Avian Influenza & pigeons Scientific
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Preface

Dear pigeon vet, pigeon fancier,

In the attached article, we tried to give a scientific based review of the different researches that has been done on Avian Influenza and the role of the pigeon.

Please feel free to inform us if you have any scientific based research that isn't mentioned here, also your comments are more than welcome!!

We want to thank Dr. Swayne, Dr. Miller, Dr. Walker and Dr. Talaber for their comments.

If you want to be kept informed about new researches about pigeons and AI or pigeons in general, please let us know.

Regards,

Gordon Chalmers, DVM, Canada
Pascal Lanneau, DVM, Belgium

Introduction

This article is completely dedicated to the Avian Influenza (AI) and the role of the pigeons in the spread of the virus.
It is based on pure scientific literature and all the comments are from people with authority concerning veterinary medicine.

There are 4 sections in this article:

1. Some Scientific articles

All the articles are abstracts from Pubmed, the National Library of Medicines from the USA

2. Comments from professors and vets all over the world

I would like to thank all the persons who gave their opinion about the AI and the role of the pigeons in it, based on scientific knowledge

3. Conclusion

4. References to articles

I would like to thank Gordon Chalmers, DVM from Canada for the references he sent to me.

Please feel free to let me know your opinion
or if you have some new information

Important note; this article will be updated when there is some new information available!!! If you want to be sure you have the latest article, please mail us: pascallanneau@skynet.be

Some Scientific articles
concerning Avian Influenza and pigeons

Dtsch Tierarztl Wochenschr. 2004 Dec; 111(12): 467-72

Review of the literature on avian influenza A viruses in pigeons and experimental studies on the susceptibility of domestic pigeons to influenza A viruses of the haemagglutinin subtype H7.

Kaleta EF, Honicke A.

Klinik fur Vogel, Reptilien, Amphibien und Fische, Fachbereich Veterinarmedizin, Justus-Liebig-Universitat Giessen, Frankfurter. erhard.f.kaleta@vetmed.uni-giessen.de

The scientific literature of the past century is reviewed on fowl plague (presently termed highly pathogenic avian influenza, HPAI) in pigeons. HPAI viruses cause epidemic disease outbreaks with high rates of losses in many avian species, particularily in chickens and turkeys. Also susceptible to disease are quails, guinea fowl, ducks, geese, ostriches, passerine birds, and birds of prey whereas conflicting reports on the susceptibility of the domestic pigeon exist. Based on literature reports and on own experiments, and applying as criteria for judgements clinically overt forms of disease, virus multiplication plus shedding and seroconversion, it is concluded that domestic pigeons are only partially susceptible to influenza A viruses of the haemagglutinin subtype H7. Infection of pigeons with H7 viruses results only in some of them in signs, virus shedding and seroconversion. Using the same criteria, pigeons appear to be even less susceptible to infection with influenza A viruses of the H5 subtype. Only one of five publications describe in 1/19 pigeons exposed to H5 influenza A virus depression one day before death, and only 2/19 multiplied and excreted virus, and 1/19 developed circulating antibodies. Consequently, pigeons play only a minor role in the epidemiology of H5 influenza viruses. In contrast, following infection with influenza A virus of the subtype H7 clinical signs in pigeons consist of conjunctivitis, tremor, paresis of wings and legs, and wet droppings. H7-infected pigeons multiply and excrete H7 viruses and develop circulating antibodies. Albeit of the status of infection, free-flying domestic pigeons can act as mechanical vectors and vehicles for long-distance transmission of any influenza A virus if plumage or feet were contaminated.

Avian Pathol. 2004 Oct 33 (5): 492-505

Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002.

Ellis TM, Bousfield RB, Bissett LA, Dyrting KC, Luk GS, Tsim ST, Sturm-Ramirez K, Webster RG, Guan Y, Malik Peiris JS.

