AVIAN POX
DEBRA BOURNE
Wildlife Information Network, Twycross Zoo — East Midland Zoological Society, Atherstone, UK
AETIOLOGY
The poxviruses affecting birds are all within the genus Avipoxvirus.
Avipoxviruses include Canarypox virus, Fowlpox virus, Pigeonpox virus, Quailpox virus, Sparrowpox virus and Starlingpox virus; many avipoxviruses have not been fully characterized. Some avipoxviruses appear to infect only one host species, whereas others have a broader host range; some of the avipoxviruses show extensive serological cross-reaction and cross-protection.Infectious Diseases of Wild Mammals and Birds in Europe, First Edition. Edited by Dolores Gavier-Widen, J. Paul Duff, and Anna Meredith. © 2012 Blackwell Publishing Ltd. Published 2012 by Blackwell Publishing Ltd. Material authored by Paul Duff remains Crown Copyright.
EPIDEMIOLOGY
Avian pox has been reported practically worldwide, although there are to date no reports from the Arctic or Antarctic. There have been reports of avian pox in wild birds for more than a century, from more than 15 countries across Europe (Table 13.1).
More than 270 bird species from at least 23 orders have been confirmed as hosts of these viruses, and pox has been reported in at least 60 native species in Europe. In general, birds endemic to remote islands (including the Spanish Canary Islands), which have encountered poxviruses only recently, tend to show more severe forms of the disease. Also, young birds generally show more severe disease than do adults. Several recent reports of pox in great tits (Parus major) in Austria, Hungary and the UK indicate that this may be an emerging infectious disease in the Paridae(7,5).
Prevalence of avian pox is higher in warmer regions with adequate available water providing suitable conditions for
TABLE 13.1 European bird species in which avipoxvirus infections have been recorded.
| Order | Family | Species | Common name | Country reported | References |
| Podicipediformes | Podicipedidae | Podiceps cristatus | Great-crested grebe | Switzerland | 1, 2 |
| Procellariformes | Procelariidae | Puffinus puffinus | Manx shearwater | UK | 1, 2 |
| Ciconiiformes | Ciconiidae | Ciconia ciconia | White stork | Switzerland | 2 |
| Ciconia nigra | Black stork | Switzerland | 1, 2 | ||
| Anseriformes | Anatidae | Anser anser | Greylag goose | Germany | 1, 2 |
| Accipitriformes | Accipitridae | Accipiter gentilis | Northern goshawk | France, Germany | 1, 2 |
| Aquila chrysaetos | Golden eagle | Germany | 1, 2 | ||
| Aquila adalberti | Spanish imperial eagle | Spain | 1, 2 | ||
| Buteo buteo | Common buzzard | Austria | 1, 2 | ||
| Circus pygargus | Montagu’s harrier | Germany | 1, 2 | ||
| Falconiformes | Falconidae | Falco peregrinus | Peregrine falcon | Germany | 2 |
| Falco tinnunculus | Common (Eurasian) kestrel | Germany | 2 | ||
| Galliformes | Phaesinidae | Tetrastes bonasia | Hazel grouse (common | France | 1, 2 |
| hazelhen) | |||||
| Lyrurus (Tetrao) tetrix | Black grouse | Denmark | 1, 2 | ||
| Alectoris rufa | Red-legged partridge | Spain | 1, 2 | ||
| Perdix perdix | Grey partridge | Austria, Denmark, | 1, 2 | ||
| Germany, Italy, UK | |||||
| Gruiformes | Gruidae | Grus grus | Eurasian crane | Germany | 1, 2, 3 |
| Otidiformes | Otidae | Otis tarda | Great bustard | Romania, Germany | 1, 2 |
| Charadriiformes | Haematopodidae | Haematopus ostralegus | Eurasian oystercatcher | UK | 1, 2 |
