Selected Infectious Diseases of Birds of Prey

Topics in Medicine and Surgery

Selected Infectious Diseases of Birds of Prey Michael P. Jones, DVM, Dip. ABVP (Avian)

Abstract Infectious diseases of bacterial, viral, fungal, and parasitic origin are common in wild and captive birds of prey presented to veterinary hospitals for medical care. Veterinarians should be knowledgeable of the infectious agents, clinical signs associated with disease, as well as diagnostic methods and treatment to increase the survival rate of raptors infected with these devastating and fatal diseases. The most commonly seen infectious diseases as well as a few emerging diseases are presented. Copyright 2006 Elsevier Inc. All rights reserved. Key words: raptor; bacterial; viral; fungal; parasitic; disease

Bacterial Diseases Pododermatitis Pododermatitis, also know as bumblefoot, is an inflammatory condition of the feet seen most commonly in captive birds of prey.1 Infection of the plantar surface of the foot is characterized by varying degrees of local abrasion, ulceration, swelling, erythema, and abscessation of the metatarsal pad or one or more of the digital pads.1-3 Infection may result from direct inoculation by puncture and devitalization of the epithelium or constant pressure or contusion.2 Predisposing factors include trauma (selfinflicted talon puncture, bite wounds, or fighting), inadequate perch size or perch substrate, obesity, inactivity, poor sanitation, and nutritional deficiencies (for example, inadequate vitamin A).1,4 The destructive process that ensues may involve the skin, underlying soft tissues, and even bone. The most common bacterial isolate is Staphylococcus aureus, although other common bacterial isolates include Escherichia coli and Proteus species.1,3,5 The most common clinical signs are swelling, inflammation, and pain. Often, the raptor will favor one foot over the other and elevate the affected foot. Classification of bumblefoot lesions is often based on a scheme proposed by Halliwell.6 Type I bumblefoot is a serious, chronic infection characterized by a diffuse cellulitis,

often of the metatarsal pads of one or more digits.1,2 Type 2 bumblefoot is similar to type 1 and appears as encapsulated, localized lesions of the digital or metatarsal pads.1,2 Type 3 is characterized by discrete lesion(s) with hyperkeratinization, localized swelling, and reddening, whereas type 4 appears as an enlargement of the distal digital pads as a result of flexor tendon rupture. Diagnosis of bumblefoot is dependent on history, physical examination, and clinical signs, whereas treatment is based on the stage of bumblefoot observed. Therapeutic options are aimed at reducing swelling and inflammation, debriding necrotic tissue, establishing drainage if abscesses are present, eliminating pathogens, protecting the wound from further infections, promoting granulation and healing with bandaging and dressings, and identifying and removing the underlying cause.1,2 Appropriate antibiotic therapy is based on bacterial culture and sensitivity. A more detailed From the University of Tennessee, College of Veterinary Medicine, Knoxville, TN 37996 USA. Address correspondence to: Michael P. Jones, DVM, The University of Tennessee, College of Veterinary Medicine, 2407 River Drive, Room C247, Knoxville, TN 37996. E-mail: [email protected] or [email protected] © 2006 Elsevier Inc. All rights reserved. 1557-5063/06/1501-$30.00 doi:10.1053/j.jepm.2005.11.008

Journal of Exotic Pet Medicine, Vol 15, No 1 ( January), 2006: pp 5-17

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Figure 1. Tuberculosis lesions in the coelomic cavity of a red-tailed hawk. (Courtesy of Phil Snow.)

review of bumblefoot and treatment options is presented in Dr. Remple’s clinical techniques article in this issue.

