Old World Aviaries

PROCEEDINGS - ASSOCIATION OF AVIAN VETERINARIANS (1997, 1998)

Vaccination to control polyomavirus in budgerigars


Branson W. Ritchie, DVM, PhD, Kenneth S. Latimer, DVM, PhD,
Denise Pesti, MS, Raymond Campagnoli, MS, Phil D. Lukert, DVM, PhD
Psittacine Disease Research Group
University of Georgia, College of Veterinary Medicine
Athens, GA 30602

Reprinted in part from Avian Viruses: Function and Control Wingers Publishing, Lake Worth, FL, 1995.


Budgerigar fledgling disease (BFD), caused by an avian polyomavirus, was first noted as a clinical syndrome in 1976 and was first reported as a disease affecting budgerigars in the United States and Canada in 1981.1 Since its initial recognition as an etiologic agent of disease in psittacine birds, polyomavirus has spread throughout aviaries and the pet trade to a point where it is a leading cause of death in psittacine birds. 2 While avian polyomavirus has been shown to be distributed world-wide, there are some apparent regional differences in the clinical changes associated with infections in budgerigars. 3-7 1,8 9,10 11 12,13 14-16 For example, in Europe a more chronic form of the disease is common in budgerigars, while in the United States and Canada an acute form of disease with high mortality is typical.

Unlike most members of the Papovaviridae family which have a restricted host range, avian polyomaviruses appear to infect a wide variety of Psittaciformes (parrots), Passeriformes (weaver finches, canaries) and gallinaceous birds (chickens and turkeys). 17 Polyomaviruses from budgerigars have been confirmed to be antigenically related to some virus isolates from finches and antigenically and genomically related to the polyomavirus isolated from non budgerigar psittacine birds. 4,18-21 DNA probes have been developed to detect specific segments of the nucleic acid found in the avian polyomavirus. These DNA probes, designed from polyomavirus recovered from budgerigars, will detect the virus in excretions, secretions and infected tissues of non budgerigar psittacine birds. 6,22,23 The genome of the polyomaviruses isolated from budgerigars, a blue and gold macaw and a chicken house have been shown to be closely related. Because of these similarities, it has been suggested that avian strains of polyomavirus be placed in the subgenus Avipolyomaviurs. 13

The type of clinical disease induced by polyomavirus in budgerigars seems to be influenced by the age and condition of a budgerigar when it is exposed to the virus. Budgerigar neonates from infected flocks may develop normally for 10 to 15 days and then die suddenly without premonitory signs. 24 Other infected hatchings may develop clinical signs, including abdominal distention, hemorrhage under the skin and reduced formation of down and contour feathers. Some infected budgerigars have been reported to develop neurologic signs characterized by ataxia (incoordination) and tremors of the head and neck several days before dying. 1,9,24-27 Infected budgerigars that die shortly after hatching routinely develop more severe and widespread lesions than do birds in which the morbid state is more prolonged. The mortality rate associated with naturally acquired avian polyomavirus infections in young budgerigars may range from 25% to 100%, depending on the age of the birds. Older birds are considered relatively resistant to disease, while at the peak of viral activity, up to 100% of exposed budgerigars less than 15 days of age may die. The mortality rate reported for older (greater than 3 weeks of age) juveniles ranges from 30% to 80%.I,8,9,24-29

Although mortality rates vary with the age of the exposed birds, polyomavirus infections in young budgerigars usually are rapidly fatal once clinical signs develop. In most aviary outbreaks, the incidence of clinically recognized disease will progressively increase during a period of several months, with peak virus activity occurring during the most active portion of the breeding season. 25 In one particularly aggressive outbreak of avian polyomavirus, 90% of young budgerigars were affected within a 2-to 3-week period.8

Reports vary on the effect of avian polyomavirus on egg and embryonic development. In one budgerigar aviary, polyomavirus was thought to have caused an 80% to 90% decrease in egg hatchability at the same time that hatchling mortality increased from 10% to 60%.8 In another study, there was no apparent increase in embryonic mortality in eggs from budgerigar hens that were considered persistently infected with avian polyomavirus. Additionally, many of the chicks from these hens were found to be infected, but remained asymptomatic. 30 Findings from the first report would suggest that avian polyomavirus can cause embryonic deaths and decreased hatchability, while findings from the second study would suggest that avian polyomavirus infections do not cause problems in embryonic development. It is possible that both findings are correct and the effect of the virus may depend on as yet unidentified factors. Like mammals, budgerigars that recover from polyomavirus infections are thought to remain persistently infected.30-32 Evidence suggests that these persistently infected budgerigars are responsible for the spread of this virus through budgerigar flocks and within the avicultural industry.

