Host biology

The high natural body temperature of birds aids resistance to novel infections in some cases (e.g. bacterial and fungal infections), but may hasten the course of disease in others (e.g. viral infections) (Alexander, Reference Alexander1982; Causey and Edwards, Reference Causey and Edwards2008). In experimental studies, strains of the highly pathogenic H5N1 avian influenza viruses (HPAI H5N1) originating in Southeast Asia are reported to cause clinical disease and death in some wild bird species within several days of inoculation (Pasick et al., Reference Pasick, Berhane, Embury-Hyatt, Copps, Kehler, Handel, Babiuk, Hooper-McGrevy, Li, Mai Le and Lien Phuong2007; Brown et al., Reference Brown, Stallknecht and Swayne2008; Kalthoff et al., Reference Kalthoff, Breithaupt, Teifke, Globig, Harder, Mettenleiter and Beer2008). In most influenza infections in wild birds, primarily LPAI, disease is rare. Evolution of LPAI viruses in their natural hosts is slow, with little antigenic drift and a few amino acid changes. This suggests that the association between wild bird hosts and influenza viruses is quite ancient, and that immunologic pressure on the system is lacking (Webster et al., Reference Webster, Krauss, Hulse-Pose and Sturm-Ramirez2007).

The developing avian immune system transitions from B lymphocytes in the Bursa of Fabricius to the T lymphocyte system during or shortly after fledging (Causey and Edwards, Reference Causey and Edwards2008). This creates a period of immunologic vulnerability at a time when young birds are experiencing increased exposure to pathogens through dispersal or migration. Supporting this hypothesis is the finding that avian influenza virus prevalence rates in Anseriformes are higher among juvenile birds than adults. Also, on the population scale, prevalence rates in Anseriformes are higher during southward migration from the breeding grounds when the proportion of juvenile birds is greater (Webster et al., Reference Webster, Bean, Gorman, Chambers and Kawaoka1992; Wallensten et al., Reference Wallensten, Munster, Latorre-Margalef, Brytting, Elmberg, Fouchier, Fransson, Haemig, Karlsson, Lundkvist, Osterhaus, Stervander, Waldenström and Björn2007).

Population behavior

Annual cycles in the behavior of avian populations bring birds in and out of contact with each other. Aggregations of migratory birds occur at several locations throughout the year: migratory stop-over points, pre-migration staging areas, breeding grounds, wintering grounds, molting areas, and locations where immature birds spend the breeding season (Artois et al., Reference Artois, Bicout, Doctrinal, Fouchier, Gavier-Widen, Globig, Hagemeijer, Mundkur, Munster and Olsen2009). Arrival times at these locations and length of stay shift as a result of environmental conditions (Balbontín et al., Reference Balbontín, Møller, Hermosell, Marzal, Reviriego and de Lope2009); this in turn influences opportunities for virus transfer. Transmission of influenza viruses occurs at these aggregation sites via the fecal–oral route (Webster et al., 1992). Maintenance of the virus in the environment for variable lengths of time, especially in wetland environments, creates the opportunity for virus transmission between avian groups that do not actually share the site temporally (Brown et al., Reference Brown, Swayne, Cooper, Burns and Stallknecht2007, Reference Brown, Stallknecht and Swayne2008).

Feeding behaviors also influence influenza infection rates in wild birds. Avian influenza virus infections are detected more frequently in dabbling ducks than other Anseriformes species (Munster et al., 2007). During experimental infections with HPAI H5N1, groups with dabbling feeding behaviors exhibited high susceptibility to influenza infection but a few clinical signs, while divers tended to experience higher morbidity and mortality rates (Brown et al., Reference Brown, Stallknecht, Beck, Suarez and Swayne2006). Mallards have been the focus of many live bird avian influenza surveillance programs as a result. Like the mallard, the northern shoveler (Anas clypeata) has also demonstrated high LPAI infection rates among the duck species (Ferro et al., Reference Ferro, El-Attrache, Fang, Rollo, Jester, Merendino, Peterson and Lupiani2008). This species has a unique bill anatomy for filtering food particles from the water column; a behavior that may act to increase exposure to pathogens such as influenza viruses (Munster et al., Reference Munster, Baas, Lexmond, Waldenström, Wallensten, Fransson, Rimmelzwaan, Beyer, Schutten, Olsen, Osterhaus and Fouchier2007).