| Charadriidae | Vanellus vanellus | Northern lapwing | Denmark | 1, 2 | |
| Pluvialis apricaria | European (Eurasian) golden | Denmark | 1, 2 | ||
| plover | |||||
| Scolopacidae | Calidris alpina | Dunlin | UK | 1, 2 | |
| Numenius arquata | Eurasian curlew | bgcolor=white>Germany1, 2 | |||
| Burhinidae | Burhinus oedicnemus | Stone curlew | Canary Islands | 4 | |
| distinctus | (Spain) | ||||
| Lariidae | Larus canus | Mew (common) gull | Denmark | 1, 2 | |
| Larus argentatus | European herring gull | GB | 1, 2 | ||
| Columbiformes | Columbidae | Columbia livia | Common pigeon (rock dove/ | Austria, The | 1, 2 |
| feral pigeon) | Netherlands | ||||
| Columbia junoniae | Laurel pigeon | Canary Islands | 2 | ||
| (Spain) | |||||
| Columba palumbus | Common wood pigeon | UK, Germany, | 1, 2, 5 |
Norway, Sweden
TABLE 13.1 (Continued)
| Order | Family | Species | Common name | Country reported | References |
| Strigiformes | Strigidae | Asio otus | Long-eared owl | Italy | 1, 2 |
| Bubo bubo | Eurasian eagle-owl | Italy | 1, 2 | ||
| Passeriformes | Alaudidae | Alauda arvensis | Eurasian skylark | Denmark | 1, 2 |
| Galerida cristata | Crested lark | Spain | 1, 2 | ||
| Calendrella rufescens | Lesser short-toed lark | Canary Islands | 2 | ||
| (Spain) | |||||
| Motacillidae | Anthus berthelotii | Berthelot’s pipit | Canary Islands | 2 | |
| (Spain) | |||||
| Troglodytidae | Troglodytes troglodytes | Wren | Denmark | 1, 2 | |
| Prunellidae | Prunella collaris | Alpine accentor | Austria | 1, 2 | |
| Prunella modularis | Dunnock | France, UK, Slovakia Poland* (*probable | 1, 2, 6 | ||
| pox) | |||||
| Turdidae | Turdus merula | Common (Eurasian) | Italy | 2 | |
| blackbird | |||||
| Turdus philomelos | Song thrush | Denmark | 1, 2 | ||
| Turdus pilaris | Fieldfare | Italy | 1, 2 | ||
| Turdus viscivorus | Mistle thrush | Italy | 1 | ||
| Sylviidae | Sylvia curruca | Lesser whitethroat | Denmark, Polanda | 1, 2, 6 | |
| Sylvia atricapilla | Eurasian blackcap | Austria, Czech | 2, 6 | ||
| Republic, Slovakia | |||||
| Paridae | Parus major | Great tit | Germany, Norway | 1, 2 | |
| Poecile (Parus) | Willow tit | Polanda | 6 | ||
| montanus | |||||
| Laniidae | Lanius collurio | Red-backed shrike | Poland | 6 | |
| Corvidae | Coloeus (Corvus) | Jackdaw | The Netherlands | 1, 2 | |
| monedula | |||||
| Corvus frugilegus | Rook | Denmark | 1, 2 | ||
| Corvus corax | Northern (common) raven | Denmark | 1, 2 | ||
| Corvus corone | Carrion crow | Denmark, UK, | 1, 2 | ||
| Germany | |||||
| Corvus cornix | Hooded crow | Germany | 1 | ||
| Pica pica | Eurasian magpie | Denmark, Norway | 1 | ||
| Sturnidae | Sturnus vulgaris | Common (European) starling | Austria, Germany | 1, 2 | |
| Passeridae | Passer domesticus | House sparrow | Germany, Norway | 1, 2, 5 | |
| Fringillidae | Fringilla coelebs | Common chaffinch | Germany, UK | 1, 2 | |
| Carduelis spinus | Eurasian siskin | Austria, Germany | 1, 2 | ||
| Carduelis carduelis | European goldfinch | Germany, UK | 1, 2 | ||
| Carduelis chloris | European greenfinch | Germany, UK | 1, 2 | ||
| Carduelis (Linaria) | Common (Eurasian) linnet | Germany | 1, 2 | ||
| cannabia | |||||
| Pyrrhula pyrrhula | Eurasian (Common) bullfinch | Austria, Germany, | 1, 2 | ||
| The Netherlands |
aprobable pox
the insects (mainly various species of mosquitoes), which act as mechanical vectors for the virus. Outbreaks occur mainly during periods when these vectors are numerous and active.
