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H5N1 HPAI in Different Species

3.3 Chickens and H5N1 HPAI

HPAI caused by Asian-lineage H5N1 viruses is one of the few diseases that is almost uniformly fatal for a particular species. In the case of chickens (Gallus domesticus) infected experimentally with these viruses by the intranasal or intravenous route, virtually all die rapidly (see for example Guan et al, 2002b). However, most experimental studies have used genetically-‘improved’ commercial chickens, with a few exceptions (notably some conducted in Hong Kong SAR which used local commercial Chinese breeds or cross-bred chickens).

There are a few anecdotal reports of chickens surviving infection in the field, although it is not clear whether these surviving birds were infected or merely exposed to the virus without subsequent development of infection. There are also some reports of small numbers of seropositive chickens in unvaccinated flocks. In one study from Viet Nam conducted one month after the last reported cases in the first wave of outbreaks in 2004 (and before introduction of vaccination), six percent of 379 chickens tested had antibodies to H5 virus, suggesting they had been exposed to an H5 virus and survived (Phuong et al, 2006). The possibility that this seroconversion was due to exposure to a low pathogenicity virus of the H5 subtype cannot be ruled out.

Chicken flocks probably do not remain infected with Asian-lineage H5N1 HPAI viruses for an extended period of time. In a commercial flock in which unvaccinated poultry are intensively reared, field experience suggests the virus will usually spread rapidly through the flock, especially if poultry are reared on litter at high stocking rates. In such cases, the virus will kill most poultry in the flock if the infection is allowed to run its course. This effect can be modified by the housing system. Observations in Hong Kong SAR during outbreaks in 2002 indicated that spread of disease in caged poultry was generally slower than for birds reared on litter (Sims, unpublished). One recent study using an H5N1 virus isolated from Japan in 2004 (Tsukamoto et al, 2007) compared the rates of transmission under experimental conditions and found that spread was enhanced if more birds were infected initially and that spread by contact was more efficient than aerosol spread. This supported the view that housing systems and stocking density influence the rate of spread. Surprisingly, a recent analysis and model of cases of HPAI caused by H7N7 viruses in the Netherlands did not find a significant difference between housing systems and rate of spread, contrary to expectations (Tiensin et al, 2007b)

3.3.1 Day-old chicks

Commercially produced day-old chicks are unlikely to be infected with H5N1 viruses when they leave the incubator given the limited likelihood that eggs from infected hens would hatch and the poor prospects for survival of exposed virus at 37oC in incubators. However, no experimental studies have been conducted using eggs contaminated or infected with H5N1 HPAI viruses to prove this and therefore this possibility cannot be ruled out (Brugh and Johnson, 1986).

This suggests that if day-old chicks are spreading disease this is more likely to be via contact with contaminated transport containers or through exposure to infection after hatching. This could be facilitated by management practices such as the sale of day-old chicks in live-poultry markets, the use of natural brooding (especially the use of surrogate poultry to brood and hatch eggs) and, as with day-old ducklings, the use of recycled transport containers or contaminated straw for packing and movement of chicks.

A report from Viet Nam (Delquiny et al, 2004) argued that introduction of two day-old broiler chicks may have been responsible for the introduction of virus to a village in which detailed investigations were carried out. It was not possible to determine whether this was due to the chicks or fomite transfer. Other articles describing the situation in 2006 in Nigeria (Brown, 2006) and in India (Grain, 2006) suggested that day-old chicks may have been responsible for introduction of infection but these claims were never verified by formal studies. If similar cases occur in the future these should be investigated thoroughly to assess whether these were the result of infected chicks and, if so, how they were infected.

Outbreaks of H5N1 HPAI on multi-age farms in Hong Kong SAR in 2002 appeared to spare young poultry (Sims et al, 2003). Although the reason for this was not established, in some parts of Asia day-old chicks would have maternal antibody because they are derived from vaccinated breeders, and this may have afforded some protection from infection or disease for the first few weeks of life.

3.3.2 Chicken eggs and fomites

Some outbreaks of avian influenza have been associated with transfer of virus by egg flats (Cardona, 2005; Power, 2005). Chicken eggs from infected hens can potentially contain virus but, because the clinical course of HPAI in chickens is extremely short, it is unlikely that many infected eggs enter market chains. A theoretical risk remains but there are no reported cases of human disease associated with consumption or handling of eggs. Surface contamination of eggs is also a possibility both for HPAI and LPAI unless eggs are cleaned or disinfected. Thus infected and at-risk countries need to implement measures to prevent eggs or contaminated egg flats from spreading virus. This requires regular disinfection of egg flats whenever they are returned to a farm.