Tai Lung Veterinary Laboratory, Agriculture Fisheries and Conservation Department, Lin Tong Mei, Sheung Shui, New Territories, Hong Kong SAR, China. ellis_trevor@afcd.gov.hk

Outbreaks of highly pathogenic H5N1 avian influenza have occurred in Hong Kong in chickens and other gallinaceous poultry in 1997, 2001, twice in 2002 and 2003. High mortality rates were seen in gallinaceous birds but not in domestic or wild waterfowl or other wild birds until late 2002 when highly pathogenic H5N1 avian influenza occurred in waterfowl (geese, ducks and swans), captive Greater Flamingo (Phoenicopterus ruber) and other wild birds (Little Egret Egretta garzetta) at two waterfowl parks and from two dead wild Grey Heron (Ardea cinerea) and a Black-headed Gull (Larus ridibundus) in Hong Kong. H5N1 avian influenza virus was also isolated from a dead feral pigeon (Columba livia) and a dead tree sparrow (Passer montanus) during the second outbreak. The first waterfowl outbreak was controlled by immediate strict quarantine and depopulation 1 week before the second outbreak commenced. Control measures implemented for the second outbreak included strict isolation, culling, increased sanitation and vaccination. Outbreaks in gallinaceous birds occurred in some live poultry markets concurrently with the second waterfowl outbreak, and infection on a chicken farm was detected 1 week after the second waterfowl park outbreak was detected, on the same day the second grey heron case was detected. Subsequent virus surveillance showed the outbreaks had been contained.

The susceptibility of pigeons to Avian Influenza A/chicken/Germany/2003 (H7N7)
O. Werner , E. Starick and J.P. Teifke

Bundesforschungsanstalt für Viruskrankheiten der Tiere Insel Riems, Germany

11 pigeons were inoculated oculonasal with the HPAIV subtype H7N7. 1 pigeon wasn’t infected and was the control. On day 1 post-infection, they placed in the same room 6 young SPF-chickens, who stayed together with the pigeons whole the time.4 SPF-chickens were inoculated oculonasal with the same virus in another room. On day 1 - 6 –8 –10 –14 post-infection, they took a throat and cloaca swab for virus isolation. On day 3 and 6 post infection, they did euthanasia on 2 pigeons and 10 different organs were taken for virus-isolation and anatomo-pathological research. Bloodsamples were taken on the day before infection, and on day 14 – 23 – 28 – 36 post-infection, searching for antibodies against Avian Influenza subtype 7. They did euthanasia after 36 days on all animals followed by an anatomo-pathological research and took bloodsamples. 2 from the 4 SPF-chickens that were infected got diarrhea, on day 2 they all were ill, on day 3 + 4 they all died.
The infected pigeons stayed all healthy without any symptoms, just like the non-infected pigeon. There were even no clinical signs and anatomo-pathological they couldn’t see any sign. The SPF-chickens who were in the same room and were not experimental inoculated showed also no clinical and anatomo-pathological sign at all. Virus isolation out of the inner organs were all negative. They could do a virusisolation out of the throat swabs from 9 of the 11 pigeons on day 1, and 2 from 11 out of the cloaca swab. On day 2 this was respectively 4 and 4. On day 3, 3 pigeons and on day 4 and 5 they could isolate virus out of the throat swabs, but from day 6 on everything was negative. Apparently there is a very small multiplication of the virus, and also some shedding of the virus, but not enough for infecting the SPF-chickens. In one pigeon stayed everything negative, just as the control animal during the time of research. The antibody titer was in 5 from 7 (who lived during the whole research period) low and never higher than 24, except from 2 animals. This can be seen as a reaction against the inoculum, because the control animal was always negative. There were never antibodies in the SPF-chickens that weren’t infected.
Important note: The pigeons will never be infected with such a high dose of virus as in this research was done

Avian Dis. 2003; 47 (3 Suppl) 849-56

The quest of influenza A viruses for new hosts.

Liu M, Guan Y,Peiris M, He S, Webby RJ, Perez D, Webster RG.

