Psittacine Beak And Feather or Psittacine Circoviral Disease: An Overview
Jeannine Miesle, M.A., M.Ed
Psittacine Circoviral Disease – previously known as Psittacine Beak And Feather Disease (PBFD) – is caused by a circovirus, is a fatal disease for which there is no treatment or cure. It presents as an immune-suppressive, feather-dystrophic illness which may also affect the beak and nails. Although not currently a serious problem in the United States, Canada, and Europe, it proliferates in Australia and the Asian countries. It is quite virulent, replicates quickly, and transmits easily from one bird to another. It is also thought to be passed vertically from hen to egg. It appears as an acute, peracute, or chronic course. Molecular diagnostic testing has made diagnosis accurate and reliable. Supportive care and treatment of concurrent illnesses may allow some birds to have a somewhat normal quality of life for an extended time before succumbing.
Psittacine Circoviral Disease is a fatal viral disease affecting all species of parrots and many other bird species. Caused by a circovirus, it is one of the most serious and contagious diseases affecting aviculture today. During the 1970’s and 1980’s, when the bird importation trade was at its peak, PBFD was widespread, and it took the lives of many birds: those who were already infected; those who became infected during quarantine and shipment; and those in pet shops, aviaries, and homes. Today, due to the natural deaths of the infected birds over the years and more care having been taken by breeders to test their flocks and to discontinue breeding the affected birds, PBFD is not seen as frequently in the U.S., Europe, and Canada as it was in the past. The positive test rate incidence in birds has shown little change in these countries since the 1990’s. Nonetheless, it is still very active in other countries, particularly in Australia, where it is rampant in the native population, and in Asia, where uncontrolled breeding has led to the widespread dissemination of the disease. Due to their inability to fly, the terms “runners” or “hikers” are used to describe their poor mobility.
Figure 1: A lovebird with PBFD. Note the feather dystrophy, elongated beak, and color changes. (Image courtesy R. Dahlhausen.)
1. Vulnerable Species
PBFD has been documented in a wide range of avian species in Australia, North America, Europe and Asia. More than 40 species of captive and free-ranging Old World psittacine birds, as well as several species of New World psittacines, have been diagnosed with the disease. Circovirus genotypes (subgroups) related to the PBFD virus have been reported in pigeons, 2 Senegal doves (Spilopelia senegalensis), canaries (Serinus canaria forma domestica), finches (Family: Fringillidae) , geese (Order: Anseriformes), southern black-backed gulls (Larus dominicanus), ostriches (Struthio camelus) , pigs, chickens and humans. 
The disease does not occur naturally in the wild in South America since New World species appear to have an inherent resistance to the circovirus.  The disease is more prevalent in Old World species; however, due to poor disease control in the shipments coming from South America and Australasia during the early pet-bird trade, the circovirus has spread rapidly across multiple species.  It is endemic in free-ranging populations of Australia and Indonesia and is now observed in a wide range of wild and captive parrot species.  As of 2005, it was reported that “up to 20 percent of free-ranging cockatoos in Victoria, Australia may have clinical signs of PBFD in any one year.” Wild, crimson rosellas (Genus: Platycercus), other wild populations of Moluccan (Cacatua moluccensis) and other cockatoos, and lovebirds (Agapornis roseicollis) are also infected with the disease in Australia. 
“Here (in the U.S.), we see mostly lories with the disease. And we only see a few birds a year. So it is not a threat to our birds that it was in the past, when birds were brought into this country in large numbers.” R Dahlhausen
There is evidence of PBFD occurring naturally in wild birds for more than 20 years in Australia where it is recognized as the main disease threat to many critically endangered birds, such as the orange-bellied parrot (Neophema chrysogaster).  Viral evidence proves that PBFD originated in the Australasian Psittaciformes rather than the African or South American Psittaciformes. The dispersion of wild-caught Australian parrot species such as the budgerigar (Melopsittacus undulatus) since the early 1840’s has most likely resulted in the global spread of PBFD. 
The first recorded description of the feather-loss syndrome that was almost certainly PBFD was by ornithologist Edwin Ashby in 1907.  He observed a flock of completely featherless, red-rumped parrots (Psephotus haematonotus) in the Adelaide Hills of South Australia in 1888. The species then disappeared from the area for several years.   Affected birds were described as “quite healthy, except for being destitute of feathers,” and PBFD was considered responsible for the decline of the species in the Adelaide Hills, since affected birds were likely to be more susceptible to predation.  The virus was first identified as a circovirus in the early 1990’s. Veterinarians were aware of the disease at this time but did not know what caused it. 
3. Etiology and Pathogenesis of the Circovirus
The virus that causes PBFD belongs to the taxonomic genus, Circovirus, family Circoviridae. . The molecular structure of the genome of the virus is roughly that of a 2,000- base, circular, single-stranded DNA.  It is a non-enveloped, 14-17 nm virus, and it is extremely resistant to environmental degradation and one of the smallest viruses known to cause disease.  “The virus is perhaps the simplest pathogen known to infect vertebrates.”  It is not known to mutate very often. The avian circoviruses share about 88% homology so they are not very diverse The circovirus is a hemagglutinating virus (one that causes clumping Here (in the U.S.), we see mostly lories with the disease. And we only see a few birds a year. So it is not a threat to our birds that it was in the past, when birds were brought into this country in large numbers. R Dahlhausen 3 of the red blood cells). “The disease is associated with ongoing massive viral excretion (continued shedding of the virus by the host), a feature that can be discovered with molecular testing. 
