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Immune Responses in Pigs Vaccinated with Adjuvanted and Non-Adjuvanted A(H1N1)Pdm/09 Influenza Vaccines Used in Human Immunization Programmes

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Immune Responses in Pigs Vaccinated with Adjuvanted and Non-Adjuvanted A(H1N1)Pdm/09 Influenza Vaccines Used in Human Immunization Programmes Immune Responses in Pigs Vaccinated with Adjuvanted and Non-Adjuvanted A(H1N1)pdm/09 Influenza Vaccines Used in Human Immunization Programmes Eric A. Lefevre1*, B. Veronica Carr1, Charlotte F. Inman2, Helen Prentice1, Ian H. Brown3, Sharon M. Brookes3, Fanny Garcon3, Michelle L. Hill1, Munir Iqbal1, Ruth A. Elderfield4, Wendy S. Barclay4, Simon Gubbins5, Mick Bailey2, Bryan Charleston1, COSI" 1 Institute for Animal Health, Compton near Newbury, United Kingdom, 2 Division of Veterinary Pathology, School of Clinical Veterinary Science, University of Bristol, Langford, Bristol, United Kingdom, 3 Animal Health and Veterinary Laboratories Agency - Weybridge, EU/OIE/FAO Reference Laboratory for Avian Influenza and Newcastle Disease, Addlestone, United Kingdom, 4 Department of Virology, Imperial College London, London, United Kingdom, 5 Institute for Animal Health, Pirbright, United Kingdom Abstract Following the emergence and global spread of a novel H1N1 influenza virus in 2009, two A(H1N1)pdm/09 influenza vaccines produced from the A/California/07/09 H1N1 strain were selected and used for the national immunisation programme in the United Kingdom: an adjuvanted split virion vaccine and a non-adjuvanted whole virion vaccine. In this study, we assessed the immune responses generated in inbred large white pigs (Babraham line) following vaccination with these vaccines and after challenge with A(H1N1)pdm/09 virus three months post-vaccination. Both vaccines elicited strong antibody responses, which included high levels of influenza-specific IgG1 and haemagglutination inhibition titres to H1 virus. Immunisation with the adjuvanted split vaccine induced significantly higher interferon gamma production, increased frequency of interferon gamma-producing cells and proliferation of CD42CD8+ (cytotoxic) and CD4+CD8+ (helper) T cells, after in vitro re-stimulation. Despite significant differences in the magnitude and breadth of immune responses in the two vaccinated and mock treated groups, similar quantities of viral RNA were detected from the nasal cavity in all pigs after live virus challenge. The present study provides support for the use of the pig as a valid experimental model for influenza infections in humans, including the assessment of protective efficacy of therapeutic interventions. Citation: Lefevre EA, Carr BV, Inman CF, Prentice H, Brown IH, et al. (2012) Immune Responses in Pigs Vaccinated with Adjuvanted and Non-Adjuvanted A(H1N1)pdm/09 Influenza Vaccines Used in Human Immunization Programmes. PLoS ONE 7(3): e32400. doi:10.1371/journal.pone.0032400 Editor: Yi Guan, The University of Hong Kong, China Received December 8, 2011; Accepted January 30, 2012; Published March 9, 2012 Copyright: ß 2012 Lefevre et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The present study was conducted within the remit of the COmbating Swine Influenza (COSI) consortium, funded by the Biotechnology and Biological Sciences Research Council (BBSRC), Medical Research Council (MRC), Department for Environment, Food and Rural Affairs (Defra) and Wellcome Trust (BB/ H014292/1). Additional financial support for this research was also provided by the Institute for Animal Health. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] " Membership of COSI is provided in the Acknowledgments. Introduction adjuvanted whole virion vaccine derived from Vero cell culture, administered twice with a minimum of 3 weeks between injections. In June 2009, the World Health Organization (WHO) declared These A(H1N1)pdm/09 vaccines were authorized under ‘‘Excep- an H1N1 influenza pandemic in response to the emergence and tional Circumstances’’ on the basis of limited to very limited safety global spread of a novel H1N1 influenza A virus - A(H1N1)pdm/ and immunogenicity data obtained with these A(H1N1)pdm/09 09 (http://www.who.int/mediacentre/news/statements/2009/ influenza vaccines and also utilised more complete safety and h1n1_pandemic_phase6_20090611/en/index.html), which con- immunogenicity data obtained with H5N1 ‘‘mock-up’’ vaccines - tained a unique combination of gene segments derived from e.g. similar versions of the A(H1N1)pdm/09 vaccines that contain multiple viruses that have been circulating in pigs for decades [1]. the whole H5N1 A/Vietnam/1203/2004 influenza virus for the Most A(H1N1)pdm/09 cases in humans resulted in mild illnesses, non-adjuvanted whole vaccine or the viral surface protein but in some people, more serious symptoms and fatalities have haemagglutinin (HA) derived from H5N1 A/Vietnam/1194/ been reported [2]. 