1,21,31,14 Stress associated with changes in weather, diet, breeding or concomitant disease may cause persistently infected budgerigars to shed virus resulting in outbreaks of disease. In polyomavirus outbreaks at 23 different budgerigar aviaries, the onset of disease could be traced to the addition of new, clinically normal breeders. 1,25

Polyomavirus inclusion bodies frequently can be detected in feathers, feather follicles, spleen, liver and Kidney from persistently infected, clinically normal adult budgerigars. 25,26 Viral inclusion bodies are common in the renal tubular epithelium. Persistence of virus in the kidneys of budgerigars, with subsequent excretion in the urine, has been proposed as a method of virus transmission. 1,26,29,33,35 Viral nucleic acid has been detected in the excrement, feathers and oral mucosa of clinically normal budgerigars. 36

The incidence of polyomavirus activity in budgerigars is high. In one study, virus was demonstrated by histology and virus isolation from all of 10 budgerigars with clinical signs of avian polyomavirus and from 5 of 10 (50%) clinically healthy budgerigars. 26 In another study, 4 of 7 (57%) nestling budgerigars had microscopic changes suggestive of avian polyomavirus, while all of 7 nestlings had viral nucleic acid in their tissues. 30 Polyomavirus nucleic acid was demonstrated in the serum of 9 of 12 (75%) 9-to 13-day-old budgerigars from a flock in which virus activity was considered enzootic. 34 The possibility that up to, 100% of the budgerigars in some flocks could be infected with avian polyomavirus was first discussed in 1984.25 This has been confirmed in subsequent studies using viral-specific DNA probes. In one study involving a flock of budgerigars with a history of repeated polyomavirus-induced disease, all of 40 clinically normal budgerigars had polyomavirus nucleic acid in their tissues. Virus-neutralizing antibodies to avian polyomavirus were detected in all 144 of another group of budgerigars. 30 Experimental data and observations with the natural disease suggest that polyomavirus transmission in budgerigars may occur by both horizontal and vertical routes, that is, both among members of a flock and between generations from parent to offspring. 1,5,27,28,30 Experimentally infected 3-to 10-day-old budgerigar neonates died 11 days after being given BFD virus intramuscularly. 37 When 25-day-old budgerigars were exposed intranasally to virus collected from the skin of diseased birds, they developed microscopic lesions characteristic of a polyomavirus infection but remained clinically normal. 1,25 These findings suggest that inhalation of aerosolized virus could be a natural route through which polyomavirus enters a susceptible bird. In one trial, young seronegative budgerigars seroconverted within 16 days after being placed in the same enclosure with seropositive birds.

Seronegative budgerigars also seroconverted when they were placed in enclosures adjacent to those containing seropositive birds. These finding suggest that direct and indirect transmission of polyomavirus can occur. 27

Unvaccinated susceptible psittacine birds may be exposed to polyomavirus through exposure to virus-contaminated feces, feather dust, urates and respiratory secretions. 17,25 Until polyomavirus can be controlled in budgerigars through a widespread vaccination program, it should be considered dangerous to house budgerigars in the same air space with unvaccinated non budgerigar psittacine birds. The potential for intraspecies transmission of polyomavirus may be a particular problem for pet retailers that maintain both budgerigars and non budgerigar psittacine birds. In one environmental study, it was found that polyomavirus nucleic acid could be detected using DNA amplification and detection techniques in all of 5 samples collected from 3 different pet shops which housed budgerigars. (Dr. Nancy Jaax, personal communication) Budgerigars should be considered the primary reservoir of polyomavirus. 'The potential for budgerigars to continue to spread this environmentally stable virus among unvaccinated psittacine birds is cause for action.

Controlling Polyomavirus in Budgerigars

It has been suggested that polyomavirus disease-free budgerigar nestlings can be produced by interrupting the breeding cycle, removing all but the older breeding birds and disinfecting the aviary. 8 Breeding cycle manipulation was used to control polyomavirus infections in budgerigars, after hatchability of fertile eggs dropped from 80% to 90% at the same time that hatching mortality increased from 10% to 60% in an aviary experiencing an avian polyomavirus outbreak. By interrupting the breeding cycle for 7 months and thoroughly cleaning the aviary with bleach, return to 80% hatchability and a cessation of hatching deaths was achieved when breeding resumed. However, in other affected aviaries, mortalities and disease have continued when breeding was resumed following a rest period. 8 In another study, it was demonstrated that older breeding budgerigars shed fewer virus particles and less frequently than young adults. 30,32 Any attempt to manage polyomavirus through manipulation of the breeding cycle has the inherent problem that persistently infected budgerigars, and thus a future source for virus shedding, remain in the flock.

In budgerigars, which are known to develop persistent polyomavirus infections, the detection of polyomavirus-neutralizing antibodies can be used to screen for infected budgerigars which should be considered a risk for transmitting the virus. 34,38 Testing budgerigars for the presence of virus-neutralizing antibodies and culling positive birds has been suggested as a method to establish flocks of polyomavirus-free budgerigars. 33,36 Additionally, depopulation of budgerigar aviaries experiencing outbreaks, followed by restocking with seronegative birds has been suggested as a method of controlling enzootic infections in this species. 8,33,36 The practical problem with using this testing strategy for controlling polyomavirus is that once a seronegative flock of budgerigars has been established, the flock would then be highly susceptible (theoretically 100% susceptible) to polyomavirus infection if the virus were inadvertently introduced to the aviary. However, by using a serologic assay to establish "polyomavirus-free" budgerigars followed by vaccination to protect the budgerigars from subsequent infection, it should be possible to prevent polyomavirus-induced disease in the budgerigar aviary and reduce the role that budgerigars play as a reservoir for polyomavirus in the pet trade.

