Elsevier

Vaccine

Volume 23, Issue 50, 30 December 2005, Pages 5743-5750
Vaccine

Highly pathogenic avian influenza (H7N7): Vaccination of zoo birds and transmission to non-poultry species

https://doi.org/10.1016/j.vaccine.2005.09.013Get rights and content

Abstract

In 2003 an outbreak of highly pathogenic avian influenza virus (H7N7) struck poultry in The Netherlands. A European Commission directive made vaccination of valuable species in zoo collections possible under strict conditions. We determined pre- and post-vaccination antibody titres in 211 birds by haemagglutination inhibition test as a measure of vaccine efficacy. After booster vaccination, 81.5% of vaccinated birds developed a titre of ≥40, while overall geometric mean titre (GMT) was 190 (95% CI: 144–251). Birds of the orders Anseriformes, Galliformes and Phoenicopteriformes showed higher GMT, and larger percentages developed titres ≥40 than those of the other orders. Antibody response decreased with increasing mean body weight in birds ≥1.5 kg body weight. In the vicinity of the outbreak, H7N7 was detected by RT-PCR in wild species (mallards and mute swans) kept in captivity together with infected poultry, illustrating the potential threat of transmission from poultry into other avian species, and the importance of protecting valuable avian species by means of vaccination.

Introduction

Avian influenza A virus (AIV) is a member of the Orthomyxoviridae family and can be classified according to the antigenicity of its surface proteins haemagglutinin (H) and neuraminidase (N), and on the basis of its pathogenicity in chickens. Highly pathogenic avian influenza (HPAI), an acute generalised disease in which mortality may be as high as 100%, is restricted to subtypes H5 and H7, although not all viruses of these subtypes necessarily cause HPAI. All other AIV strains are low pathogenic avian influenza (LPAI) virus strains and cause a much milder, primarily respiratory disease with loss of egg production [1].

The host range of AIV includes a large number of avian species [2], [3], [4], [5], with a worldwide distribution and variable morbidity per virus isolate and avian species [4], [5], [6], [7], [8], [9], [10]. Free-ranging bird species of the order Anseriformes (ducks, geese, swans and screamers) and Charadriiformes (shorebirds), are considered natural reservoirs in which morbidity is low [4], [11], [12]. HPAI outbreaks have generally been restricted to poultry (turkeys and chickens), and farmed ostriches [13], [14]. Exceptions, where HPAI outbreaks have been reported in free-ranging birds, have been in terns in 1961 [15], several species of wild migratory birds as well as captive Phoenicopteriformes (flamingos) in 2002 [16], [17], and in wild migratory birds in 2005 [18].

The Netherlands did not have an outbreak since 1927, but in March 2003 the diagnosis HPAI virus (H7N7) infection was made by RT-PCR [19], [20]. HPAI is categorised as an Office International des Epizooties (OIE) list A disease, for which the European Union (EU) has a non-vaccination policy. Eradication measures during an outbreak include confinement, stamping out of animals on the infected farm, pre-emptive culling of animals on neighbouring farms, and emergency vaccinations (EU Directive 92/40/EEC). The area of the outbreak expanded [21], and threatened to encroach on Dutch zoos. The Dutch Zoo Federation (Nederlandse vereniging van dierentuinen, NVD) proposed vaccination to avoid not only pre-emptive culling of the valuable and sometimes endangered species kept in zoo collections, but also confinement (of unknown duration) of birds, which they considered to be detrimental to welfare. Commission Decision 2003/291/EC of 25 April 2003 replaced the implementation of pre-emptive culling and confinement in zoos with the preventive vaccination of zoo bird species listed as susceptible to avian influenza: Galliformes (fowl, quail, pheasants), Anseriformes, Struthioniformes (emus, nandus and ostriches) and rock doves (Columba livia) kept for consumption, provided that far-reaching requirements were met.

Inactivated monovalent and polyvalent AIV water-in-oil emulsion vaccines have been demonstrated to be effective in reducing mortality and/or preventing morbidity, as well as reducing viral shedding [22] after HPAI virus challenge in chickens and turkeys [23]. The use of a heterologous vaccination (in which the N protein differs from the field strain) makes it possible to distinguish vaccinated birds from infected birds, while maintaining acceptable efficacy [24].

The goals of this study were to determine whether transmission of HPAI H7N7 virus from poultry to free-ranging birds during an outbreak occurred, to evaluate the efficacy and safety of an inactivated H7 vaccine in a large number of exotic avian species, and whether vaccination would be a suitable alternative to pre-emptive culling and confinement during future outbreaks of H7 HPAI virus.

Section snippets

Serology

An inactivated H7N1 vaccine, strain A/CK/Italy/473/99, inducing at least 4 log2 haemagglutination inhibition (HI) units according to potency test, with liquid paraffin adjuvant, (Nobilis influenza®, Intervet International, Boxmeer, the Netherlands) was used. The vaccine strain had a homology of 97.4% to the field strain on the basis of nucleotide sequence (1174 base pairs, excluding basic cleavage site), and 98.7% on the basis of amino acids. The vaccine was produced and assayed according to the

Serology

For 116 birds, GMT after first and second (booster) vaccination could be assessed. Overall, GMT after second vaccination [166 (95% CI: 117–237)] and percentage of birds with titre ≥40 (80.2%) were much higher than after first vaccination [20 (95% CI: 14–30) and 36.2%], demonstrating the need for booster vaccination. All but three birds (a domestic chicken, an emu and an Egyptian goose) had a pre-vaccination GMT <10. In the following text, titres after one vaccination are ignored, and only

Discussion

In the present paper, we have shown that H7 AIV vaccination of exotic birds with Nobilis influenza® is safe and is expected to be efficacious. We consider it to be useful and necessary in case of an outbreak, as transmission of H7N7 from poultry into non-poultry species did occur. Overall 81.5% of the birds tested developed to a titre ≥40, 30–60 days after the second vaccination (Fig. 1). Antibodies produced against the surface protein H act as major determinants for protection against

Acknowledgements

We would like to thank Intervet for supplying the vaccine free of charge, and the veterinarians and all other people involved in catching and handling the birds in the participating zoos: Apenheul Primate Park Apeldoorn, Artis Amsterdam Zoo, Beekse Bergen, Burger's Zoo, Dierenpark Amersfoort, Ouwehands dierenpark, Plaswijck park, Overloon Zoo Parc, Rotterdam Zoo, Wisselzoo Epe.

We are very grateful to the people from RVV Stroe, Woudenberg, municipalities in the infected area, Camping ‘de Lucht’,

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