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Viral skin diseases of birds
Viral Skin Diseases of Birds Shane R. Raidal, BVSc, PhD
Viral skin diseases that are commonly observed in avian practice are reviewed. The clinical signs of psitracine circovirus disease, avian pox, and papovavirus diseases are described. Emphasis is placed on the diagnosis and management of these diseases.
Copyright 9 1995 by W.B. Saunders Company Key words: Psittacine beak and feather diseasevirus, pox, polyomavirus, papilloma.
t least four groups of viruses that have the skin as a target organ are recognized in birds. These are psittacine beak and feather disease virus (psittacine circovirus disease virus [PCDV], avipoxviruses, papovaviruses, and herpesviruses. Viral skin diseases can be localized or generalized. Some could be considered as primary skin diseases because epidermal tissue pathology is the major disease feature. Clinicians should be alert to syndromes with an infectious epidemiology because there may be many viruses that have the skin as a target organ. In this review, viral infections that are known causes of skin disease are described.
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Psittacine Circovirus Disease (PCD) PCD describes probably the most recognisable disease of Psittaciformes. The disease is a major problem of wild psittacine birds in Australia, 1-6 and all psittacine species should be considered susceptible because the disease has been reported in both captive New and Old World psittacine species. 7-11 PCD has distinct pathological features, and the unique virus particles that can be recovered consistently from the cutaneous tissue of affected birds can cause the disease in susceptible birds. 5'12-14 The viral genome is a circular single-stranded DNA molecule, 13'15 and there is no ultrastrucFrom the School of Veterinary Studies, Murdoch University, Western Australia. Address reprint requests to Shane R. Raidal, BVSc, PhD, School of Veterinary Studies, Murdoch University, WesternAustralia, 6150 Australia. Copyright 9 1995 by W.B. Saunders Company 1055-937X/95/0402-000355.00/0 72
tural, protein, or antigenic variation in isolates from different genera of psittacine birds. TM These features place it in the proposed family Circoviridae. Disease syndromes similar to PCD have recently been reported in doves. 17'18
Clinical Signs The clinical signs and pathology of PCD have been thoroughly described.l-5'l~176 In most circumstances, a clinician can accurately diagnose PCD by clinical examination. 1,21,22 Two main clinical presentations exist: chronic and acute. Chronic PCD is insidious in its d e v e l o p m e n t and p r o g r e s s i o n ; dystrophic feathers gradually replace normal ones as they are moulted. Birds older than 10 years can succumb to the disease. 2s In cockatoos, the powder-down feathers (pulviplumes) are often the first feathers affected. PCD-affected pulviplumes may be fragile or develop an abnormally thickened outer sheath that fails to disintegrate. Alternatively, they may cease to develop and thus create bare powder-down patches. 1'24 Arrested production of powder-down causes the plumage to become dull and the beak to become glossy. The pattern of feather dystrophy is related to the stage of moult that the bird is in when the disease first begins and is usually bilaterally symmetrical and slowly progressive. Dystrophic feathers are usually short and have one or more of the following characteristics: fault lines across the vanes; a thickened or retained feather sheath; blood within the calamus; an annular constriction of the calamus; or curling. In Neophema species, apparently normal feathers that fall out or are effortlessly plucked may be the only clinical sign. The first clinical sign in birds with green plumage may be the development of yellow feathers that appear grossly normal in other respects. 24 This is probably the result of pathological changes in feather ultrastructure. On the extremities, PCD-induced hyperkeratosis can cause the skin to appear excessively scaly or it may be thickened and moist. Sun-
Seminars in Avian and Exotic Pet Medicine, Vol 4, No 2 (April), 1995: pp 72-82
Viral Skin Diseases of Birds
light-exposed skin can become darkly pigmented. 2"4 Chronic skin ulcers can occur at the elbows and wing tips, Beak, and less commonly, claw deformities occur in some PCDa f f e c t e d \ b i r d s , and particularly in cockatoos. 3'25 The beak can become abnormally soft and brittle, and the upper and lower tips can become elongated. Transverse or longitudinal fractures or delaminations often O C C U r . 2-4 In severe cases, necrosis of the oral epithelium 1 and osteomyelitis can cause the beak to slough. 3,7 Secondary disease problems commonly exist. 3'26 These include cryptosporidiosis, bacterial, mycotic, or viral infections. 27-29 Most birds with chronic disease eventually have difficulty eating, lose weight, and die.
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acute PCD cannot be definitively distinguished from psittacine polyomavirus disease by clinical investigation alone. A definitive diagnosis requires the use of PCDV-specific assays. These include electron microscopy, immunohistochemistry, hemagglutination assay, and DNA hybridization. Serology is also useful for detecting PCDVinfected flocks and for demonstrating seroconversion in individual birds. All test results must be interpreted in conjunction with the clinical signs and the age of the bird.
Acute PCD The most severe feather abnormalities occur in nestlings. ~'7'3~ Many diseased contour feathers may be shed, or only the primary flight feathers may be affected. Feather necrosis and accompanying intrapulp hemorrhage are the major clinical findings. Affected feathers fracture from the point of necrosis, usually before the feather has exsheathed. Feather tracts can become acutely inflamed, and the birds often become systemically ill, anorexic, and/or regurgitate food. Death may occur within 1 to 2 weeks of developing clinical signs. At postmortem, thymic and bursal atrophy may be evident.-~'5'~2 Most young birds recover from the acute phase only to become Chronically affected. Acutely affected birds often have mucoid or green diarrhoea.l-~ These signs are often clinically diagnosed as secondary bacterial or chlamydiat infections. 26'~'34 However, PCDV can cause acute hepatitis, and high concentrations of PCDV can be detected in the livers and bile of PCD-affected b i r d s Y Some birds (particularly juvenile gang gang cockatoos) may die o f acute hepatitis without obvious feather lesions.
Tissue Pathology Histological examination of feather follicle or feather biopsies is routinely used to confirm clinical disease. ~'s In one study, it provided an accurate diagnosis for 31 of 32 PCD-affected birds. ~1 However, it is not suitable for diagnosing incubating PCDV infection or for detecting PCDV carriers. 34'~6 Various immunohistochemical techniques have been used to identif~ PCDV antigen in tissue sections, l~176 However, these methods are not routinely used for diagnosis. In the feather follicle, necrosis of the cells of the stratum germinitivum, epidermal hyperplasia, and hyperkeratosis are the major histological lesions. 2'2~ However, the presence in the dermis and epidermis of macrophages containing sometimes relatively large purple intracytoplasmic inclusions is considered characteristic of the disease. 2-5'm'24"~2 Similar lesions can occur in the beak, bursa of Fabricius, thymus, endothelial cells, Kupffer cells, and esophageal epithelial cells. 2'5'10'12'24 Signs of acute or chronic inflammation also may exist. 5'19'2~ In interfollicular skin, ulcers I or hyperkeratosis may be observed. Affected epidermal cell nuclei may be swollen and amphophilic and do not contain easily identifiable virus particles. 7'1z However, individual virions can be detected in affected nuclei by immuno-electron microscopy. 2~
Methods for Diagnosing PCD A thorough history and a clinical examination o f all feather tracts is necessary for a diagnosis of PCD. Few other diseases can be confused with the impressive pathology of chronic PCD. However, injured feather 'follicles can produce feathers that look similar to PCD, and
Direct Electron Microscopy Direct electron microscopic examination of negatively stained feather pulp homogenates is a rapid method for diagnosing PCD.12'32 Fortunately, PCDV particles form aggregates that are readily identified amongst cellular debris. 12,32,~8
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Shane R. Raidal
Hemagglutination Assay (HA) HA is" currently the only method available for detecting PCDV that is also quantitative. It is aw~uable tool for detecting PCDV particles in feathers, liver, and fecal material. 35'38'~9 Nonspecific reactions have not been recorded with feathers from clinically normal birds. HA can be performed on actively growing feather pulp or dry keratinized feathers. PCDV antiserum is required to validate HA reactions particularly because nonspecific HA reactors sometimes occur in fecal specimens. Feather testing is preferred over fecal testing because acutely PCD-affected birds do not excrete high concentrations of virus in feces, and some chronically affected birds excrete intermittently. ~8
Polymerase Chain Reaction (PCR) and DNA Dot-Blot Assays PCR and DNA-probe assays have been used for the detection of PCDV genome in chilled blood samplesY '4~ This is probably the best m e t h o d for detecting latent or incubating PCDV infection. It does not detect PCDV particles or antigen. Retesting is recommended after 90 days if a test is positive, but clinical signs are absent. 41'42 A positive PCR product is not a demonstration of active infection because nonreplicating viral DNA may take up to 3 months to clear from the blood stream. 4~ Like other diagnostic assays, false-positive results probably occur and false-negative results do occur. 41 PCR detection systems are rapid and can theoretically be designed to detect individual viral genomes, making them the most sensitive assays available. Extreme care must be taken in the field and in the laboratory to avoid contamination of samples. PCR tests should be used together with, and not replace, conventional diagnostic regimes. The sensitivities of some PCR assays may have the same order of magnitude as conventional methods 44 or they may be significantly less sensitive. 45
Serology Hemagglutination inhibition (HI) tests have been described for PCDV serologyP s'39 The presence of antibody means that the bird has been exposed to PCDV, and a high HI titer in an adult bird is a good indicator that it does not
have chronic PCD. ~8 Nestlings with incubating PCDV infection or acute disease may have low and declining serum HI titers. 14 An agar gel diffusion test has been used to detect precipitating antibody in vaccinated birds. ~1 However, the assay had a lower sensitivity than HI and failed to detect antibody in vaccinated chicks. Detection of precipitating antibody in PCD-affected birds has not been reported.
