Surveillance of Influenza A Virus in Migratory Waterfowl in Northern Europe

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Volume 13, Number 3?March 2007

Research

Surveillance of Influenza A Virus in Migratory Waterfowl in Northern Europe

Anders Wallensten,*? Vincent J. Munster,? Neus Latorre-Margalef,? Mia Brytting,? Johan Elmberg,# Ron A.M. Fouchier,? Thord Fransson,** Paul D. Haemig,? Malin Karlsson,? ?ke Lundkvist,? Albert D.M.E. Osterhaus,? Martin Stervander,?? Jonas Waldenstr?m,??? and Bj?rn Olsen???
*Smedby Health Center, Kalmar, Sweden; ?Link?ping University, Link?ping, Sweden; ?Erasmus Medical Center, Rotterdam, the Netherlands; ?Kalmar University, Kalmar, Sweden; ?Swedish Institute for Infectious Disease Control, Solna, Sweden; #Kristianstad University, Kristianstad, Sweden; **Swedish Museum of Natural History, Stockholm, Sweden; ??Ottenby Bird Observatory, Degerhamn, Sweden; ??Lund University, Lund, Sweden; and ??Ume? University, Ume?, Sweden
Suggested citation for this article
Abstract
We conducted large-scale, systematic sampling of influenza type A virus in migratory waterfowl (mostly mallards [Anas platyrhynchos]) at Ottenby Bird Observatory, southeast Sweden. As with previous studies, we found a higher prevalence in fall than spring, and among juveniles compared with adults. However, in contrast to other studies, we found that prevalence in spring was sometimes high (mean 4.0%, highest 9.5%). This finding raises the possibility that ducks are capable of perpetuating influenza A virus of different subtypes and subtype combinations throughout the year and from 1 year to the next. Isolation of the H5 and H7 subtypes was common, which suggests risk for transmission to sensitive domestic animals such as poultry. We argue that wild bird screening can function as a sentinel system, and we give an example of how it could have been used to forecast a remote and deadly outbreak of influenza A in poultry.

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Journal of Virology, April 2005, p. 4201-4212, Vol. 79, No. 7
0022-538X/05/$08.00+0 doi:10.1128/JVI.79.7.4201-4212.2005

Isolation and Characterization of Avian Influenza Viruses, Including Highly Pathogenic H5N1, from Poultry in Live Bird Markets in Hanoi, Vietnam, in 2001

Doan C. Nguyen,1,2 Timothy M. Uyeki,1 Samadhan Jadhao,1 Taronna Maines,1 Michael Shaw,1 Yumiko Matsuoka,1 Catherine Smith,1 Thomas Rowe,1, Xiuhua Lu,1 Henrietta Hall,1 Xiyan Xu,1 Amanda Balish,1 Alexander Klimov,1 Terrence M. Tumpey,1 David E. Swayne,3 Lien P. T. Huynh,2 Ha K. Nghiem,2 Hanh H. T. Nguyen,2 Long T. Hoang,2 Nancy J. Cox,1 and Jacqueline M. Katz1*
Influenza Branch, Centers for Disease Control and Prevention, Atlanta,1 Southeast Poultry Research Laboratory, Agriculture Research Service, Department of Agriculture, Athens, Georgia,3 National Institute of Hygiene and Epidemiology, Hanoi, Vietnam2
Received 24 August 2004/ Accepted 12 November 2004

