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Flu, Grippe, Avian Influenza, Grippe Aviaire, Fowl Plague, Swine Influenza, Hog Flu, Pig Flu, Equine Influenza, Canine Influenza
Last Updated: December 29, 2009
Influenza viruses are RNA viruses in the family Orthomyxoviridae that can affect birds and mammals including humans. Influenza B and C viruses are maintained only in human populations, although they are isolated occasionally from other mammals. 1-9 Influenza A viruses can affect many species, with the vast majority of these viruses occurring among birds. Waterfowl and shorebirds seem to the reservoir hosts for avian influenza viruses, which are usually carried asymptomatically in these populations.1,10-17 Avian influenza viruses can also become established among poultry, causing two forms of disease. Low pathogenicity avian influenza (LPAI) viruses, the form usually carried in wild birds, generally cause asymptomatic infections, mild respiratory disease or decreased egg production in poultry.11,13,14,18,19 Some LPAI viruses can mutate in poultry populations to become high pathogenicity avian influenza (HPAI) viruses. HPAI viruses cause a severe illness that can kill up to 90-100% of a flock.10,11,13 A few influenza A viruses have become adapted to mammals including humans, swine, horses and dogs, and circulate in these populations. These viruses are called human influenza A viruses, swine influenza viruses, equine influenza viruses and canine influenza viruses, respectively. In the mammalian species to which they are adapted, influenza viruses cause respiratory disease with high morbidity but low mortality rates. More severe cases can occur in conjunction with other diseases or debilitation, as well as in infancy or old age. Influenza A viruses that circulate in birds and mammals are occasionally transmitted from one species to another. In most cases, these infections do not spread efficiently; they remain limited to an individual or a small group, and soon disappear from the novel host population.1-4,11,20-24 However, some of these viruses can become adapted to a new species and cause outbreaks, epidemics or pandemics. 1,2,16,20,25-32 One equine influenza virus recently began circulating in dog populations, becoming the first canine influenza virus.28-30 Similarly, avian influenza viruses have caused or contributed to past pandemics in humans and pigs. 2,20,27,31 Avian and swine influenza viruses, which are the only animal influenza viruses known to recurrently affect humans, are of the greatest concern as zoonotic agents. The effects of avian influenza viruses on people are highly variable. Although many human infections are limited to conjunctivitis or mild respiratory disease, some viruses can cause severe disease and death.2,11,12,15,26,33-41 Currently, HPAI H5N1 avian influenza viruses seem to be the greatest threat to people, as well as to poultry. These viruses first emerged in the late 1990s. They have since become established among birds in Asia, have spread to other geographic regions, and continue to threaten new areas.11,12,42 As of December 2009, H5N1 viruses have been responsible for approximately 450 human infections, generally as the result of close contact with poultry; about 60% of all laboratory confirmed cases have been fatal.43 Asian lineage H5N1 viruses have also caused disease in housecats, several species of large felids, palm civets, raccoon dogs, stone martens, a dog and a mink. 9,11,44-55 Some of these infections were fatal. In addition, H5N1 viruses have been detected in pigs and pikas, and experimental infections have been established in a variety of species including foxes, ferrets, rodents and rabbits.34,51,56-58,58-70 Unusually, numerous deaths have been reported in wild birds, which are rarely affected by avian influenza viruses.11,12,51,54,7173 There are fears that an Asian lineage H5N1 strain could eventually become adapted to humans, possibly resulting in a severe human pandemic. Other avian influenza viruses can also undergo cross-species transmission. H9N2 (LPAI) viruses, which have become endemic in poultry in parts of Asia and the Middle East, may be of particular concern.36,74,75 These viruses have caused outbreaks among poultry in many countries,75-77 and it has been recently recognized that some isolates share internal genes with H5N1 viruses.74,78,79 H9N2 viruses have been detected in pigs with respiratory disease and fatal paralysis in China. 74 Antibodies to H9N2 viruses, as well as rare clinical cases, have also been reported in humans. 3638,74,74,80,81 As of December 2009, known human H9N2 infections have been relatively mild, and fatal cases have not been reported.36-38,74 Swine influenza virus infections also occur sporadically among people. Most of these cases have been relatively mild and some may have been asymptomatic, but
Author: Anna Rovid Spickler, DVM, PhD
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severe illnesses and a few deaths have been reported.1-3,2124,82-94 Swine influenza viruses are usually not welladapted to humans, and little or no person-to-person transmission usually occurs.1,2,22,24,89 Nevertheless, these viruses appear to have been responsible for the first human pandemic of the 21st century. In April 2009, a novel virus with the subtype H1N1 began circulating in people.93,95,96 The genetic analysis of this virus suggests that it originated from North American and Eurasian swine influenza viruses that reassorted.97-99 The novel H1N1 virus has also been transmitted from people to animals. Pigs are susceptible to this virus, and sporadic outbreaks have been reported among swine herds in a number of countries.100-116 Outbreaks have also been reported in turkey flocks, and a few cases have been recognized in pet ferrets, cats and dogs, as well as in a cheetah in a zoo.117-129 may contain some genes from one parent virus and some genes from the other.20 Reassortment between different strains results in the periodic emergence of novel strains. Reassortment between subtypes can result in the emergence of a new subtype. Reassortment can also occur between avian, swine, equine, canine and human influenza A viruses. This type of reassortment can result in a „hybrid‟ virus with, for example, both avian and human influenza virus proteins. An abrupt change in the subtypes found in a host species is called an „antigenic shift.‟ Antigenic shifts can result from three mechanisms: 1) genetic reassortment between subtypes, 2) the direct transfer of a whole virus from one host species into another, or 3) the re-emergence of a virus that was found previously in a species but is no longer in circulation.1,2 For example, human viruses can continue to circulate in pigs and could re-emerge into the human population.2 Antigenic drift and antigenic shifts result in the periodic emergence of novel influenza viruses. By evading the immune response, these viruses can cause influenza epidemics and pandemics.
Avian influenza viruses
Viruses in the family Orthomyxoviridae cause influenza. There are three genera of influenza viruses: influenzavirus A, influenzavirus B and influenzavirus C.130 Separate viral species are not recognized within these genera; the members of each genus belong to the three species “influenza A virus,” “influenza B virus” or “influenza C virus,” respectively.130 These viruses are also called type A, type B and type C influenza viruses. Influenza A viruses Influenza A viruses include avian, swine, equine and canine influenza viruses, as well as the human influenza A viruses. Influenza A viruses are classified into subtypes based on two surface antigens, the hemagglutinin (H) and neuraminidase (N) proteins. There are 16 hemagglutinin antigens (H1 to H16) and nine neuraminidase antigens (N1 to N9).11,13,19,23 These two proteins are involved in cell attachment and release from cells, and are also major targets for the immune response.2,20,131 Wild birds carry most of the known hemagglutinin and neuraminidase antigens, but some, such as H14 and H15, are uncommon and seem to occur only in limited geographic areas.17 Only limited subtypes are found in each species of mammal.3 Influenza A viruses are also classified into strains. Strains of influenza viruses are described by their type, host, place of first isolation, strain number (if any), year of isolation, and antigenic subtype.1,3 [e.g., the prototype strain of the H7N7 subtype of equine influenza virus, first isolated in Czechoslovakia in 1956, is A/eq/Prague/56 (H7N7).] For human strains, the host is omitted.
Antigenic shift and drift in influenza A viruses
Influenza A viruses change frequently. Strains evolve as they accumulate point mutations during virus replication; this process is sometimes called „antigenic drift.‟3 A more abrupt change can occur during genetic reassortment. Reassortment is possible whenever two different influenza viruses infect a cell simultaneously; when the new viruses (the „progeny‟) are assembled, they
Last Updated: December 2009 © 2009
Avian influenza viruses circulate in a variety of domesticated and wild birds.1,11,14,17,34 They are also isolated occasionally from mammals including humans.1,9,11,25,26,35,37,44-53,55-57,132,133 Avian influenza viruses are classified as either high pathogenicity (HPAI) or low pathogenicity (LPAI) viruses, based on the genetic features of the virus and the severity of disease in experimentally inoculated chickens.11,13,19 Although there are exceptions (e.g., viruses that fit the genetic description of HPAI viruses but cause mild illness), HPAI viruses usually cause severe disease in poultry, while LPAI infections are generally much milder. To date, all HPAI viruses have contained the H5 or H7 hemagglutinin; subtypes that contained other hemagglutinins have been found only in the LPAI form.12,18,19 H5 and H7 LPAI viruses can evolve into high pathogenicity strains, typically while they are circulating among poultry.11,12,15 When a subtype has become established and circulates for a time, numerous variants may occur in the population. For example, multiple genotypes and a number of clades of Asian lineage H5N1 viruses are currently found among poultry.11,40,42,134,135 In wild species, avian influenza viruses are especially common among birds that live in wetlands and other aquatic environments.17 Waterfowl (order Anseriformes) and shorebirds (order Charadriiformes) seem to be the natural reservoirs for influenza A viruses, and carry all of the known subtypes, usually in the LPAI form. 1,12-17,23 Important reservoir hosts include ducks, geese, swans, gulls, terns and waders.17 The LPAI viruses found in wild birds can be divided into Eurasian and American lineages.17 Although viruses occasionally cross between these two geographic regions, this is uncommon.17 The predominant subtypes in wild ducks change periodically. 1 H3, H4 and H6 are detected most often in North
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American and northern European wild ducks, but nearly all hemagglutinin and neuraminidase antigens can be found.17 Waders (families Charadriidae and Scolopacidae) seem to have a wider variety of hemagglutinin/ neuraminidase combinations than ducks. In the eastern U.S., H1 through H12 (LPAI) viruses have been isolated from these birds; H1, H2, H5, H7 and H9-H12 viruses are particularly common.17 Gulls are often infected with H13 LPAI viruses, which are rare in other avian species.17 They can also carry H16 viruses.17 Most, though not all, infections in wild waterfowl and shorebirds are asymptomatic.1,2,11,12,136,137 Limited information is available on the subtypes found in other species of birds. Subtypes that have been detected in ratites include H3N2, H4N2, H4N6, H5N1, H5N2, H5N9, H7N1, H7N3, H9N2, H10N1, H10N4 and H10N7.18,51,138-140 Isolates from cage birds usually contain H3 or H4; however, infections with high pathogenicity subtypes containing H7 or H5 can also occur.18,51,60,71,141,142 Very few avian influenza viruses were found in wild passerine birds, pigeons and doves in one survey.143
Swine influenza viruses
Swine influenza viruses mainly affect pigs, but they can cause disease in turkeys.1,3 Outbreaks have also been described recently in ferrets and mink.91,144 Other species may also be infected, although this seems to be rare. One H1N1 swine influenza virus, which was avirulent for both poultry and pigs, was isolated from a duck in Hong Kong, and experimental infections have been reported in calves.145,146 The most common subtypes currently found in pigs are H1N1, H1N2 and H3N2; however, the situation is complex, as two or more viruses of each subtype are circulating in swine populations.2,16,20,147 One H1N1 virus found in North America is the „classical‟ H1N1 swine influenza virus. This virus, the first influenza virus known to have infected pigs, was first detected in swine populations in 1918.1,2,16,20 Reassortant H1N1 viruses, which contain the same neuraminidase and hemagglutinin as the classical H1N1 virus, but have internal proteins from triple reassortant H3N2 viruses (see below), have recently become prominent among pigs in North America.148-150 An „avian-like‟ H1N1 virus circulates mainly in European pigs.2,16,20 This virus seems to be an avian influenza virus that was transmitted whole to pigs.16,20,151 It has, in some locations, replaced the classical H1N1 virus.16,20 A different „avian-like‟ H1N1 virus has been detected, together with the classical H1N1 virus, among pigs in Asia.9,16 Other variants have also been found. For example, H1N1 reassortant viruses consisting of classical swine influenza virus genes and a human PB1 polymerase gene have been detected in pigs in Canada152 and a wholly human lineage H1N1 virus was reported from pigs in China in 2007.153 In North America, some of the most important swine influenza viruses are the triple reassortant H3N2 viruses.
Last Updated: December 2009 © 2009
These viruses first emerged in U.S. pigs in the late 1990s, mainly in the Midwest,20,34,152,154,155 and they have been detected in Canada since 2005.89,144,156 The North American H3N2 triple reassortant viruses contain hemagglutinin and neuraminidase proteins from a human influenza virus, and internal proteins from the classical swine influenza virus, an avian influenza virus and a human influenza virus.154 The particular combination of internal genes carried by these viruses is known as the triple reassortant internal gene (TRIG) cassette. This cassette seems to be especially efficient in generating swine influenza virus recombinants with new hemagglutinin and neuraminidase genes, including some from human influenza viruses.149,150 Viruses with this cassette have had increased antigenic drift compared to other swine influenza viruses.149 H3N2 viruses also occur in Europe and Asia, but these viruses seem to be the result of reassortment between a human H3N2 virus, circulating there in pigs since the 1970s, and the H1N1 „avian-like‟ virus.2 The European H3N2 viruses contain human H3 and N2 proteins, and internal proteins from the avian virus.2 In China, H3N2 viruses that have been detected include double reassortants that contain human H3 and N2 and internal genes from avian influenza viruses, and triple reassortants with human H3 and N2 and internal gene segments from both swine and avian influenza viruses.157 Some wholly human-like H3N2 viruses have also been found among pigs in China.157 The H1N2 virus in the U.S. is a reassortant of the classical H1N1 swine influenza virus and the North American triple reassortant H3N2 virus.2 Other variants have also been detected. Some H1N2 viruses isolated from Canadian pigs contained neuraminidase and hemagglutinin genes from two different human influenza viruses, the polymerase gene from human H1N2 viruses, and other internal genes from classical H1N1 swine influenza viruses.152 The H1N2 virus in Europe is a reassortant of a human H1N1 virus and the „human-like‟ European H3N2 virus.2,16 In China, both the H1N2 swine influenza virus from North America, and apparent reassortants between the H1N1 classical swine influenza virus and North American H3N2 human influenza viruses have been reported.158 Other novel reassortants of swine influenza viruses continue to be discovered.159,160 New subtypes have also been found in some swine populations. The novel subtype H3N1 has recently been isolated from pigs in the U.S.161,162 This subtype appears to contain genes from human, swine and avian influenza viruses.161,162 A different H3N1 influenza virus, containing human and swine influenza virus genes, has been found in Korea163 and an H3N1 virus which may be a novel reassortant between H3N2 and H1N1 swine influenza viruses has been reported in Italy.164 An H2N3 virus isolated from pigs with respiratory disease in the U.S. contained genes from avian and swine influenza viruses.165 An avian H9N2 virus has been reported from
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outbreaks of respiratory disease and paralysis in pigs in southeastern China, and may circulate in swine populations there.74 This subtype appears to contain neuraminidase and hemagglutinin genes from avian H9N2 viruses and internal genes from an H5N1 virus (Sw/SD/2/03) that also infects pig populations in the area.74 Avian (LPAI) H5N2 and avian/swine H5N2 reassortant viruses have been isolated from pigs in Korea.166 The avian H5N2 virus appears to have been circulating among pigs since 2006.166
The novel H1N1 virus of swine origin
Swine influenza viruses are occasionally found in humans.1-4,21-24,82-94,144 In most cases, these viruses are poorly adapted to humans, and little or no person-toperson transmission occurs. 1,2,22,24,89 In 2009, a novel H1N1 virus, which seems to have originated from one or more swine influenza viruses, emerged in human populations.97-99 This virus appears to be a reassortant between North American and Eurasian swine influenza viruses; it contains a hemagglutinin gene that is most closely related to swine influenza viruses in North America, a neuraminidase gene that is related to swine influenza viruses in Eurasia, and internal genes from two or more swine influenza viruses including the North American triple reassortant H3N2 viruses and a Eurasian virus.97-99 Similarly to some of the swine influenza viruses described above, the parental swine influenza viruses include some gene segments that originally came from avian and human influenza viruses. 98,99 In 2009, the novel H1N1 virus was the dominant influenza virus being transmitted in human populations in most parts of the world.167 It has also been transmitted to animals, including pigs, apparently from infected humans. 100117,119-129
This virus appears to be an avian influenza virus. A related virus caused influenza in a few hundred horses the following year but there were no deaths. The avian-like virus continued to circulate in horses in China for at least five years without further fatalities. One equine H3N8 virus recently jumped into dogs in North America.28,29,173 Equine influenza viruses can also infect dogs without becoming established in canine populations. A limited outbreak with an equine H3N8 (American lineage) virus was reported among foxhounds in the U.K. in 2002,32 and equine H3N8 viruses were shown to infect dogs asymptomatically during close contact with horses in an experimental study.174 Infections with equine H3N8 viruses have been reported among pigs in China.175
Canine influenza viruses
An H3N8 canine influenza virus has been reported in canine populations in a number of U.S. states. 30,176-183 This virus appears to be an equine influenza virus (Florida sublineage) that recently jumped species, and it bears a close resemblance to an isolate seen in horses in Wisconsin in 2004; however, the canine influenza virus has diverged genetically from equine influenza viruses.28-30 An H3N2 virus, isolated during an outbreak of canine respiratory disease in Korea in 2007, has the potential to become a second canine influenza virus.133 There is evidence that this virus may have been transmitted between dogs during the outbreak, and dog-to-dog transmission occurs readily in experimentally infected dogs.133,184 The H3N2 virus seems to have originated in birds.133 It contains gene segments that may have come from several different avian viruses.133 At least three different isolates of this virus have been recovered.133
Human influenza A viruses
Equine influenza viruses
Equine influenza viruses mainly infect horses and other Equidae (i.e., donkeys, mules and zebras).1,25,168,169 The two subtypes known to circulate in equine populations and cause disease are H7N7 (equine virus 1) and H3N8 (equine virus 2).1,3,25 There is less antigenic drift in these viruses than human influenza A viruses. 3,25 H7N7 equine influenza viruses have become extinct or are present at only very low levels in most parts of the world where surveillance is conducted.1,25,170 In contrast, H3N8 viruses circulate widely. H3N8 viruses have diverged into distinct Eurasian and American evolutionary lineages.171,172 The American lineage contains the classical American lineage (also called the Kentucky lineage), the Florida sublineage (originally called the Florida lineage) and the South American lineage.172 Some viruses of the American lineage (Florida sublineage) have also become established in Europe and Asia.171,172 In 1989, a novel strain of equine influenza [A/eq/Jilin/89 (H3N8)] caused a serious epidemic, with high morbidity and mortality rates, in Chinese horses. 25,170
Last Updated: December 2009 © 2009
Human influenza A viruses are mainly found in people, but they can also infect ferrets and sometimes swine.1,3,5,16,152,153,185-188 Experimental infections have been reported in raccoons.189 Human viruses can also replicate, to a limited extent, in the nasal epithelium of experimentally infected horses.170 H1N1, H1N2 and H3N2 viruses are currently in general circulation in humans.11,190 H1N2 viruses were first seen in human populations in 2001, probably as a result of genetic reassortment between the H3N2 and H1N1 viruses.190,191 H2N2 viruses circulated in the human population between 1957 and 1968.1 A novel H1N1 virus (see above) emerged in human populations in 2009. Human influenza viruses change frequently as the result of antigenic drift, and occasionally as the result of antigenic shift. Epidemics occur every few years, due to small changes in the influenza viruses.2,192 Human pandemics, resulting from antigenic shifts, were most recently reported in 1918, 1957, 1968 and 2009.
