Biological Control and Spatial Ecology Lab: HPAI H5N1 Background

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MARCH 2010

Emerging infectious diseases and agriculture intensification

        Humans are today the dominant vertebrate species in the biosphere as measured in terms of biomass, population size and geographical range (Fowley 2003). Human biomass is exceeded among vertebrates by only that of total domesticated animals, with current standing populations of 4.7 billion ruminants, 19.1 billion poultry, and 0.98 billion pigs (FAOSTAT 2007). Humanity’s demographic shifts have come to offer an expanded niche for pathogen evolution and spread. Specifically, the evolution of the most important human pathogens is associated with major changes in the size, distribution and connectivity of human and domesticated animal populations (Wolfe et al. 2007, Diamond 2002). One such major shift took place following the industrial revolution and was associated with the “third epidemiological transition” (Barrett et al. 1998). Along with the biggest increase in human population, the 20th century marked a dramatically accelerated urbanization (from 13% living in cities in 1900 to 49% in 2005). The connectivity of these populations was considerably expanded through economic globalization and travel. In parallel, following the green revolution in crop production, a livestock revolution fundamentally changed the way livestock were raised and traded (Steinfeld 2004). The main features of the livestock revolution are i) a change in practices from local multi-purpose activity into market-oriented production and integrated processes, ii) a decreasing importance of ruminants compared to monogastric species (pigs, poultry), iii) more large-scale industrial production closer to urban consumption centres, iv) an increase in the use of cereal-based feed, and v) an increase in the volume of trade of live animals and animal products.

    Whilst epidemiological theory predicts that an increase in the number and connectivity of hosts should result in higher disease persistence and spread, the effects of those dramatic changes in human and animal populations were largely compensated by the rapid parallel developments in human and animal health, with the advent of vaccination, antibiotics, and investments in disease prevention. However, as the history of emerging diseases in the 20th century demonstrated, emerging pathogens are continuously evolving to adapt to these new patterns in human and animal populations (Antia 2003) and continuously challenge our ability to control them (Jones et al. 2008, Daszak et al. 2000).

    Most emerging infectious diseases have an animal origin (Cleaveland 2001), but thee primary sources are most often found in wildlife rather than domesticated animals (Jones et al. 2008). As a consequence, even if the livestock revolution induced a rapid shift in the population of domesticated animals, its impact on emerging infectious diseases has received comparatively little attention. For example, a search of the ISI database showed that out of 11 527 records for “emerging disease,” only 67 records were found in combination with “agriculture,” and only one with “agriculture” and “intensification.”

Avian influenza as an emerging zoonose

    The emergence of highly pathogenic avian influenza (HPAI) H5N1 virus provides perhaps the most spectacular example of how changes in the conditions of poultry production and trade have led to pathogens with panzootic and pandemic potential. Whilst the disease has had a dramatic if still limited impact as a zoonosis, its potential for adapting to human populations makes it one of the most important emerging infectious diseases circulating today in animal and human populations.

    Low pathogenic avian influenza (LPAI) viruses are abundant and diverse in wild avifauna (Stallknecht and Shane 1988). The intensification of agriculture and its encroachment on undisturbed landscapes have resulted in the reduction and fragmentation of natural habitats of wild birds (Bethke and Nudds 1995). In the particular case of wild waterfowl, reduced wetlands and their conversion into agriculture have resulted in an expanded interface between domestic poultry and wild waterfowl populations, enhancing the chances of mutual transmission of pathogens (e.g., Ackerman et al. 2006). Ducks and geese are raised in the highest densities throughout Asia in areas where irrigation allows multiple-cropping and where the birds can be fed on left-over grain following harvest or on farms where grains are cheap (Gilbert et al. 2007, Teo 2001). We previously demonstrated the key role these systems play in determining HPAI risk (Gilbert et al. 2008). Irrigated production systems intertwined with natural wetlands are numerous and widespread in several parts of Asia and favour the mutual transmission of AI viruses between domestic and wild birds.

    Once in domestic poultry, the evolution of LPAI viruses into highly pathogenic forms is favoured by the genetic homogeneity and higher disease susceptibility of poultry raised in intensive production systems (Ito et al. 2001). The emergence of HPAI H5N1 virus was traced back to southern China of the late nineties (Li et al. 2004, Vijaykrishna et al. 2008) when intensification of chicken and duck production was underway at a rapid pace (Fig. 1). H5N1 became seasonally endemic in chicken, duck and geese populations (Smith et al. 2006). With increased contact between domestic and wild avifauna, and increased trade of poultry and poultry products, the rapid spread of HPAI H5N1 virus resulted from the virus’s ability to exploit multiple modes of transmission (Kilpatrick et al. 2006, Vijaykrishna et al. 2008).

Fig. 1. Increase in duck meat production 1961-2005 (FAO 2006), highlighting that the increase in duck production in China outperforms all other countries in the region (click on the figure to enlarge)



        Undoubtedly, trade of live poultry or poultry products constitutes an important transmission mechanism over short-distances (Sims 2007, Sims 2005), and may have also been implicated in a number of long-distance introductions. But it also became clear that the virus was able to infect and become vectored by wild birds of the Anatidae family (ducks, geese and swans), a notion now supported by laboratory results showing subclinical infection in migratory ducks, geese and swans (Keawcharoen et al. 2008, Brown et al. 2008).

        On the other hand, agricultural intensification also implies higher investment in animal health, such as implementation of better bio-security practices, confinement of raised animals, and use of vaccination and disease prevention methods to prevent pathogen circulation. For this reason, HPAI can not really be seen as an emerging human disease in high-income countries where production is homogeneously industrialized and where resources have been sufficiently deployed to rapidly control HPAI outbreaks in the absence of repeated introductions (e.g., the 2003 HPAI epidemic in Netherlands and Belgium) (van den Berg and Houdart 2008). Rather, high disease circulation is expected in situations where strong unbalances are observed in the conditions of poultry production and trade, where an entire gradient of intensification of poultry production is observed, and where multiple-species production systems associating chickens and ducks promote disease persistence (Gilbert et al. 2008). In conditions of widespread disease circulation in poultry, poverty, low sanitary living conditions and high exposure of people to live poultry combine to increase the number of transmission events into human populations, and with it the risk of a more human-specific pathogen.

        In summary, the global ecology of HPAI takes place in a complex mosaic of countries connected by trade and wild bird migration, with each country hosting distinct mixtures of levels of agricultural intensification and environmental conditions that ultimately determine the course of local disease introduction, spread, persistence and evolution. Those conditions are not static and have evolved through recent times (Fig. 2) and will likely still evolve in the future at a very rapid pace.

Fig. 2. Changes in poultry meat production output/input (OI) and agricultural population density (Agpd) from 1961 to 2001, for the most important poultry producers (FAO 2006). Chicken production Output/Input is an indicator of production intensity and represent the number of kg of meat one can produced by chicken through cumulated production cycles. Agricultural population density is an indicator of small holders density. The plot illustrates that in China, agricultural population grew faster than increases in productivity, hence leading to a situation where a high density of smallholders co-exists with medium to large poultry production units (click on the figure to enlarge)

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