Role of Migratory Birds in Spreading Influenza Viruses



Fig. 6.1
Role of migratory birds in transmission of avian influenza virus in poultry



Wild birds are well-known reservoirs of most influenza A virus, although there is doubt regarding the extent of involvement (Reid and Taubenberger 2003; FAO 2007; Krauss and Webster 2010; Herrick et al. 2013; Kuiken 2013), the most recent well known pandemic strain, i.e. H1N1, contains several segments originating most likely from migratory birds (Fraser et al. 2009; Horby et al. 2012; Runstadler et al. 2013). Thus, the dynamics of infections due to influenza viruses among migratory wild birds and mammals are closely concurrent (Vandegrift et al. 2010). Surveillance for avian influenza in wild birds has been in operation in many countries of the world. Active surveillance for AIVs is done to get information on potential LPAI viruses that can become highly pathogenic in poultry. Passive surveillance on dead birds is useful in detecting HPAI viruses such as H5N1 subtypes in wild birds (Gaidet et al. 2007; Munster et al. 2007; Fouchier and Munster 2009; Hesterberg et al. 2009; Breed et al. 2010, 2012; Dugan 2012; Feare 2010; Knight-Jones et al. 2010; Tracey 2010; Alba et al. 2012; Hénaux et al. 2013; Schoene et al. 2013).

There is increased chance of contact infection to domestic birds in a particular geographical location due to congregations of migratory waterfowl. Waterfowl and shorebirds are considered to be the important reservoirs for most of the subtypes of AIV (H1-H16 and N1-N9) (Liu et al. 2004, 2005; Chen et al. 2005; Sengupta et al. 2007; Lee et al. 2008, Musa et al. 2009; Abbas et al. 2011; Galsworthy et al. 2011; Soliman et al. 2012; Gaidet et al. 2012a, b; Brown et al. 2012; Hill et al. 2012a, b; Lam et al. 2012; Lu et al. 2013), and may have important role in its transmission as well as ecology (Gonzalez-Reiche et al. 2012; Parry 2013). However, most of the circulating AIVs among migratory birds belong to low pathogenicity avian influenza (LPAI) viruses (Alexander 2000; Henaux et al. 2012; Wainwrighta et al. 2012), which have been identified from migrating water fowls and shorebirds. Healthy domestic ducks and geese can transmit the viral agent to chickens and having more important roles in the perseverance of the virus and its broadcasting between domestic birds and farms (Cameron et al. 2000; Gilbert et al. 2006).

The transmission of H5N1 virus between migratory birds is quiet evident at present posing a threat to human (Dhama et al. 2005, 2012; Sakoda et al. 2012; Choi et al. 2013; Cowling et al. 2013). The dynamics of influenza infection is governed by the intimate linkage between wild migratory birds and all kinds of mammals. This is evident from the fact that several segments are contained in the latest H1N1 pandemic strain of flu virus (Vandegrift et al. 2010). The factors influencing the risk of introduction of avian influenza virus (AIV) through wild migratory birds are numerous. The most evident ones are: susceptible animal species along with number as well as age of target group; features of the geographical area of origin as well as destination; abundance of the species locally and seasonally along with gregariousness of the species during breeding as well as non-breeding seasons (Perezl et al. 2003; Artois et al. 2009).

Faecal material of waterfowl is rich source of the virus and all types of influenza viruses can be isolated from such clinical materials as these birds have probably carried the influenza viruses for centuries. But due the presence of large number of virus subtypes as well as high frequency of mixing of the virus genetically, the disease cannot be effectively controlled in water fowl population (Friend and Franson 1999; World Health Organization 2005).