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14 HPAI viruses have been eradicated from domesticated poultry in most developed nations. an equine H3N8 virus was responsible for an outbreak of respiratory disease in a foxhound kennel in 2002.197 Influenza B viruses are categorized into lineages rather than subtypes. ferrets. and accumulates few changes over time. reindeer and deer.60-64. to date.210 Swine influenza viruses are enzootic in most areas that have dense populations of pigs. Alabama.199.. Equine influenza occurs in nearly all countries with substantial numbers of horses.168-170.170 The H3N8 canine influenza virus has been reported in the U.202 Influenza C viruses have also been found in animals. and it is now co-circulating with the B/Victoria/2/87 lineage.9. Arkansas.1.198 In the 1990s.9 and swine influenza viruses have caused outbreaks in mink and ferrets.212 The H3N8 subtype is widespread in horse populations.K. sheep. viruses of the B/Yamagata/16/88 lineage circulated to a very limited extent in Asia. and are mainly associated with disease in people.47-49. any species other than birds.168. several species of large felids.201 Until recently. the B/Victoria/2/87 lineage predominated in human populations.51-58.180 Infections were first reported in the general canine population in Florida. but they are classified into strains.9 The Asian lineage H5N1 avian influenza viruses appear to have an unusually wide host range. Arizona.207. cattle.1.208 As of December 2009. humans. including the novel H1N1 virus that entered human populations in 2009.16 Although the subtypes of the swine influenza viruses found in the U.199 Recent evidence suggests that recombination between these two lineages is resulting in antigenic shifts. 4.190 Until recently. foxes. wild bird surveillance has not detected these viruses in North America or New Zealand. dogs and horses.178. stone martens.g. but they have not.1.57 there is currently no evidence that influenza viruses have become adapted to. 169 Only a few countries such as New Zealand and Iceland are known to be free from this disease. Rhode Island and Massachusetts.1. the Middle East and Africa.181-183.9. a nationwide epidemic of influenza C was reported in Japan between January and July 2004. swine. is patchy.131.177.131. The Asian lineage H5N1 HPAI outbreak began among poultry in Southeast Asia in 2003.11 Each strain is antigenically stable.11.12. raccoon dogs.1.S.214 H3N8 infections were reported from dogs in Australia during an equine influenza outbreak in 2007. Avian influenza viruses have infected pinnipeds. it caused an outbreak or was detected serologically in an area. HPAI H5N1 viruses spread into domesticated or wild birds in other regions of Asia as well as into parts of Europe.5. rodents. in some cases.200 Influenza C viruses Influenza C viruses circulate in human populations. rabbits and macaques.192. that reptiles and amphibians can be infected with influenza viruses. pikas.194-196 There are also some indications.213 There is no evidence that the canine influenza virus is currently circulating outside the U.213. all countries in Europe) eradicate these viruses whenever they occur in domesticated birds. In 2004-2006. palm civets. Texas.193 With the possible exception of H5N1 viruses in pikas.1. infections with equine influenza viruses are occasionally reported among dogs in other regions.44.203.12 From 2003 to 2007. yak.7173.193 and a variety of mammals have been infected experimentally.K.204 Last Updated: December 2009 © 2009 page 5 of 46 . though it occurs more slowly than in influenza A viruses. and can infect housecats. Colorado.34.11 Unusually. foxhounds were exposed to an H3N8 virus in 2003. they are actually different viruses (see „Etiology‟). this epizootic is ongoing and worldwide eradication is not expected in the short term.32.189. dogs. Iowa. and are circulating in.192. and influenza B viruses were said not to undergo antigenic shifts..25.9.213 The distribution of this virus in the U. They are also classified into strains.144 Antibodies to influenza viruses have been detected in other species including raccoons. These viruses can cause epidemics. goats.2.215 These cases appear to have been caused by H3N8 equine influenza viruses that did not become established in the canine population. 11.189.67-69. they had never been linked to large-scale epidemics. Kansas.132 Unpublished research suggests that some raccoons in Japan have antibodies to H5N1 viruses. cetaceans and mink. In the U. but later disappeared from that region.203 Recent evidence suggests that reassortment occurs frequently between different strains of influenza C viruses. and it has been reported from Africa. Influenza B viruses Influenza B viruses are known to circulate only in human populations.32.214 Limited serological evidence also suggests that some U.177.211 This disease is common in North and South America.45.198 This lineage emerged in various parts of the world in 2001.11 Although some countries (e.1.9. the Pacific.1 They have also been found occasionally in animals.10.1. Europe and parts of Asia.206 Avian influenza (LPAI) viruses also occur worldwide in wild birds and poultry. been responsible for pandemics.4. West Virginia.S.10. However.1-8 Influenza C viruses are not classified into subtypes.25. and Europe are the same. are found worldwide.Influenza Influenza A viruses in other species Geographic Distribution Human influenza viruses. infections were seen in racing greyhounds in a number of states including Florida.205. but the virus later spread to other states. these were also equine viruses that did not become Influenza A viruses are occasionally isolated from outbreaks or isolated cases in other species of mammals.S.91.11 Influenza B viruses undergo antigenic drift.209. mink.198.201 However.S. some Asian lineage H5N1 HPAI viruses are also circulating in wild bird populations in Eurasia. pigs.170 The H7N7 subtype is either extinct or present at very low levels.3. including the detection of viral nucleic acids by RT-PCR.
pH. salinity and the presence of organic material. however.12.216.3. 17 Wild birds usually carry only the low pathogenicity form of avian influenza viruses.11. but can persist for several hours in dried mucus. swine influenza viruses were inactivated in untreated pig slurry in 1-2.65.220 Although infected eggs are unlikely to hatch.226 They appear to survive best at low temperatures and in fresh or brackish water rather than salt water.218.190-192 Close contact and closed environments favor transmission.3. but they were inactivated more quickly when mixed with chicken manure.17 Some recent isolates of Asian lineage H5N1 (HPAI) viruses have been found in higher quantities in respiratory secretions than the feces. if it occurs at all.226 These viruses. may exchange viruses with other populations at staging. it can spread on the farm by both the fecal–oral route and aerosols.12.1.13 The feces contain large amounts of virus.15 Avian influenza viruses have also been found in the yolk and albumen of eggs from hens infected with HPAI viruses. which can fly long distances.133 poultry is controversial.41 Ingestion of H5N1 viruses has been reported in naturally infected housecats.217 Avian influenza viruses might survive indefinitely when frozen.225 Survival of influenza viruses in the environment Transmission Transmission of mammalian influenza viruses In mammals.217.49.216 One recent study suggested that H5 and H7 HPAI viruses may survive for shorter periods in water than LPAI viruses. Fomites can be important in transmission and flies may act as mechanical vectors. particularly those that live on land.207. experimentally infected cats.16. which are often transmitted between birds in feces.13.227 In other studies.216. but the current evidence suggests this is very rare.2.13 Migrating birds.226 LPAI viruses are reported to persist in distilled water for more than 100 days at 28°C (82°F) and 200 days at 17°C (63°F).25.11. ferrets.13. In one study. and for at least 20 days at 28-30°C (82-86oF).188 Transmission of avian influenza viruses among birds In birds. influenza viruses are transmitted in aerosols created by coughing and sneezing.49. and by contact with nasal discharges. It might also be possible for LPAI viruses to be shed in eggs.5 hours at 50-55°C (122-131°F). 30°C (86°F) or 37°C (18.104.22.168. either directly or on fomites. particularly at low temperatures. other felids and dogs.213 As of December 2009.13.223. leopards and tigers in zoos.12. two weeks at 20°C (68°F).229 One Asian lineage H5N1 infection occurred in a dog that had eaten infected duck carcasses.1.12.15. these viruses reassort and/or mutate to produce HPAI viruses. avian influenza viruses are shed in the feces as well as in saliva and nasal secretions. Close contact with dead or sick birds seems to be the principal way this virus is spread to humans.216 These viruses also remained viable for at least 35 days in peptone water at 4°C (39°F).63. as well as infected poultry or fomites. Similarly. it is possible that is might play a role in some species. pigs. the disease could be introduced into flocks by migratory waterfowl or shorebirds.11.217. the Asian lineage HPAI H5N1 strains appear to occur regularly in wild birds. broken eggs could transmit the virus to other chicks in the incubator.17. Transmission is best understood for the Asian lineage H5N1 (HPAI) viruses.17 Once they are introduced into poultry.Influenza adapted to dogs. stopover or wintering sites. may persist for relatively long periods in aquatic environments. but a few cases may have resulted from indirect exposure via contaminated feces.147.73 Fecal-cloacal transmission might also be possible.208.216 Various avian influenza viruses were reported to survive for four weeks at 18°C (64°F). due to the close proximity of the birds. and 9 weeks at 5°C (41°F).216 A few studies have examined virus persistence in feces.73. and swimming in contaminated water is theoretically a source of exposure. the H3N2 influenza virus has been reported only from dogs in Korea. at least in some wild birds.1.217 Respiratory transmission of LPAI viruses is thought to be unimportant in most wild birds.17 Fecal transmission is facilitated by the persistence of avian influenza viruses in aquatic environments for prolonged periods. although their importance in transmitting these viruses to Last Updated: December 2009 © 2009 The survival of avian influenza viruses in the environment is influenced by temperature.219 This suggests that.227 These viruses could survive for up to 32 days at 15-20°C (59-68oF). as well page 6 of 46 . mice and foxes. and rarely in humans. Once an avian influenza virus has entered a poultry flock. in utero transmission can occur with high viremia after experimental infection. LPAI viruses were reported to survive for at least 44 or 105 days in feces.1.217. In ferrets.6°F). and fecal-oral transmission is the predominant means of spread for LPAI viruses in wild bird populations. 228 Routes of transmission of avian influenza viruses to mammals Some avian influenza viruses can be transmitted to mammals by direct or indirect contact.17. In one study. however. LPAI viruses (H7N2) persisted for up to two weeks in feces and on cages.192 There is little information on the survival of mammalian influenza viruses in water or organic material. these strains may no longer be transmitted primarily by the fecal-oral route. However. they still persisted in fresh water for 100 days or more at 17°C (63°F) and for approximately 26-30 days at 28°C (82°F).216 Mammalian influenza viruses (which are shed in respiratory secretions) are relatively labile.45.12.224 HPAI H5N2 viruses have also been detected recently in some asymptomatic wild ducks and geese in Africa.222 In countries where HPAI has been eradicated from domesticated poultry.221.
which had been recovered from cats.3. oral and intraocular routes.34 This results in an increased opportunity for virus reassortment.69 Infected foxes can excrete this virus in both respiratory secretions and feces.42.66. It is. were apparently infected when they ate raw birds.55 In humans. horses.28. viral antigens and nucleic acids were detected in the fetus of a woman who died of an Asian lineage H5N1 infection. Some evidence also suggests that the H1N1 virus. This has happened occasionally with whole viruses that jump to new hosts. In most of the cases mentioned above. which caused the deadly 1918 „Spanish flu‟ pandemic.69 In experimentally infected dogs. the strongest evidence for oral transmission is that two people became infected with an Asian lineage H5N1 virus after eating uncooked duck blood.48.16. Over the decade that H5N1 viruses have been circulating among birds. and equine influenza viruses have infected dogs. was probably an intact avian virus that became adapted to humans.45. as well as by intranasal or intratracheal inoculation. and might have acquired the H5N1 virus from this source.2.20 It could also occur in an intermediate host.12.147 For this reason.16.11 Reassortment can occur in the new host‟s own cells.135 An early study showed that. 189 These raccoons could transmit this virus to uninfected raccoons. is a good example. avian influenza viruses have affected mink.) Recently. they have been called „mixing vessels‟ for the formation of new viruses.20 Many outbreaks end without permanent adaptation of the virus to the species.20 Pigs have receptors that can bind swine.9. there are grave concerns about the possibility that these viruses might become adapted to these species. Transmission of Asian lineage H5N1 viruses between mammals Because Asian lineage H5N1 avian influenza viruses can cause fatal disease in humans and other mammals. 230 Experimental studies suggest that Asian lineage H5N1 viruses can be transmitted to mammals by the respiratory. but pigs are known to shed it only from the respiratory tract.40. particularly a pig.53.65 Cats appear to shed these viruses from the intestinal tract as well as the respiratory tract.Influenza as some housecats.11. Repeated reassortment between human. limited transmission and cross-species jumps Ordinarily. H5N1 avian influenza viruses isolated from healthy ducks in southern China acquired the ability to replicate and cause lethal disease in page 7 of 46 .67.1. avian and swine influenza viruses has resulted in a wide variety of novel swine influenza viruses that contain segments originating from two or more species. 70 Fecal shedding of Asian lineage H5N1 virus may also be possible in humans: this virus has been recovered from a child with diarrhea. Raccoons that were intranasally inoculated with LPAI H4N8 viruses shed virus from the respiratory but not the digestive tract. Infections have been established in cats by intratracheal inoculation with Asian lineage H5N1 viruses and by feeding them H5N1-infected chicks. cattle excreted small amounts of H5N1 viruses from the respiratory tract after intranasal inoculation.31 Dissemination is more likely if the new virus reassorts with a virus that is already adapted to the species. these viruses have changed and differentiated into a number of strains and clades. efficient transmission requires a novel hemagglutinin and/or neuraminidase protein to evade the immune response.11. (See „Etiology‟ for a description of some of these viruses. After intraocular inoculation of mice and ferrets with H7 and H5N1 (HPAI) isolates. swine influenza viruses circulate only among pigs.132 Infected raccoon dogs in China were fed chicken carcasses. For example.58.26. but aerosol transmission could not be ruled out.3.68 In one experiment. swine influenza viruses have caused outbreaks in ferrets. In rural China and other regions.65 Pigs and foxes can also be infected by feeding them H5N1-infected poultry.11. one of these viruses may cause an outbreak.53.11.11. the virus eventually disappeared from the novel host population. a variety of species including ducks are kept in close proximity to each other and to humans. but fecal shedding has not been reported. however.196.23. however. 58.46.20 Occasionally. but additional routes of exposure also existed.2. together with viral proteins that are well adapted to the new host‟s cells. equine influenza viruses among the Equidae. which jumped from horses to dogs.27. many new viruses originate in Asia.235 Although reassortment can occur anywhere.50.63 Infected housecats in an animal shelter probably ingested contaminated feces from a swan while they were grooming.232. the viruses could be detected in the respiratory tract and caused systemic disease.231 In addition. Last Updated: December 2009 © 2009 avian influenza viruses among birds. and human influenza viruses among people. Although these viruses occasionally infect species other than their normal host.134.189 Transmission of influenza viruses between species – sporadic cases. from 1999 to 2002. however.133. Asian lineage H5N1 viruses have been found in respiratory secretions.233 Transplacental transmission of avian influenza viruses is not well studied in mammals. it may be found in the urine of some mammals. mink and turkeys.229 There are other human cases where ingestion probably occurred.2.91.9 The eye might act as an entry point for some HPAI viruses.32.63. The canine influenza virus.66.1. a high dose of the virus. the virus is usually poorly adapted to the new host population and often affects only one or a few individuals.20.234 There are few detailed reports of mammalian infections with avian LPAI viruses. was used to inoculate the cattle.12.4. human and avian influenza viruses.144 Generally.1. possible for a virus to become established in the new species. seals and pigs. all routes have not been reported in each species.25. quail cells have also been shown to bind both human and avian influenza viruses.