Since 1997, outbreaks of highly pathogenic (HP) H5N1 and circulation of H9N2 viruses among domestic poultry in Asia have posed a threat to public health. To better understand the extent of transmission of avian influenza viruses (AIV) to humans in Asia, we conducted a cross-sectional virologic study in live bird markets (LBM) in Hanoi, Vietnam, in October 2001. Specimens from 189 birds and 18 environmental samples were collected at 10 LBM. Four influenza A viruses of the H4N6 (n = 1), H5N2 (n = 1), and H9N3 (n = 2) subtypes were isolated from healthy ducks for an isolation frequency of over 30% from this species. Two H5N1 viruses were isolated from healthy geese. The hemagglutinin (HA) genes of these H5N1 viruses possessed multiple basic amino acid motifs at the cleavage site, were HP for experimentally infected chickens, and were thus characterized as HP AIV. These HA genes shared high amino acid identities with genes of other H5N1 viruses isolated in Asia during this period, but they were genetically distinct from those of H5N1 viruses isolated from poultry and humans in Vietnam during the early 2004 outbreaks. These viruses were not highly virulent for experimentally infected ducks, mice, or ferrets. These results establish that HP H5N1 viruses with properties similar to viruses isolated in Hong Kong and mainland China circulated in Vietnam as early as 2001, suggest a common source for H5N1 viruses circulating in these Asian countries, and provide a framework to better understand the recent widespread emergence of HP H5N1 viruses in Asia.

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Dtsch Tierarztl Wochenschr. 2005 Dec;112(12):448-56.

Avian influenza A viruses in birds --an ecological, ornithological and virological view.

Kaleta EF, Hergarten G, Yilmaz A.
Klinik fur Vogel, Reptilien, Amphibien und Fische, Fachbereich Veterinarmedizin, Justus-Liebig-Universitat Giessen. erhard.f.kaleta@vetmed.uni-giessen.de
Avian influenza A viruses (AIV) are the causative agents of the presently most important poultry disease. Ten countries in Asia and several other countries in Eastern Europe suffer high losses from the lethal effects of these viruses of the H5N1 subtype. AIV of other subtypes cause in additional countries severe losses. The threat to health and well-being of the avifauna, domestic poultry and possibly mammals including humans are worldwide of major concern. The European Union reacted with a complete import ban on untreated meat, eggs, poultry products as well as free-living and pet birds. Extensive surveillance of free-living birds and domestic poultry that is maintained in free-range and close to open waters were initiated in an attempt to gather information on the current status of infection with these viruses and to target appropriate countermeasures for the protection of domestic poultry (in-house keeping) and to safeguard food production for humans. Since the monitoring of free-living birds is labour-intensive, costly, and time-consuming, only birds should be included in the monitoring programme that harboured in the past most if not all influenza A viruses. The birds of the order Anatiformes, family Anatidae, subfamilies Anserinae and Anatinae, provided 65.9 % of all avian AIV isolates. The cosmopolitan Common Mallard (Anas platyrhynchos) is the dominant species with the highest rate of isolations among all bird species. Second in frequency is the North-American Blue-winged Teal (Spatula discors). Consequently, free-living anatiform birds of the genera Anas and Spatula should comprise the main focus for the collection of cloacal and pharyngeal swabs. With the likely exception of the most recent H5N1 viruses, signs of disease were not recorded in AIV infected anatiform birds. AIV isolations were definitely less frequently obtained from birds of the orders Phasianiformes (including domestic chickens and turkeys), Charadriiformes (plovers and lapwings), Lariformes (gulls), Columbiformes (pigeons) and Psittaciformes (psittacines) and need less attention in sampling efforts. This review presents also data on taxonomy and most suitable means for isolation and typing of haemagglutinating viruses. The different frequencies of the detection of 16 haemagglutinin (HA) subtypes and 9 subtypes of neuraminidase (NA) surface antigens are composed on the basis of extensive literature retrievals. Both antigens occure in isolates at different frequencies. Only 103 of all 144 possible HA x NA combinations were described so far. The AIV that contain the HA subtypes H3, H4, H6 are most frequently isolated whereas the AIV of the subtypes H5 and H7 were less frequently encountered. All other HAs are rather rare. AIV that possess the NA of the subtypes N2, N1, N8 and N3 are frequent and all other NAs are rarely detected.
PMID: 16425630 [PubMed - indexed for MEDLINE]

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=16425630&itool=iconabstr&query_hl=3&itool=pubmed_docsum

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Re: AI Prevalence in wild birds (migratgory waterfowl)

J Virol. 2004 Aug;78(16):8771-9.