The circovirus enters primarily “through the lymphoid tissues of the avian GI tract, including the Bursa of Fabricius.”  It replicates in intestinal lymphoid organs, then spreads secondarily to the liver, brain, thymus, epidermis, feathers, and other tissues. As a result, both the bursa and the thymus atrophy. “In addition, destruction of bone-marrow cells may leave the organs pale and yellowish, and birds may be severely anemic and leukopenic (having an abnormally low white blood cell count), depending on the time of infection.”  The main histopathologic features are feather dystrophies, liver necrosis and atrophy, and necrosis of lymphoid tissue of varying severity.”  Necrosis of these tissues leads to immune suppression and fatal secondary disease, particularly in juveniles.  
Although researchers claim to have discovered more than 200 circovirus genotypes, The International Society of Taxonomy Nomenclature does not recognize this many genotypes; this may represent genetic variability within a genotype and not represent an actual different genotype. (Dahlhausen, personal communication) It had been previously thought that different circovirus genotypes were responsible for the disease’s appearance in certain geographical areas and with certain species. Now, however, researchers believe that all species of psittacine birds are susceptible to many different viral sub-groups.   No one genotype can be considered more virulent than another.
Figure 2: The black-capped lory (Lorius lory) on the left is suffering from abnormal and discolored plumage due to PFBD. His contour feathers have changed color and are atypically yellow, and he is missing quite a few of his other feathers, including the primary flight feathers. (Image courtesy Brian Speer)
In 1991, researchers developed a very sensitive and specific DNA PCR test which detected the virus in the blood. The original PBFD virus that causes this disease is now called “Psittacine Circovirus” or PsCV. 
The PBFD virus is highly infectious and environmentally stable . It spreads quickly from one host species to another; thus, there is a wide range of species capable of developing and passing on the disease. Usually a virus will weaken as it is passed from one species to another, but the circovirus’ ability to replicate efficiently makes it unlikely that the virus will reduce in virulence over time.  This fact makes developing a vaccine extremely difficult.
The virus replicates in several tissues, including the thymus and Bursa of Fabricius (both important organs for the immune system), crop, esophagus, intestine, skin and feathers, and in circulating leukocytes (white blood cells). Necrosis of the bursa, thymus and leukocytes results in suppression of the immune system. 
Periods Incubation periods vary among species and among individuals of the same species.  The variables in incubation time are:
- The amount of virus transmitted
- The age of the bird when infected
- The stage of the bird’s feather development
- The health of the bird’s immune system
Genetic material (DNA) from this virus can be detected in a bird’s blood as soon as 2 days after natural exposure to the virus.   With the use of blood tests, circovirus infections can be detected before the onset of clinical signs. Infected nestlings may have an incubation period of only 2-4 weeks, while young adult birds may not show clinical signs until months or years have passed.   The incubation period for vertical transmission (passed from hen to egg) may vary from 32 to 80 days.  While acute forms of the disease can occur in nestling and fledgling birds, the incubation period for the chronic cases can be very long, with the slow development of feather dystrophy as molting progresses. . It can take weeks to months before an infected bird will develop feather abnormalities. 
8. Virus-induced Immunosuppression and Natural Vaccination
The circovirus targets the immune system, specifically the thymus and Bursa of Fabricius (organs which manufacture T-cells and B-cells). This prevents the organs from producing lymphocytes, thus suppressing and damaging the immune system.  The impact of the virus on bone marrow also leads to immunosuppression, with birds becoming vulnerable to a wide range of other infectious diseases. The usual outcome is death within 1 to 2 years. 
Figure 3: The Bursa of Fabricius is found attached to the colon; this image is of a chicken. (Image courtesy Cornell University, College of Veterinary medicine. http://www.poultrydisease.ir/Atlases/avian-atlas/search/lesion/375.html)
Some birds die shortly after showing signs of PBFD while others live months to years. The younger the bird is when it becomes infected, the more severe is the immunosuppression and disease. “Birds develop their antibody diversity in the Bursa of Fabricius in the first 3-6 weeks of life. If they develop the infection before that time, they will never have an adequate immune 5 system. The symptoms from the secondary infections may be the only reason the clinician is prompted to test for PBFD. 
The manner in which the clinical disease progresses and the length of the infection depend on the age and species of the bird.  “The age of the individual at the time of viral exposure and the functionality of the host immune system also determine the course of viral infection. Most immune-competent birds, when infected with the PBFD virus, will have it in their blood for a brief time, then mount an effective immune response that eliminates the virus before any recognizable feather abnormalities occur. These birds develop virus-specific antibodies and are naturally vaccinated.” 
