Anthropogenic factors and societal response to challenges in the transmission of highly pathogenic avian influenza A (H5N1)

Abstract

Research suggested that human infection with the novel avian influenza virus might be derived from live poultry markets. The sale of freshly slaughtered poultry, live poultry transportation, and mixed trading of different domestic animals in the live poultry markets all provide environments conducive to genome segment reassortment, gene mutation, and interspecies transmission of avian influenza virus. Production methods, human lifestyle, and the earth environment have been dramatically altered owning to rapid expansion of cities, industrialization, transportation, and accelerated population growth, in contrast to preserving traditional culture. People are exposed to the double burden of continued increasing incidence and mortality of the disease. In response to the huge challenge in the transmission of the disease, especially to prevent the spread of future avian influenza outbreaks, changing lifestyle and production habit should partly control the spread of the infections such as temporally closing live poultry markets, together with efforts to control the movement of illegal poultry products and wild birds. It is anticipated that by constantly seeking better solutions new models of living and development throughout society will gradually come into being.

Keywords:

• H5N1
• global trade
• anthropogenic factors
• economic loss
• live poultry markets

1. Introduction

After emerging in Asia in 1996, the highly pathogenic avian influenza (HPAI) H5N1 virus spread to Europe, the Middle East, and Africa, causing unprecedented epidemics and major economic losses (Li et al. 2004; Li, Jiang, and Xu 2014; Liang et al. 2010). Despite the low transmissibility of HPAI H5N1 from humans to humans, the high fatality rate reported in humans after the onset of the epidemic and the potential for H5N1 to become pandemic raised serious concerns (Webster and Govorkova 2006). The HPAI H5N1 virus has been able to maintain itself and spread in the poultry population in Asia (Wang et al. 2013), as well as periodically re-emerge. To determine the risk factors involved in the spread of H5N1 in poultry and to identify high-risk anthropogenic environments are critical to disease control as they would enable control measures to be targeted and surveillance to be strengthened (Jiang et al. 2014).

Live poultry markets (LPMs) is considered as the main driver in the maintenance of the virus in Asia (Zhang et al. 2014), and the movement of poultry within trade chains may have facilitated the spread of the HPAI H5N1 virus. Research suggests that the spread of HPAI H5N1 is influenced primarily by human activities related to poultry production and poultry trading (Kilpatrick et al. 2006; Wu et al. 2014). The global spread of H5N1 virus is not by chance, as without global trade the high fatality rate associated with HPAI H5N1 would remain localized. Paying special attention to the epidemic area is necessary; however, there are still many regulations of the transmission mode of carrier and host that need to be explored, and the mechanism of virus movement is still unclear. To explore the virus movement among the epidemic area will ultimately help prevent further spreading of HPAI H5N1. However, the respective roles of these pathways at the global or national scale are still unclear (Normile 2005).

We extend the discussion to risk factors associated with anthropogenic environments that may contribute to the prevalence of the H5N1 epidemics. We review the contribution by LPMs – small holder farms – factories systems on local H5N1 persistence and transmission, and highlight the influences of global trade on the spread of H5N1 virus.

2. Anthropogenic environment

Anthropogenic environmental changes, in human habitat, production habits, and human agro-ecological conditions, are considered fundamental drivers for H5N1 persistence and evolution (Gilbert et al. 2008). Paul et al. investigated the anthropogenic factors involved in the risk of HPAI in Thailand during the ‘second wave’ of the epidemic (Paul et al. 2010). The authors demonstrated that densely populated areas, short distances to a highway junction, and short distances to large cities were significantly associated with the risk of HPAI. Loth et al. identified three anthropogenic risk factors associated with HPAI H5N1 outbreaks in Bangladesh: the quadratic log-transformation of human population density, the log-transformation of the total commercial poultry population, and the number of roads per sub-district (Loth et al. 2010). Rivas et al. showed that H5N1 epidemic dispersal benefited from the highway network in Nigeria with 20% of all cases located <5 km from the nearest major road and 57% of all cases located ≤31 km from three highway intersections (Rivas et al. 2010). Village H5N1 outbreak risk was associated with villages being <5 km from a major road in Romania (Ward et al. 2008), and the minimal distance to the nearest national highway was considered an important predictive environmental variable for H5N1 risk in Mainland China (Fang et al. 2008). Anthropogenic environment was then considered to be associated with H5N1 influenza epidemic.