Pathogenesis The incubation period of PCD can be as short as 21 days, 5'12'14'31 but it is probably dependent on the dose of virus, the age of the bird, the stage of feather development, and the absence of immunity. Primary virus replication probably occurs in the bursa of Fabricius and/ or gastrointestinal tract lymphoid tissue. Secondary virus replication occurs in the liver and thymus and probably other tissues. The target organ is the epidermis, and the manifestation of skin disease requires a moult. Consequently, birds that become infected after feather development has completed may not develop clinical signs until their next moult. This could take 6 or more months. Most birds that succumb to PCD are less than 2 years of age. The disease is difficult to reproduce in adult birds. However, all age groups should be considered susceptible to PCDV infection. 2~ Perhapschronic exposure to high concentrations of PCDV and/or stress is required for infection and seroconversion in adult birds.
Prognosis Early reports of spontaneous recovery from PCDV probably concerned birds infected with polyomavirus. These cases may have been misdiagnosed histologically owing to lack of knowledge at that time regarding intracytoplasmic versus intranuclear inclusions. It is now known that complete or partial recovery from acute PCD (confirmed by HA testing and histology) can occur in some species and may or may not be associated with seroconversion. This occurs more frequently with Budgerigars (Melopsittacus undulatus), Rainbow Lorikeets (Trichoglossus haematodus), lovebirds (Agapornis species),33 and Eclectus Parrots (Eclectus roratus). The majority of psittacine species with chronic
Viral Skin Diseases of Birds
PCDV do not recover from the disease and do not respond to treatment with antibiotics, vitamins, glucocorticoids, and autogenous vaccines.
Epidemiology In Australia, PCD has been confirmed in wild Galahs (Eolophus roseicapillus), Rainbow Lorikeets, Orange-bellied Parrots (Neophema chrysogaster), Crimson Rosellas (Platycercus elegans) Eastern Rosellas (Platycercus eximius), Mallee Ringneck Parrots (Barnardius barnardi), Port Lincoln Parrots (Barnardius zonarius), Major Mitchell's Cockatoos (Cacatua leadbeateri), Gang Gang Cockatoos (Callocephalon fimbriarum), King Parrots (Alisterus scapularis) and Swift Parrotsb(Lathamus discolor). Anecdotal evidence indicates that it occurs in wild Budgerigars, Red-rumped Parrots (Psephotus haematonotus), and Yellow-tailed Black Cockatoos
(Calyptorhynchusfunereus funereus). 1-6,33 PCD has been reported in aviary flocks of
Agapornis species in Zimbabwe. 46-4s However, there is no evidence to support its occurrence in wild African birds (Dr N. Kock, personal communication, September 1993). International trafficking of psittacine birds for aviculture has probably been responsible for the occurrence of PCD in most countries where psittacine birds are kept. The disease presumably also occurs in wild Asian cockatoos because wild-caught fledglings exported from this area have developed the disease. 7 Flocks of wild cockatoos may have a disease prevalence of 20% and a seroprevalence of 60% to 80%. 4,6 Infection is probably maintained in a population by diseased birds. Virus transmission is probably predominantly by horizontal spread, but carrier birds may contribute by vertical transmission. Virus infectively probably persists in contaminated nest sites for many months or years, and this could result in cross-species transmission. Aviary flocks with a history of PCD usually hav~ a high Seroprevalence. 40 In these situations, PCD-affected birds are often the progeny of hens with low or nondetectable serum antibody levels.
Prevention and Control Aviculturists should be advised to maintain a closed flock or purchase birds from PCD-free
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flocks and to breed birds in quarantine. The appropriate use of disinfectants that are suitable for inactivating environmentally resistant viruses should be recommended for disinfecting contaminated utensils, cages, and rooms. 5~ Experimental inactivated PCD vaccines have been prepared by conventional methods. 14'31'49 Vaccination of breeding hens enhances passive transfer o f immunity, 31'40 which may interfere with vaccination of progeny. Vaccination of young birds may not prevent transient viral replication and excretion or persistent infection.a4
Avian Pox Avipoxviruses cause skin disease (pox) in m a n y species o f d o m e s t i c a t e d a n d wild birds. 52-56 Pox does not occur naturally in domestic ducks, but they are susceptible to inoculation with turkey poxvirus. 57 In psittacine birds, pox has been reported in Black-Masked Conures, 58 a Red-Winged Parrot, 54 a Military Macaw (Ara militaris mexicana)59 and Amazon P a r r o t s . 6~ A nonpathogenic budgerigar poxvirus also has been reported. 52 Avipoxviruses are epitheliotropic and typically cause localized tumors in the nonfeathered areas of skin. Internal diphtheritic and/or systemic syndromes also occur in some species. In diphtheritic pox, the oral and respiratory mucus m e m b r a n e s are p r e d o m i n a n t l y affected. 59'62 Canary poxvirus, possibly the most virulent of the avipoxviruses, can cause up to 100% mortalities in susceptible canary f l o c k s . 63-65
Avipoxviruses are designated according to their host as, for example, fowl poxvirus, canary poxvirus, and mynah poxvirus. The antigenic relationships between avipoxviruses are complicated. 52'62'66 In a heterologous host species, avipoxviruses may not replicate or they may replicate and be either nonpathogenic or pathogenic. Avipoxviruses that replicate in a heterologous host species may or may not induce immunity to other avipoxviruses that are pathogenic to that host. Quail poxvirus causes severe disease in chickens but when administered as a vaccine does not protect chickens from challenge with either fowl, pigeon, or mynah poxviruses.
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Shane R. Raidal
Also, chickens vaccinated with the latter three viruses are not protected from quail poxvirus challenge. Similarly mynah poxvirus is pathogenic for chickens but is antigenically distinct from~owl and pigeon poxviruses. 67 Psittacine poxviruses are antigenlcally distinct from quail, fowl, and pigeon poxviruses. 62'66
Clinical History Cutaneous pox is characterized by the proliferation of nodular or crusty lesions on the nonfeathered areas of skin. Lesions may occur on the beak, feet, and claws and begin as white or yellow foci that rapidly increase in size. Depending on the stage of infection, they may appear as vesicles, papules, pustules, or crusty scabs. Secondary bacterial or fungal infections can complicate the diagnosis and progression of lesions. Tumors on the eyelids; conjunctival proliferation, or blepharitis can impair vision 56'61 In lovebirds, pox may present as a dark or discolored area of skin. 52 Diphtheritic lesions may occur in conjunction or in the absence of cutaneous lesions. Caseous plaques may be observed in the mouth, pharynx, trachea, sinuses, or larynx. Canary pox may present as a sudden onset of dyspnea or sudden death. Upper respiratory tract disease, pneumonia, airsacculitis, and splenomegaly may be evident.
Diagnosis Diseases that resemble avian pox include fungal or bacterial granulomas, abscesses, parasitic cysts, or neoplasia. A presumptive clinical diagnosis of pox can be confirmed by histological examination and virus isolation. Avipoxviruses may be demonstrated by electron microscopy and are readily isolated on the chorioallantoic m e m b r a n e of embryonated chicken eggs. Various serological assays have been described for detecting antibodies to poxviruses. However, serology is rarely used or necessary for making a diagnosis.
tological sections and Borrel bodies in impression smears). The epithelium of the upper and lower respiratory tract, oral cavity, and oesophagus may be affected. 6~ Inclusions can be identified by immunoperoxidase staining. 6s
Epidemiology Avian pox is a relatively slow-spreading disease that can affect birds of all ages. Transmission is predominantly by blood-sucking insects such as mosquitoes, mites, and biting flies. 69-71 There is no replication in these vectors, but virus may remain infectious in insects for 10 months. 72,73 Infection can be initiated in traumatized epithelial tissue by indirect transmission from contaminated feed and water utensils. Direct transmission between birds can occur after the ingestion of scabs or inhalation of aerosols. The incubation period is 7 to 14 days. Recovered birds probably develop strong lifelong immunity and do not develop into virus carriers. 57
Treatment It is imperative to control mosquitoes and ectoparasites in an epidemic situation. Individual treatment is aimed at supporting the bird until it recovers. Lesions usually heal within 4 weeks, but this can be enhanced by physically removing nodules as they develop. Surgery may be necessary to remove large tumors from the face. Nonirritant detergents or shampoos, diluted with saline, are suitable for softening and removing nodular lesions from around the eye. Bleeding can be controlled by thermal or chemical cautery. Vitamin supplementation, immunostimulant, or anti-inflammatory drugs may be appropriate treatment for individual birds. Treatment with sodium salicylate or acetylsalicylic acid delayed and reduced the development of skin lesions of fowls with experimentally i n d u c e d pox. TM Antimicrobial therapies are important for the control of secondary bacterial and fungal infections.