All psittacine species are susceptible to infection from the circovirus. The most frequently affected species are cockatoos, macaws, African grey parrots, Ringneck parakeets, lories and lorikeets, eclectus parrots, pionus, and lovebirds. Although any species can fall victim to it, some are at a greater risk and develop more severe symptoms than others. PBFD is capable of spreading rapidly in lovebird and budgerigar breeding facilities. 
10. Symptoms of Selected Species
Different species may display different symptoms.
10.1 Lories [Family: Loriidae]: In a study by S. Clubb of virally infected lories at Loro Parque, it was discovered that females were affected with PBFD at a higher rate than males. This higher incidence occurred despite the fact that males were in the majority of the population. This difference occurred mostly in the juvenile birds, and the feather-damaging behavior began before sexual maturity. 
10.2 Lorikeets [Family: Loriidae]: Rainbow lorikeets (Trichoglossus moluccanus) and scalybreasted lorikeets (Trichoglossus Chlorolepidotus) are the most common wild birds affected by PBFD in Southeast Queensland, Australia. Lorikeets can become clinically ill and lose their tail and flight feathers, but after a few months, they regrow the lost feathers and appear to recover. However, some of these apparently healthy birds remain carriers of the virus. These birds are usually young. 
The following symptoms in lories and lorikeets are seen upon presentation:
- They usually shed their tail feathers and outside primary wing feathers.
- The remaining flight feathers will often fall out easily.
- They cannot fly, or they have very weak flying ability.
- The calami (shafts) have the classic abnormalities—pinching and necrosis.
- Older lorikeets with chronic disease will have color changes on the contour feathers (body feathers) which consist of yellow patches within the green normal-colored feathers, and the primaries and secondaries will be yellow in the wrong places.
- They are weak and suffer from secondary infections. 
There is evidence that the Loriinae sub-family, which includes the lorikeets, lories, fig parrots, and budgerigars, may be the “most robust or deeply adapted hosts of PBFD and are potentially super-distributors of this virus, at least throughout Australasia.” 
10.3 Finches (Family: Fringillidae): Historically, finches have been unaffected by the circovirus; however, in 2017, the virus was identified and detected in 14 zebra finches (Taeniopygia guttata) from 7 aviaries and hobby breeders using PCR and sequencing. The individual finches displayed high genetic diversity within 2 genetic subgroups. Their signs are similar to those found in psittacines:
- Nestlings, fledglings, and adult birds displayed clinical disease, varying from mild to severe.
- There was also a high rate of mortality caused by secondary infections.
- Feathering disorders, lymphocytic depletion of the spleen (inability of the spleen to generate white blood cells), and leukocytopenia (reduction of the number of white blood cells in the blood) were detected in these birds.  
10.4 Cockatoos (Cacatua [white] species and Calyptorhynchus [dark] species): Cockatoos were the first species to be diagnosed with PBFD, and they have the classic symptoms.  The disease is widespread in Australian species such as the sulphur-crested cockatoo (Cacatua galerita), little corella (Cacatua sanguinea) and galah (Eolophus roseicapilla) “The gang-gang cockatoo (Callocephalon fimbriatum) and the black cockatoo (Calyptorhynchus spp.), which occupy specialist ecologic niches, seem more susceptible to succumbing, especially from the acute phase of infection.” 
10.5 Budgies (Melopsittacus undulatus): PBFD is called “French Molt” in budgerigars. They will:
- Lose their primary tail and outside wing flight feathers
- Display twisted and disfigured incoming feathers
- Develop improved feathering after a few months. 
10.6 Cockatiels (Nymphicus hollandicus): Even though they are members of the cockatoo family, cockatiels appear to have an inherent resistance to the circovirus. They are only occasionally seen with the disease. 
10.7 Rosellas (Genus: Platycercus): They also have an inherent resistance, but occasionally test positive for the disease. 
10.8 Pigeons (Circovirus PiCV) (Family: Columbidae). Circovirus infections have been diagnosed in pigeons and doves in Europe, North America, and Australia. The pigeon circovirus, though distinct from the psittacine genotype, also suppresses the immune system. Viral inclusions are found in the bursa, spleen, intestines, and bronchial lymphoid tissue, and lesions are seen which are linked to concurrent bacterial, viral, fungal, and parasitic infections. 
10.9 Other species will display lesions similar to those found in psittacines; the differences lie in the types of feathers that are affected and the color changes they experience. In smaller grass parrots such as the Psephotus and Neophema species, the only sign of the disease may be normal-looking feathers that fall out or are easily plucked. The first (and possibly only) clinical sign in birds with green plumage may be change in feather color to yellow. The feathers appear otherwise normal. 
Figures 4-6. PBFD in an African grey and lovebird. Note the feather discoloration in the grey. (Images courtesy Sofia Sangushko. Used with permission)
Figure 7: This female eclectus parrot (Eclectus roratus) is losing her normal head and facial feathers, and the follicles are not regenerating. This has resulted in dysplastic (abnormal) feather stumps. (Image courtesy Shane Raidal)
Figure 8: A peach-faced lovebird exhibiting advanced clinical signs of feather loss and color changes. (Image courtesy Brian Speer.)
11. Forms of PBFD and Clinical Signs
Diseases present themselves in one or more of the courses listed below. PBFD presents as either acute, peracute or chronic.