Mycobacteriosis Avian mycobacteriosis is reportedly a common disease in raptors that is primarily caused by Mycobacterium avium, a Gram-positive, aerobic bacteria.7 In recent years, Mycobacterium genavense has also been associated with disease in wild birds, captive zoological species, and pet psittacines.8,9 Avian mycobacterioisis is most commonly transmitted by the fecaloral route, and is usually characterized as a chronic wasting disease despite a good appetite.10 The organism is very persistent in the environment (remaining in the soil for years and in water for months) and resistant to many commonly used disinfecting agents. Typically, mycobacteriosis affects the gastrointestinal tract and viscera in raptor species (Fig 1). However, respiratory lesions, which are more commonly seen in Anseriformes, Columbiformes, and some passerine species, may also be seen in birds of prey.10,11 Lesions affecting the skin and subcutaneous tissues are usually localized, and the result of talon wounds inflicted by other raptors.10 Other forms of transmission include ingestion of infected prey species or inhalation of the organism. Clinical signs and susceptibility to infection may vary; however, some consistent clinical findings in raptors and other avian species infected with M. avium include chronic weight loss/wasting despite an excellent appetite, recurrent diarrhea, polyuria, anemia, dull plumage, and neurologic signs.10-12 Necrosis of the base of the tongue and neurologic signs, including loss of balance and convulsions, have been reported in a goshawk (Accipiter gentilis).13 Other species reported with neurologic signs include a red-tailed

hawk (Buteo jamaicensis) and a bald eagle (Haliaeetus leucocephalus).12 Lesions may also appear within bone marrow, joints, or muscle (particularly the muscles of the legs), resulting in shifting lameness, decreased use or inability to use a limb, and arthritis of affected joints.11 Lesions within the bones are presumed to be more common in birds of prey than in other avian species.9,12,13 A presumptive diagnosis of avian mycobacteriosis is based on a thorough history, cytologic evaluation of tissues/feces by acid-fast stain, radiographs of the coelomic cavity and appendages, biopsy of affected lesions, endoscopic examination, or fecal culture. An intradermal tuberculin test is used to diagnose mycobacterioisis in poultry; however, the tuberculin skin test may no longer be recommended in wild avian species because of the frequency of false-negative results, especially in early or late stages of infection.11,12 It should be noted that the presence of acid-fast organism in the stool is not necessarily diagnostic of an active mycobacterial infection. It is important to isolate and identify mycobacterial organisms because of the emergence of M. genavense as a potential cause of mycobacteriosis in avian species.12 Treatment of birds affected with M. avium is controversial because of its zoonotic potential. Therapy for mycobacteriosis usually involves a combination of ethambutol (10 mg/kg orally every 12 hours) (Myambutol; Lederle Pharmaceutical Division, Pearl River, NY USA), isoniazid (5-15 mg/kg orally every 12 hours) (Baxter Health Care, Deerfield, IL USA), and rifampin (10-20 mg/kg orally every 12-24 hours) (Rifadinl; Eon Labs Manufacturing, Inc., Laurelton, NY USA).14

Botulism Clostridium botulinum, an anaerobic, spore-forming, motile, Gram-positive bacillus commonly found in decaying organic matter, is the etiologic agent of botulism in birds of prey; however, it is not the bacteria itself but the toxin it produces (type C exotoxin) which causes illness in affected species.15 As in pasteurellosis, botulism is more frequently seen affecting waterfowl which have consumed maggots that have fed from contaminated meat. The same also holds true for raptors that consume contaminated meat; however, raptors are considered to have reduced susceptibility to the organism. It is also possible that avian species that feed from the ground or have ceca (some species of raptors, Galliformes, Anseriformes, and so forth) could potentially have C. botulimum as normal intestinal flora. Interestingly, vultures seem to be resistant to the effects of the toxins produced by C. botulinum. Clinical signs of botulism in birds of prey include flaccid paralysis of

Infectious Diseases of Birds of Prey

the neck and limbs, paralysis of the pharyngeal muscles, respiratory paralysis, and death within hours to days after ingestion. A diagnosis is based on observation of clinical signs consistent with botulism, as well as a history of consumption of decaying meat. Culture of the organism, tissue toxin analysis from frozen liver or kidney, water analysis, and a mouse inoculation neutralization assay are also available.15 Quite often a presumptive diagnosis can be made with clinical signs alone. Treatment for birds affected with C. botulinum includes supportive care (fluids, nutritional support, warmth, and appropriate antibiotics) and the administration of C. botulimum type A or C antitoxin (0.05-1.0 mL/day).15

