Surveillance for High Pathogenicity Avian Influenza Virus in Wild Birds in the Pacific Flyway of the United States, 2006–2007

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Surveillance for High Pathogenicity Avian Influenza Virus in Wild Birds in the Pacific Flyway of the United States, 2006–2007
  Surveillance for High Pathogenicity Avian Influenza Virus in Wild Birds in the PacificFlyway of the United States, 2006–2007 Robert J. Dusek,  AF  J. Bradley Bortner, B Thomas J. DeLiberto, C  Jenny Hoskins, B  J. Christian Franson,  A  Bradley D. Bales, D Dan Yparraguirre, E Seth R. Swafford, C and Hon S. Ip  A   A  U.S. Geological Survey, National Wildlife Health Center, Madison, WI 53711 B U.S. Fish and Wildlife Service, Portland, OR 97232 C U.S. Department of Agriculture/Animal and Plant Health Inspection Service, Wildlife Services, Fort Collins, CO 80521 D Oregon Department of Fish and Wildlife, Salem, OR 97303 E California Department of Fish and Game, Sacramento, CA 95814Received 29 August 2008; Accepted and published ahead of print 17 December 2008SUMMARY. In 2006 the U.S. Department of Agriculture, U.S. Department of Interior, and cooperating state fish and wildlifeagencies began surveillance for high-pathogenicity avian influenza (HPAI) H5N1 virus in wild birds in the Pacific Flyway of theUnited States. This surveillance effort was highly integrated in California, Oregon, Washington, Idaho, Nevada, Arizona, Utah,and western Montana, with collection of samples coordinated with state agencies. Sampling focused on live wild birds, hunter-killed waterfowl during state hunting seasons, and wild bird mortality events. Of 20,888 samples collected, 18,139 were from order Anseriformes (waterfowl) and 2010 were from order Charadriiformes (shorebirds), representing the two groups of birds regarded tobe the primary reservoirs of avian influenza viruses. Although 83 birds were positive by H5 real-time reverse transcriptionpolymerase chain reaction (rRT-PCR), no HPAI H5N1 virus was found. Thirty-two virus isolates were obtained from the H5-positive samples, including low-pathogenicity H5 viruses identified as H5N2, H5N3, and H5N9.RESUMEN. Muestreo para detectar influenza aviar de alta patogenicidad en aves silvestres de la ruta migratoria del Pacı´fico delos Estados Unidos, 2006–2007.En el an˜o 2006 el Departamento de Agricultura y el Departamento del Interior de los Estados Unidos, con la cooperacio´n deagencias estatales de pesca y vida silvestre iniciaron un muestreo para detectar la influenza aviar de alta patogenicidad subtipo H5N1en aves silvestres de la ruta migratoria del Pacı´fico de los Estados Unidos. Este proyecto estuvo integrado principalmente enCalifornia, Orego´n, Washington, Idaho, Nevada, Arizona, Utah, y la parte oeste de Montana, con la recoleccio´n de muestrascoordinada por las agencias estatales. El muestreo estuvo enfocado en aves silvestres vivas, aves acua ´ticas muertas por cazadoresdurante las estaciones de caza y en eventos de mortalidad de aves silvestres. De las 20,888 muestras recolectadas, 18,139 muestrasfueron de aves del orden Anseriformes (aves acua ´ticas) y 2010 fueron de aves del orden Caradriformes (aves playeras), querepresentan los dos grupos de aves considerados como los principales reservorios de los virus de influenza aviar. Aunque 83 avesfueron positivas para la hemaglutinina 5 (H5) por la prueba de transcripcio´n reversa y reaccio´n en cadena de la polimerasa entiempo real, no se encontro´ la presencia del virus de alta patogenicidad subtipo H5N1. Treinta y dos aislamientos fueron obtenidosde las muestras positivas a H5, incluyendo virus de baja patogenicidad identificados como H5N2, H5N3 y H5N9.Key words: avian influenza, HPAI, H5N1, surveillance, United States Abbreviations: AHY  5 after hatch year; HPAI 5 high-pathogenicity avian influenza; HY  5 hatch year; LPAI 5 low-pathogenicity avian