- Acute course: sudden, severe onset; duration of a day or two; in need of urgent care; quickly fatal
- Peracute course:. Sudden and severe onset, duration of a few hours, rapid progression, quickly fatal
- Subacute course: moderate duration or severity, duration of up to a week; individual appears to be clinically well
- Chronic course: persisting for a long time and constantly occurring.
- Recurrent course: periods of normality of weeks to months. (Definitions: http://medicaldictionary.thefreedictionary.com/peracute+course)
11.1 Acute Form:
The acute form is usually seen in nestling birds around the time of fledging or after they have had their first feather growth; this molt replaces the neonatal down feathers. Chicks as young as 2 months of age or as old as 3 years of age are seen with classic symptoms of feather dystrophy. “If the chick develops clinical lesions while most of his feathers are still developing, he will exhibit the most severe feather pathology. The disease progression is less dramatic in young birds that develop clinical signs after body contour feathers are mature. In these birds, feather changes may be limited to the still-developing primary flight and tail feathers.”    Some birds have only down feathers that remain, or none at all. 
The signs for the acute course are:
- Depression (rapid onset) and lethargy
- Anorexia, regurgitation, weight loss, and diarrhea with mucus in the droppings
- Progressive and symmetric feather abnormalities with each successive molt
- Feathers that are loose, fracture easily, may bleed, fall out, and are very painful.
- Lesions on the feathers, including circular bands around the feathers which constrict the feather at its base
- Leukopenia (decrease in the number of white blood cells)
- Anemia and weakness due to viral attack on bone marrow which forms red blood cells
- Biliverdinuria (green pigment in the droppings, indicating liver disease)
- Death, following a short period of anorexia, depression, and diarrhea, with very little feather abnormality   
Due to severe immune-system suppression, multiple secondary infections develop, causing death within 2 to 4 weeks. Typical confirmation of the acute form of the disease is by necropsy; it progresses too quickly for feather and beak signs to appear. 
Other possible signs include:
- Pterylodynia (feather tract lesions) with edematous (fluid-filled) and painful wing tips caused by inflammation and vasculitis (inflammation of the blood vessels)
- Subcutaneous edema (fluid buildup under the skin).
- High viral titers in the liver and bile
- Fractures of the developing calamus (feather shaft) and intra-pulp hemorrhage.
- Feathers that fracture at places where the feather is necrotic; this usually happens before the feather has unsheathed.
- Death from hepatic necrosis (liver failure) without obvious feather lesions.  
Depending on the age of the nestling and at what stage of feather development the feather tracts are in, the bird may shed all of his feathers at once, or only the primary flight feathers. 
Figure 9: Feather destruction from the circovirus. (Image courtesy Avian Biotech) http://www.animalgenetics.us/Avian/Disease_Testing/PBFD.asp
11.2 Peracute Form
The peracute form also commonly occurs in very young birds and may begin with signs unrelated to the beak or feathers. Affected birds are often depressed and regurgitate due to crop stasis. They may develop a diarrhea-causing enteritis or pneumonia and die without displaying any lesions of the feathers or beak. There will be no feather abnormalities since these birds only have their neonatal down. Cockatoos, African greys, and lovebirds are usually seen with these signs. 
11.3 Chronic Form
If an adult bird contracts PBFD, he will develop the more commonly seen chronic form with its slow, progressive development. “Feather dysplasia is the result of virus-induced necrosis (cell death) and disruption of the epidermal collar in the feather follicle, intermediate basal epidermis in the skin, and thrombosis and hemorrhage within the feather pulp.” 
Older birds may overcome the disease with few lasting effects. In some cases, these surviving birds become carriers able to shed the disease. In other cases, birds are able to eradicate the disease from their system, leaving them with a natural immunity that can be passed on to their offspring. 
A bird can begin to show signs as late as 20 years of age, even though he had been clinically normal for most of its life. The affected birds gradually lose plumage, often without other clinical signs of illness. The pattern of ongoing plumage damage is related to the stage of the molt that the bird is in when the disease first begins. Feather abnormalities may not appear until the first molt after infection, which could be a period up to 6 months. As soon as the feather emerges from the follicle, growth will cease.   
The chronic form occurs if the bird’s immune system manages to mount a reaction to the virus and any secondary infections. In those species having powder down, signs may be visible immediately, as powder down feathers are continually replenished.  Birds with the chronic form of the disease may live for months to years before dying of a secondary infection. Secondary viral, fungal, bacterial or parasitic infections often occur as a result of diminished immunity. Secondary infections may cause death before feather abnormalities are easily recognized. 
Infections will produce the following sudden-onset signs:
- Immunosuppression and elevated white cell counts
- Crop stasis and regurgitation, loss of appetite, and rapid weight loss
- A long period of illness, with feather loss and weakness.
- Death, occurring in later stages of the disease. 