St. Jude Children's Research Hospital, Division of Virology, Department of Infectious Diseases, 332 N. Lauderdale, Memphis, TN 38105, USA.
There is increasing evidence that stable lineages of influenza viruses are being established in chickens. H9N2 viruses are established in chickens in Eurasia, and there are increasing reports of H3N2, H6N1, and H6N2 influenza viruses in chickens both in Asia and North America. Surveillance in a live poultry market in Nanchang, South Central China, reveals that influenza viruses were isolated form 1% of fecal samples taken from healthy poultry over the course of 16 months. The highest isolation rates were from chickens (1.3%) and ducks (1.2%), followed by quail (0.8%), then pigeon (0.5%). H3N6, H9N2, H2N9, and H4N6 viruses were isolated from multiple samples, while single isolates of H1N1, H3N2, and H3N3 viruses were made. Representatives of each virus subtype were experimentally inoculated into both quail and chickens. All the viruses replicated in the trachea of quail, but efficient replication in chickens was confined to 25% of the tested isolates. In quail, these viruses were shed primarily by the aerosol route, raising the possibility that quail may be the "route modulator" that changes the route of transmission of influenza viruses from fecal-oral to aerosol transmission. Thus, quail may play an important role in the natural history of influenza viruses. The pros and cons of the use of inactivated and recombinant fowl pox-influenza vaccines to control the spread of avian influenza are also evaluated.

Avian Dis. 2002 Jan-Mar; 46(1): 53-63.

Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks, and pigeons.

Perkins LE, Swayne DE.

Southeast Poultry Research Laboratory, United States Department of Agriculture, Agricultural Research Service, Athens, GA 30605, USA.

The H5N1 type A influenza viruses that emerged in Hong Kong in 1997 are a unique lineage of type A influenza viruses with the capacity to transmit directly from chickens to humans and produce significant disease and mortality in both of these hosts. The objective of this study was to ascertain the susceptibility of emus (Dramaius novaehollandiae), domestic geese (Anser anser domesticus), domestic ducks (Anas platyrhynchos), and pigeons (Columba livia) to intranasal (i.n.) inoculation with the A/chicken/Hong Kong/220/97 (H5N1) highly pathogenic avian influenza virus. No mortality occurred within 10 days postinoculation (DPI) in the four species investigated, and clinical disease, evident as neurologic dysfunction, was observed exclusively in emus and geese. Grossly, pancreatic mottling and splenomegaly were identified in these two species. In addition, the geese had cerebral malacia and thymic and bursal atrophy. Histologically, both the emus and geese developed pancreatitis, meningoencephalitis, and mild myocarditis. Influenza viral antigen was demonstrated in areas with histologic lesions up to 10 DPI in the geese. Virus was reisolated from oropharyngeal and cloacal swabs and from the lung, brain, and kidney of the emus and geese. Moderate splenomegaly was observed grossly in the ducks. Viral infection of the ducks was pneumotropic, as evidenced by mild inflammatory lesions in the respiratory tract and virus reisolation from oropharyngeal swabs and from a lung. Pigeons were resistant to HK/220 infection, lacking gross and histologic lesions, viral antigen, and reisolation of virus. These results imply that emus and geese are susceptible to i.n. inoculation with the HK/220 virus, whereas ducks and pigeons are more resistant. These latter two species probably played a minimal epidemiologic role in the perpetuation of the H5N1 Hong Kong-origin influenza viruses.

Avian Dis. 1996 Jul-Sep; 40 (3): 600-4

Susceptibility of pigeons to avian influenza.

Panigrahy B, Senne DA, Pedersen JC, Shafer AL, Pearson JE.

National Veterinary Services Laboratories, U.S. Department of Agriculture, Ames, Iowa 50010, USA.

Susceptibility to infection with avian influenza virus (AIV) was studied in pigeons inoculated via oculonasal (Experiment 1) or intravenous (Experiment 2) route. Chickens were included as susceptible hosts in both experiments. Two subtypes each of the highly pathogenic AIV (HPAIV; HP CK/PA H5N2 and HP CK/Australia H7N7) and non-pathogenic AIV (NPAIV; NP CK/PA H5N2 and NP emu/TX H7N1) at a dose of 10(5) embryo infective dose per bird were used as inoculum. The pigeons inoculated with HP CK/PA H5N2 or HP CK/Australia H7N7 remained apparently healthy throughout the 21-day observation period, did not shed viruses on 3, 7, 14, and 21 days postinoculation (DPI), and had no demonstrable levels of antibodies on 21 DPI. On the other hand, 9 of 12 chickens inoculated with the HPAIV died of highly pathogenic avian influenza; the viruses were recovered from their respiratory and intestinal tissues, and the surviving chickens had antibodies to AIV. Regarding responses of pigeons to inoculation with NP CK/PA H5N2 or NP emu/TX H7N1, the pigeons remained clinically healthy throughout the 21-day observation period and did not have detectable levels of antibodies on 21 DPI; only one pigeon yielded the NP emu/TX H7N1 on 3 DPI. The virus was isolated from a tracheal swab and was believed to be the residual inoculum virus. Based on the responses of pigeons to NPAIV and HPAIV, it was concluded that the pigeons were resistant or minimally susceptible to infection with HPAIV or NPAIV

