Introduction

Since 1980, on average one new emerging infectious disease (EID) has appeared in humans every eight months [1] with the emergence of these pathogenic infectious diseases representing a substantial global threat to human health [2,3]. Research has found that of all EIDs, 60.3% are zoonoses originating in wildlife and these represent the most significant global health threat [4–6]. Examples of key recent EID outbreaks include Ebola haemorrhagic fever [5,7], SARS coronavirus [8], highly pathogenic avian influenza (HPAI) and most recently, avian influenza A H7N9 [9].

Since late 2003, highly pathogenic avian influenza virus (HPAI) strain H5N1 has been responsible for the deaths of millions of animals, primarily poultry taxa but also a range of other avian and mammalian species [9,10]. HPAI H5N1 has been reported in poultry from over 50 countries with 375 human deaths among 630 confirmed cases (59. 5 % confirmed case fatality risk) recorded in 12 of these countries as of 30 June 2013 [9,11]. The countries of Southeast Asia have been hardest hit by HPAI H5N1 with 2681 reported outbreaks in domestic poultry in Vietnam alone by 30 June 2013. In the first five months of 2013, 15 human fatalities have occurred in the 20 cases of HPAI H5N1 so far been reported in Cambodia, China and Egypt [11].

Approximately 80% of the Vietnamese population live in rural areas and almost 80% of these rural households participate in small-scale (backyard) poultry production [12]. The Red River and Mekong River deltas are major poultry producing areas from which poultry and their products (e.g. eggs, faeces, feathers) may be transported directly to the point of sale by the breeder or pass through a number of middle-men in the trade chain.

HPAI H5N1 spread rapidly from Southeast Asia into Europe and Africa. The main mechanism for HPAI spread is the movement of poultry and their products [13,14] however the modes of poultry-to-human transmission of this virus remain poorly understood [15]. Live poultry markets are acknowledged as a reservoir for the virus within the Southeast Asia region [14,16].

Here we take a technique, Hazard Analysis of Critical Control Points (HACCP) analysis [17] and apply it to HPAI viruses within Vietnam’s poultry trade system to explore the role that this approach may have in catalysing efforts to tackle emerging infectious disease outbreaks. We identify the key stages within the poultry trade chain which pose risks for the transmission of HPAI viruses in human and poultry populations. We then discuss the potential use of HACCP assessments as a rapid response tool during the early stages of emerging infectious disease outbreaks, as a precursor to more time-consuming quantitative data collection and biomedical testing.

Methods

The HACCP assessment of Vietnam’s domestic poultry trade followed the first three HACCP principles (described in Table 1) to address our aims [17]. The initial flow chart created during the first stage of the HACCP assessment (see Figure 1) was developed based on our long-term research of Vietnam’s poultry trade. The flow chart begins with a poultry egg and tracks all the possible routes that this egg could take through Vietnam’s domestic poultry trade. This flow chart was then presented to a range of experts for critical analysis; including public health professionals, epidemiologists and wildlife disease biologists. A hazard was considered to be a process within Vietnam’s poultry trade providing an opportunity, at an unacceptable level of risk, for the transmission of HPAI either from poultry-to-human or poultry-to-poultry. Based on the frequency with which these hazards occur, they were then grouped into categories of posing a high or low-risk to poultry and/or humans.

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Figure 1. Flow chart used during the Hazard Analysis of Critical Control Points assessment conducted for the domestic poultry trade within Vietnam.

https://doi.org/10.1371/journal.pone.0072279.g001

Following the validation of the flow chart, we referred to the team of experts again to determine appropriate Critical Control Points (CCPs). A CCP is a point in poultry trade which provides an opportunity to control, prevent or eliminate the risks for HPAI transmission. Each of these first two principles required cross-referencing outputs with existing literature on HPAI virus epidemiology within Vietnam’s poultry trade. We also referred to recent reviews of the scientific literature to identify any risks which the HACCP analysis failed to identify.

Critical limits were then set for each of the CCPs identified. These critical limits are thresholds used as preventative measures to control the hazards within the system. Setting the critical limits required prior research of both Vietnam’s domestic poultry trade and consumer behaviour.

Results

Discussion

Our HACCP assessment has identified poultry flock isolation as well as the transportation, slaughter, preparation and consumption of poultry as critical control points for HPAI H5N1 transmission in Vietnam’s domestic poultry trade. Critical limits at each of these control points are recommended to control the risks of HPAI transmission from poultry-to-poultry and from poultry-to-humans.

The scope of Vietnam’s poultry trade is far-reaching both geographically and across social classes. Rural Vietnamese households typically keep a few backyard poultry and are likely to consume these birds or birds from neighbouring flocks. In urban Vietnamese households, it is less common for poultry to be kept within the household and birds are typically purchased at local markets [18]. Typically, the live poultry trade is dominated by birds sold with no animal health certification and which have been produced under questionable hygiene conditions.