H10N7 and H6N1. neuraminidase and an internal protein. it is difficult to determine whether these viruses are more likely to infect humans than other subtypes.36 Some serological evidence suggests that poultry workers. With rare exceptions.43 Because exposure to these viruses can be high in some human populations.3% of the general population were seropositive. with the possible exception of pikas.63 No animal-toanimal transmission was reported in asymptomatic cats infected by exposure to a sick swan. as of December 2009.6-5.81 Symptomatic infections have occasionally been reported in H9N2-virus infected humans.41 (thus more likely to be diagnosed). the overall seroprevalence was 4.81 In one study. during a 2003 outbreak in the Netherlands. antibodies to H4.236 Whether this modification would allow the virus to be transmitted more efficiently from person to person is unknown.80.240-242 These antibodies may be more common among people who are exposed to free-range or backyard poultry than workers in poultry confinement facilities.67 However. an Asian lineage H5N1 virus was not transmitted to one dog or three cats in contact with four experimentally infected dogs.74. 15.Influenza mice.242. No sustained person-toperson transmission has been reported. Surveys in China report that from 0% to 4. an Asian lineage H5N1 virus with the ability to bind human receptors was isolated from a person in Thailand.12 In 2007. three family members of poultry workers were also infected. which had infected a turkey herd.20 Illnesses caused by H5. these viruses have not become adapted to people.236 This particular isolate was found only once.37 In general.37. with any of the viruses currently circulating in bird populations.5% of the human populations studied have antibodies to H9 viruses.244 Most of these infections occur after direct contact with pigs.94.62 As of December 2009. have been associated with disease in Chinese pigs.36.12. H7 and H9 avian influenza viruses are documented occasionally in people.11.21-24.80 Another survey reported seroprevalences of 0% to 1.82-90.74.75 Humans can also be infected with H9N2 viruses.81.35 The virus subtype was H7N7.34. and clinical illness is typically severe 12.34. or in experimentally infected pigs. have been established in human volunteers inoculated with some subtypes including H4N8. Some currently circulating H9N2 viruses might undergo relatively frequent cross-species transmission.12.9294.23. only rare cases of limited person-toperson spread have been documented. an H1N1 swine influenza virus.243 Experimental infections.2. Limited transmission of Asian lineage H5N1 viruses has been reported among zoo tigers and experimentally infected housecats. Sustained person-to-person transmission has never been reported. to date.12. H5.132 In one study. and 1. little or no host-to-host transmission has been seen in mammals. or to three dogs in contact with infected cats.58. accompanied in some cases by mild respiratory signs and other influenza symptoms. there is recent evidence that Asian lineage H5N1 viruses might have become established among some pika populations in China. Infections with swine influenza viruses are reported sporadically in humans.38 Swine influenza viruses in humans Two of the last four human pandemics appear to have been the result of reassortment between avian and human influenza viruses.57 In humans.80. H6.2. prolonged contact.12 Zoonotic influenza viruses reported in humans Infections with avian or swine influenza viruses are reported periodically in humans.34. after contact with infected poultry. Avian influenza viruses in humans Asian lineage H5N1 avian influenza viruses have been responsible for nearly 450 confirmed clinical cases in humans. If most infections resemble human influenza.11. For example.11. which circulate among poultry in parts of Asia and the Middle East. H9. and five other proteins from a human H1N1 strain.5% of poultry retailers. H7.20 The H3N2 „Hong Kong flu‟ virus of 1968 had two new proteins from an avian virus – the new hemagglutinin and an internal protein – but kept the neuraminidase and remaining proteins from the H2N2 virus. depending on the geographic area. they may not be Last Updated: December 2009 © 2009 page 8 of 46 .20 The 1957 H2N2 („Asian flu‟) virus contained avian hemagglutinin. these viruses do not seem to cause severe clinical signs in these animals. these cases appear to be clinically indistinguishable from human influenza virus infections. H10 and H11 viruses have been found in healthy people.1.38. and may have been eliminated by infection control measures.245 How often swine influenza viruses infect people is unknown.11. was then transmitted to a laboratory technician who developed respiratory signs.11.11. to date. and these cases occurred after close.7% of farmers and other poultry workers. veterinarians and hunters may be regularly exposed to avian influenza viruses of various subtypes.50.38 Most of these infections have resulted from direct contact with infected poultry or fomites. however.5%.74 H9N2 (LPAI) viruses.15. but viruses may also spread to people through another host. 2.7% in poultry workers.2.38.2.
acids.1. anorexia. when swine influenza in humans became reportable in the U. approximately one case was reported to the Centers for Disease Control and Prevention (CDC) every 1-2 years.23.131.130. sneezing.188 Nausea. the symptoms may last up to two weeks or longer. most infections appear after one to four days. the most extensive person-to-person transmission was reported in 1976.227 Avian influenza viruses seem to be more resistant to high temperatures and low pH than mammalian influenza viruses. as well as by ionizing radiation or low pH (pH 2).22.214.171.124.250 Genetic analysis suggests that this virus was probably transmitted to people very recently.2. a novel H1N1 virus with genes of swine origin became established in human populations. These viruses are mainly thought to cause mild upper respiratory disease in children and young adults. Serological evidence and one experiment in volunteers suggest that humans might be susceptible to equine viruses. formaldehyde). myocarditis.1. 1. including pneumonia. myalgia.190. can be seen in some individuals.216. weakness.S. abdominal pain and photophobia are also possible. and febrile seizures can occur in severe cases.Influenza investigated and recognized as zoonoses.131. for this virus. Before 2005.190-192 Diarrhea. the first symptoms occur in two to five days. 3. there are few reports on their clinical features. 12 cases were reported to the CDC. oxidizing agents.216. vomiting and otitis media are common in children. 70% ethanol. In Czechoslovakia.191 In addition.. especially those with chronic respiratory or heart disease.9 Infections in Humans Incubation Period The incubation period for seasonal human influenza is short. Last Updated: December 2009 © 2009 page 9 of 46 .188. five family members of an infected laboratory worker became ill. but in some cases.99 As of December 2009.22 Until 2009.246-248 Although many swine influenza virus infections seem to be limited to a single person.12 In most cases.131.21.000 people on a military base in Fort Dix.113.103.255 The incubation period for avian influenza in humans is difficult to determine. sore throat and a nonproductive cough. pericarditis and myositis.1.93 From December 2005 through February 2009.1. Reye syndrome.249.204.40 The World Health Organization (WHO) currently suggests using an incubation period of seven days for field investigations and monitoring patient contacts.1. quaternary ammonium compounds.191 In young children.98. this swine population has not been found.22 This virus remained limited to the base and did not spread to the surrounding community.12 Clinical Signs Seasonal human influenza Uncomplicated infections with human influenza A or B viruses are usually characterized by upper respiratory symptoms. the There are no published reports of equine or canine influenza viruses causing disease in humans after natural exposure.252 Equine influenza viruses and canine influenza viruses in humans aldehydes (glutaraldehyde.253 They can also be inactivated by heat of 56°C (133°F) for a minimum of 60 minutes (or higher temperatures for shorter periods). rhinitis.192. sometimes cases are followed by a few infections among close contacts.3. the initial signs may mimic bacterial sepsis. it may range from two to eight days and could be as long as 17 days. In 2009.93 Recent serological evidence suggests that swine influenza infections might occur regularly in people who have contact with pigs. phenols.104. when approximately 500 of 12.131. several health care workers developed influenza symptoms after exposure to a pregnant woman with swine influenza in Wisconsin. but more severe cases with lower respiratory signs including bronchitis or pneumonia can also occur. headache.119-129.108.240. transverse myelitis.21 One college student transmitted the virus to his roommate. some recent descriptions suggest that clinical cases may be indistinguishable from influenza A or B.190192 Infections with the novel H1N1 virus circulating in humans usually become apparent in two to seven days.98 There is no evidence that pigs are playing an significant role in the spread of this virus among people.190.131. and that it might have been circulating among pigs in an unknown location for years before it emerged in humans.191 Most people recover in one to seven days. and it is not known how humans acquired the novel H1N1 virus.21 Similarly.192.256-258 In one recent study. New Jersey became seropositive to a swine influenza virus.1 Disinfection Influenza viruses are susceptible to a wide variety of disinfectants including sodium hypochlorite. causing a pandemic.190. who remained asymptomatic.12 Limited data from Asian lineage H5N1 infections suggest that.192 More severe syndromes. povidone-iodine and lipid solvents.2.254.251 but people might be involved in disseminating the virus to pigs and other animals. influenza A has been associated with encephalopathy.126.96.36.199-192 Secondary bacterial or viral infections may also occur.192 Because influenza C viruses are difficult to isolate. which may include fever. chills.
and may be fatal. encephalitis and multiorgan dysfunction are common in the later stages.40 The respiratory secretions and sputum are sometimes bloodtinged.264.38 High fever and upper respiratory symptoms resembling human seasonal influenza tend to be the initial signs.41 The following human infections with Asian lineage H5N1 and other avian influenza viruses were reported between 1997 and 2009: In 1997.259 Fever and cough were the most common signs in 14 patients from France.260. No other cases were found.205. very young age or pregnancy increase the risk of severe disease.268 Avian influenza infections in humans Infections with avian influenza viruses have occasionally been reported in humans.188.8.131.520-262 Vomiting and diarrhea have been reported in a significant number of cases.38 The illnesses were mild and both children recovered. abdominal pain and vomiting in Hong Kong. especially respiratory diseases such as asthma or chronic obstructive pulmonary disease.259 Serious disease was most common in children less than two years of age. Novel H1N1 virus of swine origin In most people. sore throat and cough and.39 One H5N1 infection in a child with upper respiratory signs and an uncomplicated recovery after antibiotic treatment was recognized only by routine virus surveillance.12 Many patients develop lower respiratory tract disease shortly after the first signs. all six people recovered. in some cases. coinfections with gastrointestinal pathogens were present in some but not all cases.257 Some influenza C infections may be asymptomatic.12.33.2. and their condition rapidly becomes serious.255.257 Fever. 347 total (suspected and confirmed) and 89 confirmed human infections were associated with an H7N7 HPAI outbreak among poultry in the Netherlands.38.271 In some patients.167. or gastrointestinal symptoms such as diarrhea.267-270 A significant number of serious or fatal cases have been reported in healthy children or young adults.34.267. and recover within a week.38 Asian lineage H5N1 viruses LPAI viruses. cough and rhinorrhea. cough. the novel H1N1 virus causes a relatively mild illness.12.34 The symptoms included fever.33-35. as well as those with chronic medical conditions.271 Milder cases have been reported occasionally.256. sore throat and rhinorrhea were reported in four infected children in Cuba. antibodies to an avian H7N2 virus were found in one person after an LPAI outbreak among poultry in Virginia.35 Most cases occurred in The Asian lineage H5N1 HPAI viruses appear to cause more severe disease than other HPAI viruses or Last Updated: December 2009 © 2009 page 10 of 46 . In 1999.167.34 One of the two people died.261. there may also be mucosal bleeding.255.40. bronchitis or bronchiolitis. but no testing was done.264 Multiple organ failure may be seen.261.265.258 A study from Spain reported high fever and lower respiratory tract illness.257 This study also documented lower respiratory tract signs including pneumonia and bronchiolitis in a few patients.12. avian influenza (LPAI H9N2) was confirmed in two children with upper respiratory signs. wheezing and/or otitis in some individuals. vomiting and abdominal pain. severe respiratory distress and viral pneumonia. who would not be expected to have a high risk of complications. which resembles the disease caused by other human influenza viruses. other cases.15.11 In 2003. but 29 of 179 children were hospitalized with more serious illnesses such as pneumonia. tachypnea.12. the symptoms may include chest pain.40 Heart failure. Another family member died of a respiratory illness while in China.38 In 2002. pharyngitis.12.260.12. fever.11. with rhinitis.34. In 2003.11.12 Eighteen people were hospitalized and six died.12 Some infections have been limited to conjunctivitis and/or typical influenza symptoms. two patients from southern Vietnam had acute encephalitis without symptoms to indicate respiratory involvement.260. kidney disease.12 Most patients deteriorate rapidly. have been affected.264.11. dyspnea.167. Six unrelated H9N2 infections associated with acute respiratory disease were also reported from mainland China in 1998-99. and disseminated intravascular coagulation can occur.271 Respiratory signs are not always present at diagnosis.40.12. hoarseness of the voice and crackles during inspiration. two HPAI H5N1 infections were reported in a Hong Kong family that had traveled to China.12. 12.205.265 Like other influenza viruses.39 Asymptomatic infections with Asian lineage H5N1 viruses seem to be rare.260 Severe primary viral pneumonia and/or acute respiratory distress syndrome occur in a small percentage of cases.38. headache. 256 Gastrointestinal symptoms including diarrhea and vomiting have been reported in some patients.262-265 Patients who become severely ill usually begin to deteriorate 3-5 days after the onset of the symptoms.15. in a few infants.262 Most people have a self-limiting illness.255.11. a patient from Thailand exhibited only fever and diarrhea. and some cases may be complicated by secondary bacterial infections. the novel H1N1 virus can also exacerbate chronic medical conditions. 12 Similarly.Influenza most common clinical signs were fever. the first eighteen H5N1 infections in people were reported during an HPAI outbreak among poultry in Hong Kong. severe enough to require hospitalization. particularly among children.40.266 Underlying health conditions.11. Healthy children and adults. sore throat.255. especially those caused by Asian lineage H5N1 viruses. arthralgia. often progressing to respiratory failure within 24 hours.260.2.260.167. were serious or fatal.
From 2004 to 2008. Swine influenza virus infections in humans Serological evidence suggests that swine influenza virus infections might occur regularly among people who are occupationally exposed.35 In 78 of the confirmed cases.82 Serological evidence of possible infection was found in five contacts.85 The farmer had been in contact with pigs showing signs of respiratory disease. cough and rhinorrhea in Hong Kong. who had serious underlying medical conditions.240.2. including one who died of pneumonia. (Four cases were classified as “other. these cases included both conjunctivitis and upper respiratory symptoms.) A self-limiting illness with influenza symptoms was reported in a college student infected with an H1N1 virus in 1979. As of December 11 2009.2.21. an H9N2 virus was found in a 2-monthold infant in China. A localized outbreak was reported at Fort Dix. Both people recovered after treatment with an antiviral drug. while other H7 viruses from milder human cases in North America were significantly less virulent. New Jersey in 1976.244 Serological evidence suggests that approximately 500 people on the fort had been infected by person-to-person spread.23 Reported swine influenza infections include the following cases. sporadic human illness and deaths were associated with widespread outbreaks of Asian lineage H5N1 high pathogenicity avian influenza among poultry. Swine influenza virus (H1N1) was isolated from an immunocompromised child with fulminant pneumonia who died in 1982. In 2003. 11 In 2008.Influenza poultry workers.37 She was hospitalized but recovered. Ten other infections were suspected but not confirmed. It should be kept in mind that severe or fatal cases are more likely to be investigated than mild illnesses that resemble human seasonal influenza. Several health care workers developed influenzasymptoms after exposure.43 In 2007.12.35 This virus also caused severe or fatal infections in experimentally infected ferrets and mice. 11. An H1N1 swine influenza virus was isolated from five recruits with respiratory disease. mild dehydration and cough. it is not known whether the symptoms caused by these viruses differ significantly from human influenza. (This virus is not the same virus involved in the swine-origin H1N1 pandemic of 2009.88 She apparently became infected while attending an agricultural fair. an H1N1 swine influenza virus was isolated from a pregnant woman with viral pneumonia in Wisconsin.36 The child was hospitalized but recovered. In 1986. There is no indication in the report that this case was more severe than the previously reported infections. and died shortly after giving birth.26. The virus isolated from the fatal case had accumulated a significant number of mutations.36 The symptoms included mild fever. In 1980.35 Two people had influenza symptoms such as fever.1.37 Last Updated: December 2009 © 2009 In 2009.22 There was evidence that his roommate had been infected but remained asymptomatic. coughing and muscle aches. but the infection did not spread further. but three family members also became ill. two cases of conjunctivitis and flu-like symptoms were confirmed in poultry workers in Canada. who recovered.1.21 page 11 of 46 .35 His initial symptoms included a persistent high fever and headache but no signs of respiratory disease. an H1N1 virus caused severe viral pneumonia in a 29-year-old swine farmer in the Netherlands. a mild LPAI H9N2 virus infection was reported in a 9-month-old child in Hong Kong. an H1N1 virus infection with influenza symptoms including diarrhea occurred in a young boy. In 2004. an LPAI H7N2 infection with respiratory signs was reported in a patient in New York.22 There was no evidence of spread to his family.11 The person. the other was HPAI.23. an H9N2 LPAI infection was confirmed in a child in Hong Kong. 263 cases were fatal. 445 confirmed human cases had been reported to WHO. was hospitalized but recovered.11 One virus was LPAI. an H9N2 virus infection was reported in a 3-year-old child with a fever. In 1988. All of the infections were associated with an H7N3 virus outbreak in poultry.11.35 In 2003.196 Cases of conjunctivitis have been reported after contact with HPAI H7N7 avian viruses in infected seals.246-248 Because few infections with swine influenza viruses have been described.22 Other people on the base may also have been ill with the same infection.”) The single death occurred in an otherwise healthy veterinarian who developed acute respiratory distress syndrome and other complications. while viruses from most of the other individuals had not. Five had both conjunctivitis and influenza-like illnesses. conjunctivitis was the only sign of infection.