Comments from veterinarians
concerning Avian Influenza and pigeons

David E. Swayne, DVM, PhD
Laboratory Director
Southeast Poultry Research Laboratory
USDA/ARS
934 College Station Road
Athens, Georgia
Telephone: 706-546-3433
Fax: 706-546-3161

Personal correspondence with Dr. David E Swayne (USA) concerning the AI problematic

Dear Dr. Lanneau

The email I sent to Dr. Chalmers is factually correct, the commentary he placed on my statements are not within the context which I had answered his questions over 4 months ago. The original questions he sent me were:

A nearby city of close to 1 million people (Calgary, Alberta, Canada) is proposing a bylaw to ban pigeons on the basis of their concerns about Avian Influenza, etc.. I have been asked to respond to these concerns, so was wondering if there is anything new from your research on the strain that was allegedly causing illness in pigeons and school children in SE Asia. I'd be grateful if you could provide any update on the virus and its relationship to illness in pigeons. Many thanks for any help you can offer. Kind regards, Gord Chalmers, DVM.

My response was:

Dr. Kaleta recently published review of Avian Influenza (AI) in pigeons and concluded, as I also believe, that pigeons are resistant to avian influenza viruses and have not been a reservoir or vector of the virus. DTW.Deutsche.tierarztliche.Wochenschrift 111(12):467-472, 2004.
Other studies have support the resistance of pigeons to AI virus infections. Some people have confused die-offs in pigeons to avian influenza when paramyxovirus type 1 is a common cause of neurological disease and death in pigeons and not avian influenza.
We have conducted experimental studies in pigeons using viruses isolated from dead pigeons in Thailand. Even direct inoculation of these viruses into nasal cavity of pigeons caused limited infections with between 60-80% of the pigeons not becoming infected. This suggests the mortality from H5N1 HPAI virus in pigeons may have resulted from synergy between AI infection and some other pathogen.
The "illness in school children" is an unsubstantiated rumor. No AI virus was isolated from the children and I am unaware of any evidence of infection.
With this scientific information, it is unlikely that banning pigeons will have any impact on AI ecology and will not reduce the risk AI infections of poultry or humans. The primary species that have natural infections with AI viruses are wild ducks and shorebird (turnstones, gulls, etc.). Columbiformes and passerines are not reservoirs and they are rarely incidental hosts following spill-over of the viruses from infected domestic poultry.

Some rebuttal to misinterpretation of my earlier statements.

1) The comments in the last paragraph above refer to global ecology of LPAI viruses, not specific to the Asian H5N1 HPAI virus (I used specifically different terms in the first half of the email - Asian H5N1 HPAI viruses- verses AI ecology in the last paragraph). Which is historically correct - pigeons are resistant to LPAI viruses and have not been involved in the ecology on a worldwide basis.
2) The banning of racing pigeons in Calgary, a location that does not have the Asian H5N1, would have no impact of the broad ecology of AI viruses since they are not the natural hosts of wild bird LPAI viruses. This would be predominately some species of wild ducks and shorebirds. This does not mean that pigeons are not susceptible to some AI virus; i.e. Dr. Kaleta's comment on H7 infections. However, surveys of pigeons have shown either no natural infections or rare infections (except with Asian H5N1 HPAI virus where die-offs of pigeons and infections have been identified).
3) My research data in pigeons as cited in paragraph 3 above shows that pigeons can be susceptible to the more recent Asian H5N1 HPAI viruses. This was not the case with the 1997 Hong Kong H5N1 HPAI virus where the virus did not grow in pigeons after intranasal inoculation. This would indicate, in geographic areas with new Asian H5N1 HPAI viruses circulating in wild birds or poultry, restricting the flying of pigeons would be prudent for pigeon health and to prevent addition of a new vector of the virus in the specific region. But a worldwide ban on flying pigeons is not supported by scientific information on ecology of LPAI viruses
Thanks for bringing these misinterpretations to my attention and I would hope you would disseminate my response to other pigeon veterinarians and fanciers.
Regards
David E. Swayne, DVM, PhD
Laboratory Director