Viral Diseases Poxvirus Poxvirus infections cause a variety of diseases in many different species of birds of prey.16,17 Avian poxviruses are large DNA viruses that induce intracytoplasmic, lipophilic inclusion bodies (Bollinger bodies) that infect epithelial cells of the integument, respiratory tract, and oral cavity, resulting in hyperplasia of the affected cells.17 The genus avipoxvirus is divided into 10 species; however, many of the isolated avian poxviruses are not clearly classified, or their status within the genus has not been determined.18 Members of the genus Avipoxvirus include fowlpox virus (type species of avian poxviruses), canarypox virus, juncopox virus, mynahpox virus, pigeonpox virus, psittacinepox virus, quailpox virus, sparrowpox virus, starlingpox virus, and turkeypox virus.18,19 Other avian poxvirus species that may also be in the genus Avipoxvirus include peacockpox virus, penguinpox virus, and falconpox virus.18,20 TaeJoong and coworkers20 described the characterization of a novel condorpox virus isolated from an Andean condor (Vultur gryphus). Other raptors reported to have been infected with avian pox include the prairie falcon (Falco mexicanus), lanner falcon (Falco biarmicus), lugger (Falco jugger), saker falcon (Falco cherrug), red-tailed hawk, rough-legged hawk (Buteo lagopus), goshawk, golden eagle (Aquila chrysaetos), white-tailed sea eagle (Haliaeetus albicilla), common kestrel (Falco tinnunculus), peregrine falcon (Falco peregrinus), and gyrfalcon (Falco rusticolus).17,21,22 Clinically, poxvirus infections appear in several forms: (1) a cutaneous form which is characterized by variously sized nodular proliferations of unfeathered skin around the eyes, beak, nares, and legs; (2) a diphtheritic form characterized by lesions on the mucosa, tongue, pharynx, larynx, esophagus, and

7 trachea; and (3) a septicemic form seen in canaries characterized by a ruffled appearance, depression, cyanosis, anorexia, and wart-like tumors of the skin.16,17 The cutaneous form is the most common form of disease in raptors. Transmission of avian pox requires viral contamination of broken skin.16 Mosquitoes and other blood-sucking arthropod vectors play a major role in the transmission of avianpox; however, mucous membrane or abraded skin contact with contaminated surfaces or aerosolization (dust, dried scabs, or other particles containing the virus) may also allow transmission, especially in captive raptor species. Poxvirus infections are usually confirmed through history, physical examination, clinical signs, the histologic findings of Bollinger bodies in appropriate samples of affected tissue, and electron microscopy (preferred) of scabs or other lesions.5,17 Inoculation of chicken eggs and the demonstration of pock lesion on the chorioallantoic membranes is also an effective means of diagnosis. Culture may be necessary to confirm a diagnosis in septicemic infections.17 Therapy for poxvirus infections is usually nonspecific and may include antibiotic therapy to prevent or treat secondary bacterial infections.5,16,17 Vaccination is the best method of controlling poxvirus infections in gallinaceous birds; however, further evaluation of vaccine efficacy in raptors is needed.16,17

Herpesvirus Herpesviruses, like poxviruses, are DNA viruses that affect a wide range of mammalian and avian hosts. The majority of herpesviruses that affect free living and companion species are members of the subfamily Betaherpesvirinae. The other subfamilies are the Alphaherpesvirinae and Gammaherpesvirinae. Clinical signs suggestive of herpesvirus infection include respiratory distress, ocular lesions, enteritis, liver disease, or acute death.23 Typical histologic lesions consist of hemorrhages in the respiratory/intestinal epithelium as well as multifocal necrotic lesions of the liver, spleen, and bone marrow.23 Herpesviruses seen in raptors include inclusion body hepatitis of falcons (falcon herpesvirus [FHV]), hepatosplenitis infectosa strigorum (owl herpesvirus [OHV]), and eagle herpesvirus.17,18,23,24 FHV has been demonstrated in the peregrine falcon, common kestrel, merlin (Falco columbarius), prairie falcon, and American kestrel (Falco sparverius).17 It is generally believed that FHV and pigeon herpesvirus are the same virus, and that pigeon herpesvirus, most likely transmitted when falcons consume the carcass of an infected pigeon, becomes more virulent in the falcon host. Clinical signs are noted within 1 to 2 weeks of con-