2004 for the adjuvanted split vaccine (product characteristics In the UK, two A(H1N1)pdm/09 influenza vaccines produced described in http://www.ema.europa.eu/docs/en_GB/documen- from the A/California/07/09 H1N1 strain (Cal07) were used for t_library/Other/2010/01/WC500059182.pdf and http://www. the national immunisation programme: (i) Pandemrix (Glaxo- dossiers-sos-justice.com/media/00/01/1744671157.pdf, respec- SmithKline Biologicals S.A., GSK), an AS03b-adjuvanted split tively). For both vaccines, the immunogenicity data at the time virion vaccine derived from embryonated chicken eggs, adminis- of authorization was based on the generation of anti-HA tered once in healthy adults, and (ii) Celvapan (Baxter AG), a non- antibodies following vaccination with either the A(H1N1)pdm/ PLoS ONE | www.plosone.org 1 March 2012 | Volume 7 | Issue 3 | e32400 Immune Responses to A(H1N1)pdm/09 Vaccines in Pigs 09 and/or ‘‘mock-up’’ vaccines, and included some antigenic chicken eggs. This vaccine was supplied as a suspension (antigen) cross-reactivity data. For the adjuvanted split vaccine, non-clinical and emulsion (adjuvant) multidose vial, and the volume after studies were solely based on results obtained following the mixing one vial of suspension (2.5 ml) with one vial of emulsion vaccination and challenge of ferrets with the ‘‘mock-up’’ vaccine. (2.5 ml) corresponded to ten doses of vaccine. One dose (0.5 ml) For the non-adjuvanted whole vaccine, two non-clinical studies contained: (i) 3.75 mg HA antigen; (ii) the oil-in-water AS03 were performed in ferrets vaccinated with the ‘‘mock-up’’ vaccine adjuvant composed of squalene (10.69 mg), DL-a-tocopherol and one study was performed in mice using the A(H1N1)pdm/09 (11.86 mg) and polysorbate 80 (4.86 mg); and (iii) the excipient vaccine. Regarding the latter study, Kistner et al. recently reported thiomersal (5 mg). The vaccine vials were stored at 2–8uC and that the non-adjuvanted whole vaccine provided protection used within 24 hours following mixing. against challenge with Cal07 with respect to undetectable virus The non-adjuvanted whole virion vaccine was manufactured titers in the lung tissue of vaccinated CD1 mice [3]. Since these from Cal07, grown in Vero cells and inactivated (formaldehyde A(H1N1)pdm/09 vaccines were made available, several authors and UV irradiation). This vaccine was supplied as a 5 ml have reported that both were strongly immunogenic in adults multidose vial, corresponding to ten vaccine doses. One dose and/or children [4,5]. (0.5 ml) contained 7.5 mg HA antigen. The vaccine vials were The generation of neutralising antibodies against antigenic sites stored at 2–8uC and used within 3 hours following opening of the on the HA glycoprotein of the influenza virus (as assessed by HA vial. inhibition assay or microneutralisation assay) is regarded as the criterion for evaluating immunity to influenza viruses and is Study design believed to constitute the main correlate of protection [5,6,7]. Inbred large white pigs (Babraham line) were conventionally Although cell-mediated immunity also correlates with the rate of reared at the Institute for Animal Health (Compton, UK), with viral clearance and protection of the respiratory tract after ages ranging from three to four months and weighing 15–29 kg at challenge with infectious influenza viruses [8], cellular-mediated the initiation of the study. Prior to the study, all pigs were bled and immune responses have not been assessed following vaccination shown by ELISA to be negative for anti-influenza A virus with the A(H1N1)pdm/09 vaccines and only limited data is antibodies in the serum (i.e. not previously exposed to influenza A available on the cellular-mediated immune responses elicited by viruses). The pigs (three animals per group) were intramuscularly influenza vaccines in general [9]. injected in the neck with one of the two commercial Mice and ferrets are the most routinely used animal models for A(H1N1)pdm/09 influenza vaccines mentioned above (0.5 ml the study of influenza infections and in particular for the per pig). The vaccination regime was similar to that recommended evaluation of human influenza vaccines [10,11]. In contrast, the for adult humans: the adjuvanted split virion vaccine was pig is not currently considered as a major experimental model for administered only once, whereas the whole virion vaccine was influenza viruses, despite the fact that influenza viruses are administered twice (two doses three weeks apart). Another two pigs enzootic in pigs [12] and several studies show the pig as a valuable were mock-vaccinated, i.e. received a single intramuscular model to study human influenza viruses: human influenza viruses injection in the neck with 2.5 ml uninfected allantoic fluid do replicate to a similar level in both the upper and lower (corresponding to approximately 7.5 mg total egg protein) diluted respiratory tract explants of pigs, which exhibit a similar sialic acid in a mixture of 0.25 ml PBS and 0.25 ml adjuvant (emulsion vial receptor distribution and pattern of virus attachment to humans from the adjuvanted split virion vaccine) per pig.
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