The persistence of HPAI H5N1, in circulation and in repeated outbreaks, is the result of conflict between traditional production habits and the intensive production system (Vandegrift et al. 2010). The combined effects of low biosecurity habits with intensive production ensure the safety of all poultry, domestic birds, and wild birds are placed at risk. Hogerwerf et al. investigated agro-ecological conditions associated with HPAI H5N1 persistence, identifying risk factors and assessing the impact of these conditions on HPAI H5N1 epidemiology on a global scale. Their findings suggest that some agro-ecologies were more capable of supporting HPAI H5N1 persistence than others (Hogerwerf et al. 2010). Martin et al. used outbreak data and risk-based surveillance to confirm correlations between HPAI infection in China and seven risk variables (chicken, domestic waterfowl population density, proportion of land covered by rice or surface water, cropping intensity, elevation, and human population density) (Martin et al. 2011). Several agricultural production factors, including sweet potato yield and increased buffalo density, as well as increased electricity supply, were associated with a decreased risk of HPAI outbreaks in Vietnam (Henning, Pfeiffer, and Vu 2009). In Thailand, free-grazing ducks could be brought to rice post-harvest fields in numbers as high as 4000 birds/ha, and rotated every two days or so, often by means of a truck (Gilbert et al. 2007). Cecchi et al. reported that farming landscapes with significant numbers of domestic ducks may have helped to bridge the geographical and ecological gap between waterfowl in the wetlands and the densely populated poultry-rich states (Cecchi et al. 2008). The Hadejia-Nguru wetlands in northern Nigeria, for example, sustain a dense human population and are characterized by intense and complex land-use patterns, which provide an ideal meeting place for wild and domestic waterfowl (Thompson and Polet 2000). A similar situation occurs in China, where local villagers release domestic birds onto Poyang Lake, bringing them into contact with wild birds and their habitat. Serological evidence showed that H7, H5, and H9 avian influenza virus (AIV) might coexist among birds in a city park in Jiangxi, China, and its neighbouring LPMs (Wang, Liu, et al. 2014; Wang, Zhang, et al. 2014). Lake sediment and duck faeces may act as a long-term source of influenza viruses in the aquatic habitat, allowing persistence of viruses in the environment over winter (Nazir et al. 2011). Traditional production habits play an important role in the persistence of HPAI H5N1, especially in Asia countries.

3. Local transmission networks

LPMs play an important role in the dynamics of H5N1 virus transmission and evolution in Southeast Asia (Mounts et al. 1999). Poultry from different geographical areas are introduced to the unsanitary environment of LPMs and are at high risk of exposure to infected poultry or of introducing disease themselves. Although LPMs are usually the ‘dead end’ for poultry (with most birds being slaughtered), the same cannot be said for virus transmission (Peiris, De Jong, and Guan 2007). High-density clustering of birds in LPMs has the potential to facilitate reassortment between viruses (Liu et al. 2003; Webster 2004; Cardona, Yee, and Carpenter 2009). LPM birds are usually confined to stacked cages, and AIV transmission generally occurs via indirect contact, such as aerosol and faecal exposure (Yee et al. 2009). Moreover, indirect exposures via contaminated fomites such as gloves, aprons, and rubber boots worn by LPM employees are also responsible for the spread of AIV (Tiwari et al. 2006). The transportation of infected birds to remote geographical locations also spreads the contagion (Soares Magalhães et al. 2010; Peiris, De Jong, and Guan 2007). AIV surveillance in Hong Kong SAR, Mainland China, Korea, Vietnam, Bangladesh, and Thailand reported significant detection rates of H5N1 virus (Lee et al. 2010; Liu et al. 2003; Bulaga et al. 2003; Nguyen et al. 2005; Amonsin et al. 2008; Wang et al. 2006). A virological survey of 10 LPMs in Hanoi showed that the HPAI H5N1 virus was circulating in healthy geese as early as 2001 (Nguyen et al. 2005). Similar surveillance programmes in central Thailand during July 2006–August 2007 indicated that influenza virus subtype H5N1 was detected only during winter and that the virus was genetically related to strains circulating in Thailand during 2004–2005 (Amonsin et al. 2008). LPMs have a pivotal role during the emergence of a novel influenza virus of avian origin.

The bidirectional movement of poultry between small holder farms and LPMs provides further opportunity for virus spread (Vallée et al. 2013). In some countries, the situation is further complicated by the presence of middlemen, connecting small holder farms with LPMs and the wider market. Middlemen and market sellers transport poultry on unenclosed trucks and motorbikes to markets, semi-commercial farms and stock houses, implicating vehicles and transportation methods as another mode of virus spread between villages and markets (Van Kerkhove et al. 2009; Soares Magalhães et al. 2010). Moreover, animal stress during transport has been reported to increase pathogen shedding (Ramesh et al. 2003). Virus spread also occurs with the movement of poultry, personnel, and equipment between farms (Johnson 1984; King 1984), and parasite may transmit through intense inter-village connectivity (Xu et al. 2006). The poultry trade between small holder farms was shown to have a higher risk of HPAI H5N1 infection (Paul et al. 2011; Jiang et al. 2014), and household-to-household infection rates were greater than for between communes (Minh et al. 2011).