8 suming infected pigeons or doves. FHV has an affinity for reticuloendothelial cells and hepatocytes, resulting in severe depression, weakness, anorexia, and mortality approaching 100%.24,25 Histologic lesions generally reveal focal or disseminated degeneration and necrosis in the liver, pancreas, lung, kidney, and brain.17 OHV occurs in both wild and captive owls in Europe, Asia, and the United States.17 The eagle owl (Bubo bubo), great-horned owl (Bubo virginianus), striped owl (Rhinoptynx clamator), long-eared owl (Asio otus), snowy owl (Nyctea scandiaca), little owl (Athene noctua), Tengmalm’s owl (Aeoglius funereus), and the forest eagle owl (Bubo nipalensis) are naturally affected.17 OHV affects epithelial and mesenchymal cells;17 however, clinical signs and histologic lesions are similar to FHV in many ways. Necrotic foci are seen within the liver, spleen, intestine, and jugular veins.17 Diagnosis of herpesviruses in raptors is based on clinical signs, histologic lesions, serologic identification, and virus isolation. Acyclovir given at 333 mg/kg orally every 12 hours for 7 to 14 days may be effective in treating affected captive birds.14 However, therapy is usually aimed at providing supportive care and prevention of secondary bacterial infections with broad-spectrum antibiotics.

Newcastle Disease The Family Paramyxoviridae contains several genera and can infect a wide range of avian and mammalian hosts, including humans. The paramyxoviruses that infect birds may differ in host range and are presently divided into 9 distinct serotypes according to the type(s) of birds they affect. Paramyxovirus serotype 1 (PMV-1), also know as Newcastle disease virus (NDV), has the most broad (global) and significant host range. All avian species are considered susceptible to PMV-1. PMV-1 is further divided into 4 groupings based on virulence and the type of disease induce in chickens. These classifications cannot be generalized beyond chickens.26 Lentogenic strains may cause mild or inapparent disease.26 Mesogenic strains cause mild to severe disease.26 Velogenic neurotropic strains cause severe disease with high mortality.26 Although velogenic viscerotropic strains also cause severe disease and mortality, the hemorrhage found within the intestinal tract differentiates this group from the others.26 Exotic Newcastle disease is synonymous with velogenic viscerotropic strains and velogenic neurotropic strains. At this time, California, Nevada, and, most recently, Arizona have confirmed cases of NDV. Clinical signs of NDV in birds and, in particular, raptors, may vary with species, age, overall health

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condition, and virulence of the viral strain. Interestingly, vultures and owls appear to be resistant to infection with NDV, although there have been reports of virulent avian PMV-1 isolates in a barn owl (Tyto alba) and a tawny owl (Strix aluco) in Great Britain and Germany. In fact, attempts to experimentally infect vultures with NDV have proven unsuccessful.10,26,27 Although death rates may be quite high in infected birds, some birds infected with PMV-1 may remain asymptomatic, develop disease and recover, die suddenly with no warning signs, or die after long-term (days to weeks) illness.10,26,27 Possible clinical signs include anorexia, vomiting, diarrhea, respiratory signs (gasping, coughing, nasal discharge), opisthotonus (“stargazing”), torticollis (twisting of the neck), weakness or paralysis of the wings and legs, incoordination, tremors of the head, and convulsions.10,26,27 Paramyxoviruses may be shed from infected birds through secretions (primarily respiratory tract) and excretions (primarily feces) for varying lengths of time. Interestingly, although owls and vultures appear to be resistant to PMV-1 infections, they may shed the virus in their feces if infected. Direct transmission from bird to bird, air-borne routes (dust, contaminated beading), and vectors (insects, rodents, and human) may enhance the spread of disease.10,26,27 Ingestion or inhalation of contaminated materials is the most common method of exposure to NDV. Before 1972, cases of Newcastle disease were most likely the result of unregulated importation of psittacine birds. However, since 1972, the importation of exotic birds into the United States has been closely regulated, thereby greatly reducing the incidence of NDV in the United States. It is suspected that illegally imported psittacines and poultry, as well as migratory wild bird species, play an important role in the transmission of NDV. The exact role of migratory avian species, such as waterfowl and passerines, has not been determined. Certainly, steps should be taken to prevent direct contact between wild and captive birds. Ante-mortem diagnosis of PMV-1 infections is difficult. Certainly, multiple deaths in groups of birds with clinical signs associated with NDV should lead a clinician to strongly suspect NDV. For example, NDV should be considered in the differential list for falcons showing typical signs, with a history of being fed poultry products or sick pigeons.10,26-28 In most cases, clinical signs are not sufficient enough to confirm a diagnosis. Therefore, to confirm NDV, the virus must be isolated from infected tissues or a rise in antibody levels must be demonstrated. It is necessary to isolate NDV from infected birds and characterize