Pathology Histologically, pox is c h a r a c t e r i z e d by marked epithelial hyperplasia and vacuolar degeneration of epithelial cells associated with the formation of eosinophilic ihtracytoplasmic inclusion bodies (called Bollinger bodies in his-
Prevention Virulent or attenuated vaccines are conventionally administered at an aberrant site, usually by wing stab or directly to a freshly plucked c o n t o u r f e a t h e r follicle over the
Viral Skin Diseases of Birds
thigh. 57'75'76 Only healthy birds should be vaccinated. Some birds may develop severe lesions at the site of vaccination. Horizontal transmission virus can occur under favourable conditions 76 but may not be reliable. Consequently, birds vaccinated with virulent strains are infectious for up to 8 weeks and should be isolated from susceptible birds. All healthy birds in a flock should be vaccinated. Maternal antibody does not confer effective passive immunity.57 A single vaccination should induce lifelong immunity, but annual boosters may be necessary on a flock basis. 57 A single vaccination should induce lifelong immunity, but annual boosters may be necessary on a flock basis. 57 In some situations, primary vaccination by drinking water medication 77'7s or intranasal or aerosol inoculation 7~ may be appropriate.
Papovavirus Infections The Papovaviridae are subdivided into two genera, the papillomaviruses and the polymaviruses. Paplllomavlruses are common causes of benign nodular epidermal tumors in mammals and have been demonstrated within similar tumors in many bird species. Avian polyomaviruses (APV) cause pansystemic disease in finches 81'82 and psittacine birds but have been reported as causes of skin disease only in the latter. 9
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Polyomavirus Infection of Psittaciformes APV were first reported as a cause of skin disease and mortality in juvenile budgerigars. s3-s7 Much is known about budgerigar polyomavirus, and consequently it is considered the prototype polyomavirus, ss Its entire genome has been sequenced, s~ APV from different host species appear morphologically, antigenically,~176176 and genetically similar. ~ Like PCD, APV are probably capable of causing disease in all psittacine species. However, nestling and juvenile birds are most susceptible. 01'~ Most birds that recover from the acute phase of APV disease make a complete clinical recovery9 Chronic progressive skin disease is not a feature of APV infection. However, persistent virus infection and excretion are common sequelae. Concurrent APV and PCDV infection can occur. ~
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Clinical history. In budgerigars, polyomavirus infection causes severe clinical signs in susceptible nestlings less than 15 days of age. ~ Affected nestlings may be ataxic or have head tremors. ~ There may be abdominal distension caused by hepatomegaly and ascites, subcutaneous petechiae or ecchymosis, or a generalized pallor. The mortality rate in this age group can be 100%. Death usually occurs within 48 hours of the development of clinical signs. Gross necropsy lesions may be absent. The crop is often distended with food. A severe drop in hatchability also has been reported. 97 Older budgerigar nestlings may fail t o develop normal contour feathers, and affected contour feathers may lack normal barbs9 The rectrices and secondary remiges may fail to develop. There may be a lack of down feathers on the back and abdomen and lack of contour feathers on the head and neck. s~'s7 At necropsy, there may be cardiomegaly, hydropercardium, and hepatomegaly or focal hepatic necrosis. In other species, APV can cause nonspecific signs of illness including anorexia crop stasis, depression, paresis, and ataxia. ~176 Sporadic sudden deaths may occur in juvenile or adult birds with or without the presence of feather abnormalities.~176176176 Methods for diagnosing APV infection. A presumptive diagnosis of APV infection can be made from the history and clinical and pathological features9 However, histopathological, bacteriological, and serological investigations should be used to rule out differential diagnoses9 Tests that are sensitive and APVspecific are required for making a definitive diagnosis. Histopathology. APV infections cause necrosis and marked basophilic karyomegaly in many tissues, in particular, the feather follicles, kidney, and liver. 86'06'1~176 Relatively large, amorphous, basophilic intranuclear inclusions can be found in persistently infected kidneys, but they cannot be differentiated morphologically from other viral infections. 1~176 A definitive diagnosis requires the use of electron microscopy or APV-specific c y t o c h e m i c a l staining. APV antigen has been detected in tissue sections by immunoperoxidase staining, ~176 and APV DNA has been demonstrated by in situ DNA hybridization.~
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Shane R. Raidal
Virus isolation. Psittacine polyomavirus can be cultured in vitro i n budgerigar embryo fibroblast, 1~ chicken embryo fibroblast s4 or chicken embryo kidney cell culturesY Virus isolatibn is generally not available for routine diagnosis. Polyomavirus genome detection. PCR amplification and DNA-probe assays have been described. 4~176176176 PCR and DNA-probe testing for APV is highly sensitive and specific and can be performed on serum or any tissue or secretion. However, cloacal swabs are preferred, and these are probably the least stressful to collect. These qualities in a diagnostic assay are desirable for flock monitoring. A positive DNA-probe test means that APV DNA was detected in the sample. This is an important finding on a flock basis but should be interpreted with circumspection for an individual pet bird. Serology. Antibodies to APV have been detected by immunodiffusion, 1~ virus neutralisation (VN) assay, m'l~ and indirect immunofluorescence. 1~176 Serology is Probably more sensitive than cloacal DNA probe for detecting polyomavirus infection on a flock basis. ~176176 Epidemiology. APV is excreted in feather dander and droppings, and horizontal transmission is the major method of infection in an epidemic, but vertical transmission also may occur. 83'87'01'07 Infection persists in the kidneys of carrier birds, and virus is excreted intermittently during times of stress. APV are thermostable, can withstand freeze thawing, and remain infective in contaminated environments. 84 Aviary flocks with endemic APV infection may have a seroprevalence up to 100%. 91'1~ APV carriers may be seropositive or seronegative,l~ and their serological status can change over time. Up to 100% of birds in a flock may be persistently APV-infected) ~ Prevention and control. Aviculturists with a disease-free situation, should be encouraged to maintain a closed flock with strict hygiene and quarantine procedures. This includes eliminating exposure to free-flying wild birds and regulating all food, utensils and humans with access to the birds. APV probably remain infectious u n d e r the fingernails of well-meaning visitors for long periods. New ~tock should be obtained from certified seronegative and APV-
free aviary flocks. They must be held in quarantine and confirmed as APV free, preferably both by serology and DNA-probe before being incorporated into the breeding flock. In an endemic situation, an effort should be made to eradicate horizontal transmission between birds and between batches of young birds. Accurate record keeping and regular disease monitoring are most important. It may be desirable to identify APV carriers and isolate these birds in a separate facility. Incubators and brooders must be thoroughly cleaned and disinfected between clutches. Chlorine, 97 synthetic phenol, stabilized chlorine dioxide, sodium hypochlorite, and 70% ethanol have been effective in reducing the infectivity of APV. 51 Air filtration systems that extract aerosolized virus should be used. Macaw chicks that received an experimental inactivated APV vaccine developed relatively low VN titers (1:20 to t :40). 11~ Challenge virus did not cause immunological stimulation because an increase in antibody titer and APV excretion was not detected. In contrast, viral replication probably occurred in unvaccinated birds because they seroconverted (VN titers of 1:640) and excreted APV. Vaccination was not shown to prevent disease because unvaccinated birds remained clinically normal.