Debate is still intense and controversial over migratory birds and poultry trade’s role in the spread of highly pathogenic H5N1 (Weber and Stilianakis 2008; Gunnarsson et al. 2012). Most AIV infections have not produced recognisable disease in free-living or wild birds. All these birds are the asymptomatic reservoirs of AIVs. Wild waterfowl and other aquatic birds (ducks, geese, shorebirds, gulls, swans, terns) are the primordial reservoir of all influenza viral genes (Gilsdorf et al. 2006; Songserm et al. 2006; Amonsin et al. 2008; Uchida et al. 2008; Tolf et al. 2012; Rollo et al. 2012; Gilbert et al. 2012; Hill et al. 2012a, b; Ely et al. 2013). Natural infections of wild birds with HPAI viruses are rare. Low pathogenic H5 or H7 subtypes of viruses have been isolated from free-living birds (Chen et al. 2013). There is infrequent report of the presence of these viruses in dead wild birds, usually within infected poultry farms’ flight range. Occasionally, dead wild birds (passerines) have been identified on farms with HPAI outbreaks. The re-emerging 2002 H5N1 influenza viruses of Hong Kong have been reported to be highly pathogenic to ducks causing disease outbreaks and deaths among migratory wild birds as well as resident waterfowl. Ducks developed acute systemic disease, with multiple organ malfunctions particularly the brain showing severe neurological disorder and death, and exhibited transmission efficiently. In contrast, transmission is inconsistent among ducks without significant disease outbreak as has been seen during outbreak involving H5N1 during 1997–2001. In South Africa since the report of H5N3 HPAI outbreak in 1961, it is the first reported case of lethal viral infection. Thereafter, few countries like Hong Kong, China, and others have also reported outbreaks of H5N1 disease in waterfowl, wild water birds and migratory waterfowl, killing thousands of migratory birds. Neurological symptoms, paralysis, unusual head tilt, staggering and neck thrill; and multiple organ dysfunctions including the brain are the clinical findings featured popularly in H5N1 disease in waterfowl. Transmission of H5N1 viruses via migratory birds is well documented (Sengupta et al. 2007; Lee et al. 2008; Dhama et al. 2008; Reperant et al. 2011; Ahmed et al. 2012; Gunnarsson et al. 2012; Soliman et al. 2012; Gilbert et al. 2012; Sakoda et al. 2012; Cappelle et al. 2012) and may pose a threat to humans (Sakoda et al. 2012). In China during 2005 outbreak due to H5N1 virus in migratory waterfowl (bar-headed geese, brown-headed gulls and great black-headed gulls), 1,500 migratory birds died. In Qinghai lake (China) and Erhel Lake (Mongolia), death tolls are observed showing symptoms of H5N1 subsequently confirmed by laboratory testing. In both occasions, Bar-headed Geese and Whooper Swans incurred much more casualties than any other migratory birds. The capability of wild birds in carrying the virus to new infection site is evident from the outbreaks among wild birds in Europe and Iran during 2006; surveillance between 2001 and 2006 in Canadian wild ducks and shorebirds; and gulls at New Jersey (the United States). The extent of genetic exchange between Eurasian and American virus clades or superfamilies is also significant. They reveal that waterfowl bears each of the H1 subtypes through H13 and N1 through N9 without any evidence of the presence of H14 and H15. In adult mallard duck HP Asian H5N1 subtype of virus is not evident serologically. There is no habitual exchange of influenza viruses entirely between the Eurasian and American clades as is evident from the 6,767 gene fragments and 248 complete avian influenza viruses analysis. In migratory birds there is no proof of perpetuation of HP H5N1 influenza, suggesting an unusual/accidental introduction of HP Asian H5N1 viruses in America (Krauss et al. 2007).