Figure 10: Dystrophic down feathers and wing feathers. (Image courtesy The Parrot Society http://www.theparrotsocietyuk.org/veterinary-advice/psittacine-beak-and-feather-disease)
Figure 11: Powder-down patch in a gang-gang cockatoo (Callocephalon fimbriatum) with PBFD. The loss of powder-down feathers results in the absence of powder in all the feathers. (Image courtesy Shane Raidal)
12. Classic Signs
Changes in the chronically affected bird are usually referred to as the “classic signs.”
12.1 Feather changes include:
- Symmetrical feather loss in the pterylae (feather tracts) on each side of the body
- Thinning of the rachis with a thick, retained feather sheath of the feather shaft
- Dystrophic feathers which stop growing and fall out shortly after emerging from the follicles
- Feathers that are fragile, fractured, pinched, constricted, clubbed, deformed and easily bent
- Loose, short feathers. (This is usually the first sign.)
- Contour feathers which are lost early over most of the body
- Primary feathers which are lost later in the disease process
- Annular constricting bands and curling on the calamus
- Discolored, dark red-brown patches in the shafts of developing feathers due to accumulations of dying cells. This is most often seen in African greys and young cockatoos
- Hemorrhaging within the calamus and feather pulp with fault lines across the veins
- Progressive, irreversible feather loss with dystrophic feathers growing in their place during each successive molt
- Constant, delayed molting with premature shedding of developing feathers
- Loss of powder down and powder-down feathers
- Inability to replace feathers due to follicular damage
- Feather-damaging behavior, which occurs mostly through chewing, either self-induced or performed by cage-mates. Plucking usually begins on the breast, followed by the head, wings, abdomen, legs and back
- The progression of the disease is usually predictable and occurs first to the powder-down feathers, seen over the flank region, followed by damage to the contour feathers in most of the feather tracts, then damage to the primary and secondary feathers of wings, tails, and crest.
- The overall appearance of the bird becomes disheveled, dirty, and messy. Some birds drop their tail feathers when handled. 11
- Disruption of feather growth so intense that the retained feather sheath contains only a disorganized mass of keratin
- Eventually, necrosis of the feathers and cessation of feather growth occur
- Death, which occurs in months to years.       
Figure 12: A dystrophic feather showing blood within the calamus and annular constrictions of the calamus. (Courtesy Shane Raidal)
Figures 13, 14: Feather dystrophy. Retained blood and sheath. (Images courtesy Ellen Uittenbogaard. Used with permission)
Figures and video 15-23 Feather dystrophy in a cockatoo with advanced PBFD. (Images courtesy of Faryal Gauhar. Used with permission.)
12.2 Changes in the Skin
- Exposure of bare skin to air, damaging the dermal layers
- Scarring of follicles; pustule formation in the follicles
- Color changes, such as dark pigmentation in skin of wild birds or birds maintained outdoors. This is associated with tanning as the skin is constantly exposed to the sun.
- Hyperkeratosis (too much keratin) on the extremities in severe cases. The skin becomes excessively scaly, thickened, and moist.
- Chronic skin ulcers on the elbows and wing tips
- Hypothermia (chilling)
- Secondary skin infections due to immunosuppression. These include cryptosporidiosis (a parasitic disease) and bacterial, mycotic (fungal), and other viral infections.  
12.3 Changes in the Beak
Changes in the beak are due to damage to the germinal epithelium (underlying layers of the rhamphotheca—the horny covering of the beak. Beak changes are severe, with both the maxilla and mandible becoming overgrown, blackened and fragile. The diseased beak breaks easily and become painful. Once the underlying sensitive tissues become exposed, the bird is in great pain and refuses to eat. The changes include:
- Ulcers and plaques in the roof of the mouth. There is a “viral-induced necrosis of the palatine mucosa (a mucous membrane in the roof of the mouth), causing it to separate from the beak and fill with caseous (cheese-like) material.” 
- Brown, necrotic areas inside the upper beak
- Secondary beak and oral-cavity infections
- Symmetrical lesions on the beak
- Necrosis of the oral epithelium and osteomyelitis (an infectious, painful, inflammatory, bacterial bone disease)
- Lack of powder on the beak; powder is necessary and is a result of normal preening
- Change from dull black to glossy appearance due to lack of powder
- Irregular, sunken areas in the beak
- Sloughing off of the rhampotheca
- Hyperkeratosis of the beak, leading to fractures and overgrowth. The beak elongates and becomes deformed and brittle. It will develop splits and cracks which break and peel.
- Destruction of tissues and necrosis of the hard palate caused by bacterial and fungal invasion of the abnormal beak; this condition is painful and can prevent the bird from eating, leading to starvation.      
Figures 24, 25: Beak dystrophy. (Courtesy P. Macwhirter. Used with permission)
Figure 26: Beak necrosis. (Image courtesy Cockatoo Info, http://cockatoo-info.com/health/pbfd/)
Figure 27: Necrosis of the junction of the rhinotheca and the oral mucosa in a cockatoo with advanced PBFD. (Image courtesy David Phalen)
12.4 Nail deformity
- Sloughing off of nails and deformed nails which develop well after feather and beak lesions become apparent; lesions are symmetrical.
- Cracking and peeling of the outer layers of the nails or claws.    
