donis R., Cox N., and Matsuoka Y. Development of Eurasian H7N7/PR8 high growth reassortant virus for clinical evaluation as an inactivated pandemic influenza vaccine. Vaccine 26 March (14) (2008) 1742-1750
17. Whiteley A., Major D., Legastelois I., Campitelli L., Donatelli I., Thompson C.I., et al. Generation of candidate human influenza vaccine strains in cell culture-rehearsing the European response to an H7N1 pandemic threat. Influenza Other Respir Viruses 1 4 (2007) 157-166
18. Nicolson C., Major D., Wood J.M., and Robertson J.S. Generation of influenza vaccine viruses on Vero cells by reverse genetics: an H5N1 candidate vaccine strain produced under a quality system. Vaccine 23 April (22) (2005) 2943-2952
19. Hoffmann E., Krauss S., Perez D., Webby R., and Webster R.G. Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine 20 August (25-26) (2002) 3165-3170
20. Palache A.M., Brands R., and van Scharrenburg G.J. Immunogenicity and reactogenicity of influenza subunit vaccines produced in MDCK cells or fertilized chicken eggs. J Infect Dis 176 August (Suppl 1) (1997) S20-S23
21. Ehrlich H.J., Muller M., Oh H.M., Tambyah P.A., Joukhadar C., Montomoli E., et al. A clinical trial of a whole-virus H5N1 vaccine derived from cell culture. N Engl J Med 358 June (24) (2008) 2573-2584
22. Kistner O., Barrett P.N., Mundt W., Reiter M., Schober-Bendixen S., and Dorner F. Development of a mammalian cell (Vero) derived candidate influenza virus vaccine. Vaccine 16 May-June (9-10) (1998) 960-968
23. Pau M.G., Ophorst C., Koldijk M.H., Schouten G., Mehtali M., and Uytdehaag F. The human cell line PER.C6 provides a new manufacturing system for the production of influenza vaccines. Vaccine 19 March (17-19) (2001) 2716-2721
24. Lu X., Tumpey T.M., Morken T., Zaki S.R., Cox N.J., and Katz J.M. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J Virol 73 July (7) (1999) 5903-5911
25. de Wit E., Munster V.J., Spronken M.I., Bestebroer T.M., Baas C., Beyer W.E., et al. Protection of mice against lethal infection with highly pathogenic H7N7 influenza A virus by using a recombinant low-pathogenicity vaccine strain. J Virol 79 October (19) (2005) 12401-12407
26. Keitel W.A., and Atmar R.L. Preparing for a possible pandemic: influenza A/H5N1 vaccine development. Curr Opin Pharmacol 7 October (5) (2007) 484-490
27. Stephenson I., Nicholson K.G., Wood J.M., Zambon M.C., and Katz J.M. Confronting the avian influenza threat: vaccine development for a potential pandemic. Lancet Infect Dis 4 August (8) (2004) 499-509
28. Haaheim L.R. Vaccines for an influenza pandemic: scientific and political challenges. Influenza Other Respir Viruses 1 2 (2007) 55-60
29. Hem S.L., and Hogenesch H. Relationship between physical and chemical properties of aluminum-containing adjuvants and immunopotentiation. Expert Rev Vaccines 6 October (5) (2007) 685-698
30. Capua I., Mutinelli F., Pozza M.D., Donatelli I., Puzelli S., and Cancellotti F.M. The 1999-2000 avian influenza (H7N1) epidemic in Italy: veterinary and human health implications. Acta Trop 83 July (1) (2002) 7-11
31. Banks J., Speidel E.S., Moore E., Plowright L., Piccirillo A., Capua I., et al. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch Virol 146 5 (2001) 963-973
32. Major DL, Cox RJ, Smith J, Vogel F, Haaheim LR, Wood JM. Evaluation of a PER.C6 cell grown influenza H7N1 virus vaccine in BALB/c mice. Options for the control of influenza VI. Toronto, Canada;2007.
33. WHOIfVR. Tables on the Clinical trials of pandemic influenza prototype vaccines;2008.
34. WHO Expert Committee on Biological Standardization. WHO biosafety risk assessment and guidelines for the production and quality control of human influenza pandemic vaccines. Annex 5. 2005 [cited 2005 24-28 October]; Available from: .