In non budgerigar psittacine birds, polyomavirus can be controlled using an inactivated avian polyomavirus vaccine. 3944 Controlling polyomavirus infections in budgerigars presents a different set of problems. A budgerigar infected with polyomavirus is considered to be infected for life and can shed the virus for long periods of time. This high prevalence of polyomavirus in budgerigars, and the fact that an infected budgerigar continues to shed for extended periods, renders vaccination alone of questionable value in controlling the virus in a budgerigar flock. Additionally, the cost of the inactivated vaccine makes it difficult to economically justify in commercial budgerigar flocks. None-the-less, it is important for the avicultural industry to control polyomavirus in budgerigars because this group of birds is serving as a reservoir for the virus. For the past year, we have been evaluating an economically feasible testing and vaccination program to control polyomavirus in budgerigars. We are currently testing this program in flocks of budgerigars and our data is encouraging.

This vaccine* was developed by identifying a virus isolate which, when administered intramuscularly, will cause an immune response without inducing virus shedding or detectable persistence of the virus. In one safety and immunogenicity trial, 4 recently weaned budgerigars with no detectable polyomavirus-neutralizing antibodies were injected intramuscularly with the experimental vaccine. Another budgerigar that was housed in the same enclosure with these vaccinates served as a contact control. None of the vaccinates had any clinically recognizable adverse reactions following vaccination.

The experimental vaccine designed for use in budgerigars was found to stimulate an immune response in birds inoculated intramuscularly but not in birds inoculated by the combined intraoral, intranasal and intraocular routes. A group of 5 recently weaned budgerigars that were negative for polyomavirus-neutralizing antibodies was used in this safety and immunogenicity trial. Two birds (#6 and #7) were inoculated by the combined intraoral, intranasal and intraocular routes with experimental vaccine. Three birds (#8, #9 and #10) were injected with the same suspension intramuscularly. Serum was collected from each bird on day 0, 10 and 20. None of the vaccinates had any clinically recognizable adverse reactions.

The results of this study indicated that the experimental budgerigar polyomavirus vaccine induced a detectable virus-neutralizing antibody response when injected intramuscularly (considered an unnatural route of exposure) but not in the birds inoculated by the combined intraoral, intranasal and intraocular routes (considered a natural route of exposure). This finding suggests that the polyomavirus contained in the experimental vaccine has been sufficiently altered to prevent it from inducing an infection when a bird is exposed by a natural route. In an additional safety and immunogenicity trail, 7 mature budgerigars were inoculated intramuscularly with the experimental budgerigar polyomavirus vaccine. Two birds were housed in the same enclosure with the vaccinates and served as contact controls. Serum was tested for virus-neutralizing antibodies on day 0 (which was also the day of vaccination) and approximately 1 month later. None of the vaccinates had any clinically recognizable adverse reactions.

These safety and immunogenicity trials suggest that the experimental budgerigar vaccine will induce an immune response, as detected by a significant increase in virus-neutralizing antibodies, when injected intramuscularly and that vaccinates do not shed a sufficient quantity of viable virus to be a risk for infecting birds with which they are in direct contact. It is anticipated that the ongoing studies which are necessary to obtain USDA registration of this vaccine will further confirm its safety and immunogenicity in budgerigars.

Acknowledgments

Major sustained contributions that have made this work possible have been provided by the Cowan Avian Health Foundation, the International Avian Research Foundation, Veterinary Medical Experiment Station, Dr. Joe and Sue Still, Terry Clyne, Dr. Richard and Luanne Porter, Knick Enterprises, Bobbi Brinker, Kathleen Szabo, International Aviculturist's Society, Avian Research Associates, Midwest Avian Research Exposition, National Aviary, American Budgerigar Society, Ann Arbor Cage Bird Club, Aviary and Cage Bird Club of South Florida, Avicultural Society of Puget Sound, Central Indiana Cage Bird Club, Charlotte Metrolina Cage Bird Society, Crearn City Feathered Friends, Dallas Cage Bird Society, Feathered Friends Society, Gateway Parrot Club, Georgia Cage Bird Society, Greater Brandon Avian Society, Hookbill Hobbyists of Southern California, Kentuckiana Bird Society, Kenosha Exotic Bird Club, Louisiana Aviculture Society, Northwest Ohio Exotic Bird Club, South Jersey Bird Club, Wasatch Avian Education Society, West Valley Bird Society and Zeigler Brothers Inc. Hundreds of aviculturists, bird clubs and veterinarians have also made significant contributions. A special thanks to Dr. Dick and Richard Davis for providing the polyomavirus negative budgerigars.

References


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