Papillomavirus Skin Disease Papillomaviruses have been detected in epidermal tumors in African Grey Parrots, 111,112 chaffinches, 113-115 canaries, 116 and greenfinches. 117 The main histological finding is epidermal hyperplasia and dysplasia. 116 Affected keratinocytes may be polyhedral with an amorphous, pale, or eosinophilic cytoplasm. There may be margination of nuclear chromatin, or nuclei may be vacuolated or contain a basophilic inclusion. A tentative diagnosis of papillomavirus disease can be made by clinical signs and histopathology. However, immunohistochemical techniques and/or electron microscopy are required to demonstrate papillomavirus particles or antigen in lesions. 111,116-1lS
Herpesvirus Infections In chickens, complete replication of Marek's disease virus (MDV) occurs only in feather follicle epidermal cells, la9 Histologically, intranu-
Viral Skin Diseases of Birds
clear inclusions can be found in epidermal cells. There may also be focal infiltrations of neoplastically transformed lymphocytes in the dermis adjacent to infected feather follicles. HerpesvaXr-us infections similar to MDV have not been reported in companion birds. However, herpesviruslike particles have been described in tumors on the feet of c o c k a t o o s 52'12~ and a wild mallard duck. 121 Herpesviruses may be responsible for at least some of the internal papilloma syndromes that occur in psittacine birds. 122-12s
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References 1. Perry RA: Psittacine beak and feather disease, in Hungerford T G (ed): Proceedings 55: Courses for Veterinarians. Aviary and Caged Birds. Sydney, Australia, T h e Postgraduate Committee in Veterinary Science, 1981, pp 81-108 2. Pass DA, Perry RA: The pathology of psittacine beak and feather disease. Aust Vet J 61:69-74, 1984 3. Pass DA, Perry RA: Psittacine beak and feather disease: An update. Aust Vet Pract 15:55-59, 1985 4. McOrist S, Black DG, Pass DA, et ah Beak and Feather Dystrophy in wild sulphur-crested cockatoos (Cacatua galerita). J Wildl Dis 20:120-124, 1984 5. Wylie SL, Pass DA: Experimental reproduction of psittacine beak and feather disease/French moult. Avian Pathol 16:269-281, 1987 6. Raidal SR, McElnea, CL, Cross GM: Seroprevalence of psittacine beak and feather disease in wild psittacine birds in New South Wales. Aust Vet J 70:137139, 1993 7. Jacobsen ER, Clubbs, Simpson C, et ah Feather and beak dystrophy and necrosis in cockatoos: Clinicopathologic evaluations. J Am Vet Med Assoc 189: 999-1005, 1986 8. Huff DG, Schmidt RE, Fudge AM: Psittacine beak and feather syndrome in a blue-fronted Amazon (Amazona aestiva). J Assoc Avian Vet 2:84-86, 1988 9. Allen, SK: Psittacine beak and feather disease in an african grey parrot. J Assoc Avian Vet 4:18-19, 1990 10. Latimer KS, Rakich PM, Kircher IM, et ah Extracutaneous viral inclusions in psittacine beak and feather disease. J Vet Diagn Invest 2:204, 1990 11. Greenacre CB, Latimer KS, Niagr6 FD, et ah Psittacine beak and feather disease in a scarlet macaw (Ara macao). J Assoc Avian Vet 6:95-98, 1992 12.. Wylie, SL: Studies on psittacine beak and feather disease. Doctorate thesis, Murdoch University, Perth, Western AustraLia, 1991 13. Ritchie BW, Niagro FD, Lukert PD, et ah Characterization of a new virus from cockatoos with psittacine beak and feather disease. Virology 171:83-88, 1989 14. Raidal SR, Firth GA, Cross GM: Vaccination and challenge studies with psittacine beak and feather disease virus. Aust Vet J 70:437-441, 1993 15. T o d d D, Niagro FD, Ritchie BW, et ah Comparison
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of three animal viruses with circular single-stranded DNA genomes. Arch Virol 117:129-135, 1991 Ritchie BW, Niagro FD, Latimer KS, et ah Ultrastructural, protein composition, and antigenic comparison of psittacine beak and feather disease virus purified from 4 genera of psittacine birds. J Wildl Dis 26:196-203, 1990 Pass DA, Plant SL, Sexton N: Natural infection of wild doves (Streptopelia senegalensis) with the virus of psittacine beak and feather disease. Aust Vet J 71: 307-308, 1994 Woods LW, Latimer KS, Niagro FD, et ah Circovirus infection in pigeons. Proceedings of the Association of Avian Veterinarians, Nashville, TN, 1993, pp 156157 Pass DA, Perry RA: Granulomatous dermatitis in peach-faced lovebirds. Aust Vet J 64:285-287, 1987 Latimer KS, Rakich PM, Steffens WL, et ah A novel DNA virus associated with feather inclusions in psittacine beak and feather disease. Vet Pathol, 28:300304, 199t Latimer KS, Rakich PM, Ritchie BW, et al: Recent advances in the diagnosis and pathogenesis of Psittacine Beak and Feather Disease. Proceedings of the Association of Avian Veterinarians, Seattle, WA, 1989, pp 57-59 Speer B: Clinical examination for evidence of PBFD. J Assoc Avian Vet 4:205-206, 1990 Ritchie BW, Niagro FD, Lukert PD, et ah A review of psittacine beak and feather disease. Characteristics of the PBFD virus. J Assoc Avian Vet 3:141-149, 1989 Pass DA: T h e pathology of the avian integument: A review. Avian Pathol, 18:1-72, 1989 Jergens AE, Brown TP, England TL: Psittacine beak and feather disease syndrome in a cockatoo. J Am Vet Med Assoc 10:1292-1294, 1988 Smith RE: Psittacine Beak and Feather Disease: A cluster of cases in a cockatoo breeding facility. Proceedings of the Association of Avian Veterinarians, Miami, FL, 1986, pp 17-20 Latimer KS, Steffens WL, III, Rakich PM, et al: Cryptosporidiosis in four cockatoos with psittacine beak and feather disease. J Am Vet Med Assoc 200: 707-710, 1992 Wylie SL, Pass DA: Investigations of an enteric infection of cockatoos caused by an enterovirus-like agent. Aust V e t J 66:321-324, 1989 Ritchie BW, Niagro FD, Latimer KS, et ah Routes and prevalence of shedding of psittacine beak and feather disease virus. Am J Vet Res 52:1804-1809, 1991 Perry, RA: Some feather characteristics of F r e n c h Moult in fledgling budgerigars (Melopsittacus undulatus). Aust Vet Pract 13:128, 1983 Ritchie BW, Niagro FD, Latimer KS, et ah Antibody response to and maternal immunity from an experimental psittacine beak and feather disease vaccine. A m J Vet Res 53:1512-1518, 1992 Gough RE, Collins MS, Gresham AC: A parvoviruslike agent associated with psittacine beak and feather disease. Vet Rec 66:119, 1989 Perryl RA: Bird rehabilitation, in Hungerford, T G
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Viral Skin Diseases of Birds
peroxidase technique for detection of fowlpox antigen. Avian Dis 17:274-278, 1973 69. Akey B, Nayar J, Forrester D: Avian pox in Florida wild turkeys: Culex nigripalpus and Wyeomyiavanduzeei as experimental vectors. J Wildl Dis 17:597-599, 1981 70. Nayar~J: Bionomics and physiology of Culex nigripalpus (Diptera: Culicidae) of'Florida: An important vector of diseases. Technical Bulletin No. 827, Vero Beach, Florida Agricultural Experiment Station, 1982, pp 1-73 71. Forrester D: The ecology and epizootiology of avian pox and malaria in wild turkeys. In: Proceedings, Symposium: Vectors of Wildlife Diseases, 22nd Annual SOVE Conference, Mesa, AZ. Bull Society Vector Ecol 16:127-148, 1991 72. Casas EDL, Harein P, Deshmukh D, et al: Relationship between the lesser mealworm, fowl pox, and Newcastle disease virus in poultry. J Econom Entomol 69:775-779, 1976 73. Shirinov F, Ibragimova A, Misirov Z: The dissemination of the virus of fowl pox by the mite D. gallinae. Veterinariya 4:48-49, 1972 (abstr) 74. Bartoszcze, M: Antiviral activity of some salicylic compounds against fowl pox virus. Polskie Archiwum Weterynaryjne 19:45-58, 1976 (abstr) 75. Hitchner S: Canary pox vaccination with live embryo attenuated virus. Avian Dis 25:874-881, 1981 76. Winterfield R, Clubb S, Schrader D: Immunization against psittacine pox. Avian Dis 29:886-890, 1985 77. Mayr A, Danner K: Oral immunization against pox. Studies on fowl pox as a model. Devel Biol Standardiz 33:249-259, 1976 78. Saini S, Maiti N, Sharma S: Immune response of chicks to oral vaccination with combined extra and intracellular fowl pox viruses. Trop Anim Health Product 22:165-169, t990 79. Sarma D, Sharma S: Immune response of chicks vaccinated with fowl pox virus vaccines by the intranasal route. Acta Vet Beograd 38:181-188, 1988 (abstr) 80. Mathews, REF: Classification and nomenclature of viruses. Intervirology 17:1-199, 1982 81. Forshaw D, Wylie SL, Pass DA: Infection with a virus resembling papovavirus in Gouldian finches (E~ythrura gouldiae). Aust Vet J 65:26-28, t988 82. Garcia AP, Latimer KS, Niagro FD, et al: Avian polyomavirus infection in three black-bellied seed crackers (Pyrenestes ostrinus). J Assoc Avian Vet 7:79-82, 1993 83. Bernier G, Morin M, Marsolais G: A generalized inclusion body disease in the budgerigar (Melopsittacus undulatus) caused by a papovavirus-like agent. Avian Dis 25:1083-1092, 1981 84. Bozeman LH, Davis RB, Gaudry D: Characterization of a papovavirus isolated from fledgling budgerigars. Avian Dis 25:972-980, 1981 85. Davis RB, Bozeman LH, Gaudry D: A viral disease of fledgling budgerigars. Avian Dis 25:179-183, 1981 86. Dykstra MJ, Bozeman LH: A light and electron microscope examination of budgerigar fledgling disease virus in tissue and cell culture. Avian Pathol 11 : 11-28, 1982 87. Bernier G, Morin M, Marsolais G: Papovavirus ini