Matrix gene of influenza a viruses isolated from wild aquatic birds: ecology and emergence of influenza a viruses.

Widjaja L, Krauss SL, Webby RJ, Xie T, Webster RG.
Division of Virology, Department of Infectious Diseases, Mail Stop 330, St. Jude Children's Research Hospital, 332 N. Lauderdale St., Memphis, TN 38105, USA.

Wild aquatic birds are the primary reservoir of influenza A viruses, but little is known about the viruses' gene pool in wild birds. Therefore, we investigated the ecology and emergence of influenza viruses by conducting phylogenetic analysis of 70 matrix (M) genes of influenza viruses isolated from shorebirds and gulls in the Delaware Bay region and from ducks in Alberta, Canada, during >18 years of surveillance. In our analysis, we included 61 published M genes of isolates from various hosts. We showed that M genes of Canadian duck viruses and those of shorebird and gull viruses in the Delaware Bay shared ancestors with the M genes of North American poultry viruses. We found that North American and Eurasian avian-like lineages are divided into sublineages, indicating that multiple branches of virus evolution may be maintained in wild aquatic birds. The presence of non-H13 gull viruses in the gull-like lineage and of H13 gull viruses in other avian lineages suggested that gulls' M genes do not preferentially associate with the H13 subtype or segregate into a distinct lineage. Some North American avian influenza viruses contained M genes closely related to those of Eurasian avian viruses. Therefore, there may be interregional mixing of the two clades. Reassortment of shorebird M and HA genes was evident, but there was no correlation among the HA or NA subtype, M gene sequence, and isolation time. Overall, these results support the hypothesis that influenza viruses in wild waterfowl contain distinguishable lineages of M genes.
PMID: 15280485 [PubMed - indexed for MEDLINE]

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Avian Dis. 2003;47(3 Suppl):861-6.

Circulation of influenza viruses in wild waterfowl wintering in Italy during the 1993-99 period: evidence of virus shedding and seroconversion in wild ducks.

De Marco MA, Foni GE, Campitelli L, Raffini E, Di Trani L, Delogu M, Guberti V, Barigazzi G, Donatelli I.
Istituto Nazionale per la Fauna Selvatica A. Ghigi, 9 via Ca' Fornacetta, 40064 Ozzano Emilia (BO), Italy.
The mechanisms of perpetuation of influenza A viruses in aquatic birds, their main reservoir in nature, have not yet been completely clarified. One hypothesis is that they continue to circulate in waterfowl throughout the year, even though virus isolations during the winter months are rare. We analyzed influenza virus circulation in wild ducks in Italy during six winter seasons (1993-99), using virus isolations and serological analyses. It was apparent that influenza A viruses were constantly circulating in wild birds during all the seasons considered. Moreover, seroconversion rates (obtained from ducks recaptured during the same season) suggest a frequency of influenza infections higher than expected on the basis of the virus isolation rates.
PMID: 14575078 [PubMed - indexed for MEDLINE]

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=14575078&query_hl=3&itool=pubmed_DocSum

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Virus Genes. 2003 Dec;27(3):291-6.
Phylogenetic analysis of hemagglutinin and neuraminidase genes of H9N2 viruses isolated from migratory ducks.