It also been reported that migratory birds begin their spring mission from their wintering grounds in Africa and southern Asia towards Northern Europe, Russia and Central Asia, and this plays an important role in spread of bird flu in Asian countries (www.​rferl.​org). The outbreak of H5N1 virus in Asia with subsequent spread to Russia, Middle East, Europe and Africa (Musa et al. 2009), and other parts viz., Portugal (Tolf et al. 2012) in last few years has brought into focus the increasing role of wild birds (Smith et al. 2009). From the end of 2003, the total number of countries reporting H5N1 in domestic birds till March, 2011 was 51, and the H5N1 in wild birds was 17 (OIE 2011). Huge mortality in intensive poultry rearing can occur due to evolution of HPAI viruses from some LPAI subtypes of wild bird origin (Lvov et al. 2010; Winker and Gibson 2010), resulting in domestic and international trade restrictions of poultry products, and significant impact on farmer’s livelihoods and socioeconomics (Tiensin et al. 2007; Minh et al. 2009; Iowa State University 2010; OIE 2011). In migratory birds, self-mutation of LPAI viruses or their direct entry into the poultry population later acts as precursor for the generation of deadly HPAI viruses which proves to be deadly (Ito and Kawaoka 2000). Migratory birds may transmit the inter-regional genes along with which geospatial analyses clearly proves the strong association between the presence of free grazing water fowls and distribution of outbreaks of HPAI. Whistling, white-headed and mallard duck; mute swan, whooper swan, bar-headed goose, common teal, Siberian crane, Sarus crane, great black-headed and/or brown-headed gull, mallards etc. are the major transmitters of AIV. More focus should be on migrating ducks and geese, which should be considered as particularly risky populations (Guan et al. 2000; Gambaryan et al. 2002; Squires et al. 2012).

One among the various unanswered question is the role of wild birds (especially migrants of long distance) regarding the dissemination of influenza A viruses from Southeast Asia towards other geographical regions. This question arose ever since the observation of emerging and westward spreading nature of the highly pathogenic A/H5N1 virus. Various research works have been carried out in Eurasia as Georgia bridges Western Asia and Eastern Europe, acting as home of wild water fowls from several different parts of Eurasia during the phase of migration during winter (www.​cam.​ac.​uk).

In shore birds a low prevalence of AIV has been found consistently in several sites (like Delaware Bay) which are congregation sites of shorebirds and largely seasonal. Prevalence and abundance classes are not closely related across all the sites of sampling. About a third of the entire East Atlantic flyway population qualifies clearly as one of the largest site of congregation of shorebirds due to presence of two million wintering shorebirds in the world. The higher density of migratory shore birds in the important sites of wintering in the East Atlantic coast is also responsible for spread of AIV globally (Zwarts et al. 1990).

Very narrow seasonal windows are responsible for prevalence in the peaks in AIV (Maxted et al. 2012) but the timing of these windows which are seasonal prove to be more variable in tropics rather than ecosystems in the temperate region. In the tropics, the greater variability in the seasonal rainfall and the associated fluctuations in the timing of reproduction as well as congregation of waterbirds are responsible for producing various AIV infection and seasonal dynamics between years (Hasselquist 2007). A difference in the level of the lake along with the associated differences in the density of water birds locally is responsible for difference in inter-annually observations of influenza (Clark et al. 1993; Caron et al. 2009, 2011).

The ecology of HPAI also changed after the emergence and spread of the Asian H5N1 HPAI. Spreading of the virus over Asia, Europe and Africa, results in mortalities of various wild bird species (75) in many countries (38) (Gaidet et al. 2008). Viral isolation from dead migratory birds revealed their potential role in spreading of HPAI. The exceptional circumstances that occurred in Asia lead to the spread out of infection to naive wild bird population. Risk of a wild birds introducing, spreading and maintaining an AIV to a given area is correlated to a number of factors viz. the species of susceptible animal, the number and age of target individuals, the characteristics of the geographical area, the seasonal profusion of that species and the gregariousness of the species during the breeding, migration and non-breeding seasons (Artois et al. 2009).