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duced feather abnormalities and skin lesions in the budgerigar: Clinical and pathological findings. Can VetJ 25:307-310, 1984 88. Lehn H, Muller H: Cloning and characterization of budgerigar fledgling disease virus, an avian polyomavirus. Arch Virol 151:362-370, 1986 89. Rott O, Kroger M, Muller H, et al: The genome of budgerigar fledgling disease virus, an Avian Polyomavirus. Virol 165:74-86, 1988 90. Clubb SL, Davis RB: Outbreak of a papova-like viral infection in a psittacine nursery - A retrospective view. Proceedings of the Association of Avian Veterinarians, Toronto, Canada, 1984, pp 121-129 91. Jacobson ER, Hines SA, Quesenbery K, et al: Epinortic of papova-like virus-associated disease in a psittacine nursery. J Am Vet Med Assoc 185:13371341, 1984 92. Phalen DN, Wilson VG, Graham DL: Polymerase chain reaction assay for avian polyomavirus. J Clin Microbiol 29:1030-1037, 1991 93. Stoll R, Luo D, Kouwenhoven B, et al: Molecular and biological characteristics of avian polyomaviruses: isolates from different species of birds indicate that avian polyomaviruses form a distinct subgenus within the polyomavirus genus. J Gen Virol 74:229-237, 1993 94. Graham DL, Calnek BW: Papovavirus infection in hand-fed parrots: Virus isolation and pathology. Avian Dis 31:398-410, I985 95. Latimer KS, Niagro FD, Campognoli MS: Diagnosis of concurrent avian polyomavirus and psittacine beak and feather disease virus infections using DNA probes. J Assoc Avian Vet 7:141-146 1993 96. Randall CJ, Lees S, Inglis DM: Papovavirus-like infection in budgerigars (Melopsittacusundulatus). Avian Pathol 16:623-633, 1987 97. Gough, J: Outbreaks of budgerigar fledgling disease in three aviaries in Ontario. Can. Vet J 30:672-674, 1989 98 Mathey WJ, Cho BR: Tremors of nestling budgerigars with BFD. 33rd Western Poultry Disease Conference, University of California, Davis, CA, 1984, p 102 99. Ritchie BW, Niagro FD, Latimer KS, et al: Polyomavirus infections in adult psittacine birds. J Assoc Avian Vet 5:202-206, 1991 100. Pass DA: A papovavirus-like Virus infection of lovebirds (Agapornis sp). Aust VetJ 62:318-319, 1985 101. Pass DA, Prus SE, Riddell C: A papova-like virus infection of splendid parakeets (Neophema splendida). Avian Dis 31:680-684, 1987 102. Mori F, Touchi A, Suwa T, et al: Inclusion bodies containing adenovirus-like particles in the kidneys of psittacine birds. Avian Pathol 18:197-202, 1989 103. Jacobson ER, Gardiner C, Clubb S: Adenovirus-iike infection in white-masked lovebirds (Agapornispersonata). J Assoc Avian Vet 1:32-33, 1989 104. Hirai K, Nonaka H, Fukustii H, et al: Isolation of a papovavirus-like agent from young budgerigars with feather abnormalities. Jap J Vet Sci 46:577-582, 1984 105. Phalen DN, Wilson VG, Graham DL: Organ distribution of avian polyomavirus DNA and virus-
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neutralizing antibody titers in healthy adult budgerigars.Am J Vet Res 54:2040-2046, 1993 Niagro FD, Ritchie BW, Lukert PD, et al: Avian polyomavirus: Discordance between neutrilizing antibody titers and viral shedding in an aviary. Proceedings-of the Association of Avian Veterinarians, Chicago, IL, 1991, pp 22-26 " Lynch J, Swinton J, Pettit J, et al: Isolation and experimental chicken embryo-inoculation studies with budgerigar papaovavirus. Avian Dis 28:1135-1139, 1984 Wainright PO, Lukert PD, Davis RB, et al: Serological evaluation of some psittaciformes for budgerigar fledgling disease virus. Avian Dis 31:673-676, 1987 Gaskin JM: The serodiagnosis of psittacine viral infections. Proceedings of the Association of Avian Veterinarians. Houston, TX, 1988, pp 7-10 Ritchie BW, Niagro FD, Latimer KS, et al: Efficacy of an inactivated avian polyomavirus vaccine. J Assoc Avian Vet 7:187-192, 1993 Jacobson ER, Mladinich CR, Clubb S, et al: Papilloma-like virus infection in an African gray parrot. J Am Vet Med Assoc 183:1307-1308, 1983 O'Banion M, Jacobson E, Sundberg J: Molecular cloning and partial characterization of a parrot papillomavirus. Intervirology 33:91-96, 1992 Lina P, Noord MV, Groot FD: Detection of virus in squamous papillomas of the wild bird species Fringilla coelebs (chaffinch). J Natl Cancer Inst 50:567-571, 1973 Osterhaus ADME, Ellens DJ, Horzinek MC: Identi-
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Viral skin diseases that are commonly observed in avian practice are reviewed. The clinical signs of psitracine circovirus disease, avian pox, and papovavirus diseases are described. Emphasis is placed on the diagnosis and management of these diseases.
Copyright 9 1995 by W.B. Saunders Company Key words: Psittacine beak and feather diseasevirus, pox, polyomavirus, papilloma.
t least four groups of viruses that have the skin as a target organ are recognized in birds. These are psittacine beak and feather disease virus (psittacine circovirus disease virus [PCDV], avipoxviruses, papovaviruses, and herpesviruses. Viral skin diseases can be localized or generalized. Some could be considered as primary skin diseases because epidermal tissue pathology is the major disease feature. Clinicians should be alert to syndromes with an infectious epidemiology because there may be many viruses that have the skin as a target organ. In this review, viral infections that are known causes of skin disease are described.
A
Psittacine Circovirus Disease (PCD) PCD describes probably the most recognisable disease of Psittaciformes. The disease is a major problem of wild psittacine birds in Australia, 1-6 and all psittacine species should be considered susceptible because the disease has been reported in both captive New and Old World psittacine species. 7-11 PCD has distinct pathological features, and the unique virus particles that can be recovered consistently from the cutaneous tissue of affected birds can cause the disease in susceptible birds. 5'12-14 The viral genome is a circular single-stranded DNA molecule, 13'15 and there is no ultrastrucFrom the School of Veterinary Studies, Murdoch University, Western Australia. Address reprint requests to Shane R. Raidal, BVSc, PhD, School of Veterinary Studies, Murdoch University, WesternAustralia, 6150 Australia. Copyright 9 1995 by W.B. Saunders Company 1055-937X/95/0402-000355.00/0 72
tural, protein, or antigenic variation in isolates from different genera of psittacine birds. TM These features place it in the proposed family Circoviridae. Disease syndromes similar to PCD have recently been reported in doves. 17'18
Clinical Signs The clinical signs and pathology of PCD have been thoroughly described.l-5'l~176 In most circumstances, a clinician can accurately diagnose PCD by clinical examination. 1,21,22 Two main clinical presentations exist: chronic and acute. Chronic PCD is insidious in its d e v e l o p m e n t and p r o g r e s s i o n ; dystrophic feathers gradually replace normal ones as they are moulted. Birds older than 10 years can succumb to the disease. 2s In cockatoos, the powder-down feathers (pulviplumes) are often the first feathers affected. PCD-affected pulviplumes may be fragile or develop an abnormally thickened outer sheath that fails to disintegrate. Alternatively, they may cease to develop and thus create bare powder-down patches. 1'24 Arrested production of powder-down causes the plumage to become dull and the beak to become glossy. The pattern of feather dystrophy is related to the stage of moult that the bird is in when the disease first begins and is usually bilaterally symmetrical and slowly progressive. Dystrophic feathers are usually short and have one or more of the following characteristics: fault lines across the vanes; a thickened or retained feather sheath; blood within the calamus; an annular constriction of the calamus; or curling. In Neophema species, apparently normal feathers that fall out or are effortlessly plucked may be the only clinical sign. The first clinical sign in birds with green plumage may be the development of yellow feathers that appear grossly normal in other respects. 24 This is probably the result of pathological changes in feather ultrastructure. On the extremities, PCD-induced hyperkeratosis can cause the skin to appear excessively scaly or it may be thickened and moist. Sun-
Seminars in Avian and Exotic Pet Medicine, Vol 4, No 2 (April), 1995: pp 72-82
Viral Skin Diseases of Birds
light-exposed skin can become darkly pigmented. 2"4 Chronic skin ulcers can occur at the elbows and wing tips, Beak, and less commonly, claw deformities occur in some PCDa f f e c t e d \ b i r d s , and particularly in cockatoos. 3'25 The beak can become abnormally soft and brittle, and the upper and lower tips can become elongated. Transverse or longitudinal fractures or delaminations often O C C U r . 2-4 In severe cases, necrosis of the oral epithelium 1 and osteomyelitis can cause the beak to slough. 3,7 Secondary disease problems commonly exist. 3'26 These include cryptosporidiosis, bacterial, mycotic, or viral infections. 27-29 Most birds with chronic disease eventually have difficulty eating, lose weight, and die.