Migration patterns

Avian flight is highly economical and allows birds to cover vast distances. Migration is defined as the regular movement of individuals between breeding and wintering grounds and provides a mechanism to increase breeding success and exploit seasonally abundant food sources (Elphick et al., Reference Elphick, Dunning and Sibley2001; McKinnon et al., Reference McKinnon, Smith, Nol, Martin, Doyle, Abraham, Gilchrist, Morrison and Bêty2010). A bi-product of migration is the potential transportation of infectious diseases over both short and long distances. The documentation of LPAI in migrating waterfowl (Anseriformes), shorebird species (Charadriiformes), and land-birds demonstrates that avian hosts are capable of migration while infected (Koehler et al., Reference Koehler, Pearce, Flint, Franson and Ip2008; Peterson et al., Reference Peterson, Bush, Spackman, Swayne and Ip2008; Pearce et al., Reference Pearce, Ramey, Ip and Gill2010). In fact, influenza viruses are being used to help further define migration behaviors in shorebirds and northern pintails (Anas acuta) (Koehler et al., Reference Koehler, Pearce, Flint, Franson and Ip2008; Pearce et al., Reference Pearce, Ramey, Ip and Gill2009; Pearce et al., Reference Pearce, Ramey, Ip and Gill2010).

The role of wild birds in transporting influenza viruses during migration, especially in the case of HPAI viruses, remains complicated; no direct tests have been conducted to demonstrate the ability of wild birds to migrate while infected with HPAI. Correlations between migration patterns and expansion of HPAI H5N1 outbreaks from Asia into Europe and Africa suggest that wild birds infected with HPAI may be capable of long-distance migration (Gilbert et al., Reference Gilbert, Xiao, Domenech, Lubroth, Martin and Slingenbergh2006; Si et al., Reference Si, Skidmore, Wang, de Boer, Debba, Toxopeus, Li and Prins2009). Investigation of whooper swan (Cygnus cygnus) migration patterns in Mongolia through the use of GPS transmitters, however, demonstrated that despite the overlap of H5N1 outbreaks and whooper swan movements, it is unlikely that these birds are involved in long-distance transport of the viruses (Newman et al., Reference Newman, Iverson, Takekawa, Gilbert, Prosser, Batbayar, Natsagdorj and Douglas2009). The immunologic costs of migration are high and the impact influenza viruses have on fitness and migration success continues to be investigated (Weber and Stilianakis, Reference Weber and Stilianakis2007). Evidence in mallards (Anas platyrhynchos) and Bewick's swans (Cygnus columbianus bewickii) suggests that LPAI infection decreases body weight and feeding efficiency while increasing the frequency of stopovers during migration (van Gils et al., Reference van Gils, Munster, Radersma, Liefhebber, Fouchier and Klaassen2007; Latorre-Margalef et al., Reference Latorre-Margalef, Gunnarsson, Munster, Fouchier, Osterhaus, Elmberg, Olsen, Wallensten, Haemig, Fransson, Brudin and Waldenström2009).

Environmental degradation

Habitat fragmentation and diminished ecosystem functions have resulted in unprecedented levels of disease emergence (Tabor et al., Reference Tabor, Ostfeld, Poss, Dobson, Aguirre, Soule and Orians2001; Aguirre et al., Reference Aguirre, Ostfeld, Tabor, House and Pearl2002; Aguirre and Tabor, Reference Aguirre and Tabor2008). As an example, the relationship of human land-use activities with disease dynamics has been demonstrated for both West Nile virus (WNV) in birds, and Anaplasma phagocytophilum and Ehrlichia chaffiensis exposure in white-tailed deer (Gibbs et al., Reference Gibbs, Wimberly, Madden, Masour, Yabsley and Stallknecht2006; Manangan et al., Reference Manangan, Schweitzer, Nibbelink, Yabsley, Gibbs and Wimberly2007). When focusing more closely on those avian communities potentially involved in avian influenza transmission, it is evident that active destruction and modification of wetland environments for human use is impacting avian populations drastically, causing declines in bird numbers as well as species diversity (Kingsford and Thomas, Reference Kingsford and Thomas2004; Liu et al., Reference Liu, Zhang, Li, Lu and Yang2004).