influenza; NVSL 5 National Veterinary Services Laboratories; rRT-PCR  5 real-time reverse transcriptionpolymerase chain reaction; USDA  5 United States Department of Agriculture  While wild aquatic birds are considered the principal agent forlong-distance spread and maintenance of low-pathogenicity avianinfluenza (LPAI) viruses, they have rarely been involved in high-pathogenicity avian influenza (HPAI) outbreaks (1). Historically, only one HPAI outbreak occurred primarily in wild birds not associated withan HPAI outbreak in poultry (1,4). Considerable debate exists on therole wild birds have played in the current global spread of HPAI H5N1(15,16,31,35). Most wild bird mortality due to HPAI H5N1 has beenassociated with mortality in domestic birds in urban or agricultural areas(14,24). However, experimental studies have shown that some wildbirds can be infected with HPAI H5N1 without developing clinicalsigns and may be capable of transporting this virus (5,20). A variety of mechanisms likely play a role in the geographic spreadof HPAI H5N1 (1). However, since an outbreak of HPAI H5N1that occurred primarily in bar-headed geese (  Anser indicus  ) atQinghai Lake in Western China in 2005, there is increasing evidencebeing compiled to support the hypothesis that wild birds areinvolved in the spread of HPAI H5N1 (10,26,27,34). Furthermore,recent phylogenetic analyses of HPAI H5N1 virus isolates fromoutbreaks in domestic poultry and migratory birds from otherlocations have demonstrated a close relationship with isolates fromthe Qinghai Lake outbreak (25,35,42). While HPAI H5N1 virus strains currently circulating in Asia andother parts of the world have not yet been detected in the WesternHemisphere, evidence of gene flow between Europe/Asia and North America of LPAI viruses supports the possibility of its introductionvia migratory birds (21,28). Owing to the potential impact of thisvirus on the U.S. poultry industry as well as the potential thatgenetic changes in the virus could trigger a pandemic, the U.S.government developed and instituted in 2006 the U.S. Interagency Strategic Plan (U.S. Strategic Plan) for the early detection of HPAIH5N1 (43). The goal of the strategic plan is to ‘‘describe theessential components of a unified national system for the early detection of HPAI, specifically highly pathogenic H5N1 avian  Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. government. F Corresponding author. E-mail:   AVIAN DISEASES 53:222–230, 2009 222  Fig. 1. Sampling locations for live bird and hunter-killed surveillance for high-pathogenicity avian influenza H5N1 in the Pacific Flyway,United States, April 2006–March 2007. (Base map from ESRI (2006), ArcMAP v. 9.2)Fig. 2. Number of live bird and hunter-killed samples collected for high-pathogenicity avian influenza H5N1 surveillance in the Pacific Flyway,United States, by state, April 2006–March 2007. HPAI surveillance in the U.S. Pacific Flyway   223  Table 1. Live and hunter-killed bird species sampled during surveillance for high-pathogenicity avian influenza H5N1 in the Pacific Flyway,United States, April 2006–March 2007. Family Common name Scientific name Number sampled  Anatidae Fulvous whistling-duck   Dendrocygna bicolor   1Trumpeter swan  Cygnus buccinator   7Tundra swan  Cygnus columbianus   334Greater white-fronted goose  Anser albifrons   224Snow goose  Chen caerulescens   393Ross goose  Chen rossii   2Black brant  Branta bernicla  391Cackling goose  Branta hutchinsii   717 Aleutian cackling goose  Branta hutchinsii leucopareia  413Canada goose  Branta canadensis   289 Wood duck   Aix sponsa  21Eurasian wigeon  Anas penelope   1 American wigeon  Anas americana  1166Gadwall  Anas strepera  613Green-winged teal  Anas crecca  1880Mallard  Anas platyrhynchos   5978Northern pintail  Anas acuta  3844Blue-winged teal  Anas discors   47Cinnamon teal  Anas cyanoptera  39Northern