Liu JH, Okazaki K, Shi WM, Kida H.
Laboratory of Microbiology, College of Veterinary Medicine, China Agricultural University, Beijing, 100094, People's Republic of China. ljh@cau.edu.cn
Genetic analysis indicated that the pandemic influenza strains derived from wild aquatic birds harbor viruses of 15 hemagglutinin (HA) and 9 neuraminidase (NA) antigenic subtypes. Surveillance studies have shown that H9N2 subtype viruses are worldwide in domestic poultry and could infect mammalian species, including humans. Here, we genetically analyzed the HA and NA genes of five H9N2 viruses isolated from the migratory ducks in Hokkaido, Japan, the flyway of migration from Siberia during 1997-2000. The results showed that HA and NA genes of these viruses belong to the same lineages, respectively. Compared with those of A/quail/Hong Kong/G1/97-like and A/duck/Hong Kong/Y280/97-like viruses, HA and NA of the migratory duck isolates had a close relationship with those of H9N2 viruses isolated from the chicken in Korea, indicating that the Korea H9N2 viruses might be derived from the migratory ducks. The NA genes of the five isolates were located in the same cluster as those of N2 viruses, which had caused a human pandemic in 1968, indicating that the NA genes of the previous pandemic strains are still circulating in waterfowl reservoirs. The present results further emphasize the importance of carrying out molecular epidemiological surveillance of H9N2 viruses in wild ducks to obtain more information for the future human influenza pandemics preparedness.
PMID: 14618090 [PubMed - indexed for MEDLINE]

http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=14618090&query_hl=3&itool=pubmed_DocSum

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J Gen Virol. 2004 Aug;85(Pt 8):2327-37.

Influenza A viruses in feral Canadian ducks: extensive reassortment in nature.

Hatchette TF, Walker D, Johnson C, Baker A, Pryor SP, Webster RG.
Division of Virology, Department of Infectious Diseases, St Jude Children's Research Hospital, 332 North Lauderdale Street, Memphis, TN 38105-2794, USA.

The current dogma of influenza accepts that feral aquatic birds are the reservoir for influenza A viruses. Although the genomic information of human influenza A viruses is increasing, little of this type of data is available for viruses circulating in feral waterfowl. This study presents the genetic characterization of 35 viruses isolated from wild Canadian ducks from 1983 to 2000, as the first attempt at a comprehensive genotypic analysis of influenza viruses isolated from feral ducks. This study demonstrates that influenza virus genes circulating in Canadian ducks have achieved evolutionary stasis. The majority of these duck virus genes are clustered in distinct North American clades; however, some H6 and H9 genes are clustered with those from Eurasian viruses. Genes appeared to reassort in a random fashion. None of the genotypes identified remained present throughout all of the years examined and most PA and PB2 genes that crossed over into swine were clustered in one phylogenetic grouping. Additionally, matrix genes were identified that branch very early in the evolutionary tree. These findings demonstrate the diversity of the influenza virus gene pool in Canadian ducks, and suggest that genes which cluster in specific phylogenetic groupings in the PB2 and PA genes can be used for markers of viruses with the potential for crossing the species barrier. A more comprehensive study of this important reservoir is needed to provide further insight into the genomic composition of viruses that crossover the species barrier, which would be a useful component to pandemic planning.
PMID: 15269374 [PubMed - indexed for MEDLINE]

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Arch Virol. 2000;145(5):885-93.

Precursor genes of future pandemic influenza viruses are perpetuated in ducks nesting in Siberia.

Okazaki K, Takada A, Ito T, Imai M, Takakuwa H, Hatta M, Ozaki H, Tanizaki T, Nagano T, Ninomiya A, Demenev VA, Tyaptirganov MM, Karatayeva TD, Yamnikova SS, Lvov DK, Kida H.

Department of Disease Control, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan.
Influenza A viruses of different subtypes were isolated from fecal samples of ducks in their nesting areas in Siberia in summer from 1996 to 1998. Phylogenetic analysis of the NP genes of the isolates in Siberia and those in Hokkaido, Japan on their flyway of migration from Siberia to the south in autumn revealed that they belong to the Eurasian lineage of avian influenza viruses. It is noted that the genes of the isolates in Siberia are closely related to those of H5N1 influenza virus strains isolated from chickens and humans in Hong Kong in 1997 as well as to those of isolates from domestic birds in southern China. The results indicate that influenza viruses perpetuated in ducks nesting in Siberia should have contributed genes in the emergence of the H5N1 virus in Hong Kong. Vaccine prepared from avirulent A/duck/Hokkaido/4/96 (H5N3) influenza virus was potent enough to protect mice from challenge with lethal dose of the pathogenic H5N1 virus [19]. Intensive surveillance study of aquatic birds especially in Siberia is, therefore, stressed to provide information on the future pandemic influenza virus strains and for vaccine preparation.
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J Vet Med B Infect Dis Vet Public Health. 2006 Apr;53(3):105-10.