Work specifically investigating the link between habitat fragmentation and avian influenza transmission patterns is limited. One example is found in the Hadajia-Nguru wetlands in Nigeria. This area illustrates how land-use patterns can intensify the interactions between wild birds and domestic poultry. There, agricultural activities include rice-farming, irrigation, and flood-recession agriculture. These anthropogenic changes in the ecosystem are combined with widespread domestic duck rearing under free-ranging conditions (Cecchi et al., Reference Cecchi, Ilemobade, Le Brun, Hogerwerf and Slingenbergh2008). Waterfowl there must compete with agricultural activities for wetland resources during their wintering season, heightening the opportunity for disease transmission between wild and domestic birds. In the Hadajia-Nguru area, outbreaks of HPAI H5N1 in poultry have occurred during the wintering season of both 2006 and 2007.

Decreased biodiversity has also been linked to heightened disease transmission in several disease systems. A study investigating the prevalence of Hantavirus in Panama illustrates the link between habitat fragmentation and decreased species diversity (Suzan et al., Reference Suzán, Marcé, Giermakowski, Armién, Pascale, Mills, Ceballos, Gómez, Aguirre, Salazar-Bravo, Armién, Parmenter and Yates2008). In this study, the researchers found that the prevalence of Hantavirus antibodies was higher in experimental plots from which species were successively removed as compared to control sites. Investigation into the effects of avian diversity on WNV infection demonstrated the dilution effect, in which greater avian host diversity was associated with a lower incidence of human disease (Swaddle and Calos, Reference Swaddle and Calos2008). Combined, habitat fragmentation and decreased biodiversity may serve to increase the potential of avian influenza exposure, amplification, and transmission.

Legal and illegal trade in wild birds

Legal and illegal trade in wild birds present a significant risk for introduction of exotic diseases. Live wild birds are in demand for consumption, for display in zoological parks, as pets, as prayer birds, and for falconry. Products derived from wild birds include hunting trophies, trinkets for tourists and collectors, artwork, and items for religious or spiritual purposes. Many countries face severe limitations on their capacity for inspection of legal avian importations and lack the necessary information on illegal importation routes to reduce the practice. Sparse legal expertise and few supporting laws for the investigation and prosecution of illegal bird trade exacerbate the problem.

Live bird markets for legal trade in domestic poultry (waterfowl as well as Galliformes) have been identified as prime locations for the maintenance and spread of both LPAI and HPAI (van den Berg, Reference van den Berg2009). These markets, especially those in Southeast Asia, often house both wild birds and poultry. This set-up provides a rich environment for exchange of viruses between the two bird groups. The market chains form a complicated web connecting urban centers with agricultural and natural areas. Birds that are not sold on a given day in the market may be taken to a holding facility for transfer to other areas or are returned to the same market on subsequent days; this provides further opportunity for virus exchange.

Prayer animal release, for which birds are primarily wild-caught and sold in bulk, is a fairly widespread practice in Southeast Asia (Severinghaus and Chi, Reference Severinghaus and Chi1999). These birds go through both legal and illegal channels for sale and are released in the thousands at individual events. Prayer birds are often exotic to the site of release and as a result have the opportunity to introduce infectious diseases to new areas. Released birds are highly stressed by capture, transport, and holding; this likely decreases immune resistance to infectious diseases present in the market chain. As evidence of this problem, H5N1 HPAI has been isolated from several bird species found dead in Hong Kong that are presumed to be prayer birds (species that are exotic to the area and are commonly released as prayer birds) (Promed Mail, 2007; Ellis et al., Reference Ellis, Dyrting, Wong, Chadwick, Chan, Chiang, Li, Li, Smith, Guan and Malik Peiris2009).