shoveler  Anas clypeata  1330Unidentified teal  Anas   sp. 2Canvasback   Aythya valisineria  20Redhead  Aythya americana  128Ring-necked duck   Aythya collaris   106Greater scaup  Aythya marila  15Lesser scaup  Aythya affinis   22Harlequin duck   Histrionicus histrionicus   1Surf scoter  Melanitta perspicillata  64 White-winged scoter  Melanitta fusca  14Common goldeneye  Bucephala clangula  35Bufflehead  Bucephala albeola  23Common merganser  Mergus merganser   4Ruddy duck   Oxyura jamaicensis   15 Waterfowl total 18,139Recurvirostridae American avocet  Recurvirostra americana  1Charadriidae Semipalmated plover  Charadrius semipalmatus   39Killdeer  Charadrius vociferus   1Scolopacidae Short-billed dowitcher  Limnodromus griseus   37Long-billed dowitcher  Limnodromus scolopaceus   532Marbled godwit  Limosa fedoa  1Lesser yellowlegs  Tringa flavipes   1Ruddy turnstone  Arenaria interpres   1Red knot  Calidris canutus   2Sanderling   Calidris alba  12 Western sandpiper  Calidris mauri   689Least sandpiper  Calidris minuta  125Dunlin  Calidris alpina  521Red-necked phalarope  Phalaropus lobatus   48Shorebirds total 2010Podicipedidae Pied-billed grebe  Podilymbus podiceps   2 Western grebe  Aechmophorus occidentalis   1 Ardeidae Great blue heron  Ardea herodias   1Great egret  Ardea alba  2 Accipitridae Swainson hawk   Buteo swainsoni   1Red-tailed hawk   Buteo jamaicensis   1Tetraonidae Spruce grouse  Falcipennis canadensis   1Phasianidae Ring-necked pheasant  Phasianus colchicus   5Gruidae Sandhill crane  Grus canadensis   162Rallidae American coot  Fulica americana  43Corvidae Common raven  Corvus corax   3Other species total 222Grand total 20,371 224  R. J. Dusek   et al.  influenza, in migratory birds. While the immediate concern is a potential introduction of highly pathogenic H5N1 avian influenza into the U.S., the development of a system that is capable of detecting the introduction of all HPAI viruses through migratory birds would significantly improve the biosecurity of the Nation.’’ Asa part of that plan, surveillance for HPAI H5N1 in live and hunter-killed wild migratory birds was outlined, as well as investigation of its occurrence during morbidity and mortality events in wild birds.In addition, detection for LPAI H5 and H7 subtypes is included inthe national surveillance efforts, since these viruses can be precursorsto HPAI viruses in domestic poultry (30). Alaska has been considered the most likely location for early introduction of HPAI H5N1 by migratory birds in North America (43).ThisisduetoitsproximitytoAsiaandthenumbersofmigratory birds that move between Asia and North America across the Bering Sea. The western continental United States (lower Pacific Flyway) isalso consideredan area of increasedconcern becauseof thenumbers of species that breed in northern Russia and Alaska, in the same habitatsas birds that migrate to Asia, and that migrate via the North AmericanPacific Flyway into or through the western United States. In 2006–2007 webegan surveillance for HPAIH5N1 inwildbirdsin the lowerPacific Flyway of the United States. This report describes thedevelopment of the program and presents the results for the firstsurveillance season (April 1, 2006, through March 31, 2007). MATERIALS AND METHODSPlanning.  The 2006 U.S. Strategic Plan provided a nationalframework for surveillance for HPAI H5N1 in wild migratory birdsthroughout the United States (43). This plan recommended a flyway approach for conducting surveillance activities and prioritizing speciesfor sampling. In the lower Pacific Flyway (Fig. 1), state wildlife agencies,the U.S. Fish and Wildlife Service, the U.S. Department of  Agriculture—Wildlife Services, and partners refined the U.S. StrategicPlan into a Pacific Flyway Strategic Plan (Pacific Flyway Plan) for avianinfluenza surveillance sampling in 2006 (32). Prioritization of speciestargeted for sampling was based on expert knowledge of the ecology andspatial and temporal distribution of migratory birds throughout theflyway. Each of the eight states in the lower Pacific Flyway furtherstepped down the Pacific Flyway Plan into interagency state surveillanceplans for implementing specific surveillance strategies. Species selection, sample size, and temporal considerations.  