Equine and canine influenza virus infections in humans Antibodies to equine H3N8 viruses have been reported in humans. In 2007. All cases were described in the literature as upper respiratory disease. but was not tested for the virus.1 There are no reports of clinical cases caused by natural exposure to equine influenza viruses or canine influenza viruses.21 Thirteen of the cases were from the outbreak at Fort Dix. Between 2005 and February 2009. Last Updated: December 2009 © 2009 Centers for Disease Control and Prevention (CDC). diarrhea. which was also found in sick pigs on the farm. Most patients recovered. Nine of the patients had a history of contact with pigs. self-limited case of H1N1 swine influenza was reported from a 50year-old woman who worked on a swine farm in Spain. headache. Other workers on the farm were treated prophylactically and did not become ill.191 Severely immunocompromised individuals may remain infectious for weeks to months.‟ Twenty of the 37 civilian patients were previously healthy. but lived on a communal farm. a 26-year-old previously healthy woman and a 48-year-old woman with asthma and a history of smoking.192 Young children can shed virus for up to six days before. myalgia. the estimated period of communicability is from 1 day before the symptoms appear. an H3N2 swine influenza virus was isolated from an infant with respiratory disease in Canada.87 The physician who treated her reported an influenza-like illness shortly afterward.153. dizziness and occasional vomiting. the remainder were H1N1.1 Human volunteers inoculated with an equine virus became ill. Communicability Human influenza viruses are readily transmitted from person to person. In 1993. vomiting.90 The child was hospitalized but recovered. others had immunosuppressive conditions including cancer and pregnancy. but recovered.185.190. a mild. The virus appeared to be a reassortant. He had no direct contact with animals.83 He had close contact with pigs in a research facility.3. but seven deaths were reported. Infected adults usually begin to shed influenza A viruses the day before the symptoms appear. Four cases involved H3N2 viruses. sore throat. Four of 7 household members and 4 of 46 other people on the farm had antibodies to this virus.24 He recovered without complications. a healthy young laboratory animal caretaker in Maryland died of pneumonia caused by an H1N1 influenza virus.89 The virus. an H1N1 swine influenza virus caused severe viral pneumonia in a 5-year-old child who lived on a pig farm in the Netherlands. 11 human infections with triple reassortant H1N1 swine influenza viruses were reported to the U.1. One patient had three family members with suspected but unconfirmed swine influenza virus infections. Two children were hospitalized for dehydration.86 This case was diagnosed only because the physician participated in an influenza surveillance program and collected a laboratory sample for virus identification. to as long as 7 days after their page 12 of 46 . acute respiratory disease or pneumonia. a recombinant swine influenza virus was recovered from a farm worker with influenza symptoms in Canada. No other potential cases were associated with this infection. A recent literature review summarized 49 cases of swine influenza that had been documented in scientific journals as of April 2006 (including many of the cases described above). fever and myalgia. and only one person was seropositive.S. the other 37 were described as „cases in civilians. In 2005.190.85 In 2004.84 The symptoms included fever. but all of the gene segments were of swine influenza virus origin.24 The child recovered without complications. and are infectious for 3-5 days after the initial signs. In November 2008. and recovered uneventfully. an Asian H1N1 swine influenza virus was isolated from a 4-year-old boy in Thailand with rhinorrhea. was a triple reassortant H3N2 virus with genes from swine.Influenza In 1991. and one case was thought to have been transmitted from person to person. coughing. shortness of breath and conjunctivitis. and one additional case identified in an ongoing survey of swine influenza among farmers.191 Humans have transmitted influenza viruses to ferrets and occasionally to swine.187 For the novel (2009 pandemic) H1N1 virus. but recovered without other complications. 190. human and avian influenza viruses. The infected individual was given antiviral drugs. In 2005. Two patients. and 10 or more days after they become ill. There was no evidence of person-to-person transmission. experienced severe illness with pneumonia and respiratory failure. No one who had been in contact with the caretaker became ill. and virus could be isolated for up to 10 days. an Asian H1N2 swine influenza virus was isolated in the Philippines from a 25-yearold man with symptoms of influenza including high fever. and there was no evidence that the virus had infected others.
278 Current recommendations for the treatment of infections with the novel H1N1 virus.190 During the 2006-2008 flu seasons. the virus did not spread to the surrounding community.252 Rare cases of probable person-to-person transmission.277 Amantadine and rimantadine (adamantanes) are active against human influenza A viruses.22.190.. including the use of antiviral drugs. and virus could be isolated for 1 to 7 days.275 Samples should be collected as soon as possible after the onset of illness.190.S. on average.11.2184.108.40.206. 231 Transmission of this virus across the placenta may also be possible. Drug resistance develops rapidly in viruses exposed to amantadine or rimantadine. 275 Last Updated: December 2009 © 2009 page 13 of 46 .93.190-192.131.are used to treat influenza.249 People may shed this virus for as long as they are ill.190.40 Enhanced BSL 3+ laboratory conditions are needed for the isolation of H5N1 HPAI viruses. are available on the CDC and WHO Web sites (see Internet Resources). but does not detect the hemagglutinins in common human influenza viruses suggests a novel. rimantadine.22 The other is the 2009 H1N1 pandemic in humans. however.113.191. have been reported in humans infected with avian influenza viruses. may be treated with antiviral drugs. but they are currently uncommon.274. including neuropsychiatric events.191 Infections can also be diagnosed by serology.272 Atypical prolonged shedding up to 28 days (by PCR) has been reported in healthy adults with severe or relatively severe cases.93.40 In the U. however.40 RT-PCR is usually the primary test for infection with Asian lineage H5N1 viruses.191 Testing must be done to determine each individual virus‟s drug susceptibility. if treatment is begun within the first 48 hours.277 The CDC recommends that these two drugs be avoided until the circulating strains become susceptible again. samples that test positive by PCR or antigen tests are confirmed by the CDC. and Canada exhibited high resistance to amantadine and rimantadine. possibly zoonotic.119-129.93.1. turkeys. influenza virus.280. The microneutralization assay is the most reliable test for detecting antibodies to avian influenza viruses. One was a localized outbreak among recruits infected with an H1N1 virus at a military base in Fort Dix.234 Swine influenza viruses have typically been transmitted only to a few close contacts.35 Fecal shedding of the Asian lineage H5N1 virus has been documented in a child with diarrhea.272 Children and people who are immunocompromised might be infectious for longer.190. and in some cases.278-280 Oseltamivir-resistant isolates of this virus have been reported sporadically. but it is usually sensitive to oseltamivir and zanamivir.277 Side effects.22.273 Humans can transmit the novel H1N1 virus to animals as well as people.000 people.94 Approximately 500 people on the base. for 2-3 days after the fever has resolved.38. Four drugs amantadine.131.191 RT-PCR or culture can be used for the diagnosis of influenza C.220.127.116.117 Zanamivir and oseltamivir are effective for both influenza A and influenza B. RT-PCR and antigen testing of avian influenza viruses must be carried out in Biosafety Level (BSL) 2 laboratory conditions.2. ferrets.276 Treatment Supportive care for uncomplicated influenza in humans includes fluids and rest. at most. The current immunofluorescence or rapid antigen tests for human influenza cannot distinguish other human influenza viruses from the novel H1N1 virus.191. felids and dogs have apparently been infected from human contacts. More severe cases.277Treatment usually results in milder symptoms and recovery. zanamivir and oseltamivir .261.21. human influenza viruses circulating in the U.281 Diagnostic Tests Human influenza A and influenza B infections can be diagnosed by virus isolation or by the detection of antigens or nucleic acids. one day sooner.131. and may emerge during treatment. may occur.190-192.179.191 RT-PCR techniques are also available. antigen detection or virus isolation from respiratory and throat swab samples.18.104.22.168. and no cases of sustained transmission. 249 One study presented at a recent conference found that viral nucleic acids could be detected by reverse transcription polymerase chain reaction (RT-PCR) assays in children for 1 to 13 days after they became febrile.2. The viruses can be isolated in cell lines or chicken embryos. this appears to be less common than resistance to adamantanes.11.191 Commercial rapid diagnostic test kits can provide a diagnosis within 30 minutes. or infections that have an elevated risk of complications.40 Serology has been used for surveillance. hemagglutination inhibition and immunodiffusion.110.S.11. Serological tests include complement fixation.167.Influenza onset.40 Virus isolation is done at World Health Organization (WHO) H5 Reference Laboratories. Avian influenza viruses can be identified by RTPCR.103. Antigens can be detected in respiratory secretions by immunofluorescence or enzyme-linked immunosorbent assays (ELISAs).191.131.277 The novel (swine origin) H1N1 virus circulating among humans in 2009 is resistant to amantadine and rimantadine (adamantanes).82 There are two known outbreaks with more extensive spread. which contained 12. Swine herds.275 Serology is currently used mainly in epidemiology and research.277 Laboratory studies have shown that influenza viruses can also become resistant to zanamivir and oseltamivir. with identification by hemagglutination and neuraminidase inhibition tests or by RT-PCR.40 An influenza test that is positive for influenza A. New Jersey. were infected or exposed. a rising titer must be seen.202 Infections with the novel H1N1 virus can be confirmed by RT-PCR or virus isolation from respiratory secretions.
it is currently uncommon. and other common sense hygiene measures.131.187 If contact is unavoidable.191.292.93. and recommendations for vaccination in specific population groups are available from the CDC. and they are not ordinarily expected to occur outside these tissues (e. cats (both housecats and other felines) and dogs.190 The vaccine is given in the fall before the flu season.284 Last Updated: December 2009 © 2009 page 14 of 46 . Preventative measures for the novel H1N1 virus circulating in humans Preventative measures are similar to those for seasonal human influenza. in meat). and it is updated annually.290 The CDC has published specific guidelines for self-isolation and treatment. communities or non-healthcare occupational settings.190.284 To protect others. people who are ill should avoid contact with these animals. anyone with an undiagnosed flu-like illness should also avoid unnecessary close contact with species susceptible to the latter virus. the prevention of crosscontamination of foods or surfaces used for food preparation.40. particularly on the optimum dose and duration of treatment. Preventative measures for swine influenza viruses occurring in pigs Good hygiene and sanitation.287 The CDC Web site has detailed information on the current recommendations.93. the mouth and nose should be covered when coughing or sneezing. people may be monitored.290.292 Prevention Preventative measures for seasonal human influenza viruses An annual vaccine is available for influenza A and B. as influenza viruses have been transmitted occasionally to or from this species. including frequent hand washing. people at an increased risk for complications should consider avoiding crowded conditions or close contact with others. but they may be used voluntarily by individuals at risk for complications.amantadine.12.11 Although resistance to zanamivir and oseltamivir has also been reported in H5N1 viruses. and the use of hot soapy water to wash contaminated surfaces would be protective if any viruses survived long enough to reach consumers. particularly if it is given early. as well as hand washing and other hygiene measures.190. and stay home except for necessities (for instance.291 People who remain home should minimize contact with others in the household during their illness.289. the avoidance of unnecessary hand contact with the eyes. the CDC recommends that these two drugs be avoided in the U. can help prevent human infections with swine influenza viruses.g.261.249. There is no indication that any swine influenza virus can be acquired by eating well-cooked pork. is still needed.263.190. as well as recommendations for infection control measures in health care settings (see Internet Resources).1°C).282 Further testing.277 Due to the high resistance of currently circulating viruses to amantadine and rimantadine. gloves and other personal protective equipment also reduce exposure. Where limited quantities of these vaccines are available. good hygiene and the use of face masks and/or other measures that prevent accidental droplet transmission from coughs and sneezes may be helpful.40 These viruses are resistant to amantadine and rimantadine. as well as frequent hand washing.286 Antiviral drugs may be used for prophylaxis in some high risk populations after exposure.can be used for prophylaxis in high-risk populations such as the elderly or immunocompromised.287 In other cases.191 Three antiviral drugs .40.12.157. and treated at the first sign of disease. Details on vaccine efficacy.288 The CDC currently recommends that anyone infected with the novel H1N1 virus and anyone who has an undiagnosed flu-like illness limit contact with others.S. nose or mouth.191.285 but vaccines for the novel H1N1 virus became available in Fall 2009. and by cooking pork to an internal temperature of 160°F (71. ferrets. swine influenza viruses replicate in the lungs and upper respiratory tract. anyone who has a flu-like illness should avoid contact with this species. rimantadine and oseltamivir . Because infections with seasonal human influenza viruses cannot be distinguished clinically from infections with the novel (pandemic) H1N1 virus.271. vaccine types.249.249. specific risk groups may be targeted first for vaccination. Care should also be taken to avoid spreading the virus to other animals. 211 Ordinary food safety precautions including hand washing before and after handling raw meat..293 In pigs. and include the avoidance of close contact (approximately 6 feet) with people who have flu-like illnesses.131 It contains the viral strains that are most likely to produce epidemics during the following winter. seeking medical care).1. and recombination can occur between human and swine influenza viruses.277 Other preventative measures include the avoidance of contact with people with symptomatic disease.283 There appears to be little or no cross-reactivity with the H1N1 strains in the current seasonal human influenza vaccine. Protective clothing. particularly turkeys.291 Face masks and respirators are no longer recommended in homes. To protect ferrets from infection with human influenza.287 In areas where infections with the novel H1N1 virus are common.284 To prevent virus transmission to pigs.11. until the influenza strains become susceptible again.Influenza Oseltamivir appears to increase the chance of survival in patients infected with Asian lineage H5N1 viruses.292 Influenza viruses are also killed by sanitizing cutting boards with 1 tbsp bleach in a gallon of water. Avoidance of contact with swine should also be considered.
11.131.20 They are also discouraged from having contact with sick birds while suffering flu symptoms. coveralls. crowded conditions and close contact with other people should be avoided.191 Pandemics.12 People working with infected birds should follow good hygiene practices and wear appropriate protective clothing such as boots (or shoe covers). cancellation of social events and voluntary quarantines of infected individuals can limit the spread of disease.1. 1957. a pandemic or as sporadic cases.S. the World Health Organization recommends prophylaxis with antiviral drugs in people who cull birds infected with Asian lineage H5N1 HPAI viruses.295 The hands. 15% to 40% of the population may be infected.11 Cutting boards and utensils should be washed with soap and hot water.16. Antibodies offer limited or no protection against other virus types or subtypes.20.11.11 Eggs should be cooked until the whites and yolks are both firm. During a pandemic.190.201 However.131. but can occur.0006% in persons under 50 years old.131.20.294 Avian influenza vaccines for humans are not commercially available in the U.297 Morbidity and Mortality Seasonal human influenza Although the morbidity rate for seasonal influenza is high.16.295 If an avian influenza pandemic occurs in humans. close contact is discouraged. an epidemic.190 The estimated mortality rate from seasonal influenza is 0. influenza appears first among schoolaged children.0004 .20 The outbreak usually lasts for three to six weeks.188.296 Respirators and other protective equipment may be advisable during close contact with an infected individual.11.190.11 Less is known about influenza C than influenza A or B.Influenza Preventative measures for avian influenza viruses Controlling avian influenza epidemics in poultry decreases the risk of exposure for humans.192. drinking. After a pandemic.20 H5N1 vaccines have also been developed. in 1918. and these birds could be the initial source of infection in an area.1. people in contact with infected birds should be vaccinated against human influenza.295 Hunters should not handle or eat sick game.1.11 Precautions should also be taken when handling raw meat and eggs. are caused by antigenic shifts in influenza A viruses.1.1. the morbidity and mortality rates may increase dramatically in all age groups.11 The hands should be washed thoroughly with soap and warm water after handling poultry products. 296 In addition. these viruses were thought to cause only sporadic cases of influenza and minor localized outbreaks. which last occurred in 1918. gloves and respirators.192 Since 1968. Until recently. or rubbing the eyes.190 Human influenza can occur as a localized outbreak.” epidemics in temperate regions usually do not begin until after school starts in the fall. tribal or federal natural resource agencies.131 During a typical epidemic.2. then spreads to preschool children and adults. people with respiratory or cardiac disease.131 It should be noted that antiviral drugs and antibiotics were not available at the time. an epidemic of influenza A usually occurs every 1. 296.1.2 In North America.11. the hands should be washed with soap and water before eating. a nationwide influenza C epidemic was reported in Japan. 1968 and 2009. and 0.131 Epidemics in tropical regions are not usually seasonal.1 Antigenic drift is usually responsible for small-scale epidemics and localized outbreaks.S.190-192 Influenza-related deaths are usually the result of pneumonia or the exacerbation of a cardiopulmonary condition or other chronic disease. and those who are immunosuppressed.191 Deaths are rare in children. poultry farms and live bird markets should be avoided.131.12. the type A (H3N2) viruses have caused the most serious outbreaks with the highest mortality rates.1% in those over 65.190.3 years.S.191 In the most severe pandemic. smoking. these vaccines are stockpiled by the government and will be distributed by public health officials if they are needed.131 During influenza pandemics. In areas where H5N1 viruses might be present in domesticated poultry.192 Infections are more severe in the elderly. and intensive care procedures were less effective. 0.191 Over 90% of these deaths occur in the elderly. in 2004.202 Influenza C infections seem to be most serious in very young Last Updated: December 2009 © 2009 page 15 of 46 . Sanitary precautions and cooking methods recommended to destroy Salmonella and other poultry pathogens are sufficient to kill avian influenza viruses.000 deaths were reported in the U..1.20 Although a new virus may spread among a population before the “flu season. Wild birds should be observed from a distance. additional precautions will be necessary.11 Avian influenza viruses can be carried in wild birds.131 During epidemics. and they should always wear rubber or latex gloves while handling and cleaning wild birds.2. uncomplicated infections with human influenza viruses are rarely fatal in healthy individuals.11 In addition.295 If birds or contaminated surfaces are touched.0075% between the ages of 50 and 64.20. young children (particularly infants). the morbidity rate was 25-40% and the case fatality rate 2-5%. infection control measures such as good hygiene.0.20 Approximately 500.191 Immunity to the viral surface antigens (the hemagglutinin and neuraminidase) reduces the risk of infection and severity of disease. should be thoroughly washed after dressing the carcass.12 To prevent reassortment between human and avian influenza viruses. and an estimated 20-50 million deaths worldwide.11 Poultry should be cooked to a temperature of at least 74°C (165ºF).295 All game should be cooked thoroughly.294 In the U.295 Dead or diseased wildlife should be reported to state. an influenza virus usually becomes established in the population and circulates for years. as well as equipment and surfaces. and an epidemic of influenza B every 3-4 years.
