Movements of birds and avian influenza from Asia into Alaska.
Asian-origin avian influenza avian influenza: see influenza. (AI) viruses are spread in part by migratory birds. In Alaska, diverse avian hosts from Asia and the Americas overlap in a region of intercontinental avifaunal a·vi·fau·na
The birds of a specific region or period.
[Latin avis, bird; see awi- in Indo-European roots + fauna. mixing. This region is hypothesized to be a zone of Asia-to-America virus transfer because birds there can mingle in waters contaminated by wild-bird-origin AI viruses. Our 7 years of AI virus surveillance among waterfowl waterfowl, common term for members of the order Anseriformes, wild, aquatic, typically freshwater birds including ducks, geese, and screamers. In Great Britain the term is also used to designate species kept for ornamental purposes on private lakes or ponds, while in and shorebirds in this region (1998-2004; 8,254 samples) showed remarkably low infection rates (0.06%). Our findings suggest an Arctic effect on viral ecology, caused perhaps by low ecosystem productivity and low host densities relative to available water. Combined with a synthesis of avian diversity and abundance, intercontinental host movements, and genetic analyses, our results suggest that the risk and probably the frequency of intercontinental virus transfer in this region are relatively low.
In Alaska, diverse avian hosts from Asia and the Americas overlap in a region of intercontinental avifaunal mixing hypothesized to be an important zone of Asia-to-America virus transfer. Aquatic birds, especially waterfowl and shorebirds, provide a source of influenza viruses for transmission to mammals and poultry (1-3). Even without disease, when infected these avian hosts tend to shed high concentrations of virus in their feces (4-6). Cross-host infections in wild birds probably occur most frequently when other birds of the same or different species feed, drink, or bathe in waters contaminated by the feces of infected birds. On rare occasions, some of these avian influenza (AI) viruses, generally of low pathogenicity, have crossed species barriers from wild birds to poultry, in which mutations can produce highly pathogenic strains. From poultry, low and high pathogenicity viruses (or genomic segments of these viruses) can be introduced to humans, causing some fatal infections (7). This wild-bird reservoir can thus provide the genes for the next pandemic pandemic /pan·dem·ic/ (pan-dem´ik)
1. a widespread epidemic of a disease.
2. widely epidemic.
Epidemic over a wide geographic area.
n. in humans or epizootic ep·i·zo·ot·ic
Affecting a large number of animals at the same time within a particular region or geographic area. Used of a disease.
ep in domestic animals and presents an ongoing risk.
The rapid spread of highly pathogenic avian influenza A (H5N1) viruses from Asia across Eurasia (8,9) demonstrated how avian vectors can be involved in the distribution of avian and mammalian infections. Key activities for successful global influenza mitigation measures are surveillance, risk assessment, and epidemiologic modeling and prediction of AI virus infection in wild birds (10,11). Anthropogenic an·thro·po·gen·ic
1. Of or relating to anthropogenesis.
2. Caused by humans: anthropogenic degradation of the environment. factors will also affect the evolution and distribution of avian influenza viruses. However, we focused on the natural virus transport system that migratory birds represent in an important high-latitude region with low levels of human presence.
We obtained our baseline data on viruses and vectors by screening wild birds for AI virus in western Alaska, starting in 1998. We focused on western Alaska because of the unparalleled overlap of Old World and New World bird migration systems in this region. To estimate the risk of Asian-origin AI viruses being delivered by migratory birds to North America through Alaska, we evaluated AI virus infection rates, bird movements, and the diversity and degree of intercontinental host overlap.
During the boreal bo·re·al
1. Of or relating to the north; northern.
2. Of or concerning the north wind.
3. Boreal summer, birds come to Alaska to breed from 6 continents: North and South America, Asia, Africa, Australia, and Antarctica. Alaska, thus, has direct, real-time connections with AI virus vectors from much of the world. It is a critical Old World-New World crossover zone and almost certainly a region of intercontinental virus transfer. Eurasian birds are common in Alaska during summer. Within 2 of the most important vector groups, waterfowl and shorebirds, at least 43 species regularly found in this region winter primarily in the eastern or southeastern parts of Asia; most are aquatic (online Appendix Table, available from www.cdc.gov/EID/content13/4/547-appT.htm). Additionally, many species are shared with Asia across the Bering Sea (online Appendix Table). This extensive crossover of migratory Old World and New World birds offers excellent potential for virus exchange and transfer to the New World. Outbreaks of avian influenza that have killed persons in southeastern Asia (7) and occurrences of highly pathogenic AI (H5N1) infection in migratory birds (8,9) highlight the global importance of the Alaska migration system for intercontinental virus transport.