Dr. Gordon Chalmers from Canada

Personal correspondence with Dr. Gordon Chalmers (Canada) concerning AI problematic

If you examine the previous statement from Dr Swayne, you will see that, even though 60-80% of the inoculated birds did not become infected, 20-40% developed 'limited infections', so it seems that, yes, pigeons can be infected at times with AI viruses, in this case an H5N1 virus.
Dr Kaleta feels that H7 AI viruses seem to be able to infect pigeons more readily than H5 viruses.

With this information and the current problems in Europe and Asia, I think it is important for pigeon fanciers to be very careful for the future, especially because of the H5N1 virus now in Europe.

The Dutch authorities this summer showed the value of isolating their poultry flocks to protect them from contact with wild birds that might be carrying influenza viruses. We should learn from their experience and isolate our pigeons for the same reasons. This means no outside exercise, no access to aviaries, no loft visiting, no exchanges of birds, no visits to poultry shows, and if necessary, no racing either. Our birds can live to race another day!

Dr. Paul Miller from America
Part I

Personal correspondence with Dr. Paul Miller (USA) concerning the AI problem

Hello Dr. Lanneau,

Thank you for your e-mail and attached literature survey.

I am currently attending the AAVLD convention, and the topic is to be discussed at length by the experts tomorrow. I briefly talked with one of them, Dr. D. J. King from Southeastern Poultry Lab in Athens, GA on Saturday. He feels that there is some variation between the H types, but that in general, pigeons make very poor hosts for AI. In some cases they can be infected to the point that they seroconvert, that is, the immune system 'sees' the AI antigen, considers it to be 'foreign' and responds. I will try to give you a more detailed commentary after the convention is over.
My personal view of all the AI publicity is that it is media hype and pure fear mongering. All the human deaths are in countries with very poor sanitation and hygiene standards, and abysmal medical infrastructure. The fact is that, with West Nile fading fast, the medical establishment needs a new poster child, a disease that will 'kill us all' if we don't give them billions of $$$. The US government is caving in to this nonsense with a $7.1B control program to forestall this phantom disease.
I will let you know what the pigeon aspect of this is after the convention. Dr. King told me that he has just submitted a draft of a new paper he has written on Newcastle in pigeons; it should be out in a few months, probably in Avian Diseases.
There was also some question about Adeno Virus in pigeons; some feel that it is an intestinal form of Circo. There has been some difficulty identifying the inclusion bodies in the intestine under Electron Microscopy as true Adenovirus. Sorry to be so brief. I'll try to be more complete later. Hope all is well with you. Kindest Regards,
Paul Miller

Dr. Paul Miller from America
Part II

Pigeons play a very minimal role in the entire Avian Influenza scene. Up until the emergence of the virulent H5N1 about a year ago, they did not get H5 at all. About a year ago, the H5N1 in Asia and Europe became more virulent, even pathogenic to its natural host, ducks, and this virulent form can infect pigeons to a limited degree. Dr. David Swayne from Athens, GA gave a talk yesterday at the AAVLD convention in which he presented this information. There is some variation among the H-types, but none go into pigeons very well, and pigeons do not transmit Avian Influenza well at all.

This new pathogenic strain of H5N1 (in Europe and Asia) has been put into pigeons; it infects only a small percentage of the birds exposed. It will even kill a few. Pigeons are still very poor hosts for Avian Influenza. For further information, I would suggest that you contact Dr. David Swayne directly at the South Eastern Poultry Research Lab in Athens, GA.