13. Transient, Subclinical infections
Transient, subclinical infections are possible and have the following characteristics:
- The bird’s immune system is able to eliminate the virus. This viral elimination is usually seen in captive macaws and all older, immune-competent psittacine species, including cockatoos.
- Although the bird had previously tested positive, it now appears normal and displays no clinical symptoms.
- After the second testing 90 days from the first test, if the bird has eliminated the virus, the test will come back negative.
- If results come back positive, it means the bird is carrying the virus in latent form and will probably exhibit signs of clinical disease later in its life.
- Most birds which carry the circovirus show no outward clinical signs of having the disease. “They are transiently infected with the PBFD virus and have a mature, intact immune system which is capable of mounting an effective, protective immune response which results in apparent viral elimination.”  
- Most infections are now transient in nature
13.1 Transient Infection Case Study
In one case, a 4-week-old African grey had tested negative before its sale to a store. It was sold at 8 weeks of age, and at that time, it tested positive for PBFD. The pet store was swabbed and its nursery was found to be contaminated. Other hand-fed young birds also tested positive in that store. Since the 8-week-old bird was not showing signs of disease, it was not euthanized. This was a case of a transient rather than progressive viral infection. The bird was isolated and retested 4 weeks later. Although it still tested positive, the circulating virus levels were considerably lower. Tests performed at 60 and 90 days later were negative, and the bird remained negative and clinically normal. 
Figure 28: Tookie, diagnosed with PBFD and beginning to show visible signs. (Image by Debi Pearson, courtesy Beautyofbirds.com. Used with permission.)
Figure 29: 2013 update. Tookie, at 4 years old (Photo by Debi Pearson, courtesy BeautyofBirds.com). Used with permission)
14. Differential Diagnoses
In the past, PBFD was the first ailment avian veterinarians thought of when presented with birds having dystrophic feathers. Today, however, In the United States, Canada, and European countries, due to the efforts of clinicians to educate breeders and bird owners, improved aviary management, and widespread use of diagnostic tests, most feather abnormalities are caused by diseases or conditions other than PBFD virus. 
A diagnosis of PBFD cannot be made based solely on feather examination. Other illnesses can be responsible for the dystrophic feathers seen in PBFD virus; damaged feathers can be caused by any condition which disrupts the blood supply to the developing feather.  Many other diseases and conditions can cause the same signs as PBFD in its early stages, but testing will distinguish PBFD from other causes. These diseases and conditions include:
- Polyoma virus, which produces feather loss in a pattern similar to the PBFD virus, especially in budgerigars. It can cause a high number of fatalities in young chicks without causing any feathering abnormalities.
- Adenovirus, known for affecting the tissue linings of the respiratory tract, urinary tract, upper and lower intestines, and the eyes
- Excessive preening and allopreening (birds preening each other) which can result in damage to head and neck feathers
- Bacterial and fungal infections, including folliculitis
- Metabolic and endocrine diseases such as hypothyroidism which causes lack of feather regrowth
- Liver diseases, such as hepatic lipidosis, which cause narrowing of the feathers and color changes
- Poor nutrition, which also causes feathering abnormalities and color changes
- General health issues: Chronically sick birds will present with poor feathering which might be mistaken for PBFD. Cockatoos will start to lose their powder-down feathers and develop stunting of the down feathers as a consequence of poor health.
- Septicemia (bacterial infection in the blood)
- Some drug reactions, particularly to penicillins and cephalosporins    
It is important to notice where the feathers are missing. If they are missing from the body and not the head, it is most probably due to one of the above causes. But if the feathers on the head and crest are missing, an area the bird cannot reach, it’s probably due to PBFD. A skin and feather biopsy can be used to eliminate other causes of abnormal skin and feathers. It is not 100% diagnostic for PBFD but can be strongly indicative of it. 
Figure 30: Two-year-old sulphur-crested cockatoo, rescued from the wild in Queensland, Australia. (Image by Miranda Lennox, courtesy Beautyofbirds.com. Used with permission)
15. Testing and Diagnosis
In the past, clinicians had difficulty with testing methods because some failed to detect the viruses; this made interpretation of the results difficult. It was not uncommon for false negative and false positive results to come back. Today, though, molecular diagnostic testing has improved the reliability of the findings. “Testing utilizing blood and tissue swab samples has 15 proven 99.7% accurate for birds testing positive and 100% accurate for birds testing negative.” 
DNA testing must also be performed on any birds of species which are considered vulnerable to rule out latent infections. DNA testing also needs to be done on aviary equipment and the aviary environment to test for possible contamination. The following tests are recommended to determine if the circovirus is present in a bird’s tissues:
- Surgical skin biopsy
- Surgical biopsy of abnormal feathers, feather follicles, calami, and shafts (histopathology); however, since the PBFD virus does not affect all feathers simultaneously, this method of evaluating a sample may have a high degree of error
- Use of DNA probes and cytology on feather pulp
- Polymerase chain reaction (PCR). A blood test using a DNA probe is the best way to diagnose the disease, especially in acute cases. Birds with PBFD can have normal feathers, so the PCR test is the most effective method available for detecting the virus in birds before feather lesions develop.