Illegal trade in live wild birds and bird products continues to occur globally. Reports describing capture of individuals as well as organized groups attempting to smuggle birds across borders are steady (van den Berg, Reference van den Berg2009). The extent of the problem is difficult to quantify due to the illicit nature of the trade and shifting preferences in desired species. Additionally, intercepted illegal importations of wild birds are not routinely tested for a battery of infectious diseases in some countries unless the animals show obvious clinical signs of disease. Wildlife diseases frequently fall through the regulatory cracks since agencies specializing in wildlife importation control often do not have disease expertise. A report on the carriage of two HPAI H5N1-infected crested eagle-hawks (Spizaetus nipalensis) on an airplane from Thailand into Belgium most likely represents the very tip of the iceberg (Van Borm et al., Reference Van Borm, Thomas, Hanquet, Lambrecht, Boschmans, Dupont, Decaestecker, Snacken and van den Berg2005).

Detecting exposure

In areas where HPAI H5N1 is enzootic, work has focused on describing the role of wild birds in the maintenance and transmission of the virus as well as defining the connection between wild birds and the poultry industry. Studies in Indonesia have compared virus shedding and antibody prevalence rates between captive, resident, and migratory birds on the island of Java; this work found that H5N1 exposure was significantly higher in the captive birds (Stoops et al., Reference Stoops, Barbara, Indrawan, Ibrahim, Petrus, Wijaya, Farzeli, Antonjaya, Sin, Hidayatullah, Kristanto, Tampubolon, Purnama, Supriatna, Burgess, Williams, Putnam, Tobias and Blair2009). In Mongolia, where outbreaks of H5N1 in wild birds have occurred in the absence of a large poultry industry, investigation into the phylogenetics of avian influenza viruses in wild birds identified a variety of LPAI viruses of European and Asian lineage, but no HPAI H5N1 (Spackman et al., Reference Spackman, McCracken, Winker and Swayne2009). Large-scale surveillance of waterbirds in western, northern, and eastern Africa found evidence that the tropical ecosystems in Africa provide the necessary environment for persistence and transmission of avian influenza viruses (Gaidet et al., Reference Gaidet, Dodman, Caron, Balança, Desvaux, Goutard, Cattoli, Lamarque, Hagemeijer and Monicat2007).

Risk modeling

Work in northeastern Africa and the Middle East has investigated the use of environmental niches as predictors of avian influenza case distribution and found that avian influenza viruses are most common within areas with a broad range of normalized difference vegetation index and in areas with seasonal variation (Williams and Peterson, Reference Williams and Peterson2009). Programs in the European Union are focused on wild bird species considered to be a high risk of introducing the virus to poultry holdings based on migratory routes and likelihood of interaction with poultry (Hesterberg et al., Reference Hesterberg, Harris, Stroud, Guberti, Busani, Pittman, Piazza, Cook and Brown2009). Studies in Great Britain have used spatial models combining wild bird movements and poultry farms to determine geographic areas at high risk of HPAI H5N1 incursion (Snow et al., Reference Snow, Newson, Musgrove, Cranswick, Crick and Wilesmith2007). The paucity of H5N1 cases in wild birds in Great Britain and the trace-back of recent H5N1 outbreaks in poultry to transfer within the industry have made it difficult to validate this work however.

Detection of incursion

In regions that have not yet experienced outbreaks of HPAI H5N1 Asian lineage, wild bird surveillance efforts for avian influenza have focused on introduction of HPAI H5N1 via migration and the ecology of LPAI within the wild bird populations. In North America, a strong emphasis has been placed on H5N1 incursion detection as an early warning system to alert the poultry and human health sectors (DOI, 2006). Surveillance in North America has targeted migratory bird populations which cross the Bering Strait, or those that comingle with avian species from Southeast Asia (DOI, 2006; Koehler et al., Reference Koehler, Pearce, Flint, Franson and Ip2008; Wahlgren et al., Reference Wahlgren, Waldenström, Sahlin, Haemig, Fanchier, Osterhaus, Pinhassi, Bonnedahl, Pisareva, Grundinin, Kiselev, Hernandez, Falk, Lundkvist and Olsen2008). Phylogenetic evaluation of viruses isolated from birds captured in the areas on both sides of the Bering Strait identified North American and Eurasian lineages (Wahlgren et al., Reference Wahlgren, Waldenström, Sahlin, Haemig, Fanchier, Osterhaus, Pinhassi, Bonnedahl, Pisareva, Grundinin, Kiselev, Hernandez, Falk, Lundkvist and Olsen2009). Whole-genome analysis of LPAI isolates from northern pintails (A. acuta) captured in Alaska revealed that nearly half of the isolates had at least one gene segment that was more closely related to Asian than North American LPAI (Koehler et al., Reference Koehler, Pearce, Flint, Franson and Ip2008).