The close link between small holders and the industrial poultry system provides many opportunities for the former to act as virus reservoirs and facilitate virus evolution (Wang et al. 2013). The industry system is connected to small holder farms through markets, and market inputs include day-old chicks, feed, and veterinary services. It is difficult for small holder farms to detect and prevent virus spread from sources originating from industry systems. There is strong evidence to suggest that the movements of industry staff contribute to the spread of virus both on to and through farms (Alexander 2007). However, to date there have been few studies conducted on poultry movement between industry systems and small holder farms.

4. Global trade

The potential role of wild bird migration in spreading H5N1 into new geographic areas has been the focus of much debate (Tian et al. 2014). Migratory birds were considered to play important roles in the geographic spread of AIV and various zoonotic agents, HPAI H5N1 is rarely reported in living and healthy wild birds (Olsen et al. 2006). However, international trade involves the movement (‘migration’) of millions of poultry every day. International trade in merchandise has increased three- to fourfold over the period 1980–2000, with most of the increase occurring in Asia, where there was a fivefold increase in the value of exports (Sutherst 2004). International trade of live poultry has also been increasingly regulated or banned from some countries (Bruschke, Pittman, and Laddomada 2009). Over the past decade, European Union (EU) countries are estimated to have exported over 18 million live poultry and over 750,000 live swine to North America (UN ComTrade 2009). Owing to the large numbers of birds involved, the poultry trade can facilitate the rapid spread of H5N1, particularly for developing countries which have infrequent testing or quarantine, have less regulated trade, and are more susceptible to illegal trade. Authorities in Vietnam estimate that up to 70% of poultry that are illegally transported from China go undetected (Yee, Carpenter, and Cardona 2009).

The international wildlife trade is estimated to be a US$6 billion industry (Check 2004). With regard to the live animal trade, it is estimated that approximately 40,000 primates, 4 million birds, 640,000 reptiles, and 350 million tropical fish are traded globally each year (Karesh et al. 2005). However, precise estimates of the wildlife trade are problematic because much of it is conducted illegally through underground national and international networks (Fèvre et al. 2006). Karesh et al. estimated that tens of millions of wild animals are shipped each year, both regionally and from around the world, to East and Southeast Asia for food or for use in traditional medicine (Karesh et al. 2005). Inevitably, this must increase the likelihood of H5N1 being transported to other countries. Occasionally, wild birds exported as part of the extensive trade in pet birds (including the illegal trade) have been infected with HPAI H5N1 virus, promoting the dissemination of virus both nationally and internationally (Sims et al. 2005; Peiris, De Jong, and Guan 2007). Millions of wild birds, mostly passerines for aviculture, are imported into Europe both legally and illegally from Asia (Broad, Mulliken, and Roe 2003). HPAI H5N1 was first detected in Europe in October 2004 in two Thai eagles illegally imported into Belgium from Thailand (Van Borm et al. 2005). The second incidence involved the deaths of captive caged birds imported from Taiwan and held in quarantine in England (Defra 2005). Kilpatrick et al. concluded that the H5N1 outbreaks in South Korea, Japan, Russia, Mongolia, Nigeria, India, Pakistan, and Cameroon were most likely attributed to the unreported or illegal trade of poultry, poultry products or wild birds (Kilpatrick et al. 2006). It is essential to pay more attention to the global wildlife trade, especially the illegal trade, which facilitates viral spread significantly.

Domestic ducks have been shown to excrete H5N1 for more than 2 weeks (Li et al. 2004), and Gauthier-Clerc et al. suggested that this would have allowed the virus to spread undiscovered over a vast zone, thanks to trade (Gauthier-Clerc, Lebarbenchon, and Thomas 2007). Gauthier-Clerc et al. also noted the extended absence of H5N1 during 2004–2007, following stringent trade control and surveillance in Taiwan, Japan, and South Korea. All the while, migratory birds continued to pass through these countries during spring and autumn (Gauthier-Clerc, Lebarbenchon, and Thomas 2007). Moreover, the H5N1 viruses isolated in Hanoi’s LPMs in 2005 were reported to be genetically related to virus isolated from Hong Kong in 1997 (Nguyen et al. 2005) and were genetically distinct from strains isolated in northern Vietnam in early 2004. These results suggest that the northern Vietnam outbreaks were most likely attributed to multiple introductions of virus primarily through transboundary trade with southern China (Wang et al. 2008). Human cases and domestic poultry outbreaks occur with greater frequency during traditional festivals. For example, most epidemic waves in Vietnam occur during the period of active poultry production immediately prior to the Vietnamese New Year (Tết festival) and wedding season (Minh et al. 2009). In Cambodia, significant increases in H5N1 outbreaks and poultry trade volume are reported during the weeks preceding the Chinese and Khmer New Year festivals (Van Kerkhove et al. 2009). In Hong Kong, yearly outbreaks have occurred in poultry since 2001, usually in the winter months, and coinciding with an increase in imported poultry to meet the demand due to Lunar New Year activities (Smith et al. 2006). In conclusion, human commercial activities, particularly those associated with poultry and wild bird trades, may play a major role in the global dispersal of H5N1.