Poultry provides an important source of income as well as a low-cost protein source for many rural Vietnamese households [18]. The HPAI H5N1 epidemic has been both a public health and an economic problem for many Vietnamese people particularly the rural poor when pre-emptive culling has been one of key interventions against H5N1.

If the management of infectious zoonotic diseases is to be successfully implemented, controlling the transmission chain from infected to uninfected animals is essential [13]. Pathogen spread between rural poultry flocks may occur when these mix or birds are moved within live markets, communal vaccination centres or during transportation and fighting cock contests [19].

Incubation periods differ between chickens and ducks with reports of deaths occurring within one to five days for chickens and up to seven days for ducks [20]. As a result, at all stages, flocks which have mixed with other poultry flocks should undergo a week-long quarantine period, after which, asymptomatic birds can be released. It has been noted that transmission of HPAI H5N1 between poultry appears to have shifted from the faecal/oral route towards the respiratory route [13] which underlines the risks of mixing poultry flocks.

Poultry and its products are often transported in considerable numbers across large spatial scales. During transportation, HPAI material may be shed by infected individuals and lead to other poultry coming into contact with viral material. Consultation of published literature has shown that exposure to an environment contaminated with viral material (for example via soil, fomites, feathers, water etc.) can also pose a risk for viral transmission [21–23]. The mixing and movement of poultry through ‘wet’ markets (those selling live animals) is known to play an important role in the transmission and spread of HPAI viruses [16,24]. It has been reported that exposure to live poultry at wet markets increases human/ HPAI H5N1 exposure four-fold [25]. Within some wet bird markets such as those in Hong Kong, current successful control programmes for HPAI viruses incorporate ‘rest days’ whereby the markets are closed and poultry stalls cleaned [16]. Implementation of such a practice is recommended in Vietnam’s cities.

The H5N1 virus can survive in poultry carcasses kept at room temperature for several days or longer at cooler temperatures [26]. Human infection with the H5N1 virus is associated with recent exposure to live poultry [25], direct contact with dead poultry [27] and the preparation or cooking of sick or dead poultry [28–30]. As a result, poultry market workers and poultry slaughterers are at particular risk of human HPAI H5N1 infection [24].

Within Vietnamese households it is typical to consume the meat, eggs and organs of both chickens and ducks. The consumption of chicken and chicken products varies from that of ducks with regard to the parts consumed [31]. Uncooked duck blood is commonly consumed for special occasions, a practice that has been implicated in poultry to human HPAI transmission [21,28].

Exposure to hazards iii) and iv) will depend on the vaccination system employed and the suitability of the birds for cock-fighting. In some communes the Department of Animal Health (DAH) organises door-to-door vaccinations by local veterinarians. In more remote villages, the DAH organises communal vaccination days where households from several villages bring their poultry to one centralised location for vaccination. This latter vaccination system encourages the mixing of poultry flocks from different localities, promoting contact within poultry flocks, and given the time-lag before the HPAI H5N1 vaccine becomes effective, presents a high risk for the transmission of HPAI viruses. Door-to-door vaccinations ensure a lower risk of inter-flock viral transmission and are recommended. Should this approach prove impractical, the isolation of flocks whilst at the communal vaccination centre would limit the chances of inter-flock viral transmission. It is also noted that vaccination programmes are currently lacking any system of coordinated monitoring [13] which would reduce virus spread.

Fighting cock contests may play a role in the transmission of HPAI viruses to humans [14,28]. Fighting cocks are valuable possessions and owners may transport birds large distances to participate in bouts and even lick the wounds sustained by their fighting cocks [32]. This practice likely aids the geographic spread of HPAI viruses and is a risky activity for poultry to human HPAI transmission [9].

Although not highlighted by this HACCP analysis, the review of existing literature also identified the care of poultry as a risk factor for HPAI H5N1 viral transmission from poultry to humans [22].

Introducing the preventative measures highlighted by this HACCP evaluation should reduce the occurrence of HPAI outbreaks. The parallel findings of our rapid HACCP assessment with the existing literature cited, provides strong evidence for the potential that HACCP analyses may have as a framework for helping local personnel to formulate a rapid response to an emerging health threat. Indeed, because the involvement of local personnel is a critical aspect of the HACCP process, we would argue that the process not only identifies key critical control points and suggests control strategies but provides those local personnel with the knowledge, understanding and ownership to more reliably implement any identified control measures.

Acknowledgments

We thank the Centre for Natural Resources and Environmental Studies and the Wildlife Conservation Society in Hanoi for providing logistical support. We are also grateful to all those health and disease professionals who commented on the flow chart and hazard analysis aspects of this manuscript.