22. most (75%) in people who had other health issues. the novel H1N1 virus has been transmitted most widely during the traditional flu season.269 Although the vast majority of cases have been mild and uncomplicated.244 One review reported that.260.262.268. 30% of the children hospitalized with severe infections were less than two years old. this occurred first in the Southern Hemisphere.259 however.167.302-304 This was followed by the identification of the virus among travelers in other countries.800 deaths attributed to this virus had been reported to the World Health Organization.21 Four of these patients had primary viral pneumonia. visitors at agricultural fairs or livestock shows. other probable cases were suspected.279.309.2.0 to 31.279. and those who are obese.264. and serological evidence of infection was found in approximately 500 of 12.95.265.262.93. 1. one had secondary bacterial infection.167. a human pandemic was declared. In one study.269 Peru reported 8381 confirmed cases and 143 deaths.305 Cases were reported in both the Northern and Southern Hemispheres during the initial stage of the outbreak. one was pregnant.307 HIV infection was linked to more severe illness in South Africa.269 Transmission of the novel H1N1 virus appears to have declined normally after the flu season in the temperate regions of the Southern Hemisphere. more than 622. and a meat packer.1 per million population.307.84 Most sporadic cases of swine influenza have been relatively mild and some may have been asymptomatic. like other human influenza viruses. Because the virus emerged in April. Australia.2. laboratory workers.260. six cases were fatal.267-270.269 but data from other countries suggest that this is not necessarily the case among HIV-infected individuals who are receiving antiretroviral drugs. However. previously healthy individuals. 85% of these critically ill patients survived. people with underlying health conditions such as chronic respiratory disease.22.306 Secondary bacterial infections have also contributed to some severe cases and deaths.255.96. with 20% of hospitalized patients transferred to an intensive care unit (ICU).264. Australia.222.214.171.1248 Some older people may have some immunity to the novel H1N1 virus. particular those that are mild.260.8 per 100.206. but severe illness was seen in some high risk groups.205.21.1. at least twelve additional cases thought to be swine influenza were reported.82.250 As of November 27 2009. 279 The autumn flu season in the Northern Hemisphere has been very active in the initial stages.279. of 37 other cases reported in the literature.284.269 The mortality rate in the Southern Hemisphere was relatively low.167.264.000 population in most countries. the overall mortality rate from influenza was lower than in previous years.95. and 0.306 In New South Wales.000 cases and 7. some cardiovascular conditions or immunosuppression. viral pneumonia has been a significant concern with this virus. who are not ordinarily expected to be at high risk.264. severe or fatal cases have also been reported among some young.265. serological evidence suggests that exposure may be relatively common among people who work with pigs. depending on the country and the conditions that are defined as predisposing.167. During the flu season in the Southern Hemisphere.259 Symptomatic influenza C infections are reported less often than illnesses caused by influenza A or B viruses.269 In Victoria.22.310 and this group has had lower morbidity rates than expected.269 A small number of H1N1 infections may be asymptomatic. then by the recognition of sustained person-to-person transmission outside Mexico.306. the reported hospitalization rates from various countries ranged from 2. however. with hospitalization and mortality rates that were 3-7 times greater than in non-indigenous groups.23.205. but they are more likely to have severe symptoms if they become ill. In a series of 11 infections with North American triple reassortant Last Updated: December 2009 © 2009 page 16 of 46 .83 The health status of one person was not known.265 In Victoria.305. the mortality rate among 91 hospitalized patients was approximately 10%.1. pregnant women.000 people on the base.1.96.298-301 2009 pandemic: Novel H1N1 virus of swine origin Morbidity and mortality information for the novel H1N1 virus are still preliminary. individual countries reported mortality rates from 0 to 36.206.21 Two patients who died were described as previously healthy.82-90 During the outbreak at the Fort Dix military base.265 In Taiwan.307 The impact of the novel H1N1 virus has been greater among indigenous people in both the Northern and Southern Hemispheres.246-248 Swine influenza infections have been reported among farm workers.307 The reported percentage of hospitalized patients who have had no significant preexisting conditions ranges from approximately 24% to 59%.3% of those infected were hospitalized.167 Unusually. and one had extensive involvement of the abdominal organs.269 Zoonotic swine influenza The overall prevalence of swine influenza virus infections in humans is unknown. and two were immunosuppressed by cancer. and an additional 12% were between the ages of two and five.22.305 Because many countries no longer count or report individual cases. 21.266 The risk of severe illness has been greatest in children under the age of 2 years (especially infants under a year of age).256.2.279.267.302-304 In June. which begins in the autumn.21 Infections not associated with swine contact have included instances of limited person-to-person transmission and some published cases with no known connection to swine.257. approximately 5% of the population is thought to have become ill. this underestimates the number of cases.Influenza children.21. with less than 1 death per 100. but some severe illnesses and a few deaths have been reported. The initial outbreak with this virus occurred in Mexico in April.000 population.249.24.2. serological studies suggest that a large percentage of the population is exposed to influenza C viruses in childhood. one person died of pneumonia.
11.69.43 The overall case fatality rate.16. pigeons (order Columbiformes).71. as well as housecats. coots and sultans (order Gruiformes). kestrels. swans and geese) and Charadriiformes (shore birds.44-53. a dog. A single death was reported in an otherwise healthy veterinarian who became infected with an H7N7 virus. orioles. appear to be the natural reservoir hosts. cats. was 59%.196 Waterfowl and shorebirds.36-38.9. dogs. and severe illnesses were reported in a previously healthy 26year-old woman and a 48-year-old woman with asthma and a history of smoking. budgerigars (order Psittaciformes).11 Most patients infected with these viruses have been young and have had no predisposing conditions. During an H7N3 LPAI outbreak in Italy in 2003.58. owls (order Strigiformes).71. ravens.74 The reported infections with H9N2 viruses have resembled human influenza.40 From 2003 through December 11 2009. ferrets. 445 laboratory confirmed human H5N1 avian virus infections. Wang2009 /id] Whether these antibodies result from productive infections. farmed ostriches.208. 3. red-billed leiothrix (Leiothrix lutea). leopards (Panthera pardus). which tend to carry these viruses asymptomatically. horses.136 Disease can also occur in passeriform birds.13. H6.55.319 Symptomatic or fatal infections have also been reported in pheasants. egrets.67.224 In a recent study from Thailand. Zoonotic avian influenza The severity of avian influenza varies with the virus isolate. storks and herons (order Ciconiiformes). circulate in some of these species. H9.51.60. jungle fowl.311-313 A few milder cases have been documented.57. raccoon dogs and captive palm civets (Chrotogale owstoni).1. 51.71.72. only individual cases or limited outbreaks have been reported in others. stone martens (Mustela foina). there was no apparent difference in the prevalence of the H5N1 virus between waterfowl and other birds.2. eagles. Jia2009 /id. 263 of them fatal. crakes.12.4455 Asymptomatic infections have been reported in some Last Updated: December 2009 © 2009 page 17 of 46 . watercocks.35 Some isolates may also cause asymptomatic or mild.138-142.51.11. Many H5N1 viruses have been isolated from birds in the order Anseriformes.43 Higher or lower case fatality rates have been reported in smaller series.142.224 Symptomatic infections with Asian lineage H5N1 viruses have also been reported in mammals including captive tigers (Panthera tigris). guineafowl and peafowl (order Galliformes). shrikes. no seropositive individuals were identified in serum samples collected during H7N1 epidemics from 1999-2002.84 All of the patients in this study recovered. cranes. emus (order Struthioniformes).73.38. terns. emus and passerine birds. however. and buzzards/ vultures (order Falconiformes).39 The prevalence of human infections with Asian lineage H5N1 viruses is unknown. but some strains can also infect and/or cause disease in mammals.11. such as the Asian lineage H5N1 viruses or an H5N3 virus isolated from terns in the 1960s.26. species that can be affected include finches. and they have not been-fatal. pinnipeds and cetaceans. munias. unrecognized infections. house sparrows (Passer domesticus).16 Poultry can develop serious or mild disease.34. exposure to antigens or crossreactions with human influenza viruses remains to be determined. cormorants and pelicans (order Pelecaniformes). veterinarians and waterfowl hunters.194. H7. partridges.136. asymptomatic infections seem to be rare.317 Asian lineage H5N1 viruses have also been found in a variety of birds that appeared healthy.271. A few isolates. were reported to WHO.38. but influenza symptoms have also been seen.51.71. starlings.33-38.9. Influenza viruses Asian lineage H5N1 viruses can infect and/or cause disease in many species of birds in addition to poultry. H5.74 Most infections with H7 viruses have been limited to conjunctivitis. kites. particularly among children. wood ducks. Eurasian tree sparrows (Passer montanus).41 Human disease has also been reported occasionally after infection with various H7 viruses and H9N2 viruses.39 One H5N1 infection in a child with upper respiratory signs and an uncomplicated recovery after antibiotic treatment was recognized only by routine virus surveillance. particularly the families Anatidae (ducks.61-63. moorhens.34. crows. H10 and H11 avian influenza viruses have been found in poultry workers.1. antibodies to H4. Cong2007 /id. lions (Panthera leo) and Asiatic golden cats (Catopuma temminckii). depending on the subtype and strain of the virus. mink.11. quail.314 Interestingly. mynahs.207.12. clouded leopards (Neofelis nebulos).Influenza H1N1 swine influenza viruses between 2005 and 2009. goshawks. bustards.51.8% of poultry workers tested developed antibodies to H7 viruses.25. grebes (order Podicipediformes). falcons. varying with the country and the clade of the virus.54.65. Peiris2009 /id.12. Avian influenza viruses Avian influenza viruses mainly infect birds.11. two children were hospitalized for dehydration.137. gulls and terns). can also cause serious disease in other avian species including gulls. hornbills (order Coraciiformes) and flamingos (order Phoenicopteriformes).54. jackdaws. Particularly severe infections have been reported with Asian lineage H5N1 (HPAI) viruses. Japanese white-eye (Zosterops japonicus) and magpies.26. a wild mink (Mustela vison).240-242.11. Oriental magpie robins (Copsychus saularis). as of December 11.314 In other studies.315-318 Host range of the Asian lineage H5N1 avian influenza viruses Infections in Animals Species Affected Influenza A viruses Influenza A viruses can cause disease in birds and many mammals including swine. mesias.
1.173 The new H3N8 canine influenza viruses have diverged genetically from the viruses found among horses.58. H8N4 and H11N4 viruses.1.9Antibodies to influenza A viruses have been reported in sea lions and porpoises.324-327 In 1984. chickens exposed to infected pigs did not become infected. reindeer and deer.126.96.36.199.322 In one experiment.213 Recently. but they can also occur in zebras.9 Antibodies to H1. dogs.1. and viruses have been isolated rarely from pigs in China.146 Experimental infections have been reported in calves. foxes. cattle and birds. dogs. H4. sheep. dogs and swine. H1N1 swine influenza virus.170.185-188 They can also infect pigs.310.132 During outbreaks in poultry.1.59 Unpublished research suggests that some raccoons in Japan also have antibodies to H5N1 viruses.2. H4N5 and H4N6 viruses. mice and cynomolgus macaques (Macaca fascicularis).9 There is evidence that some of these viruses were avian.34. but they can also cause disease in turkeys.189 Novel H1N1 virus of swine origin In ferrets. toads and frogs.91. was isolated from a duck in Hong Kong.153 Experimental infections have been established in horses and raccoons.133.145 Human influenza viruses Human seasonal influenza A viruses mainly cause disease in people and ferrets.119122. a cheetah in a zoo.58.1. and have been reported in dogs. 9 Serological evidence of infection with influenza A viruses has also been reported from some other mammals including cattle.328 Serological studies from the U. horses and seals. rodents.1.328 Influenza A infections have been reported sporadically in cetaceans. have serological evidence of infection with H1. H7N7.K.215 Clinical cases have also been reported in dogs exposed to infected horses. 9 Antibodies to influenza A viruses have been reported in reptiles and amphibians including snakes.168. H8 and H12 viruses have also been found in these animals. H3.4. and they can be infected experimentally with avian LPAI H4N8 viruses and human H3N2 viruses.144 One H1N1 swine influenza virus.51. swine and equine influenza viruses have also been established in this species. but the animals remained asymptomatic despite shedding virus.184 Swine influenza viruses Swine influenza viruses mainly affect pigs. and influenza A viruses have been detected by RT-PCR in caimans. donkeys and mules.165. cynomolgus macaques and rabbits.5 The novel (swine origin) H1N1 virus circulating in humans has infected pigs and turkeys. infections with equine H3N8 viruses were reported among pigs in China. which was avirulent for both poultry and pigs.60-70 Cattle can be experimentally infected with viruses isolated from cats.189 Unpublished research suggests that some raccoons in Japan have antibodies to H5N1 viruses.56.9 Influenza B viruses Influenza B viruses can cause disease in humans. alligators. To date.321] A few clinical cases have also been reported in pet ferrets.170.70 The currently circulating H5N1 strains are continuing to evolve.32.Influenza housecats. human and equine influenza viruses. becoming the first canine influenza virus. suggest that influenza B infections in swine are sporadic and do not spread to other pigs.262. goats.262.174. crocodiles. H7.32. H13N2 and H13N9 viruses have been isolated from whales. and antibodies to equine H3N8 viruses have been detected in dogs and humans. dogs and humans. have been isolated from seals. caimans. closely related to avian viruses.310. and Asian lineage H5N1 viruses have been recovered from populations of apparently healthy wild pikas. H4 and H10 viruses.30 and circulate only in dogs. 9 Human influenza viruses have been isolated from some of these species.125.25.185-188 the novel (swine origin) H1N1 virus.1.126-129 Experimental infections have been established in ferrets.S.5. cats.1.5. H7N7.3. and other species may also be susceptible to infection and/or disease.9 Raccoons in the U.9 This virus is thought to have been of avian origin. and an H3N2 virus isolated from cattle caused an illness resembling influenza in calves.9. An H3N2 swine influenza virus caused a recent outbreak in mink.3 Outbreaks have been described recently in ferrets and mink. H3N8 equine influenza virus.119-124. H3. and H3N8 and H4N6 avian influenza viruses have been established in mink. clinical cases or outbreaks have been reported in animals infected with human influenza viruses.197 Serological evidence of infection has been found in pigs.238.100-118. and H1N3. alligators and crocodiles.9 Mink can also be infected with H5N3.196. 175 Experimental infections have been established in cattle. pigs.57. serological evidence of infection or exposure has been reported in cats.28.169 Recently. and these viruses have also been isolated from pigs and a horse. an H10N4 virus was isolated from mink during an epidemic in Sweden.29. Equine and canine influenza viruses Influenza viruses in other species Equine influenza viruses mainly affect horses.323 Last Updated: December 2009 © 2009 page 18 of 46 .320.91 Experimental infections with avian.1.193 Influenza A viruses can infect pinnipeds and cetaceans. including humans.232.193 Experimental infections have been established in housecats. H3N3. and dogs.144 Experimental infections with H1N1 and H3N2 human influenza viruses. yak.9. ferrets.322 and an H1N1 swine influenza virus.29 An H3N2 virus has been reported in dogs in Korea. an H3N8 equine influenza virus jumped into dogs. H6. ferrets and seals. canine influenza virus infections have not been reported in other species.