35. Bresson J.L., Perronne C., Launay O., Gerdil C., Saville M., Wood J., et al. Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet 367 May (9523) (2006) 1657-1664
36. Cox R.J., Brokstad K.A., Zuckerman M.A., Wood J.M., Haaheim L.R., and Oxford J.S. An early humoral immune response in peripheral blood following parenteral inactivated influenza vaccination. Vaccine 12 August (11) (1994) 993-999
37. Eriksson J-C, Cox RJ, Szyszko E, Davidsson Å, Brokstad KA. Local and systemic cytokine and chemokine responses after parenteral influenza vaccination. Influenza Other Respir Viruses 2007;1(4):139-46.
38. Stephenson I., Wood J.M., Nicholson K.G., and Zambon M.C. Sialic acid receptor specificity on erythrocytes affects detection of antibody to avian influenza haemagglutinin. J Med Virol 70 July (3) (2003) 391-398
39. Puzelli S., Di Trani L., Fabiani C., Campitelli L., De Marco M.A., Capua I., et al. Serological analysis of serum samples from humans exposed to avian H7 influenza viruses in Italy between 1999 and 2003. J Infect Dis 192 October (8) (2005) 1318-1322
40. Rowe T., Abernathy R.A., Hu-Primmer J., Thompson W.W., Lu X., Lim W., et al. Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J Clin Microbiol 37 April (4) (1999) 937-943
41. Brokstad K.A., Cox R.J., Olofsson J., Jonsson R., and Haaheim L.R. Parenteral influenza vaccination induces a rapid systemic and local immune response. J Infect Dis 171 January (1) (1995) 198-203
42. Committee. Note for guidance on harmonization of requirements for influenza vaccines (CPMP/BWP/214/96). European Agency for the Evaluation of Medicinal Products, March 12, 1997; 1996.
43. Palache A.M., Scheepers H.S., de Regt V., van Ewijk P., Baljet M., Brands R., et al. Safety, reactogenicity and immunogenicity of Madin Darby Canine Kidney cell-derived inactivated influenza subunit vaccine. A meta-analysis of clinical studies. In: Brown F., Robertson J.S., Schild G.C., and Wood J.M. (Eds). Inactivated influenza vaccines prepared in cell culture. Dev Biol Stand vol. 98 (1999), Karger, Basel 115-125
44. Rumke H.C., Bayas J.M., de Juanes J.R., Caso C., Richardus J.H., Campins M., et al. Safety and reactogenicity profile of an adjuvanted H5N1 pandemic candidate vaccine in adults within a phase III safety trial. Vaccine 26 May (19) (2008) 2378-2388
45. Bernstein D.I., Edwards K.M., Dekker C.L., Belshe R., Talbot H.K., Graham I.L., et al. Effects of adjuvants on the safety and immunogenicity of an avian influenza H5N1 vaccine in adults. J Infect Dis 197 March (5) (2008) 667-675
46. Lin J., Zhang J., Dong X., Fang H., Chen J., Su N., et al. Safety and immunogenicity of an inactivated adjuvanted whole-virion influenza A (H5N1) vaccine: a phase I randomised controlled trial. Lancet 368 September (9540) (2006) 991-997
47. 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 370 August (9587) (2007) 580-589
48. Stephenson I., Nicholson K.G., Gluck R., Mischler R., Newman R.W., Palache A.M., et al. Safety and antigenicity of whole virus and subunit influenza A/Hong Kong/1073/99 (H9N2) vaccine in healthy adults: phase I randomised trial. Lancet 362 December (9400) (2003) 1959-1966
49. Hehme N., Engelmann H., Kuenzel W., Neumeier E., and Saenger R. Immunogenicity of a monovalent, aluminum-adjuvanted influenza whole virus vaccine for pandemic use. Virus Res 103 July (1-2) (2004) 163-171
50. Treanor J.J., Wilkinson B.E., Masseoud F., Hu-Primmer J., Battaglia R., O'Brien D., et al. Safety and immunogenicity of a recombinant hemagglutinin vaccine for H5 influenza in humans. Vaccine 19 February (13-14) (2001) 1732-1737
51. Nolan T., Bernstein D.I., Block S.L., Hilty M., Keyserling H.L., Marchant C., et al. Safety and immunogenicity of concurrent administration of live attenuated influenza vaccine with measles-mumps-rubella and varicella vaccines to infants 12 to 15 months of age. Pediatrics 121 March (3) (2008) 508-516
52. Nolan T.M., Richmond P.C., Skeljo M.V., Pearce G., Hartel G., Formica N.T., et al. Phase I and II randomised trials of the safety and immunogenicity of a prototype adjuvanted inactivated split-virus influenza A (H5N1) vaccine in healthy adults. Vaccine 26 August (33) (2008) 4160-4167