In South America, wild bird involvement in avian influenza transmission has been investigated in Argentina, Chile, and Bolivia to further describe avian influenza ecology on the continent and provide an early warning system in the event of HPAI H5N1 introduction (Spackman et al., 2006; Hanson et al., Reference Hanson, Luttrell, Goekjian, Niles, Swayne, Senne and Stallknecht2008; Pereda et al., Reference Pereda, Uhart, Perez, Zaccagnini, La Sala, Decarre, Goijaman, Solari, Suarez, Craig, Vagnozzi, König, Terrera, Kalognlian, Song, Sorrell and Perez2008). Evidence of localized evolution of influenza viruses in Argentina was countered by the finding in Bolivia of viruses with gene segments most closely related to North American wild bird isolates. Natural movements of Anseriformes between Asia and Australia are very limited, and as a result the risk of wild bird introduction of HPAI H5N1 to the Australian continent is considered low; however, a wild bird surveillance program has been put in place for early detection (Arzey, Reference Arzey2007). Australia's program includes mortality investigation, live-bird testing in ducks and shorebirds, and testing of avian species in zoo collections (AUSVETPLAN, 2009). This work has revealed that LPAI prevalence within the population is low (1.0%); however, LPAI H5 and H7 subtypes were identified (Haynes et al., Reference Haynes, Arzey, Bell, Buchanan, Burgess, Cronan, Dickason, Field, Gibbs, Hansbro, Hollingsworth, Hurt, Kirkland, McCracken, O'Connor, Tracey, Wallner, Warner, Woods and Bunn2009). Avian influenza positives in this study coincided with the arrival of migrants and the breeding season.

Evaluation of surveillance techniques

Several techniques for sampling wild birds for influenza viruses have been applied: targeted testing of live birds considered to be high risk, sampling of hunter-killed birds (waterfowl and shorebirds in some areas), dead bird surveillance, placement and regular testing of sentinel birds, sampling of wild birds in live bird markets, and environmental sampling. Benefits, problems, and biases exist for each method. Dead bird surveillance detection is strongly influenced by carcass scavenging, the rate of decomposition, and efficiency of carcass searching (Prosser et al., Reference Prosser, Nattrass and Prosser2008). Sentinel bird testing for avian influenza viruses yielded a variety of LPAI subtypes in Germany, Switzerland, and Austria; however, HPAI H5N1 was not detected despite its circulation in the area the previous year (Globig et al., Reference Globig, Baumer, Nevilla-Fernández, Beer, Wodak and Fink2009). Live bird surveillance is influenced by a host of factors including the timing of wild bird movements, alignment of collections with capture operations for other activities such as banding, the method of capture, and the species of focus. In Europe, HPAI H5N1 was found in live sampled wild birds only very rarely; active surveillance of apparently healthy birds is therefore not seen as an efficient method for early detection of the virus (Artois et al., Reference Artois, Bicout, Doctrinal, Fouchier, Gavier-Widen, Globig, Hagemeijer, Mundkur, Munster and Olsen2009).

A study conducted on the efficiency of live bird avian influenza surveillance in Germany illustrates the difficulty in maintaining a strong surveillance effort (Wilking et al., Reference Wilking, Ziller, Staubach, Globig, Harder and Conraths2009). In this work, assessment of the monitoring program demonstrated that confidence in prevalence estimates decreased after the initial intensity of surveillance, and also fell as a result of species and geographic bias. Statistical evaluation of this work found that sample numbers would need to be increased by four-fold from existing levels to exclude infections below 1% prevalence in the population (Wilking et al., Reference Wilking, Ziller, Staubach, Globig, Harder and Conraths2009). Maintaining such a high level of surveillance over an extended period of time is in most cases cost prohibitive.