73
acute PCD cannot be definitively distinguished from psittacine polyomavirus disease by clinical investigation alone. A definitive diagnosis requires the use of PCDV-specific assays. These include electron microscopy, immunohistochemistry, hemagglutination assay, and DNA hybridization. Serology is also useful for detecting PCDVinfected flocks and for demonstrating seroconversion in individual birds. All test results must be interpreted in conjunction with the clinical signs and the age of the bird.
Acute PCD The most severe feather abnormalities occur in nestlings. ~'7'3~ Many diseased contour feathers may be shed, or only the primary flight feathers may be affected. Feather necrosis and accompanying intrapulp hemorrhage are the major clinical findings. Affected feathers fracture from the point of necrosis, usually before the feather has exsheathed. Feather tracts can become acutely inflamed, and the birds often become systemically ill, anorexic, and/or regurgitate food. Death may occur within 1 to 2 weeks of developing clinical signs. At postmortem, thymic and bursal atrophy may be evident.-~'5'~2 Most young birds recover from the acute phase only to become Chronically affected. Acutely affected birds often have mucoid or green diarrhoea.l-~ These signs are often clinically diagnosed as secondary bacterial or chlamydiat infections. 26'~'34 However, PCDV can cause acute hepatitis, and high concentrations of PCDV can be detected in the livers and bile of PCD-affected b i r d s Y Some birds (particularly juvenile gang gang cockatoos) may die o f acute hepatitis without obvious feather lesions.
Tissue Pathology Histological examination of feather follicle or feather biopsies is routinely used to confirm clinical disease. ~'s In one study, it provided an accurate diagnosis for 31 of 32 PCD-affected birds. ~1 However, it is not suitable for diagnosing incubating PCDV infection or for detecting PCDV carriers. 34'~6 Various immunohistochemical techniques have been used to identif~ PCDV antigen in tissue sections, l~176 However, these methods are not routinely used for diagnosis. In the feather follicle, necrosis of the cells of the stratum germinitivum, epidermal hyperplasia, and hyperkeratosis are the major histological lesions. 2'2~ However, the presence in the dermis and epidermis of macrophages containing sometimes relatively large purple intracytoplasmic inclusions is considered characteristic of the disease. 2-5'm'24"~2 Similar lesions can occur in the beak, bursa of Fabricius, thymus, endothelial cells, Kupffer cells, and esophageal epithelial cells. 2'5'10'12'24 Signs of acute or chronic inflammation also may exist. 5'19'2~ In interfollicular skin, ulcers I or hyperkeratosis may be observed. Affected epidermal cell nuclei may be swollen and amphophilic and do not contain easily identifiable virus particles. 7'1z However, individual virions can be detected in affected nuclei by immuno-electron microscopy. 2~
Methods for Diagnosing PCD A thorough history and a clinical examination o f all feather tracts is necessary for a diagnosis of PCD. Few other diseases can be confused with the impressive pathology of chronic PCD. However, injured feather 'follicles can produce feathers that look similar to PCD, and
Direct Electron Microscopy Direct electron microscopic examination of negatively stained feather pulp homogenates is a rapid method for diagnosing PCD.12'32 Fortunately, PCDV particles form aggregates that are readily identified amongst cellular debris. 12,32,~8
74
Shane R. Raidal
Hemagglutination Assay (HA) HA is" currently the only method available for detecting PCDV that is also quantitative. It is aw~uable tool for detecting PCDV particles in feathers, liver, and fecal material. 35'38'~9 Nonspecific reactions have not been recorded with feathers from clinically normal birds. HA can be performed on actively growing feather pulp or dry keratinized feathers. PCDV antiserum is required to validate HA reactions particularly because nonspecific HA reactors sometimes occur in fecal specimens. Feather testing is preferred over fecal testing because acutely PCD-affected birds do not excrete high concentrations of virus in feces, and some chronically affected birds excrete intermittently. ~8
Polymerase Chain Reaction (PCR) and DNA Dot-Blot Assays PCR and DNA-probe assays have been used for the detection of PCDV genome in chilled blood samplesY '4~ This is probably the best m e t h o d for detecting latent or incubating PCDV infection. It does not detect PCDV particles or antigen. Retesting is recommended after 90 days if a test is positive, but clinical signs are absent. 41'42 A positive PCR product is not a demonstration of active infection because nonreplicating viral DNA may take up to 3 months to clear from the blood stream. 4~ Like other diagnostic assays, false-positive results probably occur and false-negative results do occur. 41 PCR detection systems are rapid and can theoretically be designed to detect individual viral genomes, making them the most sensitive assays available. Extreme care must be taken in the field and in the laboratory to avoid contamination of samples. PCR tests should be used together with, and not replace, conventional diagnostic regimes. The sensitivities of some PCR assays may have the same order of magnitude as conventional methods 44 or they may be significantly less sensitive. 45
Serology Hemagglutination inhibition (HI) tests have been described for PCDV serologyP s'39 The presence of antibody means that the bird has been exposed to PCDV, and a high HI titer in an adult bird is a good indicator that it does not
have chronic PCD. ~8 Nestlings with incubating PCDV infection or acute disease may have low and declining serum HI titers. 14 An agar gel diffusion test has been used to detect precipitating antibody in vaccinated birds. ~1 However, the assay had a lower sensitivity than HI and failed to detect antibody in vaccinated chicks. Detection of precipitating antibody in PCD-affected birds has not been reported.
Pathogenesis The incubation period of PCD can be as short as 21 days, 5'12'14'31 but it is probably dependent on the dose of virus, the age of the bird, the stage of feather development, and the absence of immunity. Primary virus replication probably occurs in the bursa of Fabricius and/ or gastrointestinal tract lymphoid tissue. Secondary virus replication occurs in the liver and thymus and probably other tissues. The target organ is the epidermis, and the manifestation of skin disease requires a moult. Consequently, birds that become infected after feather development has completed may not develop clinical signs until their next moult. This could take 6 or more months. Most birds that succumb to PCD are less than 2 years of age. The disease is difficult to reproduce in adult birds. However, all age groups should be considered susceptible to PCDV infection. 2~ Perhapschronic exposure to high concentrations of PCDV and/or stress is required for infection and seroconversion in adult birds.
Prognosis Early reports of spontaneous recovery from PCDV probably concerned birds infected with polyomavirus. These cases may have been misdiagnosed histologically owing to lack of knowledge at that time regarding intracytoplasmic versus intranuclear inclusions. It is now known that complete or partial recovery from acute PCD (confirmed by HA testing and histology) can occur in some species and may or may not be associated with seroconversion. This occurs more frequently with Budgerigars (Melopsittacus undulatus), Rainbow Lorikeets (Trichoglossus haematodus), lovebirds (Agapornis species),33 and Eclectus Parrots (Eclectus roratus). The majority of psittacine species with chronic
Viral Skin Diseases of Birds
PCDV do not recover from the disease and do not respond to treatment with antibiotics, vitamins, glucocorticoids, and autogenous vaccines.