Pigeons and poultry are as different as day and night. It is obvious from the Taxonomy: Galliformes and Columbiformes. From an Avian Influenza point of view, pigeons are different from any other bird: they just do not host Influenza well. Viruses in general are quite particular about the cell type and the cell surface that they will use for replication. Apparently pigeons lack the cell surface receptors and the cell physiology to accommodate the Influenza virus. It has to do with the cellular nature of the bird. Even if you take a pathogenic strain, such as the current Asian H5N1, they still can not be efficiently infected; only a few can be infected.
The basic situation here is this. The current hype about Avian Influenza mutating into a form highly contagious and fatal to humans is nothing short of fear mongering. Such an event is theoretically possible, but highly improbable, especially in the current state of medical preparedness. All the people who have died of Avian Influenza were in situations of compromised hygiene and sanitation with substandard medical care. Many lived with their chickens in the same house. Since the decline of West Nile as a significant health threat in the US, the medical bureaucracy has needed a new ‘poster child’, a menacing disease which will surely ‘kill us all’ if we don’t give them billions of dollars. Avian Influenza fills that need, and obviously the drug and vaccine companies have jumped onto the band wagon. You would have a better chance of winning the lottery than you would of getting Avian Influenza; the chances are that slim.

At a meeting I was at yesterday at the AAVLD convention, I asked a CDC (Center for Disease Control) representative after a talk on Avian Influenza about the chances of any of this happening. She refused to even discuss the subject of what are the possibilities that this will actually happen. All she wanted to talk about is how horrendous things would be if it actually did happen: fear mongering, plain and simple. The CDC, WHO, OIE and several other medical bureaucracies obviously need more money, and their ticket is fear mongering some phantom Avian Influenza outbreak into a full blown crisis.

Dr. Colin Walker from Australia

Personal correspondence with Dr. Walker Colin (Australia) concerning the AI problematic

Pascal,
As you say AI is very topical at the moment particularly in Australia because of our proximity to Indonesia and also because we did recently have 3 pigeons in quarantine test positive for AI antibodies. My understanding of AI in pigeons is that pigeons can catch AI but tend to be a rather resistant species so that if they do become infected the symptoms are fairly mild, they quickly recover and the carrier state does not occur.
Regards
Colin Walker, BVSc

Dr. Zsolt Talaber from Hungary

Personal correspondence with Dr. Zsolt Talaber (Hungary) concerning the AI problematic

I think that pigeons can be infected with AI viruses. It seems like the pigeons have more resistance against the AI viruses as other bird species, but at times pigeons can catch this viruses and the illness can develop in them. Moreover, pigeons can spread the AI viruses mechanically, on their plumage, feet etc

In case of AI we should say the pigeons are like as the other bird species. Theoretically ALL bird species can spread the AI viruses mechanically, and a lot of them can fall ill with avian influenza. So the answer: pigeons must be separated from other birds, but literally. Moreover, the AI viruses are capable of mutation, and a "successful" mutation of AI can be with extraordinary consequences in pigeons. The chance of it is bigger if pigeons fall in with AI viruses frequently.

Conclusion
concerning Avian Influenza and pigeons

If you read all the recent articles, I think there is consequently one opinion that is important.

Although the pigeons are very resistant to the Low pathogenic Avian Influenza (LPAI), there is a chance that they become infected with the high Pathogenic Avian Influenza(HPAI, H5N1), this is confirmed by recent research. This means that we have to be careful in this matter concerning the outbreak of the AI.
Pigeons don’t play a very important role in the transmission of the AI, but not important doesn’t mean that they don’t play a role at all!!!

We don’t have to exaggerate the role of the pigeon in this matter at all, but don’t minimize it also!!!

I would like to conclude with the words of my friend Dr. Gordon Chalmers from Canada, which are almost the same as those from Dr. Paul Miller from USA, and also my opinion concerning this very hot item:

As pigeon fanciers and pigeon veterinarians, we have to be aware that there are some evidences that pigeons can be infected by the presently active Highly Pathogenic Avian Influenza H5N1.
This means that we have to be carefull in times of infection in the local areas with that strain!!
This means that quarantine could be very useful when a country or region is infected to protect against exposure from wild birds that could carry the virus.

References
concerning Avian Influenza and pigeons

Easterday, B.C. and V.S. Hinshaw. 1991. Influenza. In: Calnek, B.W. ed, Diseases of Poultry, 9th Ed. pps 532-551. Iowa State University Press, Ames.