13.329 although incubation periods up to 5 days have been reported in some horses.317 Laughing gulls (Larus atricilla) developed severe neurological disease.319 Strains known to cause fatal illness include some of the currently circulating Asian lineage H5N1 viruses. respiratory distress and/or neurological signs were seen.13 Because a virus can be defined as HPAI based on its genetic composition. misshapen eggs.142.137 Some captive wild birds infected with these viruses have died suddenly. these birds are generally found dead. cyanosis of the head. loss of egg pigmentation and deformed or shell-less eggs.13-188.8.131.52 Swans have been severely affected by H5N1 viruses. within a few hours. however.13 Sinusitis.19 Last Updated: December 2009 © 2009 page 19 of 46 .184 Clinical Signs Avian influenza HPAI viruses usually cause severe disease in poultry. without apparent clinical signs.3.19 In addition. One gull that recovered had a persistent head tilt.170.140 Avian influenza is often subclinical in wild birds. and ruffled feathers.142 In one study. and all of the birds died within five days of inoculation.136.143 Experimental infections with H5N1 viruses in call ducks (Anas platyrhyncha var.6. but some strains can cause illness and death.3. sneezing.219.54 In other cases.Influenza Influenza C viruses Influenza C viruses have been isolated from humans and swine. These viruses can cause serious infections in some species of birds on a farm while leaving others unaffected. and starlings.12.253. blue-winged teals (Anas crecca) and redheads (Aythya americana) remained asymptomatic when inoculated with one of these strains.317 Incubation Period In poultry. and green to white diarrhea may also be seen. lacrimation.344 Diving ducks.1.136. the most common signs are sinusitis. northern pintails (Anas acuta).19 Most of the flock usually dies. Ostriches that were experimentally infected with an HPAI H7N1 virus developed mild depression and hemorrhagic diarrhea. which remained asymptomatic.73.72 However.4. ecchymoses on the shanks and feet.136 Most infected gulls died. there can be coughing. H5N1 infections were mild in house sparrows.168.142 House finches and budgerigars developed anorexia.72. house sparrows but not starlings had severe.14 A 21-day incubation period. The clinical signs usually appear within 1-3 days in horses.13 The incubation period for mammalian influenza viruses is also short.13-15 However.18.13. some recent H5N1 isolates have caused severe acute disease with neurological signs and high mortality rates in domesticated ducks.5.25.17. can occur if the birds are concurrently infected with other viruses or there are other exacerbating factors. is used for an avian population in the context of disease control. another recovered completely. blood-tinged oral and nasal discharges.136. edema of the head.140 Green diarrhea was the only sign of illness in ostriches inoculated with an LPAI virus of the same subtype. but most cases appear in 2-3 days.137. and sudden death may occur with few other signs. turkeys and other gallinaceous birds.18 Decreased egg production.213 Little is known about H3N2 influenza virus in dogs.343 There are few descriptions of the clinical signs in other domesticated birds. respiratory signs.60.10.147. and other clinical signs began 2-8 days after inoculation. diarrhea and increased mortality. 1.1. severe weakness and neurological signs. with death within 12 days. incoordination and torticollis. including most HPAI viruses.11-13.13 The clinical signs are variable.136. and died rapidly. a cross between wild and domesticated ducks) or wood ducks (Aix sponsa) resulted in drowsiness. neurological disease. pigs or seals.11. decreased egg production. often fatal infections.140 High mortality is occasionally seen in young ostriches infected with either LPAI or HPAI viruses. it is also possible for an HPAI virus to be isolated from gallinaceous birds showing mild signs consistent with LPAI. depression and neurological signs. the incubation period can be a few hours to a week.18.343 Symptomatic infections with H5N1 viruses have also been reported in experimentally infected gulls and passerine or psittacine birds. extreme lethargy. or somewhat increased flock mortality rates may be seen.3. but some indigenous North American ducks including mallards (Anas platyrhynchos).54. comb and wattle.319 Experimental infections with H5N1 viruses resulted in severe neurological disease in some mute swans and sudden death in others. may be noted in chickens.3. In ducks.19 Sudden death of large numbers of birds is a common presentation.137.13 Systemic signs.13. and in some cases.330 The incubation period for H3N8 canine influenza can be two to five days. while some birds shed virus subclinically.14. dogs and horses. ruffled feathers. anorexia. the clinical signs included weakness.3. domestica. grebes and mergansers also seem to be highly susceptible to these viruses.54. which takes into account the transmission dynamics of the virus.332-342 More severe disease.142 In another study. cloudy eyes.201 These viruses can cause disease in experimentally infected dogs. fever first appeared at 24 hours in experimentally infected dogs. respiratory signs.1 Serological evidence of infection has been found in pigs. decreased feed and water consumption.60. with decreased feed and water consumption. none of these signs is pathognomonic.1-4.331 LPAI viruses usually cause subclinical infections or mild illness in poultry.71-73. 1.178.8 Clinical signs tend to be minimal in ducks and geese infected with avian influenza viruses. lethargy.3. decreased fertility or hatchability of the eggs.7.323. mimicking high pathogenicity avian influenza. which experienced only mild depression and survived. The birds can be markedly depressed. Anorexia and depression occurred in experimentally infected zebra finches. dark green diarrhea.13.
229 Cattle inoculated with high titers of H5N1 viruses isolated from infected cats remained asymptomatic but could transiently shed virus. myalgia.168 Secondary bacterial infections prolong recovery. or produce abnormal eggs. 168. infections in mice varied with the isolate and the route of inoculation (respiratory or intragastric).330 Postinfection encephalopathy has also been reported in foals.25. convulsions and ataxia.46.25. although no naturally infected animals have been reported.25. Although fatal infections have been reported in some housecats. the pathogenicity varied with the specific isolate and the route of inoculation (intranasal or intragastric).65. with panting and lethargy.213 In this form.169. leopards and Asiatic golden cats were lethargic and had decreased appetites without respiratory signs for 5-7 days.48. respiratory disease.66 Similarly. an initial (usually low grade) fever is followed by a persistent cough and sometimes a purulent Last Updated: December 2009 © 2009 page 20 of 46 .177.253 In severely affected animals. protrusion of the third eyelid. In naïve horses. Canine influenza (H3N8) Canine influenza is an emerging disease in dogs.55 Captive palm civets had neurological signs. extreme lethargy. dyspnea. high fever and neurological signs before death. dyspnea and death. conjunctivitis. H5N1-infected swan. 25 Sequelae may include chronic pharyngitis.253.47 One of the latter cats was apparently well up to 24 hours before its death.25.70 Equine influenza Equine influenza usually spreads rapidly in a group of animals. with a high mortality rate.9 A wild stone marten was also found with neurological signs.45.253 Young foals without maternal antibodies can develop rapidly fatal viral pneumonia.55 Other raccoon dogs on the same farm had died with respiratory signs and/or diarrhea before the virus was found.Influenza Other subtypes can also be pathogenic to some wild birds.9. the clinical signs included fever.253. chronic bronchiolitis and emphysema.57 Asian lineage H5N1 infections in pigs appear to be mild or asymptomatic.66 The clinical signs in severe cases included high fever.63. captive lions.25. and enteritis (spasmodic impaction colic) has been reported in some epidemics. the syndromes ranged from very mild upper respiratory infections to severe.132 In experimentally infected housecats.330 There may be edema of the legs and scrotum.46 During an outbreak in Cambodia. encephalitis and hepatitis at necropsy. apathy and anorexia.61. however.168. corneal opacity and enlarged submandibular lymph nodes.330 Healthy adult horses usually recover within 1-3 weeks.28.25. mice and cattle. there was no evidence that the pika population was seriously affected.54 Other mammals may also be affected by Asian lineage H5N1 viruses. asymptomatic infections were reported in housecats that had been accidentally exposed to a sick. with evidence of interstitial pneumonia.25. but the cough may persist longer.3 Avian H5N1 influenza in mammals Both symptomatic and subclinical Asian lineage H5N1 virus infections have been seen in felids. lung lesions were reported at necropsy.168 Death in adult horses usually results from bacterial pneumonia. tigers. and died the following day. in canaries and a siskin141 and an H5N3 HPAI virus caused an outbreak with a high mortality rate among South African terns in the 1960s.11. diarrhea and neurological signs.9 HPAI H5N1 viruses have been isolated from wild pikas. Mild respiratory signs including cough.9 Some infections in palm civets were fatal.66 One group reported that miniature pigs were resistant to infection. atypical infections with little or no coughing or fever.1 The virus could be isolated for up to five days.253. ferrets. but other clinical signs were not seen. convalescence can take up to six months.168.3. dry cough.61. A dog that ate infected poultry developed a high fever. photophobia.179.176. depression. The most common presentation seen with H3N8 viruses is relatively mild and resembles kennel cough.25.330 Other clinical signs may include a serous to mucopurulent nasal discharge. fever and transient anorexia were observed in some experimentally infected pigs. however.67 Fatal infections have also been reported in some captive tigers and leopards.1. serosanguineous nasal discharge.3.318 Other influenza viruses in birds Turkeys infected with swine influenza viruses may develop respiratory disease.253 Loss of eyesight has also been reported.169. anorexia.53 little is known about the clinical signs after natural exposure in this species.68 Fatal respiratory disease was reported in infected raccoon dogs. 47 In contrast.58 In another study.67.1.330 Equine influenza is sometimes complicated by secondary bacterial infections.69 In ferrets. but recovered. and lung lesions were much less severe than those caused by swine influenza viruses. pleuritis or purpura hemorrhagica. lethargy. Some infected foxes developed fever but no other clinical signs.253 Animals with partial immunity can have milder.168. One cat had fever. some Asian lineage H5N1 strains caused slight and transient weight loss.253 Interstitial myocarditis can occur during or after the infection.253 Other influenza viruses in horses Horses experimentally infected with human influenza virus (H3N2 „Hong Kong‟) developed a mild febrile illness.48 and a few infected housecats were found dead. fatal disease. the first sign is usually a high fever. An H7N1 (HPAI) virus caused conjunctivitis. 184.108.40.206 Experimental infections have been established in foxes. weight loss. 47.50 Some of these animals exhibited respiratory distress. have decreased egg production. inappetence. followed by a deep.49 Experimentally infected dogs have been asymptomatic or developed only transient fever and conjunctivitis.
174 The only known outbreak of H3N2 canine influenza was characterized by severe respiratory disease with fever.113.105.188 The infection is not usually fatal in adult animals.91 Some severely affected animals died.185.123 Although some animals apparently had milder cases. suggesting that secondary bacterial infections may be important in this disease.127 An infected cheetah developed lethargy.120. which persisted for 10 days.103.28 Other influenza viruses in dogs In the U.4.32 Asymptomatic infections were reported in an experimental study with a Japanese H3N8 (Florida sublineage) isolate.188 More severe or fatal disease can be seen in neonates. was characterized by coughing. but one died. sneezing. with no mortality or other clinical signs. anorexia.310 Infected turkey flocks reported in Chile and Canada experienced only decreased egg production and reduced quality of the eggs. and swine influenza viruses can circulate in pigs with few or no clinical signs. but does not seem to be prominent in pets. but one death was reported.177.119.211 Coughing can occur in the later stages of the disease. weakness and decreased Last Updated: December 2009 © 2009 appetite have been reported.213 Lethargy and anorexia are common. sneezing. sneezing. sneezing.4.129 The illness lasted for several weeks in some animals.123.185. and two cats died. nasal discharge and ruffled fur were reported in one study. and severe dyspnea.179. miniature pigs remained asymptomatic although they shed the virus.125 Upper or lower respiratory signs including sneezing and coughing in some cases.184 The clinical signs in dogs experimentally infected with influenza C virus included nasal discharge and conjunctivitis. which generally recover in five days to two weeks. this syndrome has been seen in racing greyhounds.30.2. listlessness.2.122 In experimentally infected ferrets. which was diagnosed as bronchointerstitial pneumonia. depression.32 One dog died and several were euthanized.186.178 More severely affected dogs exhibit a high fever with an increased respiratory rate and other signs of pneumonia or bronchopneumonia.S. sneezing and fever as the most prominent signs.147 Severe. nasal discharge. and the clinical signs have resembled those caused by other swine influenza viruses.107.188 Infections with the novel 2009 H1N1 (swine origin) virus have also been reported after contact with humans.30.211 Sneezing. in another. which may include fever.127.1 Swine influenza Swine influenza is an acute upper respiratory disease characterized by a variety of clinical signs. was ill with clinical signs of lethargy.262 and lethargy and weight loss.108.323 In one study.100-111. anorexia.133.111.S. anorexia and a cough. which was used to infect dogs via close contact with horses.322 Influenza viruses in ferrets Ferrets are susceptible to human influenza viruses.119. potentially fatal bronchopneumonia is occasionally seen. 133 Four of five pet dogs seen at veterinary clinics died.213 Some dogs have been found dead peracutely with evidence of hemorrhages in the respiratory tract. have been described in cats. weight loss and labored breathing.28.321 The illness has been mild.32 The disease. The clinical signs (see previous section) appeared to be similar to those caused by human seasonal influenza viruses.149 Complications may include secondary bacterial or viral infections. fever and coughing.323.. nasal discharge.124 and a dog in the U.129 Some cats with respiratory disease did not have a fever.S. crusting of the nose and eyes.1. anorexia.187. but the novel H1N1 virus was isolated from sick animals in China. conjunctivitis and/or abortions may also be seen.147 Some outbreaks are more severe than others. with little sneezing. 129 There is little information on cases in dogs. coughing and nasal discharges occurred in experimentally inoculated dogs. page 21 of 46 . lethargy.213 Asymptomatic seroconversion also occurs.74 Novel H1N1 virus of swine origin in mammals A number of swine herds have been infected with the novel H1N1 virus circulating in humans.111 Experimentally infected pigs developed mild disease.118 Decreased egg production was also reported in a turkey flock in the U.Influenza nasal discharge. 103. with little or no mortality.173.2. and severe pathological changes were seen in the lungs.16. sneezing.346 Diarrhea was reported in some experimentally infected animals. coughing. with nasal discharge. nasal discharge.119.100. fever. decreased appetite.2.103.114-116.28.114.K. lethargy.108.123. The clinical signs may include fever.345 Coughing. nasal discharge and weakness.321. lethargy and weakness.120.252 Abortions or diarrhea have also been seen in some herds.147. purulent nasal discharge and coughing.3 H9N2 influenza viruses in pigs An avian H9N2 virus caused respiratory disease and paralysis in pigs in southeastern China.178 The nasal discharge appears to resolve with antibiotics.110. was hospitalized and treated with supportive care including antibiotics. 133 Fever.30.1-4. one cat became dyspneic and severely ill but recovered with medical care. sometimes progressing to loss of consciousness. coughing. and pneumonia in others.122 Several ferrets recovered.213 The clinical signs can last for up to a month regardless of treatment.178. the clinical signs included fever. and recovered. coughing and anorexia.113-116. and radiological evidence of pneumonia. and the clinical signs included sneezing.91 The virus was a triple reassortant H1N1 swine influenza virus.128 Respiratory disease has been reported in naturally infected ferrets. an H3N8 equine influenza (American lineage) virus caused a limited outbreak among foxhounds in 2002.128 The dog in the U.117.122 A single outbreak caused by a swine influenza virus has been reported in ferrets. but recovered.