- DNA probes performed on bone marrow (especially for acute cases)
- Complete blood count (CBC) In acute cases, diagnosis is often confirmed at necropsy; in these cases, a sample of the Bursa of Fabricius is essential.    
15.1 If the bird tests positive
- Some birds infected with the virus test positive yet never show clinical signs of feather dystrophy.
- A positive result from a bird with no feather problems may mean either that the bird is a carrier or that it has been recently exposed to the virus. In this case, it is best to isolate the bird and re-test in 90 days. The second sample should be collected by venipuncture to ensure that contamination does not occur. 
- It is recommended to retest all PBFD positive birds 60-90 days after the initial testing was completed.
- If the second sample remains positive, the bird should be considered a carrier and will be permanently infected. Eventually, it will show clinical symptoms of the disease.
- Birds that test positive twice, yet show no signs, should be considered to be infected and will most likely break with the disease at a later date.
- Controlling the disease involves testing susceptible birds and isolating or culling any that test positive twice, 90 days apart, even if they have no lesions of PBFD.
- Other birds which test positive may develop an immune response sufficient enough to fight off the infection and may test negative after 30-90 days.
- Some young birds will initially test positive and should be retested 30 days later. If the bird still tests positive, then there may be a lowering of the circulating virus; however, eventually these birds will test negative and remain clinically normal for the rest of their lives.  
Figure 31: Wild Australian king parrot (Alisterus scapularis) with early clinical signs of PBFD. There are plumage deficits around the face and head. (Image courtesy Shane Raidal)
15.2 If the bird tests negative
A negative blood test may not mean that the bird is free of disease. Once the bird is infected, the virus is in the blood. The bone marrow is constantly producing infected white blood cells, and they will circulate the virus throughout the body. If a bird is transiently infected, he’ll test positive almost immediately, and the test performed at 90 days will come back positive. If the bird has a competent immune system, his body will be able to rid itself of the virus. (R. Dahlhausen, personal communication)
16. Decline of PBFD numbers
In data analysis performed in 1993, Eclectus species had an overall positive rate of 10.2% followed by 8.7% for cockatoos and 8% for African grey species. In 1997, the same laboratory analyzed 10,000 tests.  The results of these tests were:
- 5% of birds tested positive for PBFD. Most of these birds were not exhibiting feather abnormalities or other outward signs of PBFD disease. They were subclinical and transiently infected.
- Eclectus parrots had an overall positive rate of 10%, followed by 8.7% for cockatoos, and 8% for African greys.
- The rate for macaws and Amazons was 4 % each, and lovebirds exceeded 30%. 
The statistics had not changed in the four-year period between the two analyses. Old World psittacine species displayed the highest number of positive test results while New World species exhibit a much lower incidence of positive tests with a rate of 4.2% for macaws and 4.1% for Amazon species. 
As of 1997, “Clinicians saw a dramatic decrease in the number of cases of PBFD, mainly due to testing, isolation, euthanasia, and careful breeding.”  In 2016, even fewer cases were seen; most were among the lovebird species. (R. Dahlhausen, personal communication)
The PBFD circovirus is not zoonotic, so humans and other animals cannot contract it. It is specific to birds. 
17.1 Horizontal transmission
PBFD is highly contagious. Circovirus particles can remain viable in the environment for months, long after the infected bird is has died. The exact duration of time that the virus is viable in the environment is not known; nevertheless, this is a very stable virus, and it will survive under a wide range of environmental conditions for quite a long time. High concentrations of the virus are found in the liver tissue, bile, crop secretions, feces and feathers.    17 Juvenile or young adult psittacine birds are highly susceptible to PBFD, but birds of all ages can contract and succumb to the disease. Birds kept in isolation for many decades can become infected when exposed to affected psittacine birds or contaminated areas.  
Horizontal transmission of the virus (from one individual to another) is primarily through these means:
- Direct contact from feather and skin particles which become airborne. Feather dander is easily dispersed and can contaminate food and water bowls and the environment
- Inhalation or ingestion of feather dander, either directly or through preening
- Oral or intra-cloacal ingestion of fresh or dried infected droppings This was proven in studies using experimental infection.
- In the wild, in tree hollows where there is strong competition for reproductive opportunities.
- Fomites (shared objects), such as:
- Bird carriers and cages
- Crop-feeding formula and crop contents
- Utensils, food, and food dishes
- Feet, hands, clothing and nesting materials.    
All efforts should be made to prevent the virus from entering an aviary or collection of birds since it is very difficult to eliminate. Because it is so easily transmitted, any bird with PBFD should not be housed in the same area as other susceptible birds. Those who handle these birds should change clothing and shower before handling non-infected birds or even getting in close proximity to them.  Bird owners need to understand that if they handle other people’s birds, it may be possible for them to bring the virus into their home and infect their birds. Contaminated nurseries are prime sources of viral contamination and transmission. In studies in which testing with swabs was done, “Multiple clutches of baby birds have tested positive and shown clinical disease even though the parent birds tested negative.” 
17.2 Vertical Transmission
The circovirus is also suspected to be transmitted vertically since the viral DNA has been discovered in embryos from infected hens; however, there has been no conclusive confirmation of this. Raidal believes that the vertical route is not as actively responsible for disease transmission as is the horizontal route since the virus is able to switch from host-to-host easily.  On the other hand, Pyne believes that vertical transmission is highly probable, and chicks are infected before they hatch. 