Wildbird species that use areas in both North America and Asia wereidentified in the U.S. Strategic Plan and were ranked based on fivecriteria (43). Briefly, ranking was done by assigning a score to eachspecies based on each of the following factors: 1) the proportion of thepopulation occurring in Asia, 2) contact with a known area affected by HPAI H5N1, 3) habitats used in Asia, 4) the population size in Alaska,5) and the probability of obtaining a sufficient number of birds forsampling (43). Scores were summed to list species by priority. ThePacific Flyway Plan then identified  primary   species based on thesecriteria and that were available for sampling in the lower Pacific Flyway and  secondary   species that may comingle with these primary species. Itwas determined that monitoring of abundant secondary species, such asmallards (  Anas platyrhynchus  ), would be useful if Asian HPAI H5N1went undetected in primary species. Primary species sampled weretundra swan ( Cygnus columbianus  ), lesser snow goose ( Chen caerulescens  ),Pacific brant ( Branta bernicla ), Aleutian cackling goose ( Brantahutchinsii leucopareia ), northern pintail (  Anas acuta ), long-billeddowitcher ( Limnodromus scolopaceus  ), red knot ( Calidris canutus  ), ruddy turnstone (  Arenaria interpres  ), western sandpiper ( Calidris mauri  ),dunlin ( Calidris alpina ), and red-necked phalarope ( Phalaropus lobatus  ).Secondary species sampled were cackling goose ( Branta hutchinsii  ),greater white-fronted goose (  Anser albifrons  ), mallard, American wigeon(  Anas americana ), green-winged teal (  Anas crecca ), and northern shoveler(  Anas clypeata ).Sampling plans were developed for each state in the flyway toimplement specific surveillance activities for the highest ranking species.Development of state-specific plans allowed experts to use localknowledge, such as targeting birds with known srcins from Alaska (based on banding analyses or other information), to implementsurveillance strategies efficiently at a fine scale. Local experts (primarily state and federal agency migratory bird biologists and managers) usedtheir knowledge of spatial and temporal variation in migration timing,species abundance and availability, and habitat conditions to designsampling efforts to achieve target sample sizes. Surveillance in live birdsand hunter-harvested birds often used existing field studies, managementprograms, and hunter check stations. The U.S. Strategic Plan did notdictate rigid sampling objectives but recommended general guidance of a target sample size of 200 birds from spatially or temporally segregated‘‘populations’’ (e.g., northern pintails arriving in August and Septemberin the San Joaquin Valley, California). This was derived under theassumption that the goal would be to detect a minimum prevalence of 1.5% with a 95% statistical power (43). In addition, mallards weretargeted for sampling during the summer and early autumn because of their susceptibility to H5 and H7 AI subtypes (30,44). They were alsoabundant and easy to capture, so they could serve as sensitive indicatorsof HPAI H5N1 introduction (44,45). Other species were opportunis-tically sampled when they were captured in conjunction with plannedsampling. Additional avian influenza sampling occurred during investigation of morbidity and mortality events, which occur annually in the Pacific Flyway. Field sampling of wild birds.  