The spatiotemporal analysis was used to develop a diffusion model to determine how the bird migration and poultry distribution influence the geographic spread of H7N9 infection (Shi et al. 2013). Surveillance and tracking of migratory and resident wild birds should be heightened (Takekawa et al. 2011). This must be strengthened with ecological information in confirmed H5N1 outbreak cases. Maximising the value of gathered information need ornithological expertise in case of outbreak in wild birds. Laboratory-based research on avian influenza has been mostly carried out in domestic animals due to lack of epidemiological information of H5N1 in wild birds and viral behaviour in a wider environment. More studies are needed to analyse the ecology of H5N1 in natural environments; river network; migratory bird staging areas; improving understanding of strain-specific pathogenecity or that in host; degree of viral shedding; and the routes of transmission between wild birds (Horacek 2011). New viruses may be regularly added to the vast pool of viruses in domestic poultry if there is seeding of influenza viruses into backyard farms seasonally. Seeing the importance of these birds in transmitting AIV, United Nations has launched an early warning system on bird flu alarming the spread of deadly virus via incoming migratory birds. Apart from migratory birds and other water fowls, AIVs are adapted innately to wider temperature range: host body temperature (40 to 42 °C) and, probably to temperature below freezing point (as low as −54 °C in certain regions of Siberia), in which the virus can thrive in subclinically infected birds, prior to attaining freezing point. The virus is having good cryostability. Therefore, various unexplained phenomena could be clarified and vindicated, as preservation of the virus in ice has got its implication significantly in epidemiological as well as environmental studies (Henaux et al. 2012; Shoham et al. 2012).


6.1 Intercontinental Spread of Avian Influenza via Migratory Birds


With respect to the role played in the pandemic threat in lower animals and domestic poultry along with humans, there lies overall agreement between the various influenza surveillance studies’ findings. Between the influenza surveillance findings in aquatic birds in America and in Europe, the only difference that significantly affects is the role played by shore birds. Till date in Europe the influenza viruses have been isolated rarely from shore birds. On the other hand, there is definite evidence for the notion that shore birds act as the carrier of the influenza virus from North America to South America during the month of May every year. Studies have shown that the potential precursors to highly pathogenic H5 and H7 avian influenza viruses in the Americas are the shore birds (Krauss et al. 2004) whereas duck species act as the potential transmitter of the disease in Eurasia (Suss et al. 1994; Munster et al. 2005).

Shorebirds along with gulls and terns are the birds in the order Charadriiformes occur in all continents in large proportion. Influenza infection pattern in Charadriiforms differs from that in Anseriforms slightly (Winker et al. 2007). In Charadriiformes first two haemagglutinin subtypes viz., H13 and H16 have been isolated almost exclusively (Krauss et al. 2004). Second, in the Americas (at least) peak infection is shown in shorebirds in the late spring and early summer (Krauss et al. 2004) while in the fall, ducks have higher prevalence of infection prior to winter ground migration suggesting the importance of shore birds in the maintenance and long-term persistence (overwinter) of the viruses in wild birds as they are responsible for spreading the virus in spring to the northern breeding areas (Chen et al. 2006; Iverson et al. 2008).

There lies overlaps between the migratory pathways of migratory water fowls between eastern Eurasia and Alaska as well as between Europe and eastern parts of North America (Kilpatrick et al. 2006) leading to the query why there is no arrival of highly pathogenic H5N1 viruses in the Americas from this part of the globe (Webster et al. 1992; Olsen et al. 2006). The H14 and H15 subtypes of the avian influenza viruses have only been detected in Eurasia whereas most of the known subtypes of influenza A viruses have been detected in each hemisphere. The rate of exchange of all eight segments of avian influenza viruses is unknown while either whole influenza virus or their gene segments have been found to be exchanged between parts of Eurasia and the Americas (Makarova et al. 1999; Wallensten et al. 2005). It is, however, quiet predictable that there may be infrequent exchange of whole influenza viruses on the basis of phylogenetic separation into two super families (Reid and Taubenberger 2003). In order to estimate the frequency of occurrence of genetic reassortment, the genomic information from 248 sequences of influenza viruses (complete) as well as 6,767 gene segments have been utilised (Obenauer et al. 2006).