Epidemiology In Australia, PCD has been confirmed in wild Galahs (Eolophus roseicapillus), Rainbow Lorikeets, Orange-bellied Parrots (Neophema chrysogaster), Crimson Rosellas (Platycercus elegans) Eastern Rosellas (Platycercus eximius), Mallee Ringneck Parrots (Barnardius barnardi), Port Lincoln Parrots (Barnardius zonarius), Major Mitchell's Cockatoos (Cacatua leadbeateri), Gang Gang Cockatoos (Callocephalon fimbriarum), King Parrots (Alisterus scapularis) and Swift Parrotsb(Lathamus discolor). Anecdotal evidence indicates that it occurs in wild Budgerigars, Red-rumped Parrots (Psephotus haematonotus), and Yellow-tailed Black Cockatoos
(Calyptorhynchusfunereus funereus). 1-6,33 PCD has been reported in aviary flocks of
Agapornis species in Zimbabwe. 46-4s However, there is no evidence to support its occurrence in wild African birds (Dr N. Kock, personal communication, September 1993). International trafficking of psittacine birds for aviculture has probably been responsible for the occurrence of PCD in most countries where psittacine birds are kept. The disease presumably also occurs in wild Asian cockatoos because wild-caught fledglings exported from this area have developed the disease. 7 Flocks of wild cockatoos may have a disease prevalence of 20% and a seroprevalence of 60% to 80%. 4,6 Infection is probably maintained in a population by diseased birds. Virus transmission is probably predominantly by horizontal spread, but carrier birds may contribute by vertical transmission. Virus infectively probably persists in contaminated nest sites for many months or years, and this could result in cross-species transmission. Aviary flocks with a history of PCD usually hav~ a high Seroprevalence. 40 In these situations, PCD-affected birds are often the progeny of hens with low or nondetectable serum antibody levels.
Prevention and Control Aviculturists should be advised to maintain a closed flock or purchase birds from PCD-free
75
flocks and to breed birds in quarantine. The appropriate use of disinfectants that are suitable for inactivating environmentally resistant viruses should be recommended for disinfecting contaminated utensils, cages, and rooms. 5~ Experimental inactivated PCD vaccines have been prepared by conventional methods. 14'31'49 Vaccination of breeding hens enhances passive transfer o f immunity, 31'40 which may interfere with vaccination of progeny. Vaccination of young birds may not prevent transient viral replication and excretion or persistent infection.a4
Avian Pox Avipoxviruses cause skin disease (pox) in m a n y species o f d o m e s t i c a t e d a n d wild birds. 52-56 Pox does not occur naturally in domestic ducks, but they are susceptible to inoculation with turkey poxvirus. 57 In psittacine birds, pox has been reported in Black-Masked Conures, 58 a Red-Winged Parrot, 54 a Military Macaw (Ara militaris mexicana)59 and Amazon P a r r o t s . 6~ A nonpathogenic budgerigar poxvirus also has been reported. 52 Avipoxviruses are epitheliotropic and typically cause localized tumors in the nonfeathered areas of skin. Internal diphtheritic and/or systemic syndromes also occur in some species. In diphtheritic pox, the oral and respiratory mucus m e m b r a n e s are p r e d o m i n a n t l y affected. 59'62 Canary poxvirus, possibly the most virulent of the avipoxviruses, can cause up to 100% mortalities in susceptible canary f l o c k s . 63-65
Avipoxviruses are designated according to their host as, for example, fowl poxvirus, canary poxvirus, and mynah poxvirus. The antigenic relationships between avipoxviruses are complicated. 52'62'66 In a heterologous host species, avipoxviruses may not replicate or they may replicate and be either nonpathogenic or pathogenic. Avipoxviruses that replicate in a heterologous host species may or may not induce immunity to other avipoxviruses that are pathogenic to that host. Quail poxvirus causes severe disease in chickens but when administered as a vaccine does not protect chickens from challenge with either fowl, pigeon, or mynah poxviruses.
76
Shane R. Raidal
Also, chickens vaccinated with the latter three viruses are not protected from quail poxvirus challenge. Similarly mynah poxvirus is pathogenic for chickens but is antigenically distinct from~owl and pigeon poxviruses. 67 Psittacine poxviruses are antigenlcally distinct from quail, fowl, and pigeon poxviruses. 62'66
Clinical History Cutaneous pox is characterized by the proliferation of nodular or crusty lesions on the nonfeathered areas of skin. Lesions may occur on the beak, feet, and claws and begin as white or yellow foci that rapidly increase in size. Depending on the stage of infection, they may appear as vesicles, papules, pustules, or crusty scabs. Secondary bacterial or fungal infections can complicate the diagnosis and progression of lesions. Tumors on the eyelids; conjunctival proliferation, or blepharitis can impair vision 56'61 In lovebirds, pox may present as a dark or discolored area of skin. 52 Diphtheritic lesions may occur in conjunction or in the absence of cutaneous lesions. Caseous plaques may be observed in the mouth, pharynx, trachea, sinuses, or larynx. Canary pox may present as a sudden onset of dyspnea or sudden death. Upper respiratory tract disease, pneumonia, airsacculitis, and splenomegaly may be evident.
Diagnosis Diseases that resemble avian pox include fungal or bacterial granulomas, abscesses, parasitic cysts, or neoplasia. A presumptive clinical diagnosis of pox can be confirmed by histological examination and virus isolation. Avipoxviruses may be demonstrated by electron microscopy and are readily isolated on the chorioallantoic m e m b r a n e of embryonated chicken eggs. Various serological assays have been described for detecting antibodies to poxviruses. However, serology is rarely used or necessary for making a diagnosis.
tological sections and Borrel bodies in impression smears). The epithelium of the upper and lower respiratory tract, oral cavity, and oesophagus may be affected. 6~ Inclusions can be identified by immunoperoxidase staining. 6s
Epidemiology Avian pox is a relatively slow-spreading disease that can affect birds of all ages. Transmission is predominantly by blood-sucking insects such as mosquitoes, mites, and biting flies. 69-71 There is no replication in these vectors, but virus may remain infectious in insects for 10 months. 72,73 Infection can be initiated in traumatized epithelial tissue by indirect transmission from contaminated feed and water utensils. Direct transmission between birds can occur after the ingestion of scabs or inhalation of aerosols. The incubation period is 7 to 14 days. Recovered birds probably develop strong lifelong immunity and do not develop into virus carriers. 57
Treatment It is imperative to control mosquitoes and ectoparasites in an epidemic situation. Individual treatment is aimed at supporting the bird until it recovers. Lesions usually heal within 4 weeks, but this can be enhanced by physically removing nodules as they develop. Surgery may be necessary to remove large tumors from the face. Nonirritant detergents or shampoos, diluted with saline, are suitable for softening and removing nodular lesions from around the eye. Bleeding can be controlled by thermal or chemical cautery. Vitamin supplementation, immunostimulant, or anti-inflammatory drugs may be appropriate treatment for individual birds. Treatment with sodium salicylate or acetylsalicylic acid delayed and reduced the development of skin lesions of fowls with experimentally i n d u c e d pox. TM Antimicrobial therapies are important for the control of secondary bacterial and fungal infections.
Pathology Histologically, pox is c h a r a c t e r i z e d by marked epithelial hyperplasia and vacuolar degeneration of epithelial cells associated with the formation of eosinophilic ihtracytoplasmic inclusion bodies (called Bollinger bodies in his-
Prevention Virulent or attenuated vaccines are conventionally administered at an aberrant site, usually by wing stab or directly to a freshly plucked c o n t o u r f e a t h e r follicle over the
Viral Skin Diseases of Birds
thigh. 57'75'76 Only healthy birds should be vaccinated. Some birds may develop severe lesions at the site of vaccination. Horizontal transmission virus can occur under favourable conditions 76 but may not be reliable. Consequently, birds vaccinated with virulent strains are infectious for up to 8 weeks and should be isolated from susceptible birds. All healthy birds in a flock should be vaccinated. Maternal antibody does not confer effective passive immunity.57 A single vaccination should induce lifelong immunity, but annual boosters may be necessary on a flock basis. 57 A single vaccination should induce lifelong immunity, but annual boosters may be necessary on a flock basis. 57 In some situations, primary vaccination by drinking water medication 77'7s or intranasal or aerosol inoculation 7~ may be appropriate.