In Alaska, 5 major factors are involved in the natural intercontinental movement of avian-origin viruses: 1) Asian species coming to Alaska; 2) North American North American
named after North America.
North American blastomycosis
see North American blastomycosis.
North American cattle tick
see boophilusannulatus. migrant birds (Asian-origin migrants that return to North America in autumn) breeding in Asia; 3) individual birds of species that winter on both sides of the Pacific moving between the continents; 4) species that have limited movements or are resident in the region; and 5) water (it has been inferred that live AI virus remains viable in fresh water at high latitudes through the cold northern winters) (12).
When we began our study, the role of migratory birds in the transport of highly pathogenic Al was uncertain, but wild birds have been found with these viruses, and with infection several species appear susceptible to severe disease and death (9,13). In previously reported cases of infection of wild birds with the highly pathogenic virus, transmission was thought to be from infected chickens, the species in which the shift to increased pathogenicity had originally occurred. Experimental and field studies (9,14,15) have identified highly pathogenic AI (H5NI) infection in ducks without clinical disease, which implicates healthy wild birds in transmission. Although in this regard the Asian AI (H5NI) subtype (programming) subtype - If S is a subtype of T then an expression of type S may be used anywhere that one of type T can and an implicit type conversion will be applied to convert it to type T. appears unique among highly pathogenic AI viruses, wild birds may be considered as potentially important vectors for strains of low and high pathogenicity.
Surveillance, Isolation, and Sequencing
We sampled ducks and shorebirds, 2 groups of aquatic birds important as subsistence foods in rural Alaska, widely associated with Alaska waters and common among those species that winter in southeastern Asia (online Appendix Table). We sampled migratory birds that come to North America from southeastern Asian wintering grounds or Asian breeding grounds, as well as North American birds <onlyinclude> This list of North American birds is a comprehensive listing of all the bird species known from the North American continent north of Mexico. </onlyinclude> , which mingle with Old World birds on shared breeding and fall staging grounds. Intensive and extensive taxonomic sampling enabled us to obtain the best possible vectorwide prevalence estimates at our sampling sites. Our animal sampling was done according to protocols approved by the Institutional Animal Care and Use Committee Institutional Animal Care and Use Committees are of central importance to the application of laws to animal research in the United States. Most research involving laboratory animals is funded by the United States National Institutes of Health or other federal agencies. .
From May through October, 1998-2004, totals of 7,751 cloacal cloacal
emanating from or pertaining to cloaca.
the contact which occurs during insemination in birds when the vent of the female is everted exposing the cloacal mucosa against which the phallus of the male is pressed. swabs and 503 fecal samples were collected from waterfowl (Anatidae) and shorebirds (Charadriidae and Scolopacidae), primarily at sites on the Yukon-Kuskokwim Delta, Alaska Peninsula, Seward Peninsula, the North Slope, and the Aleutian Islands. Most samples were obtained after the breeding season (Figure; online Appendix Table). Each of these areas is internationally renowned for its avian diversity and abundance during the migration periods and the boreal summer.
Swabs and fresh fecal samples were placed in sterile medium (brain-heart infusion buffer with 10,000 U/mL penicillin G penicillin G
The most commonly used penicillin compound, used primarily in the form of its stable salts. Also called benzylpenicillin. , 1 mg/mL gentamicin gentamicin /gen·ta·mi·cin/ (jen?tah-mi´sin) an aminoglycoside antibiotic complex isolated from bacteria of the genus Micromonospora, , 20 [micro]g/mL amphotericin B amphotericin B (ăm'fətĕr`ĭsĭn), antibiotic that halts the growth of several disease-causing fungi. Discovered in 1956, it is produced by bacteria of the genus Streptomyces. ) in the field and cooled before transport to the University of Alaska Museum laboratory. Transportation times were generally short ([approximately equal to] 2-14 days), during which time samples were kept cool (mechanically refrigerated or buried above permafrost permafrost, permanently frozen soil, subsoil, or other deposit, characteristic of arctic and some subarctic regions; similar conditions are also found at very high altitudes in mountain ranges. ), frozen at 20[degrees]C, or kept on liquid nitrogen. Upon arrival at the laboratory, they were placed in a 70[degrees]C freezer. They were then shipped overnight to the Southeast Poultry Research Laboratory in Athens, Georgia, USA, in thick coolers with -70[degrees]C ice packs. Samples were not exposed to freeze-thaw cycles but were thawed for analysis.