Transmission of avipoxviruses occurs by contact of virus to scarified, lacerated or otherwise injured skin. This may occur by mechanical transmission by insect vectors, or by direct or indirect contact between an infected bird and a potential host. The virus cannot penetrate intact skin, but even small breaks in the cutaneous barrier, including those caused by mosquitoes, fleas etc. when feeding, allow infection. When the virus is present in an aerosol, it can reach and penetrate apparently intact mucous membranes; aerosols of feathers and dried scabs containing virus may allow both cutaneous and respiratory infection.
In wild birds, the main mode of infection is mechanical transmission by mosquitoes feeding on an infected bird and then on a susceptible individual. Once a mosquito has bitten an infected bird, infectious virus may remain in the mosquito’s salivary glands for 2 to 8 weeks. Territorial interactions leading to skin damage allows direct transmission between birds. Additionally, transmission of infection may be increased where birds are fed by humans, a situation which increases local bird density and the possibility of direct or indirect contact via contaminated bird tables or bird feeders. Transmission is also increased in wild birds maintained in captivity for short periods (e.g. during rehabilitation) or for longer periods such as game-bird rearing or breeding for reintroduction. Because avipoxvirus is relatively resistant it can persist, for example on contaminated bird feeders or perches, for long periods. In situations where there are large numbers of birds housed in close quarters, such as canary aviaries, transmission may occur by inhalation of virus-laden dust.
Pathogenesis, pathology and immunity
Following entry into the host epithelium, the virus penetrates cell membranes within an hour and uncoats. Whereas non-pathogenic or low pathogenic strains remain localized at the site of entry, causing localized lesions, with pathogenic strains, following an initial viraemia, the virus becomes distributed to the liver and bone marrow, with further replication, secondary viraemia and generalized clinical disease.
The initial incubation period varies from as short as 4 days in poultry and pigeons to as long as several months reported in some wild birds, and depends on both the virus strain and the host species. Additionally, the process of development of lesions, regression and healing may take longer in wild birds than in domestic poultry.
I n ‘dry’ pox (cutaneous pox), initial nodules may be white, rapidly growing and turning yellow, then grey or brown, sometimes coalescing with adjacent lesions. The nodule base becomes inflamed and haemorrhagic after about 2 weeks. The scab, covering a haemorrhaging granulating surface with a moist seropurulent exudate layer, may last for 1 or 2 weeks, after which the degenerated epithelial layer desquamates to leave a smooth scar, not always visible. In ‘wet’ pox, necrotic, moist diphtheritic lesions or membranes are present on the mucous membranes of the mouth, upper respiratory tract (pharynx and larynx, rarely the bronchi) and sometimes the upper gastrointestinal tract (oesophagus and crop). Initially lesions are discrete, whitish and slightly raised; later coalescing lesions may form a yellowish cheesy pseudomembrane.
Histologically, there is localized epithelial hyperplasia and hypertrophy. In the layers above the stratum germino- sum, maturing cells show hypertrophy and large granular eosinophilic (acidophilic) intracytoplasmic inclusions (Bollinger bodies) are present. Often, there is necrosis in the centre of the lesion and the lesion may be covered by a crust. In the septicaemic form (seen mainly in canaries), the bronchial and parabronchial epithelium show marked proliferation.
Cell-mediated immunity is most important in the host’s response, although antibodies can also play a role in the immune response to the virus. Birds that recover from infection are generally immune to reinfection with that strain of avipoxvirus, but they may be susceptible to a different strain.
CLINICAL SIGNS AND TREATMENT
Clinical signs of avipoxvirus infection in birds vary depending particularly on the host susceptibility and virus virulence, but also on distribution of lesions and complicating factors such as traumatic damage to lesions, and secondary bacterial or fungal infection.
In dry pox, nodular, wart-like lesions are found on featherless areas of the body: around the beak and eyelids, on the wattles and/or comb (in gallinaceous birds), the featherless parts of the legs and feet and sometimes parts of the wings. In perching birds, early lesions are smooth reddish domes, which crack or burst, developing into the typical proliferating lesions. In birds with webbed feet, nodules appear along the blood vessels of the webs, mainly on the plantar surface, with initial focal proliferation and later sloughing. Usually, there are only one or two nodular lesions in wild birds, for example on one or two toes, and they regress spontaneously with no visible scars. However, lesions may be easily damaged with subsequent secondary bacterial or fungal infections. Mortality rates with cutaneous lesions are generally low; however, they may be higher if secondary bacterial infection occurs. Additionally, large lesions, and those around the eyes in particular, may interfere with feeding, leading to debility and predation or death; in some cases lesions around the eyes may blind the bird. Loss of digits may occur as a result of infection.