When the question of how influenza viruses in wild migratory birds establish lineages by spreading from Eurasia to the Americas, doubt still prevails and raises question of great concern to veterinary as well as public health officials. Supportive evidence indicates the circulation of the Asian HP H5N1 in several countries of Eurasia continuously and re-emergence of the same virus during the winter months in several countries of Asia viz., China and Japan; South Korea and Thailand. This supports the contention that this particular H5N1 virus is being perpetuated in this region (Stallknecht and Shane 1988; Krauss et al. 2007).


6.2 Bridge Species


Several species of familiar songbirds or perching birds (Passeriformes) such as crows (Corvidae family), sparrows (Passeridae family), mynas (Sturnidae family) and the ubiquitous feral pigeon (Columba livia) of the Columbiformes order, have broad and diverse habitat preferences. These have adapted to exploit anthropogenic food sources. Their close association with humans often results in close contact with domestic poultry, especially at open poultry farms where food is readily available. The H5N1 AIV has been reported to fatally infect them. Thus, these species may serve as links between wild birds in natural habitats and domestic poultry, acting as a ‘bridge’ in the transmission of AI viruses from poultry to wildlife or vice versa (Boon et al. 2007; Pillai et al. 2008; Nagarajan et al. 2010; Columba et al. 2012; Jiao et al. 2012; Teru et al. 2012). Specific surveillance as well as monitoring efforts in these potential ‘bridge’ species should be undertaken at HPAI poultry outbreaks and wildlife mortality events, to determine their potential for contracting the disease and possible role in transmitting the virus to or from wild habitats.


6.3 International Scientific Task Force on Avian Influenza and Wild Birds


In August, 2005 UNEP Convention on Migratory Species (CMS) along with Agreement on the Conservation of African Eurasian Migratory Water birds (AEWA) established a Scientific Task Force on Avian Influenza and Wild Birds. Role of migratory water fowls as the potential transmitter of highly pathogenic Avian Influenza (HPAI) virus subtype H5N1 has lead to this establishment. Thirteen members are included in this task force that includes: UN bodies and wildlife treaties; specialist intergovernmental and non-governmental organizations.

Task Force members are 1. The UNEP African–Eurasian Water bird Agreement (AEWA), 2. Birdlife International, 3. UNEP Convention on Biological Diversity (CBD), 4. International Council for Game and Wildlife Conservation (CIC), 5. UNEP Convention on Migratory Species of Wild Animals (CMS), 6. Ramsar Convention on Wetlands (Ramsar), 7. Wetlands International, 8. Wildlife Conservation Society (WCS), 9. The Zoological Society of London.

Task Force observers are 1. The UN Food and Agriculture Organization (FAO), 2. World Organization for Animal Health (WOAH/OIE), 3. United Nations Environment Programme (UNEP) 4. World Health Organization (WHO).

The objectives of this Task Force are (i) combining the best scientific advice to conserve impact of the spread of avian influenza, (ii) assessing migratory birds’s role as viral vectors, (iii) issuing advisory comments on most important factors resulting in epidemic and measures that are technically sound in order to combat bird flu and (iv) developing systems of early warning.


References



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Ahmed SS, Ersbøll AK, Biswas PK et al (2012) Ecological determinants of highly pathogenic avian influenza (H5N1) outbreaks in Bangladesh. PLoS ONE 7(3):e33938PubMedCentralPubMed


Alba A, Bicout DJ, Vidal F et al (2012) Model to track wild birds for avian influenza by means of population dynamics and surveillance information. PLoS ONE 7(8):e44354PubMedCentralPubMed


Alexander DJ (2000) A review of avian influenza in different bird species. Vet Microbiol 74:3–13PubMed


Amonsin A, Choatrakol C, Lapkuntod J et al (2008) Influenza virus (H5N1) in live bird markets and food markets, Thailand. Emerg Infect Dis 14:1739–1742PubMedCentralPubMed

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Sep 17, 2016 | Posted by in GENERAL | Comments Off on Role of Migratory Birds in Spreading Influenza Viruses

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