5. Economic loss

The spread of the HPAI H5N1 virus and its persistence have resulted in enormous economic losses. Evidence suggests that H5N1 outbreaks were responsible for a significant decline in the scale of wild bird trade in Hanoi (Brooks-Moizer et al. 2010). The 2003–2004 H5N1 outbreak led to the culling of 45 million birds at an estimated cost of almost US$118 million to Vietnam (Rushton et al. 2005). Furthermore, the poultry export market was banned in Vietnam, Thailand, and Indonesia. Exports fell by 93% from US$597.6 million to US$43.5 million during the H5N1 outbreak in Thailand (FAO 2004). It was estimated that H5N1 outbreaks caused the deaths of 140 million domestic birds, with economic losses at US$10 billion by 2005 in Southeast Asia alone (FAO 2005). From 2003 to 2008, over 3.542 million poultry were destroyed in order to control epidemics in China (Chen 2009). Virus outbreaks in developing countries have devastating and far-reaching consequences, from family farms to the national economy.

An important issue is low biosecurity production systems and a lack of information, knowledge, and training towards HPAI-safe family poultry. This will cause high-level exposure to the H5N1 virus within poor and poorly educated settings across Southeast and East Asia (Liao et al. 2009). Model results indicate that the introduction of HPAI into EU member states through poultry trade is unlikely because of the stricter quarantine and biosecurity measures, early detection, and stamping out that are enforced in these countries (Sánchez-Vizcaíno et al. 2010). However, the exposure risk is the same for both developed and developing countries, with all production systems having experienced outbreaks (Sims 2008). Modelling studies of HPAI H5N1 outbreaks in Great Britain indicated that infection can cause large clusters of disease in areas with dense poultry flocks (Truscott et al. 2007). By 2009, H5N1 outbreaks had killed or forced the culling of more than 260 million birds and caused an estimated US$20 billion in economic losses across the globe (FAO 2010).

An increasing human population, high-density living, and the predominantly low economic status of developing countries may influence the spread of infectious diseases (Jones et al. 2008), affect many ecological and societal driving forces (Pimentel et al. 2007), and bring about changes in H5N1 persistence and transmission. Increases in human population growth coincide with increases in protein consumption. In developing countries, family poultry generates 19–50% of rural family income, comprises about 77% of the national flock, and contributes about 98% of poultry products consumed in villages (Sonaiya 2007). Therefore, family poultry is both an important income source and protein source in rural areas. Unfortunately, the effects of H5N1 outbreaks for many developing countries were far-reaching, affecting food production, poultry export, and the economy. Furthermore, H5N1 virus is detected not only in poultry meat but on eggs (on the shell and within) (Beato et al. 2007; Pantin-Jackwood et al. 2007; Li et al. 2006; Promkuntod, Antarasena, and Prommuang 2006; Beato, Capua, and Alexander 2009), and thus infection poses a risk of spreading and transmission through commodity (Swayne and Beck 2005), especially between regions in developing countries with low capacities to detect the virus.

6. Conclusions

The adage ‘a dime of prevention is better than a pound of treatment’ applies to HPAI H5N1 infections. HPAI H5N1 virus has an expanding host range and high natural variability, and if a capacity for efficient and sustained human-to-human transmission is attained, a pandemic with potential catastrophic consequences to human society could occur. Future prevention strategies should consider historical spatiotemporal patterns, probable transmission routes, and environments of virus persistence. What has been learned over the last decade is that there is no ‘one size fits all’ approach to this disease. Differences between developed and developing countries, production systems, and ecological and societal environments require the implementation of appropriate response and adaptation strategies specific for individual situations (Xu et al. 2013). The inclusion of vaccination and stamping-out strategies should take into consideration the impact of selection pressure on HPAI H5N1 virus evolution and the increasing inevitable side effort. Societal response to the challenges in the transmission of the virus would vary from developed countries to developing countries, from industrialized economies to self-sustained farming communities. The continued evolution, widespread transmission, and persistence of HPAI H5N1 virus are the result of conflict between traditional production habits and the intense poultry production industry. Thus, unless the fundamental drivers for H5N1 are identified, outbreaks will continue to occur and future pandemics would be inevitable.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported by the National Natural Science Foundation of China [grant number 41271099] and the Ministry of Science and Technology, China [grant numbers 2010CB530300, 2012CB955501, 2012AA12A407].