The role of backyard poultry flocks in the epidemic of highly pathogenic avian influenza virus (H7N7) in the Netherlands in 2003

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Abstract

In recent years, outbreaks of highly pathogenic avian influenza (HPAI) viruses have caused the death of millions of poultry and of more than 200 humans worldwide. A proper understanding of the transmission dynamics and risk factors for epidemic spread of these viruses is key to devising effective control strategies. The aim of this study was to quantify the epidemiological contributions of backyard flocks using data from the H7N7 HPAI epidemic in the Netherlands in 2003. A dataset was constructed in which flocks in the affected area were classified as susceptible (S), infected but not yet infectious (E), infectious (I), and removed (R). The analyses were based on a two-type SEIR epidemic model, with the two types representing commercial poultry farms and backyard poultry flocks. The analyses were aimed at estimation of the susceptibility (g) and infectiousness (f) of backyard flocks relative to commercial farms. The results show that backyard flocks were considerably less susceptible to infection than commercial farms (gˆ=0.014;95%CI=0.00710.023), while estimates of the relative infectiousness of backyard flocks varied widely (0fˆ5). Our results indicate that, from an epidemiological perspective, backyard flocks played a marginal role in the outbreak of highly pathogenic avian influenza in the Netherlands in 2003.

Introduction

Highly pathogenic avian influenza (HPAI) is a devastating disease for poultry, causing high mortality rates and huge economic damage due to production losses and export bans (Alexander, 2000, Alexander, 2003, Henzler et al., 2003). Moreover, since the start of outbreaks of subtype H5N1 in South East Asia in 1997, the fear of a human influenza pandemic has arisen (e.g. Webby and Webster, 2003). Although the focus is currently on HPAI H5N1, outbreaks of other subtypes, mainly H7, have occurred in recent years (Alexander, 2007), for example in Italy (Capua et al., 2003), the Americas (OIE, 2003, Max et al., 2007), the Netherlands (Stegeman et al., 2004) and South Africa (OIE, 2003, Bowes et al., 2004).

Outbreaks of HPAI are usually controlled by measures such as culling of infected flocks to reduce virus output and pre-emptive depopulation of contiguous flocks, as for example during the H7N7 epidemic in The Netherlands in 2003 (Stegeman et al., 2004). This epidemic was successfully controlled, but only after the killing of 30 million birds and infection of 89 humans (Koopmans et al., 2004, Fouchier et al., 2004). The measures were applied to commercial holdings as well as to non-commercial backyard poultry flocks, which are generally assumed to be at risk for AI virus introduction from migratory birds or spill over from contiguous commercial flocks as hypothesized for example for Europe (e.g. Stegeman et al., 2004, Gilbert et al., 2006, Terregino et al., 2007), Nigeria (Ducatez et al., 2006), and Indonesia (Sedyaningsih et al., 2007).

Public opinion, however, turned against the massive pre-emptive culling of often healthy-poultry (Thomas et al., 2005). Especially the owners of small backyard flocks did not consider their poultry an important factor in the spread of HPAI virus and were strongly opposed pre-emptive culling of their flocks, which they considered to be in the interest of the commercial poultry sector only. They argued that because the size of backyard flocks was much smaller than commercial flocks the risk of virus introduction would also be much smaller (Refregier-Petton et al., 2001, Akey, 2003). Moreover, they mentioned that the housing systems of backyard poultry often did not have a forced ventilation system, and that there would be hardly any contact with commercial holdings (Thomas et al., 2005). Some even argued that backyard poultry would be intrinsically less susceptible than commercial poultry as the backyard flocks and commercial farms generally contain different breeds.

In contrast to the Dutch situation, backyard poultry is considered being an important source of spread and persistence of HPAI H5N1 in, for example, South East Asia. In Thailand, for instance, 83% of the total outbreaks concerned backyard chickens and free-grazing ducks (Tiensin et al., 2005). As the animal husbandry systems differ substantially between countries, the question is whether this may also be valid for the Netherlands or other European countries.

During the Dutch H7N7 epidemic in 2003 unique data were collected for epidemiological studies about evaluation of control measures. So far, the analyses were restricted to data from commercial holdings (Stegeman et al., 2004, Thomas et al., 2005, Boender et al., 2007), whereas poultry on many premises were held in backyards. To gain more insight in the epidemiology of HPAI and to improve the control strategy for a future epidemic we provide a retrospective analysis of the epidemic of HPAI H7N7 in the Netherlands in 2003, with the goal to determine the actual role of backyard flocks in that epidemic. We carried out statistical analyses based on a stochastic epidemic model, which yield quantitative estimates of epidemiological parameters such as the transmissibility of HPAI virus, and the relative susceptibility and infectiousness of backyard flocks.

Section snippets

Study population

In the Netherlands, backyard hobby flocks were mainly kept outdoors in a confined space. The Dutch Ministry of Agriculture, Nature and Food Quality (LNV) defined a flock as hobby or backyard flock, when they consisted of fewer than 500 birds or did not have a unique farm number (LNV, 2003). The first outbreak with the H7N7 strain occurred in the central part of the Netherlands (the Gelderse Vallei), and later, the virus had spread to the province of Limburg (Stegeman et al., 2004). In the

Descriptive statistics

During and after the epidemic, 30 million birds were killed of which approximately 180,000 were kept in backyard flocks. The number of poultry in backyard flocks varied between 4 and 99 birds (LNV, 2003). Fig. 1 shows a map of the Gelderse Vallei and the approximate location of all commercial farms (n = 984), all infected commercial farms (n = 183), and all infected backyard flocks (n = 12) in the area. All premises were defined as being infected when HPAI virus strain H7N7 was isolated by RT-PCR.

Six

Discussion

Backyard poultry is considered a risk for becoming infected with AI virus (e.g. Sedyaningsih et al., 2007, Gilbert et al., 2006, Ducatez et al., 2006, Saad et al., 2007, Gall-Reculé et al., 2008, Lee et al., 2008), but their role in the spread of the virus during the epidemic in the Netherlands in 2003 was disputed. The aim of this study was to estimate the relative susceptibility and infectiousness of these flocks in comparison to commercial poultry farms. The relative susceptibility of

Conflict of interest statement

The authors do not have commercial or other relationships that might pose a conflict of interest.

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    This study was financed by the Netherlands Organisation for Scientific Research (NWO).

    1

    Current address: Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, The Netherlands.

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