A virological survey in migrating waders and other waterfowl in one of the most important resting sites of Germany.

Hlinak A, Muhle RU, Werner O, Globig A, Starick E, Schirrmeier H, Hoffmann B, Engelhardt A, Hubner D, Conraths FJ, Wallschlager D, Kruckenberg H, Muller T.
State Laboratory Brandenburg, Frankfurt (Oder), D-15236 Frankfurt (Oder), Germany. andreas.hlinak@llb.brandenburg.de
Wild birds are considered a potential reservoir or a carrier of viral diseases and may therefore play a role in the epidemiology of economically important or zoonotic diseases. In 2001 and 2002, a survey with special emphasis on virus isolation in migrating waders and some other birds were conducted. In one of the most important inland resting sites for migratory waterfowl, tracheal and cloacal swabs were collected from 465 waders representing 19 different species, and 165 other birds that were not captured on purpose. A total of 42 avian viruses were isolated, 34 of these were identified as paramyxoviruses (PMVs). The majority of isolates came from waders and wild ducks, and were characterized as PMV-1. In contrast, PMV-4 was found in wild ducks only, PMV-6 was mainly detected in wader species. Four avian influenza viruses (AIVs), belonging to H4 and H3 haemagglutinin subtype, were isolated from wild duck species. Furthermore, four reo-like viruses were isolated from one particular wader species for the first time. The majority of virus positive birds were <1 year old and did not show any clinical symptoms. There was no evidence for the presence of West Nile virus in these birds. These results confirm that the restricted resting sites in Western Europe must be considered as important locations for the intra- and interspecies transmission of avian viruses.
PMID: 16629720 [PubMed - indexed for MEDLINE]

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Acta Vet Scand. 2005;46(4):193-202.

Screening of feral pigeon (Colomba livia), mallard (Anas platyrhynchos) and graylag goose (Anser anser) populations for Campylobacter spp., Salmonella spp., avian influenza virus and avian paramyxovirus.

Lillehaug A, Monceyron Jonassen C, Bergsjo B, Hofshagen M, Tharaldsen J, Nesse LL, Handeland K.
Section for Wildlife Diseases, National Veterinary Institute, Oslo Norway. atle.lillehaug@vetinst.no

A total of 119 fresh faecal samples were collected from graylag geese migrating northwards in April. Also, cloacal swabs were taken from 100 carcasses of graylag geese shot during the hunting season in August. In addition, samples were taken from 200 feral pigeons and five mallards. The cultivation of bacteria detected Campylobacter jejuni jejuni in six of the pigeons, and in one of the mallards. Salmonella diarizona 14: k: z53 was detected in one graylag goose, while all pigeons and mallards were negative for salmonellae. No avian paramyxovirus was found in any of the samples tested. One mallard, from an Oslo river, was influenza A virus positive, confirmed by RT-PCR and by inoculation of embryonated eggs. The isolate termed A/Duck/Norway/ 1/03 was found to be of H3N8 type based on sequence analyses of the hemagglutinin and neuraminidase segments, and serological tests. This is the first time an avian influenza virus has been isolated in Norway. The study demonstrates that the wild bird species examined may constitute a reservoir for important bird pathogens and zoonotic agents in Norway.
PMID: 16398331 [PubMed - indexed for MEDLINE]
ft= http://www.pubmedcentral.nih.gov/art...medid=16398331

[Shannon Bennett]

Re: AI Prevalence in wild birds (migratgory waterfowl)

I have come to the conclusion after reading all of these imports that these people don't talk to each other. Ducks are obviously ONE key component and very possibly the most important culprit to the H5N1 problem but, apparently not the only key. In 1918 the culprits were probably gulls that landed on the decks of the two ill fated ships that were the first to harbor the pandemic. One off the coast of western Africa and the other off Marseilles. Something else that greatly concerns me is the small sampling sizes listed in the above imports. How could anyone get a grasp of the situation with 200 samples or less? Apparently we are fighting the battle of H5N1 with one hand tied behind our backs.