Figure 32: Caique with PBFD. It lived for 7 years. (Image Courtesy Caique Clowns http://caiqueclowns.blogspot.com/2008/10/pbfd-in-caiques-tias-story.html)
18. Prevention Vaccines
Currently, there is no commercially available vaccine for the circovirus. Studies are being conducted using experimental, inactivated vaccine or recombinant proteins to determine their effectiveness.  It has not been released to the public due to the risk it poses to alreadyexposed birds.  “As no cell culture system has been developed to grow the virus successfully in vitro, recombinant techniques show the most promise for the development of effective vaccines that may be produced on a large scale. Even if a vaccine is developed, it will not prevent viral replication, so measures will always need to be taken to control PBFD using diagnostic testing, hygiene measures, and the maintenance of high levels of flock immunity.” 
“The real problem with vaccine development was that they could not inactivate the virus effectively and ended up transmitting the infection when it was given.” R. Dahlhausen
19.1 Quarantine and Screening
Any new birds introduced to a flock should be isolated to stop the spread of the disease, and diagnostic screening using several different assays should be conducted to detect the virus. In countries where the wild bird population is infected, pet and aviary birds must be protected from possible infection by the dander and feces of the wild flocks.  Owners should purchase birds only from those reputable breeders and suppliers which can prove their birds are free of disease. The birds should be tested and the testing repeated in 3-4 weeks to allow for the incubation period to occur. Infected birds should be removed from the breeding program and isolated from other birds, and juvenile birds should be housed separately from adults. Prevention is crucial to the management of this disease. Known carriers should not be introduced into the flock or given new cages which might be used by non-infected birds in the future. 
Contaminated avian environments remain the major source of PBFD viral transmission.  Cleanness and sanitation are a must in all environments, but even moreso in any environment in which the circovirus has been reported. There is no known disinfectant that kills this virus since the circovirus is resistant to extremes of temperature and many chemical disinfectants. Nevertheless, “Stringent hygiene protocols should be in place, including regular cleaning with an appropriate disinfectant such as Virkon S in a 1% solution, which has been used with some success and has been shown to inactivate non-enveloped viruses and bacterial spores.” 
20. Treatment and supportive care
PBFD is a fatal disease. There is no cure or specific treatment for it. Supportive care consists of providing good nutrition, supplementary heat (incubator), beak trimming, and treatment of secondary infections. Birds which are featherless or have only a few feathers should be given a wrap or sweater of some type to preserve body warmth.
Figures 33,34: A cockatoo wearing a sweater for warmth. (Images by Miranda Lennox, Courtesy Beautyofbirds.com. Used with permission)
This is a progressive disease, and very few birds recover. If only the feathers are affected and the bird suffers no other symptoms, it can usually experience an acceptable quality of life. Death usually occurs naturally within 6 months to 2 years of developing the disease. However, if the bird’s beak or nails are affected to the point it cannot eat or grip, or if it is in great pain, veterinarians should recommend euthanasia.  In some chronic cases, Interferon is being prescribed to boost the immune system. Also, vitamin, mineral and probiotic supplements are recommended to improve the immune system. 
The pet bird with PBFD may live for several years if can be in a stress-free environment; however, it must never come in contact with other birds because of the possibility of spreading the virus. If the bird survives the initial infection, it will shed the virus for the remainder of its life, thus spreading the disease to other captive birds and possibly to those in the wild. If the birds dies naturally, it is usually from a secondary infection since their immune systems have been critically suppressed.  
21. Avicultural Threat
Viral diseases in pet birds have had a severe impact on the pet population, both from an emotional and economic standpoint. They are the most difficult diseases to confirm with testing and to manage medically.   The legal and illegal international bird trade—both of which still continue—has placed PBFD as a major threat to wild and captive birds. Cases of PBFD have now been reported in at least 78 psittacine species. In Australia, at least 38 of the 50 native species are affected by PBFD, both captive and wild. In 2004, the Australian Commonwealth Government listed PBFD as a major threat to the survival of five endangered species, “including one of the few remaining species of migratory parrots, the orange-bellied parrot (Neophema chrysogaster), of which only an estimated 60 mating pairs remained in 2006.” 
Although the number of birds suffering from PBFD has decreased in recent years in North America and Europe, other countries, particularly in the Mid-East and Australia, are experiencing epidemics of the infection. Education of the breeders and practitioners in these countries concerning the need for testing is crucial in stopping the spread of the disease. With 20 proper supportive and palliative care, the afflicted bird may experience a reasonably good quality of life for an extended amount of time.
The author wishes to express her gratitude to Drs. Robert Dahlhausen, Sofia Sangushko, and Fayal Gauhar, and to Ellen Uittenbogaard for sharing their images. Additional thanks to Robert Dahlhausen for providing additional information and for reviewing and approving this paper. Images of R. Dahlhausen copyrighted February, 2016. All rights reserved. Images and videos may not be reproduced or used without the express written consent of the owner.
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