Tudor, D.C. 1991. Avian Influenza. In: Pigeon Health and Disease, 41 -
44. Iowa State University Press, Ames

Gregory, D. 1993. Avian Influenza in U. S.A. In: Information Bulletin,
January 25, 1993. Food and Inspection Branch, Agriculture Canada, Ottawa,
Ontario.

Nettles, V.F., J.M. Wood, and R.G. Webster. 1985. Wildlife surveillance associated with an outbreak of lethal H5N2 avian influenza virus in domestic poultry. Avian Dis 29: 733-741.

Lang, G., B.T. Rouse, 0. Narayan, A.E. Ferguson and M.C. Connell. 1968. A new influenza virus infection in turkeys, 1. Isolation and characterization of virus 6213. Can. Vet. J. 9: 22-29.

Narayan, 0., G. Lang, and B. T. Rouse. 1969. A new influenza A virus infection in turkeys. IV. Experimental susceptibility of domestic birds to virus strain Turkey/Ontario/7732/1966. Arch. Gesamte Virusforsch. 26: 149-165,

Slemons, R.D. and B.C. Easterday. 1972. Host response differences among 5 avian species to an influenza virus -- A/Turkey/Ontario/7732/66 (HaV5N?). Bull. World Health Org. 47: 521-525.

Additional References:

Hinshaw, V.S. 1987. The nature of avian influenza in migrating waterfowl, including interspecies transmission, Proc, 2nd Internat Symp, Avian Influenza., pp 133-141, U.S. Animal Health Assoc., Athens Ga.

Hinshaw, V.S., V.F. Nettles, L.E. Schoff, J.M. Wood, and R.G. Webster. 1986. Influenza virus surveillance in waterfowl in Pennsylvania after the HSN2 avian outbreak. Avian Dis 30: 207 - 211.

Most recent references:

Panigrahy B, DA Senne, JC Pedersen, AL Shafer and JE Pearson. 1996. Susceptibility of pigeons to avian influenza. Avian Dis 40: 600-604.

Guan Y, KF Shortridge, S Kraus, PS Chin, KC Dyrting, TM Ellis, RG Webster and TM Peiris. 2000. H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in Southern China. J Virol 74: 9372-9380.

Perkins LE and DE Swayne. 2002. Pathogenicity of a Hong Kong-origin H5N1 highly avian influenza virus for emus, geese, ducks, and pigeons. Avian Dis 46: 53-63. (dswayne@seprl.usda.gov)

Kaleta EF and A Honicke. 2004. Review of the literature on avian influenza A viruses in pigeons and experimental studies on the susceptibility of domestic pigeons to influenza A viruses of the haemagglutinin subtype H7. Dtsch Tierarztl Wochenschr 111: 467-472.

Capua I, F Mutinelli, MA Bozza, C Terregino and G Catoli. 2000. Highly pathogenic avian influenza (H7N1) in ostriches (Struthio camellus). Avian Pathol 29: 643-646.

Ellis TM, RB Bousfield, LA Bissett, KC Dyrting, GSM Luk, ST Tsim, K Sturm-Ramirez, RG Webster, Y Guan and JSM Peiris. 2004. Investigations of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathol 33: 492-505.

Guan Y, JSM Peiris, AS Lipatov, TM Ellis, KC Dyrting, S Krauss, LJ Zhang, RG Webster and KF Shortridge. Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proc Nat Acad Sci (PNAS) 99: 8950-8955.

Kaleta EF and A Hönicke. 2005. A retrospective description of a highly pathogenic avian influenza virus (H7N1/Carduelis/Germany/72) in a free-living siskin (Carduelis spinus Linnaeus, 1758) and its accidental transmission to yellow canaries (Serinus canaria Linnaeus, 1758). Dtsch. Tieräztl Wschr 112: 1-40.

Liu M, Y Guan, M Peiris, S He, RJ Webby, D Perez and RG Webster. 2003. The quest of influenza A viruses for new hosts. Avian Dis 47: 849-856.

Manvell RJ, P McKinney, U Wernery and K Frost. 2000. Isolation of a highly pathogenic influenza A virus subtype H7N3 from a peregrine falcon (Falco peregrinus). Avian Pathol 29: 635-637

Gordon Chalmers, DVM, Canada
Pascal Lanneau, DVM, Belgium

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