Samples were processed for virus isolation (1998-2000) or screened by real-time reverse transcriptase-PCR (rRT-PCR) for influenza A influenza A
Influenza caused by infection with a strain of influenza virus type A.
influenza A Infectious disease An avian virus, especially of ducks–which in China live near the pig reservoir and 'vector'; virus (2001-2004), and all rRT-PCR-positive samples were subjected to virus isolation. Virus isolation was performed in embryonating chickens eggs as per standard procedures (16). For rRTPCR, RNA RNA: see nucleic acid.
in full ribonucleic acid
One of the two main types of nucleic acid (the other being DNA), which functions in cellular protein synthesis in all living cells and replaces DNA as the carrier of genetic was extracted from cloacal swab material with Trizol LS reagent (Invitrogen, Inc., Carlsbad, CA, USA) in accordance with manufacturer's instructions. RNA was tested for avian influenza virus matrix (M) gene, which detects all type A influenza viruses (17). The recovery rate was no better when virus isolation was used (of the 5 isolates, 3 were from rRT-PCR and 2 were from direct virus isolation). Several thousand samples have been processed by rRT-PCR at the Southeast Poultry Research Laboratory with an internal positive control; the recovery rate between the methods is equivalent, which indicates that inhibition was not a major factor in our study.
Mapping and Abundance
Delimitation of the Alaska portion of the overlap zone between Old World and New World migration systems in this region was done by using published and unpublished data on Alaska birds from the University of Alaska Museum. Abundance estimates were taken from the literature (18-23) and unpublished data (D.D.G., K.W., and University of Alaska Museum). Maps were created and species richness values were calculated by using ArcView 3.3 and ArcGIS 9.1 (Environmental Systems Research Institute, Inc., Redlands, CA, USA).
We used complementary population genetic approaches to assess approximate levels of individual intercontinental movement for 2 vector species of ducks: green-winged teal (Arias crecca) and mallards (Anas platyrhynchos Anas platyrhynchos
the mallard, a monogamous, broad-billed dabbling duck. One of the original ducks from which the domestic ducks have originated. ). Gene flow between green-winged teal populations in eastern Asia (n = 14) and Alaska (n = 40) was determined by using amplified fragment-length polymorphisms (AFLPs). Whole genomic DNA was extracted from tissues by using the DNeasy Tissue Kit (QIAGEN, Valencia, CA, USA). AFLP data were generated by using the Applied Biosystems AFLP Plant Mapping Kit (Foster City, CA, USA) and protocol as described (24). Two fluorescently labeled primer pairs were run on an ABI Abi (ā`bī) [short for Abijah], in the Bible, King Hezekiah's mother.
(Application Binary Interface) A specification for a specific hardware platform combined with the operating system. PRISM 3100 Genetic Analyzer (Applied Biosystems). Electropherograms were scored manually and 218 loci loci
[L.] plural of locus.
loci Plural of locus, see there were identified. STRUCTURE 2.1 (25) was used to indirectly estimate gene flow by using prior geographic information about each population and determining whether individuals were assigned genetically to their population of origin. Misassigned individuals are likely to have been immigrants or to have had recent immigrant ancestors (25). Because AFLPs provide dominant data, each locus is treated as a haploid haploid /hap·loid/ (hap´loid)
1. having half the number of chromosomes characteristically found in the somatic (diploid) cells of an organism; typical of the gametes of a species whose union restores the diploid number. allele allele (əlēl`): see genetics.