In wet pox, grey to brown necrotic lesions develop on the mucous membranes of the mouth, pharynx and larynx; if the diphtheritic membrane over the lesions is disturbed, severe bleeding is likely. This form has a higher mortality rate than with dry pox. Combined development of both cutaneous and mucous membrane lesions can occur. The relative paucity of reports of diphtheritic pox in wild birds may indicate lower occurrence or lower detection of this form in free-living birds.
A third, systemic, form of avipox infection is seen mainly in canaries and is rarely reported in wild birds. This presents with acute onset anorexia, somnolence, ruffled feathers and cyanosis; most affected birds die within 3 days of showing signs, and cutaneous lesions are rare.
Treatment of free-living birds is not practical. Where wild birds are in human care, supportive care includes ensuring affected birds have access to food and water; fluid therapy and assisted feeding may be necessary in some individuals.
Ophthalmic ointment may be used to protect the bird’s eyes and keep them moist, and antibiotic treatment may be used to prevent secondary infection, particularly if lesions become traumatized.DIAGNOSIS
Diagnosis of avian pox, as for other pox diseases, is usually based on compatible clinical signs in conjunction with the presence of typical poxvirus Bollinger bodies on histopathological examination and detection of typical pox virions using transmission electron microscopy (TEM).
There have been recent advances in molecular based detection and identification assays, including polymerase chain reaction (PCR) tests, restriction fragment length polymorphism (RFLP) analysis and use of oligonucleotide probes(8). With cutaneous avian pox, the skin lesions are characteristic but should be differentiated from other diseases. Ante mortem diagnosis of the septicaemic form is difficult. Culture of the virus may be required for confirmation of the septicaemic form. Because the host’s immune reactions are mainly cell-mediated, humoral antibodies may not be produced following infection; if present, they may be detected by a virus neutralization test.
MANAGEMENT, CONTROL AND REGULATIONS
Control requires preventing transmission of the virus. This may be possible in a small, confined population but is more difficult in larger areas. Control of vectors, particularly mosquitoes, is important; breeding and resting sites for mosquitoes should be identified and eliminated, and pesticides may be used to control adult mosquitoes. Removal of heavily infected individuals reduces the source of virus for vectors to transmit, as well as reducing direct contact transmission. Where outbreaks occur around wild bird feeders, disinfection of the feeding site and feeders, e.g. using 5% sodium hypochlorite solution (domestic bleach), emptying, drying and refilling of bird baths daily, and temporary discontinuation of feeding (e.g. for a month) before resuming with a smaller quantity of food is recommended. In captive situations such as rehabilitation centres, perches, cages/enclosures, clothing, debris etc. need to be treated with an effective disinfectant such as 5% bleach solution.
PUBLIC HEALTH CONCERN
There is no public health concern associated with avian pox.
SIGNIFICANCE AND IMPLICATIONS FOR ANIMAL HEALTH
Some avipoxviruses of wild birds may also infect domestic poultry, intensively reared game birds, domestic waterfowl and domestic pigeons. Poxvirus infections of wild birds are generally not significant on a population level. However, they may be more important in populations of wild birds endemic to remote islands; a study of birds captured during 2002—2003 on the Spanish Canary Islands found that 50% of 395 short-toed larks (Caland- rella rufescenspolatzeki) and 28% of 139 Berthelot’s pipits (Anthus berthelotti) had typical poxvirus lesions, mainly on the legs, sometimes with large lesions and missing nails or digits; there were few lesions on the head. One bird died after being handled and was found to have diphtheritic pox(9). In free-living red-legged partridges (Alectoris rufa) in Spain, 41% of radio- tagged juveniles (but no adults) were found to have pox-type lesions when captured. While only a few deaths directly due to pox were recorded, and there were no significant differences between survival of juveniles with and without lesions, sample sizes were small; it was noted that indirect effects (reduced weight gain, increased susceptibility to predation) might also contribute to mortality(10).