H4 and H10 viruses has been reported in wild raccoons. sneezing.61. weight loss.329 A white or bloody nasal discharge was seen in some animals. Cats can shed these viruses from the intestinal tract as well as the respiratory tract. coughing.9.132 Limited animal-to-animal transmission was reported among tigers in a zoo. Mink naturally infected with a Canadian H3N2 swine influenza virus had respiratory signs including pneumonia. an H10N4 avian influenza virus caused an epidemic on 33 mink farms in Sweden.189 page 22 of 46 . and developed no other clinical signs. the signs were nonspecific and included extreme emaciation. nasal discharge.3. the pathogenicity varied with the specific isolate and the route of inoculation (intranasal or intragastric).61.65 In contrast.193 Influenza in marine mammals Influenza A viruses have been associated with outbreaks of pneumonia in seals and disease in a pilot whale. and nasal and ocular discharges. with the currently circulating Asian lineage H5N1 viruses.1. 66-68 but in experimentally infected foxes. the recent isolation of H5N1 viruses from pikas suggests that these viruses may be maintained in this population. with increased mortality particularly on ranches where the mink were co-infected with other pathogens. and typically shed the viruses for 7-10 days.66 Some of these infections were fatal.324.222 Most chickens shed LPAI influenza viruses for only a week.147 Shedding up to four months has been documented in one pig. and for less than two weeks. extreme lethargy.16.67 Experimentally infected cats shed Asian lineage H5N1 viruses by the third day postinoculation.226 Waterfowl are often infected subclinically.66 The clinical signs in severe cases included high fever. 2. transient weight loss and respiratory signs.65.61.50 Horizontal transmission of Asian lineage H5N1 viruses has not been reported inexperimentally infected dogs.25. these viruses were found in both respiratory secretions and feces.196 In another experiment. difficulty maneuvering and Last Updated: December 2009 © 2009 sloughing skin. with sneezing and shivering. anorexia. asymptomatic cats appeared to shed Asian lineage H5N1 viruses only sporadically. suggesting that co-infections may have increased the severity of the clinical signs. under some conditions.1.58. severe weight loss. virus shedding has been described. Chickens can begin shedding avian influenza viruses as soon as 1-2 days after infection. respiratory signs.66.16.326 In one study. and shedding for as long as 36 days has been reported in experimentally infected birds. pigs. the inoculation of an HPAI H7 virus from a fatal case in a Dutch veterinarian resulted in severe disease with fever. Experimental infections with these viruses were milder or asymptomatic. naturally infected. incoordination.326 Experimental Asian lineage H5N1 virus infections in ferrets ranged from very mild upper respiratory infections to severe. and were able to infect sentinel cats in close contact.9 Communicability Influenza viruses are readily transmitted between animals in the species to which they are adapted.189 Raccoons that were experimentally infected with avian LPAI H4N8 or human H3N2 viruses shed these viruses but remained asymptomatic. but did not have an elevated temperature. fatal disease. Limited animal-to-animal transmission seems to occur. diarrhea and neurological signs. but a minority of the flock can excrete the virus in feces for up to two weeks. 189 According to yet unpublished research.329 Influenza B infections have been reported in some stranded seals.144 Influenza in raccoons Serological evidence of infection with H1. including birds.26. but ferrets have been infected experimentally with a few of these viruses. diarrhea. Raccoons that were experimentally infected with an avian LPAI H4N8 virus shed this virus in respiratory secretions but not from the digestive tract.94 Horses begin excreting equine influenza viruses during the incubation period.69 As of December 2009.132 Horizontal transmission was not observed in this instance.63.253 Animals that have been infected with influenza viruses from other species may or may not transmit the virus.324 Animals inoculated with avian H7 (LPAI and HPAI) viruses from recent outbreaks developed illness of varying severity. H5N1 viruses have been detected only in respiratory secretions.9 In the single known case in a whale. However.53.227 Turkeys may excrete some avian influenza viruses for up to 72 days. dyspnea and subcutaneous emphysema of the neck. antibodies to H5N1 viruses have also been found among raccoons in Japan. anorexia. but whether clinical signs occur is unknown.57 A recent study suggests that raccoons may be able to transmit some influenza viruses.26 Clinical signs in seals included weakness. and many mink died. and usually shed these viruses for 4-5 days or less after the onset of clinical signs. dyspnea and neurological signs. lethargy. and ducks can shed these viruses for up to 30 days.66 Influenza in mink In 1984. but minimal intestinal shedding was also reported. and could infect other raccoons in contact. ferrets inoculated with influenza viruses from various species.Influenza Natural infections with avian influenza viruses have not been documented.196.329 The viruses appeared to be of avian origin.226. 189 The H3N2 virus was not transmitted to uninfected raccoons.189 Raccoons that were inoculated with a human H3N2 virus shed virus mainly from respiratory secretions. sustained or prolonged transmission of Asian lineage H5N1 viruses has not been reported in any of these mammals. H3. foxes or cattle.196 Although most viruses caused relatively mild illness with fever.66-69 In experimentally infected dogs and pigs.9 The clinical signs included anorexia. however.226 Pigs may begin excreting swine influenza viruses within 24 hours of infection.94.61. developed rhinitis. ferrets infected with an H7N3 (LPAI) virus had only a transient elevation in temperature.
and severe hemorrhagic pancreatitis have been reported in naturally infected cats. cats infected by ingestion also had enlarged tonsils with multifocal petechial hemorrhages. the sinuses may be swollen. edema of the wattles and/or neck.13 The oviduct may also be edematous. swelling and hemorrhages of the conjunctivae. 69 More severe lesions were seen in foxes inoculated intratracheally than in animals fed infected birds.347 Hemorrhages may also be seen on the mucosa and in the glands of the proventriculus. conjunctivitis.13. with mild to moderate bronchiolitis and alveolitis detected on histopathologic examination. hemorrhages in the intestinal serosa. and they may exude fluid when cut. or petechial hemorrhages in the proventriculus may be particularly suggestive of an HPAI infection.347 Postmortem lesions have occasionally been described in wild birds infected with Asian lineage H5N1 viruses. perirenal tissue and/or diaphragm.46 Bloody nasal discharge.136 More extensive lesions were reported in experimentally infected laughing gulls.58 In one study. 66 Experimentally infected foxes also developed lesions mainly in the lung.14. especially when there is acute high morbidity in the flock. dark red to purplered. the gross lesions included severe pulmonary consolidation and multifocal hemorrhages in multiple organs including the lung. and congestion of the spleen. as well as serous or serofibrinous pleuritis.14 Some birds may have signs of acute renal failure and visceral urate deposition. kidney and liver were reported in a naturally infected dog. intestines. beneath the lining of the gizzard. 319 Pancreatic lesions alone or no gross lesions have also been seen in some swans. and the comb and wattle are often edematous. and less frequently. as well as enlarged mandibular and/ or retropharyngeal lymph nodes.13 The ovary can be hemorrhagic in laying hens. fluid (which may contain blood) in the nares and oral cavity. and they can sometimes be found in the muscles. with areas of necrosis.13. congested and/or cyanotic. house finches and budgerigars despite high mortality rates in these species.142 Low pathogenicity avian influenza Rhinitis and catarrhal to purulent sinusitis are often seen in young birds infected with LPAI viruses. and in one cat.4 The airways are often dilated and filled with mucopurulent exudate.13. multifocal hepatic necrosis.14 Avian H5N1 influenza viruses in mammals Pulmonary edema.13 The lungs may be reddened from hemorrhages and congestion. hemorrhagic. tracheitis.4 Severe pulmonary edema.48.65 Petechial hemorrhages occurred in the liver of some cats.14 Lower respiratory tract lesions such as pneumonia are usually Last Updated: December 2009 © 2009 seen only in birds with secondary bacterial infections. liver and lymph nodes.347 There may be subcutaneous edema on the head and neck. Asian lineage H5N1infected pigs had mild to minimal gross lung lesions. with exudates in the lumen. stomach. and can cause severe air sacculitis and peritonitis. subepicardial hemorrhages. and sharply demarcated.65 These lesions were similar whether the cats were infected intratracheally or by the ingestion of infected chicks. the tracheal lesions may be limited to excess mucoid exudate. apex of the heart.63. 4 Some strains of swine influenza viruses produce more marked lesions page 23 of 46 .347 Birds that die peracutely and young birds may have few or no lesions.13 The kidneys can be severely congested and are sometimes plugged with urate deposits. heart.14.13 Congestion and inflammation may also occur in the trachea.13.10. but they are usually more extensive in the ventral regions. and congestion. the liver lesions were accompanied by generalized icterus. with multiple to coalescing foci of pulmonary consolidation. and pulmonary congestion and edema.13 A study of the 2003 H7N7 outbreak in the Netherlands suggested that the occurrence of peritonitis. renal and splenic congestion. which may cause severe airsacculitis and peritonitis. Experimentally infected wood ducks had multiple petechial hemorrhages in the pancreas.49 Pulmonary lesions including interstitial pneumonia have been noted in some experimentally infected pigs.13 Yolk may be present in the abdominal cavity. on serosal surfaces and on the peritoneum. severe pulmonary congestion and edema. pneumonia. may also be seen. the gross lesions are mainly those of a viral pneumonia.65 In naturally infected tigers and leopards.2.Influenza Post Mortem Lesions Click to view images High pathogenicity avian influenza The lesions in chickens and turkeys are highly variable and resemble those found in other systemic avian diseases. In one study.14.348 Mild or absent gross lesions were reported in experimentally infected zebra finches.347 In other cases. in others. and in the intestinal mucosa. with involuted and degenerated ova. 47.2. in these birds.2 Affected parts of the lungs are depressed and consolidated.4 Lesions may be found throughout the lungs. and some of these animals also had histopathologic evidence of encephalitis and myocarditis. thymus. lymph nodes.13.136 In naturally infected swans. edema and diffuse subcutaneous hemorrhages on the feet and shanks.4 Other parts of the lungs may be pale and emphysematous.13 The ovaries may be hemorrhagic or degenerated.14 Hemorrhagic tracheitis can be seen in some birds.53 The lungs were also affected in experimentally infected cats.13 Petechiae may be noted throughout the abdominal fat. The peritoneal cavity often contains yolk from ruptured ova. one study reported that the most consistent lesions were multifocal hemorrhagic necrosis in the pancreas.2.13. 69 Swine influenza In uncomplicated infections. cerebrum and pancreas.4 The bronchial and mediastinal lymph nodes are typically edematous but not congested. cerebral. petechial hemorrhages were found in the ventriculus. the lungs.
184 Mild to moderate thickening of the alveolar septa was also seen.26.14. lungs. multifocal to coalescing reddish consolidation was found in the lungs. but there was no evidence of severe hemorrhagic pneumonia. AGID tests are not reliable for detecting avian influenza in ducks or geese. are used to differentiate LPAI from HPAI viruses. air sacs.13.13. cannot be collected without harming the bird). and can replace virus isolation in some cases. Feces can be substituted in small birds if cloacal samples are not practical (e.Influenza than others.213 In animals that were inoculated with Korean H3N2 viruses isolated from dogs. hepatic congestion and pulmonary consolidation were reported in one outbreak of severe disease in swine. which are most often seen in young foals.349 Serological tests including agar gel immunodiffusion. spleen.173.329 Acute interstitial pneumonia was seen in mink infected with a swine influenza virus.330 Ventral edema of the trunk and lower limbs can also occur.253 Interstitial pneumonia. suppurative secondary bacterial pneumonia may be seen alone.19 Oropharyngeal.133 Influenza in other mammals In seals infected with avian influenza viruses. hemagglutination. AGID tests can recognize all avian influenza subtypes in poultry. kidney.196 The extent of the lesions varied with the isolate. the lungs were hemorrhagic and a hilar lymph node was greatly enlarged.13 In wild birds. including a diffusely non-collapsed parenchyma. peritonitis and interrupted follicular development were the only lesions reported in turkeys. hemagglutination inhibition and ELISAs are useful as supplemental tests.253 Canine influenza In dogs that die of canine influenza (H3N8). hemagglutinating activity indicates the presence of influenza virus.30 Fibrinous pleuritis may also be noted.136 Swine influenza Last Updated: December 2009 © 2009 page 24 of 46 . have been reported with some strains.184 The histopathologic lesions included severe multilobular or diffuse necrotizing tracheobronchitis.184 No lesions were found outside the respiratory tract. liver and heart) are tested in dead birds.2 Generalized lymphadenopathy.19 Virus isolation is performed in embryonated eggs.213 There is limited information on the lesions found in mild cases.19 Although most gallinaceous birds and other susceptible birds die before developing antibodies. tracheal and/ or cloacal swabs in live birds.349 As of 2008. the bronchial lymph nodes were edematous.g. 19 Some rapid tests.19.19 Real-time RT-PCR is the method of choice for diagnosis in many laboratories.170.213 Hemorrhagic lesions are not always present in fatal cases. bronchiolitis. focal areas of pulmonary discoloration and pervasive discoloration of the liver.329 In a single case in a whale. bronchitis. serology can be valuable for surveillance and to demonstrate freedom from infection.. intestine. hemorrhages may be found in the lungs.14.13.9 The gross lesions in ferrets inoculated with zoonotic avian H7 viruses ranged from mild pulmonary lesions to widespread hemorrhages. and severe multilobular bronchiolitis and alveolitis.170. pneumonia with necrotizing bronchitis. including various PCR assays. as well as catarrhal or hemorrhagic enteritis. 133.133.19 These viruses can be recovered from oropharyngeal. tracheal and cloacal swabs (or intestinal contents). In experimentally infected puppies with this form. were evaluated and compared in a recent review. together with genetic tests to identify characteristic patterns in the hemagglutinin.213 On histological examination.173 The lungs may exhibit signs of severe pneumonia. and can be dark red to black. 253 Severe necrotizing myocarditis.19 The virus can be identified as an influenza A virus with agar gel immunodiffusion (AGID) or ELISAs. 117 Equine influenza The gross lesions are typically those of an upper respiratory infection (including nasal discharge).28. bronchitis and bronchiolitis have been reported in fatal cases.13. but hemagglutination inhibition tests are subtype specific and may miss some infections. and cranioventral lung consolidation was rarely seen.173.1 Novel H1N1 virus of swine origin Typical swine influenza lesions in the lungs. some serological tests may underestimate the prevalence of H5N1 infections.13.173. Diagnostic Tests Avian influenza Avian influenza can be diagnosed by a variety of techniques including virus isolation. rubbery texture and areas of bronchiopneumonia were reported in pigs experimentally infected with the novel H1N1 virus.25. in some cases. and severe interstitial or bronchointerstitial pneumonia. and are often accompanied by enlargement of the lymph nodes of the head. there may be tracheitis.323 Salpingitis.13. the World Organization for Animal Health (OIE) recommended that antigen detection tests be used to identify avian influenza only in flocks and not in individual birds.19 Viral antigens can be detected with ELISAs including rapid tests.19 Virulence tests in susceptible birds. and organ samples (trachea. Avian influenza viruses are subtyped with specific antisera in AGID or hemagglutination and neuraminidase inhibition tests.19 RT-PCR assays can identify avian influenza viruses in clinical samples. brain.213 The most severely affected puppies had small focal areas of pulmonary hemorrhage scattered throughout the lungs.19. bronchiolitis and hemorrhagic alveolitis has been reported.28.14. mediastinum and pleural cavity.253.349 These tests can also distinguish some subtypes.
peak virus shedding is thought to occur during the first 24 to 48 hours of fever. Treatment Animals with influenza are usually treated with supportive care and rest. and ELISAs.168. dogs and.168. Influenza vaccines may change periodically to reflect the current subtypes and strains in a geographic area.147 RT-PCR assays are used to detect viral RNA. and these vaccines are changed less often. using paired serum samples.Influenza Swine influenza can be diagnosed by virus isolation. which is subtype specific.4. samples should be collected within the first 3-5 days after the onset of clinical signs..213 Little is known about testing for Korean H3N2 viruses in dogs. virus recovery should be attempted in both embryonated eggs and cell cultures.3. the detection of viral antigens (e. 213 Acute and convalescent titers should be submitted if possible.4..14. probably because the amount of virus shed is low. the detection of viral antigens or nucleic acids.10. or most other countries. single titers are still considered to be less useful. the indirect fluorescent antibody test and virus neutralization. 133 RT-PCR can also detect this virus.1. the disease is confirmed by virus isolation.213 The H3N8 canine influenza virus can be found in lung tissue samples taken post-mortem. In horses.2.168 As in swine.168.3. 24-48 hours after the onset of illness.19. 133 Serology is expected to be useful.350 In experimental infections.25.g.4.253 Antibiotics may be used to control secondary bacterial infections.169 The most commonly used serological tests in horses are the hemagglutination inhibition test and a single-radial hemolysis (SRH) test. whenever possible.147 Other antigen detection tests include immunohistochemistry on fixed tissue samples. but other cell types can also be used. nasal swabs have been more likely to yield virus than nasopharyngeal swabs. ferrets have been treated with amantadine as well as antihistamines.179 Antiviral drugs are not generally given to most animals.213 However. nations may consider vaccination as a preventative or adjunct control measure during an outbreak.352 The vaccines do not always prevent infection or virus shedding.4.2.350 Because canine influenza is an emerging disease.147. horses. Uncommonly used serological tests in swine include agar gel immunodiffusion.353 Avian vaccines are usually autogenous or from viruses of the same subtype or page 25 of 46 .25.2.147 These viruses can be isolated from lung tissues at necropsy.2 ELISA kits are available.350 RT-PCR is the most reliable method to detect the virus directly.147 Serology on paired samples can diagnose swine influenza retrospectively. 133 In experimentally infected dogs. however. 213 Virus neutralization (microneutralization test) can also be done.350 The H3N8 canine influenza virus has been isolated in both embryonated eggs and cell cultures (MDCK cells) 213.213. by ELISA).350 Virus isolation may also be successful in some dogs. in some countries.177. In general.2.147 Swine influenza viruses are often recovered in Madin–Darby canine kidney cells.28. nasal epithelial cells or bronchoalveolar lavage.147 Equine influenza Equine influenza may tentatively be diagnosed based on the clinical signs.213. and from nasal or pharyngeal swabs taken from acutely ill pigs. avian influenza vaccines are used most often in turkeys and are intended only to prevent infection by LPAI viruses.25. but the disease is usually milder if it occurs. however.351 Poultry flocks infected with HPAI viruses are depopulated and are not treated.147 Isolated viruses can be subtyped with hemagglutination inhibition and neuraminidase inhibition tests or RT-PCR. 213.147 Immunofluorescent techniques can detect antigens in fresh lung tissue.2. but only during the early stages of disease before antibodies develop.4. these viruses were shed in nasal secretions from one to six days after inoculation.25 In the U. these tests may be able to detect H3N8 canine influenza during outbreaks at kennels or other large facilities. antibiotics and other supportive therapy. 213 This test can be used on nasal swabs Last Updated: December 2009 © 2009 from live animals or lung tissue samples at necropsy. swine and equine viruses display less antigenic drift than human viruses.168 In horses. but virus isolation fails to detect the virus in many infected dogs that do not die of the disease. most dogs are not expected to have pre-existing titers to the canine influenza virus.3.213. or the detection of nucleic acids by RT-PCR.169 Ideally.169 Canine influenza At this time.14.4 The hemagglutination inhibition test.2. Some H3N2 viruses were isolated from nasal swabs taken from dogs during an outbreak. prolonged recovery and more severe disease have been associated with increased stress.147 It may not detect new viruses.3.147 Recovery is best from an animal with a fever.168.25.25. serology and RT-PCR are the most reliable methods for detecting H3N8 canine influenza. birds.169 Equine influenza viruses can be isolated from nasopharyngeal swabs or nasal and tracheal washes. and serology. is most often used.2.13. they seem to be particularly important in the treatment of canine influenza.185 Antiviral drugs could also be of use in valuable horses.213.350 Hemagglutination inhibition is the most commonly used serological test.169 Equine influenza can also be diagnosed retrospectively by serology.S. however.S.25.11 Prevention Vaccines Influenza vaccines are available for pigs.25. Antigen-capture ELISA tests do not seem to be reliable in individual dogs.19 HPAI vaccines are not used routinely in the U. but this test is usually too cumbersome for routine use.177. Mammalian influenza viruses can be isolated in embryonated chicken eggs or cell cultures.169.213.