53. Keitel W.A., Campbell J.D., Treanor J.J., Walter E.B., Patel S.M., He F., et al. Safety and immunogenicity of an inactivated influenza A/H5N1 vaccine given with or without aluminum hydroxide to healthy adults: results of a phase I-II randomized clinical trial. J Infect Dis 198 November (9) (2008) 1309-1316
54. Stephenson I., Bugarini R., Nicholson K.G., Podda A., Wood J.M., Zambon M.C., et al. Cross-reactivity to highly pathogenic avian influenza H5N1 viruses after vaccination with nonadjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a potential priming strategy. J Infect Dis 191 April (8) (2005) 1210-1215
55. Stephenson I., Nicholson K.G., Colegate A., Podda A., Wood J., Ypma E., et al. Boosting immunity to influenza H5N1 with MF59-adjuvanted H5N3 A/Duck/Singapore/97 vaccine in a primed human population. Vaccine 21 April (15) (2003) 1687-1693
56. Baras B., Stittelaar K.J., Simon J.H., Thoolen R.J., Mossman S.P., Pistoor F.H., et al. Cross-protection against lethal H5N1 challenge in ferrets with an adjuvanted pandemic influenza vaccine. PLoS ONE 3 1 (2008) e1401
57. Höschler K., Gopal R., Andrews N., Saville M., Pepin S., Wood J., et al. Gross-neutralisation of antibodies elicited by an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine in healthy adults against H5N1 clade 2 strains. Influenza Other Respir Viruses 1 5-6 (2008) 199-206
58. Skowronski D.M., Li Y., Tweed S.A., Tam T.W., Petric M., David S.T., et al. Protective measures and human antibody response during an avian influenza H7N3 outbreak in poultry in British Columbia, Canada. CMAJ 176 January (1) (2007) 47-53
59. el-Madhun A.S., Cox R.J., Soreide A., Olofsson J., and Haaheim L.R. Systemic and mucosal immune responses in young children and adults after parenteral influenza vaccination. J Infect Dis 178 October (4) (1998) 933-939
60. Sasaki S., Jaimes M.C., Holmes T.H., Dekker C.L., Mahmood K., Kemble G.W., et al. Comparison of the influenza virus-specific effector and memory B-cell responses to immunization of children and adults with live attenuated or inactivated influenza virus vaccines. J Virol 81 January (1) (2007) 215-228
61. Litjens N.H., Huisman M., Hijdra D., Lambrecht B.M., Stittelaar K.J., and Betjes M.G. IL-2 producing memory CD4 + T lymphocytes are closely associated with the generation of IgG-secreting plasma cells. J Immunol 181 September (5) (2008) 3665-3673
62. Longini Jr. I.M., Nizam A., Xu S., Ungchusak K., Hanshaoworakul W., Cummings D.A., et al. Containing pandemic influenza at the source. Science 309 August (5737) (2005) 1083-1087
63. Ferguson N.M., Cummings D.A., Fraser C., Cajka J.C., Cooley P.C., and Burke D.S. Strategies for mitigating an influenza pandemic. Nature 442 July (7101) (2006) 448-452
64. Cox R.J., Hauge S., Madhun A.S., Sjursen H., Major D., Kuhne M., et al. The safety, immunogenicity and protective efficacy of a Per. C6 cell grown influenza H7N1 virus vaccine in preclincial and clinical studies. The third European influenza conference. Vilmoura, Portugal (2008)
65. Ninomiya A., Imai M., Tashiro M., and Odagiri T. Inactivated influenza H5N1 whole-virus vaccine with aluminum adjuvant induces homologous and heterologous protective immunities against lethal challenge with highly pathogenic H5N1 avian influenza viruses in a mouse model. Vaccine 25 May (18) (2007) 3554-3560
66. Lipatov A.S., Hoffmann E., Salomon R., Yen H.L., and Webster R.G. Cross-protectiveness and immunogenicity of influenza A/Duck/Singapore/3/97(H5) vaccines against infection with A/Vietnam/1203/04(H5N1) virus in ferrets. J Infect Dis 194 October (8) (2006) 1040-1043
67. Suguitan Jr. A.L., McAuliffe J., Mills K.L., Jin H., Duke G., Lu B., et al. Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med 3 September (9) (2006) e360
68. Mahmood K., Bright R.A., Mytle N., Carter D.M., Crevar C.J., Achenbach J.E., et al. H5N1 VLP vaccine induced protection in ferrets against lethal challenge with highly pathogenic H5N1 influenza viruses. Vaccine 26 October (42) (2008) 5393-5399