3.3.3 Native chickens, commercial chickens and resistance to infection

It has been suggested that native chickens may be less susceptible to infection with H5N1 HPAI (and other) viruses (Grain, 2006) but so far no experimental studies supporting this suggestion have been conducted, and evidence from the field remains anecdotal.

Considerable natural variation in the resistance of poultry to diseases exists and the mechanisms involved have been reviewed elsewhere (Zekarias et al, 2002). It has also been proposed that poultry resistant to HPAI could be bred, possibly through the introduction of RNAi transgenes to breeding stock (O’Neill, 2007).

It is possible that advantages conferred through natural selection make native poultry more capable of surviving under harsh village conditions (Kitaliyi, 1998) but there is limited evidence so far to suggest that this has led to selection of chickens resistant to HPAI. The only published data available are provided in a study of dead and live poultry from infected flocks in Thailand in which certain MHC class 1 haplotypes appeared to be associated with survival. (Boonyanuwat et al, 2006). This work needs to be verified through laboratory-based experiments.

If resistance to H5N1 HPAI is present in native chickens it is unlikely that this is due to selection pressure arising from infection with H5N1 HPAI viruses. HPAI has been recorded rarely in the past and there are no reports of H5N1 HPAI in Asia before 1996. It may, however, occur through selection for innate resistance to other viral infections such as Newcastle disease that have caused severe disease in poultry for many years.

No systematic studies have been conducted to assess whether absence of disease in certain village flocks or parts of flocks in infected areas is due to resistance to infection/disease or to low stocking densities, which could result in some poultry avoiding exposure to virus. Even commercial chickens are resistant to infection if exposed to very low doses of virus below the infective dose (Swayne, 2006) and some poultry in infected flocks can escape infection when stocking densities are low.

Under experimental conditions, virtually all chickens exposed to an infectious dose of Asian-lineage H5N1 HPAI die. This includes ‘local’ Chinese breeds (or their crosses) of chicken such as those raised in Hong Kong SAR, as demonstrated by experimental infection and by the high level mortality in some naturally-infected commercial flocks of these birds (Sims et al, 2003; Ellis et al, 2006).

Short-lived broiler chickens have been bred for growth characteristics which appear to have reduced and modified both their humoral and cellular immune responses compared with slower growing layers. (Koenen et al, 2002). This may affect their response to avian influenza vaccination and subsequent resistance to infection. Anecdotal reports suggest that serological responses in fast growing broilers vaccinated with vaccines containing killed H5 antigen are inferior to those produced in layers but no formal studies have been published on this. Such a difference, if demonstrated, could influence control and preventive strategies for H5N1 HPAI in broiler flocks.

It has been suggested that the gene pool of native breeds is more diverse than that of western-style broilers and this potentially provides greater protection against disease. Some studies have shown that genetic diversity was low in inbred poultry such as certain fancy breeds but higher in non-commercial Asian populations, which correlated with the management of the population studied (Hillel et al, 2003; Granevitze et al, 2007). However, this does not provide a conclusive answer to the question of whether certain local breeds and varieties of chicken are more resistant to HPAI. This could also be confounded by the environment in which the poultry are reared, which will influence the level of viral challenge.

A number of recent articles have made the erroneous suggestion that village chickens live harmoniously with pathogens (see for example Grain, 2006). This does not reflect the high mortality seen in this production sector, much of which, in the past, was usually attributed to Newcastle disease (Johnston, 1990; Kitaliyi, 1998).

Nevertheless, some poultry do demonstrate some resistance to certain diseases (FAO, 1999) and no efforts should be spared in retaining genetic diversity of poultry to ensure that the special characteristics of native poultry and local breeds remain available. As will be discussed in Chapter 6, methods should be found to protect valuable breeding animals when stamping out H5N1 HPAI, as was done in Hong Kong SAR in 1997, allowing conservation of rare Chinese breeds in several uninfected flocks that would otherwise have been culled (Sims, unpublished). In addition, further work should be conducted to determine whether certain breeds display any natural resistance to infection or disease caused by Asian-lineage H5N1 HPAI viruses, including assessment of the role of specific variants of proteins such as Mx (Ko et al, 2002; Balkissoon et al, 2007) and MHC genotypes.

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