2-220.127.116.11.2. up to 90-100%.73. depopulation. Avian influenza Avian influenza outbreaks occur in most countries including the U.187 If contact is unavoidable. good biosecurity is important. may be helpful. Felids (including housecats and a cheetah) and dogs have Last Updated: December 2009 © 2009 also been infected with the novel H1N1 virus from humans.19 High mortality is occasionally seen in young ostriches infected with either LPAI or HPAI viruses. low mortality rates and rapid recovery.11. as well as by contact with wild birds. but outbreaks with high pathogenicity H5 and H7 viruses are also seen occasionally.12.Influenza hemagglutinin type. and people with influenza should avoid contact with this species. 3. outbreaks of high pathogenicity avian influenza are controlled by eradication. however. some of the Asian lineage H5N1 viruses have caused outbreaks with high mortality rates.1.10.54.S.216 Mammals should not be fed poultry or other birds that may be infected with the avian influenza viruses.S. swine workers who are ill should avoid contact with pigs. but it may be the result of multiple factors such as increased virus survival in the cold. increased poultry trade during winter festivals. and might eventually result in the evolution of vaccine-resistant isolates.283 The reason for the seasonality is unknown. prolong recovery and result in complications such as pneumonia.18. USDA approval.168.357 Other preventative measures Poultry can be infected by contact with newly introduced birds or fomites. During outbreaks of H5N1 avian influenza. this virus has tended to reemerge during colder temperatures in the Northern Hemisphere.15 Keeping flocks indoors is often recommended in areas where the H5N1 virus has been isolated from wild birds. as well as the use of face masks and/or other measures to prevent droplet transmission from coughs and sneezes.353.358.13. good management can decrease the severity of disease. Rest decreases virus shedding in horses.13. In mammals.168 Similarly to birds.15 Illegal poultry movements may be of primary importance in transmission in some regions.11. Because H5 and H7 LPAI viruses can mutate to become HPAI viruses. an outbreak that began at Qinghai Lake in central China resulted in the death of more than 6000 migratory wild birds.3.10.354. good hygiene. Strict hygiene is necessary to prevent virus transmission on fomites. and by preventing any contact with wild birds or their water sources. and are being controlled similarly in many countries. and the use of sentinel birds. however.94 Isolation of newly acquired animals can decrease the risk of transmission to the rest of the herd.25. and wild bird movements.19 Morbidity and Mortality The severity of an influenza virus infection varies with the dose and strain of virus and the host‟s immunity.360 Once a herd of swine has been infected with a swine influenza virus. but may also mimic HPAI viruses. cats and dogs should be kept indoors whenever possible.11 Seasonality has been reported in the current H5N1 epidemic.13 Any surviving birds are usually in poor condition.2.353-355 Methods used to recognize infections with field viruses in vaccinated flocks include “DIVA” (differentiating vaccinated from infected animals) strategies. LPAI viruses usually result in mild or asymptomatic infections.71. the virus usually persists in the herd and causes periodic outbreaks.170. Because vaccines may allow birds to shed virus while remaining asymptomatic.4. particularly birds and humans. in a number of countries. good surveillance and movement controls are critical in a vaccination campaign. The use of these vaccines requires the approval of the state veterinarian and.10-12. particularly waterfowl and shorebirds.10.16.16. and the public should be restricted from entering swine operations. strict hygiene and biosecurity measures are necessary to prevent virus transmission on fomites. uncomplicated infections are usually associated with high morbidity rates.51. include inactivated whole virus and recombinant fowlpox.94 Ferrets can be infected by human influenza viruses (including the novel H1N1 virus).1-4.140 Symptomatic infections are unusual in wild birds.45 They should also kept from contact with potentially infected flocks and wild birds. Poultry should not be returned to the farm from live bird markets or other slaughter channels.4.72.355.15 In addition.359 The risk of infection can be decreased by all-in/ all-out flock management.73 In April 2005.19 Currently licensed vaccines in the U. In poultry.330 Secondary bacterial infections can exacerbate the clinical signs.12 Asian lineage H5N1 viruses have also been isolated sporadically from other dead birds.H5 vaccines.1. these infections are reportable to the OIE.147.119-124. cleaning and disinfection.25 Infected facilities should be cleaned and disinfected after the outbreak.356 Vaccination may place selection pressures on avian influenza viruses.16.127-129 Eradication and prevention of virus transmission during outbreaks During an outbreak of influenza among mammals.25 Good hygiene can keep the virus from spreading on fomites. quarantines and isolation of infected animals help prevent virus dissemination.13. In pigs and horses. 283 In domesticated poultry (particularly chickens).94 Infected swine herds can be cleared of influenza viruses by depopulation.11 The outbreak is managed by quarantine. To prevent human influenza viruses from entering a herd.319 High mortality rates have been reported in some but not page 26 of 46 .168 Pigs should also be protected from the influenza viruses found in other species. Low pathogenicity forms occur most often. and surveillance around the affected flocks. influenza is usually introduced into a facility in a new animal. in the case of H5 and H7 vaccines. high pathogenicity avian influenza has very high morbidity and mortality rates. including waterfowl.
56 and these viruses have been isolated rarely from pigs in China. the virus spreads rapidly in pigs of all ages. A serological study conducted in Vietnam found that a low percentage of pigs (0. deaths have not been reported among experimentally infected pigs. and some experimentally infected cats exhibited severe disease and high mortality rates.201 In the U.16. Experimental infections also suggest that the clinical signs may be mild in this species.2. the case fatality rate has ranged from less than 1% to 4%. but only sporadic infections with the human influenza B viruses were found.Influenza all experimentally infected wild birds.4. Mallard. In one study. up to 100% of the animals may become ill but most animals recover within 3-7 days if there are no secondary bacterial infections or other complications. tigers.25%) had been exposed to H5N1 influenza viruses in 2004.45-50.2. the severity of the clinical signs varied with the specific isolate and the route of inoculation (intranasal or intragastric). pigs can be infected with human influenza A. 24.65 In contrast.94 Many infections in endemically infected herds are subclinical. the morbidity rate was page 27 of 46 . and none became ill despite the presence of other viral and bacterial infections.28 In Japan. In a turkeys flock in Chile. both mild and severe cases have been reported in several of these species.16 In addition. and all starlings remained asymptomatic.8. antibodies to these viruses were found in 8 of 11 cats and 160 of 629 dogs. In an unpublished study from Thailand. all six laughing gulls infected with recent strains of H5N1 became severely ill. Fatal cases were reported in some naturally infected housecats. occur mainly during the colder months. but all house sparrows experienced mild disease and survived.1.94 Annual outbreaks are often seen.66 However. or if the infection is exacerbated by factors such as poor husbandry.59 In contrast.66 Interestingly. In one study. fatal cases were reported among captive tigers and leopards in Thailand. a study found antibodies to both swine and human influenza viruses in 14% of all pigs.48.94 Influenza epidemics can occur if a virus infects a population without immunity to the virus.252. and high stress levels in this population.136 Three of the sick ducks died and one recovered.142 In a study with a different Asian lineage H5N1 virus.107. typical signs of influenza may occur in only 25% to 30% of the pigs.47. and can survive in a few carrier animals for up to four months.9.53. some large felids.4.16 In the epidemic form. Approximately 25-33% of 6-7 month-old finishing pigs and 45% of breeding pigs have antibodies to the classical swine H1N1 virus in the U.16.63.321 Experimental studies support this view.108.56 Although Asian lineage H5N1 viruses have been reported in pigs.57 and Asian lineage H5N1 viruses isolated from Indonesian pigs were less virulent in mice than isolates from poultry.132 Similarly. and four died.61..58 However.K. deaths have been reported in housecats.46. 61. house finches and budgerigars. 147 In the 1918 epizootic. northern pintail.9.1-18.104.22.168. Morbidity rates from less than 1% to as high as 90% have been reported.4 Once the virus has been introduced. 317 Avian H5N1 influenza in mammals Asian lineage H5N1 viruses have been reported in a variety of mammalian species. B and C viruses.1. but no deaths were seen in starlings.54 Asymptomatic or mild infections have been reported in experimentally infected dogs. secondary infections or cold weather.60 Swine influenza Influenza is a major cause of acute respiratory disease in finishing pigs.22.214.171.124. and thousands of the infections were fatal.323. palm civets and experimentally infected ferrets9.103. there are no reports of severe illness among swine.66 and miniature pigs were resistant to infection in one study.310. the mortality rate was 66-100% in house sparrows.58.1 Novel H1N1 virus of swine origin The H1N1 virus circulating in humans appears to cause mild disease in pigs.108.346 Decreased egg production may be the main effect in turkeys.3.132 Few of these cats shed virus.58 Asian lineage H5N1 viruses have also been detected in swine in Last Updated: December 2009 © 2009 Indonesia.1.3.136 Morbidity and mortality rates in passerine and psittacine birds have varied with the species.16 Approximately 10% of the pigs were seropositive for influenza C viruses.136 Four of six infected wood ducks also became severely ill while two others remained asymptomatic. but little or no mortality has been seen. 49.2.S. asymptomatic infections were reported in cats exposed to an infected swan in an animal shelter. there is no evidence that HPAI H5N1 viruses are causing significant illness among infected pikas in China.1. millions of pigs developed influenza.111116.107. severe disease does not seem to occur in this species. blue-winged teal and redhead ducks inoculated with the same viral strains did not become ill.50.94 In a newly infected herd. but captive leopards.16. a similar study found antibodies to the type C viruses in 19% of pigs. and in temperate regions. it usually persists in the herd.16.5.102-104.68 In experimentally infected ferrets and mice.8 Swine influenza viruses are usually introduced into a herd in an infected animal.1.345.361 Some infections with Asian lineage H5N1 viruses have been fatal.2.16 High seroprevalence rates to swine influenza viruses have also been reported in other countries.94 Maternal antibodies decrease the severity of disease in young pigs.147 In uncomplicated cases. mortality rates approached 100% in zebra finches. Asiatic golden cats and lions at a wildlife rescue center in Cambodia all recovered after an illness lasting 5-7 days. raccoon dogs. a dog. but one death was reported in a naturally infected dog. stress. no antibodies were detected in 171 cats from areas of Austria and Germany where infections had been reported in wild birds.2 Viruses may also infect the herd with few or no clinical signs.
in Canada. tracheal clearance rates can be depressed for up to a month after infection. and are usually the result of secondary bacterial infections. crowding and transportation are typical risk factors for disease.28.28. healthy adult horses usually recover within 1-3 weeks.177.178 In kennels.183.119-124.25. and some cats apparently had milder cases. 178. races and other events where horses congregate.1 The morbidity rate was nearly 100%. egg production dropped by approximately 80%.25.122 Two infected cats died. Because dogs have not been exposed to the canine influenza virus before. at first.119. but one died. a Yorkshire terrier and two Jindo dogs ( a Korean breed of hunting dog). was ill with pneumonia.179.117 Egg production in this flock dropped from 70% to 31%. The H3N2 virus has been reported from outbreaks at three veterinary hospitals and a kennel in South Korea.213 At one Florida greyhound racetrack.177.Influenza 61%.128 Experimental studies in mice. the infection rate may reach 100%.28. the morbidity rate was 8% and the mortality rate was 0. 25 Avian influenza viruses have rarely been reported in horses. is not yet known. an avian H10N4 virus caused an outbreak on Swedish mink farms.25. The avian-like virus continued to circulate in horses for at least five years without further fatalities.262.179 Higher case fatality rates have been reported in small groups of greyhounds.168.170 The morbidity rate was at least 80% and the mortality rate was 20-35%.9 In an outbreak caused by a triple reassortant H1N1 swine influenza virus in ferrets. the case fatality rate was 36%. appeared to be confined to this breed.213 In dogs with severe disease.25.118 Although a slight increase in flock mortality occurred in the latter case. It affected 33 farms and killed 3. the case fatality rate was estimated to be 20% in one outbreak with an H7N7 virus.3.123. H3N8 canine influenza has been seen in a variety of breeds at veterinary clinics and animal shelters in several states. Similarly.168. 133 Cases were described in a miniature schnauzer.129 An infected dog in the U.25 Unless there are complications.170 The virus appeared to be an avian influenza virus.25 Close contact with other horses.329 and they may be more severe if the animals are co-infected with other pathogens.25 Most outbreaks are associated with sales. donkeys and zebras. although coughing can persist. and clinical signs can occur in 60-80% of the dogs infected. influenza outbreaks are not as seasonal as they are in pigs or humans.176.28 High case fatality rates are not expected in most canine populations. In the province of Ontario.1.000 animals and killed several hundred.181.121. it may have been unrelated to the H1N1 infection.S.1. animals in poor condition. in affected turkey flocks in Canada. as well as 13 dogs of unknown breed at an animal shelter.310. One study suggests that canine influenza is rare.322 Equine influenza In horses.168.213 Most dogs are expected to develop the less severe form of the disease.25 Deaths are rare in adult horses. pet ferrets and dogs have been infected naturally with the novel H1N1 virus. with a mortality rate of 3%.30.177.253 The H3N8 viruses usually cause more severe disease than the H7N7 viruses. greyhound populations as early as 1999.1. turkey flock.213 The prevalence of this disease in the U.179. but no deaths were seen.127-129 Several ferrets recovered.25. 170 Widespread epidemics can be seen.1.6%. and may have been infected there. and recover.1 Explosive epidemics in seals are thought to be exacerbated by high population densities and unseasonably warm temperatures.S.179.330 In 1987. if it exists at all. 25 In populations that have been previously exposed. the overall mortality rate is thought to be 1-5%. In 1989. but recovered.9 Internet Resources page 28 of 46 .000 mink. a cocker spaniel.S.364 This dog was a greyhound that had come from a racetrack in Florida. severe disease is more likely in dogs that are in poor condition or are concurrently exposed to other pathogens. or that the illness might last longer. and 4% in an outbreak with an H4N5 virus.213 Although this disease was first reported in 2004. Influenza in other mammals In 1984. A related virus caused influenza in a few hundred horses the following year but there were no deaths.S.178.1. It had no recent history of respiratory disease. an equine influenza epidemic in India affected more than 27. a survey found antibodies to the H3N8 virus in only one of 225 dogs in 2006. The fate of the dogs in the animal shelter was not stated.330 In horses.180. with morbidity rates of 60-90% or greater.173. however. 91 In seals. new evidence suggests that the H3N8 virus may Last Updated: December 2009 © 2009 have been circulating in U. however. a more severe form with pneumonia may occur in a minority.363 More recently. ferrets and nonhuman primates suggest that this virus might cause more severe lung pathology and/or clinical signs than seasonal human H1N1 viruses. and required hospitalization and supportive care. Canine influenza Canine H3N8 influenza was first reported in racing greyhounds and. most of the population is expected to be fully susceptible. in naïve populations. a novel strain of equine influenza [A/eq/Jilin/89 (H3N8)] caused a serious epidemic in Chinese horses.213 All dogs regardless of breed or age are now considered to be susceptible.330 Higher mortality rates have been reported in foals.120. another developed severe illness with dyspnea but recovered with medical care.253.25. cases are seen mainly in young and newly introduced animals.125 A few cats.362 Decreased egg production and no mortality were reported in a U.133 Only one of the five dogs seen at veterinary clinics survived.
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