Any one of two or more alternative forms of a gene that may occur alternatively at a given site on a chromosome. ; the no-admixture model with correlated allele frequencies was used. Multiple independent simulations were run at different lengths. Results are based on 100,000 bum-ins and 200,000 subsequent iterations. Pairwise [F.sub.ST] estimates (AFLP-SURV 1.0, ) gave comparable results (not shown). To estimate gene flow between mallards in Alaska (n = 39) and eastern Asia (n = 105), we used Migrate software (27) to estimate the neutral parameter theta Theta
A measure of the rate of decline in the value of an option due to the passage of time. Theta can also be referred to as the time decay on the value of an option. If everything is held constant, then the option will lose value as time moves closer to the maturity of the option. (4N [sub.e][mu]) and the migration rates between continents (4N [sub.e]m) based on sequence data of 256 bp from intron Intron
In split genes, a portion that is included in ribonucleic acid (RNA) transcripts but is removed from within a transcript during RNA processing and is rapidly degraded. 6 of ornithine decarboxylase (28). Multiple factors (e.g., mutation rates, effective vs. census population sizes, and percentage of immigrants successfully breeding) made it difficult to convert estimates based on population genetics Population genetics
The study of both experimental and theoretical consequences of mendelian heredity on the population level, in contradistinction to classical genetics which deals with the offspring of specified parents on the familial level. to absolute numbers of immigrant individuals. Consequently, we chose a range of values commensurate with the moderate levels of gene flow found (online Appendix Table).
Estimating Asia-to-America Influenza Influxes
To estimate a baseline delivery rate of Asian-origin AI viruses to Alaska through these overlapping migration systems, we considered movement rates (M) of individuals from Asia (i) to Alaska (j) in conjunction with infection rates (I) and the incidence of specific influenza virus strains ([V.sub.x]) that we detected in this study. Measuring the risk associated with this threat thus becomes [M.sub.ij] x I = Asian-origin infected bird arrival; strain-specific incidence ([V.sub.x]) can be added to assess the narrower risk for subtypes, e.g., H5.
Within Alaska, the complexities of bird migration shape the taxonomic and geographic space where Asian-origin AI viruses are most likely to appear. Using Asian species as a guide, we coupled their distributions with those of American migrants (which are necessary to effectively transfer Asian AI virus to the greater New World) to define the extensive overlap of intercontinental avifaunas in northwestern North America (Figure) as the Beringian Crucible. Because of the mingling of intercontinental avifaunas, this area is most likely to harbor host switching and genetic reassortment among AI viruses from Asia and the Americas.
Our surveillance of wild-bird AI virus focused on the eastern, or North American, part of the Beringian Crucible (Figure). We found low rates of infection among the 8,254 samples obtained from the most important host groups, waterfowl (Anatidae) and shorebirds (Charadriidae and Scolopacidae; online Appendix Table). From these samples we obtained only 5 isolates, which represent an infection rate of just 0.061%. These isolates included hemagglutinin hemagglutinin /he·mag·glu·ti·nin/ (-gloo´ti-nin) an antibody that causes agglutination of erythrocytes.
cold hemagglutinin one which acts only at temperatures near 4° C. subtypes H3, H4, and H6 (29). The 5 isolates were found in 3 (0.2%) of 1,477 green-winged teal (Anas crecca), 1 (0.76%) of 131 mallards (Anas platyrhynchos), and 1 (0.03%) of 3,703 northern pintails (Anas acuta). We found neither evidence of a clearly Eurasian origin for any of the virus genes sequenced from these Alaska isolates (29) nor H5 subtypes. Our data do show a remarkably close genetic association between avian influenza (H6) virus in Alaska ducks and a poultry outbreak in California in nucleoprotein nucleoprotein
Macromolecular complex consisting of a protein linked to a nucleic acid, either DNA or RNA. The proteins that combine with DNA are generally of characteristic types called histones and protamines. and nonstructural protein A genes (29). This finding reflects real-time connections of migratory ducks between Alaska and California, and this vector connection extends into the Russian Far East Russian Far East, formerly Soviet Far East, federal district (1989 est. pop. 7,941,000), c.2,400,000 sq mi (6,216,000 sq km), encompassing the entire northeast coast of Asia and including the Sakha Republic, Maritime Territory (Primorsky Kray), (30). These findings affirm the intracontinental importance and risk posed by this region.