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Re: AI Prevalence in wild birds (migratgory waterfowl)

Though it has been said that a more detailled knowledge of the epidemiology of AI in birds is essential to better understand and predict the evolution of AI, I have the impression there is a distinct difference between words and deeds and the political will to finance it.

Still two years ago, in Germany swan surveillance programs were classified "irrelevant" and stopped. Not even one year later swans played a key role in the outbreak of early 2006, and (of course) nobody had the slightest idea about how this could happen. Not even the regional migratory pattern of the mute and whistling swans was really established. A couple of years before the government had cut the budget for ornitological programs and shut down one orn. station.

You will hardly find surveillance studies focussed on the crucial point of the immunological status of wildlife birds.

The question is: Why?

Because taking blood samples it is to costintensive and much more diffucult than collecting droppings and testing them for RNA?

Because the fact that wild birds can survive HPAI infection and gain immunity, does not fit with a widespread criteria of HPAI H5?

In Austria a further study of the famous resistant swans was given up because the HI tests were not" validated for swans" and there was no "budget for validation" (source: personal contact). It will be thrilling how things will go on in the "Constance project"

[AlaskaDenise]

Re: AI Prevalence in wild birds (migratgory waterfowl)

Is this the "Constance Project" you are referencing?

http://constance.geneva21.biz/

Our Mission

The purpose and objective of Project Constance is to provide informational resources to mitigate, prevent and to confront some of the crucial problems, issues and challenges that threaten to annihilate Mankind, and perhaps this whole planet. We may not be able to do everything, but we can at least do something.


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Re: AI Prevalence in wild birds (migratgory waterfowl)

Is this the "Constance Project" you are referencing?

No, the Constanze project is an international AI research initiative financed by the countries neighboring the Lake Constance. The programm puts focus on the role of wild birds in particular waterfowl in thepropagation and persistence of AI and it contrast to the majoity of the current surveillance studies - emcompasses serologic testing and a sentinel system.

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Re: AI Prevalence in wild birds (migratgory waterfowl)

The Constanze project:

In early 2006, avian influenza A (H5N1) was detected in 32 bird samples in the vicinity of the Lake of Constance. In the context of this outbreak, a joint multi-national, multidisciplinary research programme is proposed. This consists of 5 individual scientific subprojects including their management. The questions of the proposed research programme are focused on (i) the species of wild birds found in the area of Lake Constance, (ii) the climate in this area and (iii) the any Influenza A virus serotypes isolated in 2006/2007. Any new virus found will be further characterized regarding pathogenicity in wild birds, poultry and pigs. Furthermore, H5N1 isolate (CH 2006) will be tested for pathogenicity in selected species such as waterfowl, poultry and pigs. In addition to the diagnostic tools available, species independent and type-specific ELISA will be developed. In order to detect the presence of H5N1 in the region, sampling of healthy wild birds and sentinel mallard ducks will be carried out and tested for the presence of Influenza virus A including H5N1. The role of the migration pattern of wild birds resident on the Lake Constance will be analysed. For this purpose, available data on bird ring findings will be evaluated. Results derived from this research project will allow for a risk-based monitoring of wild birds and an improvement of present surveillance programmes in general. The improvement includes the way of handling the sampling (e.g. the comparison of different swaps), the diagnostics (serology and virology) as well as the species of wild birds, the location, the point of time and the number of birds that have to be sampled. The results of this research project may have an impact on the Swiss legislation (modification of the TSG, TSV, technische Weisungen).

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