The transmission of H5 and H7 low pathogenic avian influenza viruses

2014 
Avian influenza viruses (AIVs) are a diverse group of viruses that are a major global threat to the poultry industry. To date, 16 HA and 9 NA subtypes of avian influenza have been observed in birds. Most of these subtypes cause no or only mild disease in poultry and are therefore classified as low pathogenic avian influenza viruses (LPAIVs). However, as a result of mutations, LPAIVs belonging to the H5 or H7 subtypes (LPNAIVs) may evolve into a highly pathogenic avian influenza virus (HPAIV) when they are circulating in poultry. Since these HPAIVs cause severe sickness and mortality in poultry and are able to spread rapidly, such an outbreak can wreak havoc among poultry holdings in a large region. In order to prevent the emergence of a HPAIV, it is important that LPNAI outbreaks in poultry are detected as soon as possible and that control measures can be applied before the virus has the opportunity to become widespread. In order to achieve this, active surveillance programs directed towards an early detection of LPNAIV in poultry holdings are established. It is believed that focusing the current active surveillance programs on those sectors of the poultry industry that are more susceptible to a LPNAIV infection, would lead to an earlier detection of LPNAIV. To this end, it is necessary that those factors that determine whether a poultry holding is at increased risk for infection with LPNAIV are identified. In this thesis, transmission experiments were designed to identify and study some putative risk factors for LPNAIV infection in poultry holdings. In a first series of transmission experiments (Chapter 3), the transmission of three LPNAIVs between SPF chickens was studied. A H5N2 LPAIV, which had been isolated from chickens and a H7N1 LPAIV which had also been isolated from chickens, were found to be highly infectious and transmissible to SPF chickens. In contrary, a H5N3 LPAIV that had been isolated from wild ducks proved to be low infectious to SPF chickens and was not transmitted between them. It was additionally examined whether keeping chickens in cage or barn housing could influence the transmission of LPNAIV. To achieve this, differences in virus transmission were studied between SPF chickens housed on a grid (to simulate housing in enriched cages) and SPF chickens housed on a floor covered with wood shavings (to simulate floor-based housing). The obtained results suggest that the transmission of LPNAIVs may be slightly enhanced by the accumulation of fecal matter as it occurs in floor-based housing systems. However, no large impact was observed. In order to decide whether this factor should be regarded as a risk factor and be included in the active LPNAI surveillance programs, further investigation should be conducted. This could be realized by conducting additional transmission experiments or by conducting an epidemiological study looking for a relationship between LPNAI outbreaks and the type of housing system. A second set of transmission experiments (Chapter 4) was dedicated to the investigation of the transmission of LPNAIVs between ducks and chickens. In these experiments, the transmission of the duck originated H5N3 LPAIV that was also used in chapter 3 was investigated between pekin ducks and SPF chickens. Despite this virus was previously found to be low infectious to SPF chickens, it was found to be efficiently transmitted from pekin ducks to SPF chickens, suggesting that this virus can be efficiently introduced in chicken farms if contact with wild waterfowl is possible. Additionally, from experiments with a special setting, it was suggested that drinking water that is fecally contaminated by visiting waterfowl may be one of the most important fomites by which LPNAIVs are introduced to poultry holdings. From these results, it can be suggested that the risk of a wild bird originated LPNAIV becoming established in poultry is only realistic if the virus itself has a high infectious potential to poultry. Indeed, our results suggest that, despite the fact that they can be relatively easily introduced, a LPNAIV with a low infectious potential to chickens has a significant risk of dying out spontaneously when it is introduced in an all-chicken population. On the other hand, in mixed poultry farms where contact between domestic waterfowl and gallinaceous poultry is possible, these low infectious LPNAIVs may be of a bigger problem; It is possible that such a LPNAIV can circulate among the holding’s waterfowl and can then be repeatedly passed on to the chickens. This would theoretically enable the virus to adapt to chickens, which means that these mixed poultry holdings can act as a bridge for the virus to cross the species barrier from its natural host to gallinaceous poultry. In a third study (Chapter 5); it was evaluated if transmission of the H5N2 and H7N1 LPAIVs used in chapter 3 still occurs when a more natural infection pressure is used. Indeed, it is often assumed that the inoculation of animals, as carried out in standard transmission experiments, may lead to a higher infectivity and thus to an artificially enhanced transmission. Extended transmission experiments in which susceptible SPF chickens were exposed to naturally infected SPF chickens were carried out. For the H5N2 LPAIV, it was observed that the reproduction ratio was similar to the one obtained in chapter 3. This suggests a similar infectivity for naturally infected SPF chickens as for inoculated SPF chickens, at least for this virus. Unfortunately, for the H7N1 LPAIV, no conclusions could be drawn; naturally infected SPF chickens could not be obtained, most likely due to problems in the design of the experiment. In a final study (Chapter 6), the multispecies NP-ELISA kit that was used throughout the thesis for the determination of infection was compared with other commercially available multispecies NP-ELISA kits. A selection of chicken and duck sera from the transmission experiments (chapter 3 and 4) were analyzed and results were compared. As these kits are also widely used in the active surveillance of LPNAIV in wild waterfowl, some additional field sera from wild geese, swans and ducks were included. The results suggest that the currently available commercial multispecies NP-ELISA kits perform equivalent for the analysis of chicken sera, and that they are most probably more sensitive than the current standard, the HI test. For wild bird sera however, a high degree of inconsistency between the different kits was observed. This indicates that, whilst the currently available commercial multispecies NP-ELISA kits are reliable for the active LPNAI surveillance in chickens, they can give unreliable results for wild bird sera. Hence, either these kits need to be better calibrated for the use in these species, or more reliable alternatives need to be investigated.
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