The number of individuals of the most important host groups (waterfowl and shorebirds) that come to Alaska from Asia is an important and heretofore unknown variable that affects the level of risk posed by these birds. Asian species are easiest to enumerate To count or list one by one. For example, an enumerated data type defines a list of all possible values for a variable, and no other value can then be placed into it. See device enumeration and ENUM. , because species-level identity indicates origin. However, many key vector species occur on both sides of the North Pacific and move regularly between Asia and North America (online Appendix Table) and thus represent another important group of species for risk assessment. Within-species intercontinental movements of taxa taxa: see taxon. that are distributed across both Asia and North America are challenging to quantify. Most species-level information is inadequate, and methods such as bird banding have not provided numeric estimates of these movements. We have summarized available data and used population genetics in 2 key vector species to estimate degrees of intercontinental avifaunal interchange in this region (online Appendix Table; an expanded version is available from the authors). Our population genetic work used 2 complementary methods and focused on 2 duck species carrying AI viruses in this region. For green-winged teal, assignment tests using AFLP markers showed that [approximately equal to] 2 (5%) of 40 individuals from Alaska appeared to be recent immigrants from Asia. In mallards, migration-rate values (4N [sub.e]m, the number of immigrants in relation to effective population size) for individuals coming from Asia to Alaska were 1,064-1,727 (95% confidence interval confidence interval,
n a statistical device used to determine the range within which an acceptable datum would fall. Confidence intervals are usually expressed in percentages, typically 95% or 99%. ) effective immigrants per generation. In each of these host species, intercontinental gene flow thus appears to be moderate (neither very low nor high), which indicates that thousands of individuals of these species may be coming to Alaska from Asia each year (online Appendix Table). These results corroborate To support or enhance the believability of a fact or assertion by the presentation of additional information that confirms the truthfulness of the item.
The testimony of a witness is corroborated if subsequent evidence, such as a coroner's report or the testimony of other the limited observational evidence from which we understood these movements to be well above zero but not high.
We estimate that 1.5-2.3 million birds from the families Anatidae, Charadriidae, and Scolopacidae come to Alaska from Asia each year (online Appendix Table). Multiplying this vector flow by the 0.061% AI infection rate that we measured among these families in Alaska suggests that 901-1,389 Asian-origin viruses may come from this source. However, our measure of infection rates is based on ducks in autumn, a taxonomic group and time known for increased infection rates (31,32). Although a few of our autumn duck samples are probably from birds coming from Asian breeding grounds, we have no isolates from Scolopacidae, perhaps due to fewer samples. Scolopacidae is the numerically dominant host group and is more likely to bring Asian-origin viruses in spring (online Appendix Table, ). Thus, our estimates of virus coming to Alaska from Asia can be considered to be high. Asian-origin AI virus arrival would most likely occur in the Beringian Crucible (Figure), which in western Alaska is 256,400 [km.sup.2], about the size of the United Kingdom or the US states of Wyoming or Oregon. Insofar in·so·far
To such an extent.
Adv. 1. insofar - to the degree or extent that; "insofar as it can be ascertained, the horse lung is comparable to that of man"; "so far as it is reasonably practical he should practice as we have not detected H5 or H7 subtypes among our 8,254 samples, their incidence has been too low to effectively measure. Given the statistical power of our sample, their delivery rate from Asia through this system appears to be very low.
Our surveillance did not show a "hotspot" of AI virus infection among avian hosts. Much higher infection rates are known from other multiyear surveillance studies at lower latitudes, e.g., Delaware Bay ([approximately equal to] 4.7%, ), southern Minnesota (10.8%, ), and Alberta (22.2%, ) and British Columbia in Canada (55%, although only a single-year study, ). The infection rates we found are substantially lower than those found for interior Alaska (9%, ). Arctic conditions in Alaska prevail well south of the Arctic Circle in the treeless regions of western Alaska, and the US Arctic includes the Alaska Peninsula and Aleutian Archipelago (34), a tundra ecosystem where our sampling was concentrated (Figure). Aerial surveys aerial surveys
an epidemiological technique for surveying animal populations and their habitat, especially the latter, over a very wide area. Requires special techniques adapted to sensing of electronically marked animals from a distance, and infrared scanning of vegetation. of waterfowl across Alaska show more ponds and fewer ducks per unit area on tundra; the number of ducks per pond on tundra habitat (2.1) is less than half the number found in the boreal-forest dominated interior (5.5, ). This simple ecologic factor (perhaps due to the lower productivity of these tundra ecosystems), resulting in the dilution of virus in waters with fewer available hosts, may in part explain our results. This is the first geographically and taxonomically extensive Arctic AI surveillance in North America, and it suggests that some Arctic effect lowers infection rates, thus lowering the risk of intercontinental viral transfer in these high-latitude regions. Our infection rates are low, comparable to those occurring at much lower latitudes (e.g., 9,35), whereas mid-latitude rates can be 2-3 orders of magnitude higher (33).