Papovavirus Infections The Papovaviridae are subdivided into two genera, the papillomaviruses and the polymaviruses. Paplllomavlruses are common causes of benign nodular epidermal tumors in mammals and have been demonstrated within similar tumors in many bird species. Avian polyomaviruses (APV) cause pansystemic disease in finches 81'82 and psittacine birds but have been reported as causes of skin disease only in the latter. 9
80
-
"
Polyomavirus Infection of Psittaciformes APV were first reported as a cause of skin disease and mortality in juvenile budgerigars. s3-s7 Much is known about budgerigar polyomavirus, and consequently it is considered the prototype polyomavirus, ss Its entire genome has been sequenced, s~ APV from different host species appear morphologically, antigenically,~176176 and genetically similar. ~ Like PCD, APV are probably capable of causing disease in all psittacine species. However, nestling and juvenile birds are most susceptible. 01'~ Most birds that recover from the acute phase of APV disease make a complete clinical recovery9 Chronic progressive skin disease is not a feature of APV infection. However, persistent virus infection and excretion are common sequelae. Concurrent APV and PCDV infection can occur. ~
77
Clinical history. In budgerigars, polyomavirus infection causes severe clinical signs in susceptible nestlings less than 15 days of age. ~ Affected nestlings may be ataxic or have head tremors. ~ There may be abdominal distension caused by hepatomegaly and ascites, subcutaneous petechiae or ecchymosis, or a generalized pallor. The mortality rate in this age group can be 100%. Death usually occurs within 48 hours of the development of clinical signs. Gross necropsy lesions may be absent. The crop is often distended with food. A severe drop in hatchability also has been reported. 97 Older budgerigar nestlings may fail t o develop normal contour feathers, and affected contour feathers may lack normal barbs9 The rectrices and secondary remiges may fail to develop. There may be a lack of down feathers on the back and abdomen and lack of contour feathers on the head and neck. s~'s7 At necropsy, there may be cardiomegaly, hydropercardium, and hepatomegaly or focal hepatic necrosis. In other species, APV can cause nonspecific signs of illness including anorexia crop stasis, depression, paresis, and ataxia. ~176 Sporadic sudden deaths may occur in juvenile or adult birds with or without the presence of feather abnormalities.~176176176 Methods for diagnosing APV infection. A presumptive diagnosis of APV infection can be made from the history and clinical and pathological features9 However, histopathological, bacteriological, and serological investigations should be used to rule out differential diagnoses9 Tests that are sensitive and APVspecific are required for making a definitive diagnosis. Histopathology. APV infections cause necrosis and marked basophilic karyomegaly in many tissues, in particular, the feather follicles, kidney, and liver. 86'06'1~176 Relatively large, amorphous, basophilic intranuclear inclusions can be found in persistently infected kidneys, but they cannot be differentiated morphologically from other viral infections. 1~176 A definitive diagnosis requires the use of electron microscopy or APV-specific c y t o c h e m i c a l staining. APV antigen has been detected in tissue sections by immunoperoxidase staining, ~176 and APV DNA has been demonstrated by in situ DNA hybridization.~
78
Shane R. Raidal
Virus isolation. Psittacine polyomavirus can be cultured in vitro i n budgerigar embryo fibroblast, 1~ chicken embryo fibroblast s4 or chicken embryo kidney cell culturesY Virus isolatibn is generally not available for routine diagnosis. Polyomavirus genome detection. PCR amplification and DNA-probe assays have been described. 4~176176176 PCR and DNA-probe testing for APV is highly sensitive and specific and can be performed on serum or any tissue or secretion. However, cloacal swabs are preferred, and these are probably the least stressful to collect. These qualities in a diagnostic assay are desirable for flock monitoring. A positive DNA-probe test means that APV DNA was detected in the sample. This is an important finding on a flock basis but should be interpreted with circumspection for an individual pet bird. Serology. Antibodies to APV have been detected by immunodiffusion, 1~ virus neutralisation (VN) assay, m'l~ and indirect immunofluorescence. 1~176 Serology is Probably more sensitive than cloacal DNA probe for detecting polyomavirus infection on a flock basis. ~176176 Epidemiology. APV is excreted in feather dander and droppings, and horizontal transmission is the major method of infection in an epidemic, but vertical transmission also may occur. 83'87'01'07 Infection persists in the kidneys of carrier birds, and virus is excreted intermittently during times of stress. APV are thermostable, can withstand freeze thawing, and remain infective in contaminated environments. 84 Aviary flocks with endemic APV infection may have a seroprevalence up to 100%. 91'1~ APV carriers may be seropositive or seronegative,l~ and their serological status can change over time. Up to 100% of birds in a flock may be persistently APV-infected) ~ Prevention and control. Aviculturists with a disease-free situation, should be encouraged to maintain a closed flock with strict hygiene and quarantine procedures. This includes eliminating exposure to free-flying wild birds and regulating all food, utensils and humans with access to the birds. APV probably remain infectious u n d e r the fingernails of well-meaning visitors for long periods. New ~tock should be obtained from certified seronegative and APV-
free aviary flocks. They must be held in quarantine and confirmed as APV free, preferably both by serology and DNA-probe before being incorporated into the breeding flock. In an endemic situation, an effort should be made to eradicate horizontal transmission between birds and between batches of young birds. Accurate record keeping and regular disease monitoring are most important. It may be desirable to identify APV carriers and isolate these birds in a separate facility. Incubators and brooders must be thoroughly cleaned and disinfected between clutches. Chlorine, 97 synthetic phenol, stabilized chlorine dioxide, sodium hypochlorite, and 70% ethanol have been effective in reducing the infectivity of APV. 51 Air filtration systems that extract aerosolized virus should be used. Macaw chicks that received an experimental inactivated APV vaccine developed relatively low VN titers (1:20 to t :40). 11~ Challenge virus did not cause immunological stimulation because an increase in antibody titer and APV excretion was not detected. In contrast, viral replication probably occurred in unvaccinated birds because they seroconverted (VN titers of 1:640) and excreted APV. Vaccination was not shown to prevent disease because unvaccinated birds remained clinically normal.
Papillomavirus Skin Disease Papillomaviruses have been detected in epidermal tumors in African Grey Parrots, 111,112 chaffinches, 113-115 canaries, 116 and greenfinches. 117 The main histological finding is epidermal hyperplasia and dysplasia. 116 Affected keratinocytes may be polyhedral with an amorphous, pale, or eosinophilic cytoplasm. There may be margination of nuclear chromatin, or nuclei may be vacuolated or contain a basophilic inclusion. A tentative diagnosis of papillomavirus disease can be made by clinical signs and histopathology. However, immunohistochemical techniques and/or electron microscopy are required to demonstrate papillomavirus particles or antigen in lesions. 111,116-1lS
Herpesvirus Infections In chickens, complete replication of Marek's disease virus (MDV) occurs only in feather follicle epidermal cells, la9 Histologically, intranu-
Viral Skin Diseases of Birds
clear inclusions can be found in epidermal cells. There may also be focal infiltrations of neoplastically transformed lymphocytes in the dermis adjacent to infected feather follicles. HerpesvaXr-us infections similar to MDV have not been reported in companion birds. However, herpesviruslike particles have been described in tumors on the feet of c o c k a t o o s 52'12~ and a wild mallard duck. 121 Herpesviruses may be responsible for at least some of the internal papilloma syndromes that occur in psittacine birds. 122-12s
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References 1. Perry RA: Psittacine beak and feather disease, in Hungerford T G (ed): Proceedings 55: Courses for Veterinarians. Aviary and Caged Birds. Sydney, Australia, T h e Postgraduate Committee in Veterinary Science, 1981, pp 81-108 2. Pass DA, Perry RA: The pathology of psittacine beak and feather disease. Aust Vet J 61:69-74, 1984 3. Pass DA, Perry RA: Psittacine beak and feather disease: An update. Aust Vet Pract 15:55-59, 1985 4. McOrist S, Black DG, Pass DA, et ah Beak and Feather Dystrophy in wild sulphur-crested cockatoos (Cacatua galerita). J Wildl Dis 20:120-124, 1984 5. Wylie SL, Pass DA: Experimental reproduction of psittacine beak and feather disease/French moult. Avian Pathol 16:269-281, 1987 6. Raidal SR, McElnea, CL, Cross GM: Seroprevalence of psittacine beak and feather disease in wild psittacine birds in New South Wales. Aust Vet J 70:137139, 1993 7. Jacobsen ER, Clubbs, Simpson C, et ah Feather and beak dystrophy and necrosis in cockatoos: Clinicopathologic evaluations. J Am Vet Med Assoc 189: 999-1005, 1986 8. Huff DG, Schmidt RE, Fudge AM: Psittacine beak and feather syndrome in a blue-fronted Amazon (Amazona aestiva). J Assoc Avian Vet 2:84-86, 1988 9. Allen, SK: Psittacine beak and feather disease in an african grey parrot. J Assoc Avian Vet 4:18-19, 1990 10. Latimer KS, Rakich PM, Kircher IM, et ah Extracutaneous viral inclusions in psittacine beak and feather disease. J Vet Diagn Invest 2:204, 1990 11. Greenacre CB, Latimer KS, Niagr6 FD, et ah Psittacine beak and feather disease in a scarlet macaw (Ara macao). J Assoc Avian Vet 6:95-98, 1992 12.. Wylie, SL: Studies on psittacine beak and feather disease. Doctorate thesis, Murdoch University, Perth, Western AustraLia, 1991 13. Ritchie BW, Niagro FD, Lukert PD, et ah Characterization of a new virus from cockatoos with psittacine beak and feather disease. Virology 171:83-88, 1989 14. Raidal SR, Firth GA, Cross GM: Vaccination and challenge studies with psittacine beak and feather disease virus. Aust Vet J 70:437-441, 1993 15. T o d d D, Niagro FD, Ritchie BW, et ah Comparison
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Viral Skin Diseases of Birds
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