Capture locations for live sampledbirds were selected based on known occurrence of high-priority species.Techniques for capturing birds varied but primarily involved rocket netsfor waterfowl and larger shorebirds and mist nets for smaller shorebirds(6). Hunter-harvested birds were sampled during autumn and wintersport hunting seasons. Hunters were contacted at check stations at stateor federal wildlife areas or boat ramps. Locations for sampling hunter-harvested birds were selected based on known harvest areas for high-priority species and existing harvest check stations.Table 2. Summary of H and N combinations detected from individual H5 rRT-PCR positive samples, Pacific Flyway, United States, April2006–March 2007. Species H4N2 H4N3 H4N6 H5N2 H5N3 H5N9 H6N2 NVI  A  Mallard (  A. platyrhynchos  ) 2 1 2 16 1 34Northern pintail (  A. acuta ) 1 2 1 4Northern shoveler (  A. clypeata ) 2 1 6 American wigeon (  A. americana ) 2 3Green-winged teal (  A. crecca ) 2Snow goose ( C. caerulescens  ) 1 0Cackling goose ( B. hutchinsii  ) 1Tundra swan ( C. columbianus  ) 1  A  NVI  5 No virus isolated. HPAI surveillance in the U.S. Pacific Flyway   225  Table 3. Results of virus isolation from H5 rRT-PCR positive samples collected during live bird and hunter-killed bird surveillance for high-pathogenicity avian influenza H5N1 in the Pacific Flyway, United States, April 2006–March 2007. Common name Scientific name Sex Age  A  State County Date collected V.I. subtype B No. of birds Tundra swan  C. columbianus   U AHY UT Box Elder Nov. 11, 2006 NVI C 1Cackling goose  B. hutchinsii   M HY OR Lane Dec. 6, 2006 NVI 1Snow goose  C. caerulescens   U HY MT Teton Nov. 4, 2006 H5N2 1 American wigeon  A. americana  F HY ID Bingham Oct. 7, 2006 NVI 1F AHY WA Clark Nov. 4, 2006 H5N2 1F HY OR Columbia Nov. 9, 2006 H5N2 1M HY OR Coos Nov. 18, 2006 NVI 1F AHY OR Columbia Nov. 21, 2006 NVI 1Green-winged teal  A. crecca  M HY ID Cassia Oct. 7, 2006 NVI 1F HY UT Davis Nov. 11, 2006 NVI 1Mallard  A. platyrhynchos   F HY WA Grant Jul. 22, 2006 NVI 1M HY NV Churchill Jul. 24, 2006 H5N2 5F HY NV Churchill Jul. 28, 2006 NVI 1M HY NV Churchill Jul. 28, 2006 H5N2 3M HY NV Churchill Jul. 28, 2006 NVI 1F HY WA Yakima Aug. 4, 2006 H4N3 1F HY WA Yakima Aug. 4, 2006 NVI 1F U WA Yakima Aug. 4, 2006 H4N6 1M HY WA Yakima Aug. 4, 2006 H4N6 1M HY WA Yakima Aug. 4, 2006 NVI 2F HY OR Multnomah Aug. 8, 2006 NVI 1F HY WA Grant Aug. 10, 2006 H5N2 1F HY WA Grant Aug. 18, 2006 NVI 1F HY WA Yakima Aug. 23, 2006 NVI 2F HY NV Lyon Aug. 24, 2006 H4N2 1M HY NV Lyon Aug. 24, 2006 H5N2 2M HY NV Lyon Aug. 24, 2006 NVI 1F HY OR Multnomah Aug. 29, 2006 NVI 1F HY WA Skagit Aug. 29, 2006 NVI 1M HY WA Grant Aug. 29, 2006 NVI 1M HY MT Lake Aug. 29, 2006 NVI 1M HY OR Multnomah Aug. 29, 2006 NVI 1F HY WA Yakima Aug. 30, 2006 NVI 2M HY WA Grant Aug. 30, 2006 NVI 1M HY WA Yakima Aug. 30, 2006 H5N2 1M HY WA Yakima Aug. 30, 2006 NVI 4M AHY AZ Maricopa Sep. 6, 2006 H5N2 1M HY ID Jefferson Sep. 6, 2006 NVI 1M HY ID Kootenai Sep. 7, 2006 H5N2 1M HY ID Kootenai Sep. 7, 2006 NVI 2M HY WA Whatcom Sep. 8, 2006 H5N2 1M HY MT Cascade Sep. 13, 2006 H6N2 1M HY MT Cascade Sep. 19, 2006 NVI 1M HY MT Cascade Sep. 20, 2006 H5N2 1F AHY UT Davis Oct. 7, 2006 NVI 1M AHY ID Bonneville Oct. 7, 2006 NVI 1M U UT Box Elder Oct. 7, 2006 NVI 2F AHY ID Benewah Oct. 9, 2006 H4N2 1M AHY ID Jefferson Oct. 11, 2006 NVI 1M AHY WA Whatcom Nov. 12, 2006 NVI 1M AHY MT Gallatin Nov. 30, 2006 NVI 1Northern pintail  A. acuta  M AHY CA Kern Aug. 29, 2006 NVI 1F AHY MT Cascade Sep. 7, 2006 NVI 1F HY MT Cascade Sep. 14, 2006 H5N3 1M HY MT Cascade Sep. 14, 2006 H5N3 1M HY CA Siskiyou Oct. 3, 2006 H5N9 1F HY CA Siskiyou Oct. 5, 2006 H5N2 1M AHY AZ Mohave Oct. 28, 2006 NVI 1M AHY WA Clark Nov. 2, 2006 NVI 1Northern shoveler  A. clypeata  F AHY UT Davis Oct. 7, 2006 H5N2 1F HY OR Columbia Oct. 24, 2006 NVI 1F AHY WA Clark Nov. 4, 2006 H5N2 1M AHY UT Davis Nov. 4, 2006 H5N3 1 226  R. J. Dusek   et al.
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