Human population densities in Alaska are relatively low, especially in the Beringian Crucible, and Alaska lacks a large agricultural sector. However, mammalian carnivores abound and could be susceptible hosts (36). Direct human infection from wild birds is possible, but transmission from birds to humans is difficult (37,38). Nevertheless, exposure in this region may be considerable; hunters kill [approximately equal to] 99,000 waterbirds for food each year on the Yukon-Kuskokwim Delta alone (39).
Although the existence of North American and Eurasian viral lineages is well established in the literature, evidence from other regions of North America has shown that geographic structure has been insufficient to prevent sporadic intercontinental exchange of some hemagglutinin subtypes (29,40). Our results can be considered to confirm the comparative rarity of such events in this important region of Alaska. Despite high diversity of host species and high numbers of individual birds in Alaska making intercontinental movements, the low AI infection rates and the genetic attributes of virus isolates (29) suggest that at most only small numbers of Asian-origin AI viruses or genes likely arrive in Alaska annually. Although AI viruses from Alaska have a clear link with other viruses in the lower 48 US states (29), the predominance of Arctic ecologic conditions and the lack of agriculture in the Alaska region most affected suggest a low risk for intercontinental viral transfer in this region.
We thank the many people who helped us collect samples; Robert Gill and the Alaska Shorebird Working Group, who provided advanced report data; the 2 reviewers who provided helpful comments; and the US Coast Guard, Yukon-Delta National Wildlife Refuge National Wildlife Refuge , Izembek National Wildlife Refuge, Alaska Maritime National Wildlife Refuge The Alaska Maritime National Wildlife Refuge (often shortened to Alaska Maritime or AMNWR) is a United States National Wildlife Refuge comprising 2,400 islands, headlands, rocks, islets, spires and reefs in Alaska, with a total area of 4. , Alaska Department of Fish and Game (Nome), and Bureau of Land Management, which provided logistical support.
The US Department of Agriculture (SCA (Single Connector Attachment) An 80-pin plug and socket used to connect peripherals. With a SCSI drive, it rolls three cables (power, data channel and ID configuration) into one connector for fast installation and removal. 58-6612-8-022 & SCA 58-6612-2-217), the University of Alaska Museum, the Arctic Archival Observatory (NSF NSF - National Science Foundation DEB-9981915), and the US Fish and Wildlife Service provided financial support.
Dr Winker is curator of birds and associate professor at the University of Alaska Fairbanks UAF is home to seven major research units: the Agricultural and Forestry Experiment Station; the Geophysical Institute, which operates the Poker Flat Research Range; the International Arctic Research Center; the Arctic Region Supercomputing Center; the Institute of Arctic Biology; the . His research interests include avian evolution, cyclic migration, and birds as disease vectors.
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Address for correspondence: Kevin Winker, University of Alaska Museum, 907 Yukon Dr, Fairbanks, AK 99775, USA; email: ffksw@ uaf.edu
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* University of Alaska Museum, Fairbanks, Alaska, USA; ([dagger]) Institute of Arctic Biology, Fairbanks, Alaska, USA; ([double dagger]) Yukon Delta National Wildlife Refuge The Yukon Delta National Wildlife Refuge is a United States National Wildlife Refuge covering about 19 million acres (77,000 km²) in southwestern Alaska. It is a coastal plain extending to the Bering Sea, covering the delta created by the Yukon and Kuskokwim rivers. , Bethel, Alaska, USA; ([section]) Russian Academy of Sciences Russian Academy of Sciences (Russian: Росси́йская Акаде́мия Нау́к, , Vladivostok, Russia; ([paragraph]) World Health Organization, Geneva Geneva, canton and city, Switzerland
Geneva (jənē`və), Fr. Genève, canton (1990 pop. 373,019), 109 sq mi (282 sq km), SW Switzerland, surrounding the southwest tip of the Lake of Geneva. , Switzerland; and (#) United States Department of Agriculture United States Department of Agriculture (USDA),
n.pr established in 1862, USDA is responsible for the safety of meat, poultry, and egg products. It conducts ongoing research in areas from human nutrition to new crop technologies and also helps ensure open , Athens, Georgia, USA
Kevin Winker, * Kevin G. McCracken, * ([dagger]) Daniel D. Gibson, * Christin L. Pruett, * ([dagger]) Rose Meier, * Falk Huettmann, ([dagger]) Michael Wege, ([double dagger]) Irina V. Kulikova, ([section]) Yuri N. Zhuravlev, ([section]) Michael L. Perdue, ([paragraph], #) Erica Spackman, (#) David L. Suarez, (#) and David E. Swayne (#)