Infectious Diseases of Birds of Prey

the virus to exclude viruses of low virulence, which are found in feral birds throughout the world or live vaccines.28 The virus may be isolated from spleen, brain, lung, liver, and trachea by inoculating chick embryos or chicken embryo cell cultures. Differential diagnoses for NDV infection should include psittacosis, salmonellosis, lead or zinc toxicity, low blood calcium, and bacterial infections of the nervous system and the intestinal tract. Unfortunately, as is the case in most viral diseases, there is no specific treatment for NDV. Affected animals should be provided appropriate supportive care, including broad-spectrum antibiotics to prevent secondary bacterial infections, fluids to maintain hydration, and proper nutrition. Most birds, including raptors infected with NDV, will die despite supportive care efforts. Practicing good hygiene, providing appropriate nutrition, and immunizing susceptible flocks may reduce the likelihood of NDV outbreaks in captive aviaries. Currently, NDV vaccines are available for pigeons and poultry and may be considered as a preventive in raptors; however, very little information is available concerning their use in birds of prey in the United States. Dr. David Remple instituted a vaccination program at the Dubai Falcon Hospital, Dubai, United Arab Emirates, using very high titer killed poultry and pigeon Paramyxovirus vaccines. He noted that only a very small percentage of the thousands of falcons vaccinated developed Newcastle disease. The few birds that developed the disease after vaccination may have already been incubating the virus at the time of vaccination. As a final note, it is important to remember that Newcastle disease is a zoonotic disease, although the frequency is rare (most commonly poultry workers). Signs in people include sinusitis and conjunctivitis. Although NDV is zoonotic, recovery is usually rapid (within 7-10 days). However, anyone infected with NDV should not handle birds until their clinical signs have cleared, because their ocular secretions may contain NDV.

West Nile Virus West Nile virus (WNV) infection is a rapidly fatal disease in avian species caused by a Flavivirus (Family Flaviviridae, genus Flavivirus), and is closely related to St. Louis encephalitis virus (North/South America) and Japanese encephalitis virus (East Asia).29 WNV, which may not represent a single virus but a genetically diverse population of genomes in nature,30,31 was first isolated from a woman in the West Nile region of Uganda in 1937.29 The first human case reported in North

9 America occurred in New York City in August 199929; however, epizootics and epidemics have occurred in North America, France, Romania, Italy, Russia, and Israel.29-31 The particular strain of WNV reported in New York City was virtually identical to a strain from Israel.31 Morbidity and mortality in avian species initially occurred in and around the Bronx Zoo in mid-August 1999.29,32 Although many species of birds can be infected with WNV, the American crow (Corvus brachyrhynchos) and other corvids (ravens, jays, magpies, and nutcrackers) were the most commonly reported avian species to suffer high morbidity and mortality. Mortality rates in experimentally infected corvids may reach 100%.33-35 Numerous species of raptors, including Falconiformes and Strigiforms, have also been reported to have been infected and died from WNV.36 During the summers of 2002 and 2003, large numbers of raptors were affected in the Midwestern United States.37 Transmission of WNV occurs primarily through ornithophilic mosquitoes (Culex univittatus in the Middle East and C. pipiens in Europe and North America). The other North American species of mosquitoes considered to be vectors of WNV include C. nigripalpus, C. quinquefasciatus, C. restuans, C. salinarius, Coquillettidia perturbans, Aedes species, and Ochlerotatus species.38 Raptors are most commonly infected when bitten by an infected mosquito; however, mosquito-independent transmission from bird to bird may occur experimentally through ingestion of infected mosquitoes, infected mice, and contaminated water.31 Tesh and coworkers39 described persistent infection and continued shedding (for up to 8 months) of infectious WNV in the urine of experimentally infected golden hamsters (Mesocricetus auratus), despite what would appear to be an appropriate humoral immune response. WNV could be recovered from hamsters that survived initial infection by means of urine culture and cocultivation of renal tissue for up to 347 days after initial infection.39 Clinical signs of WNV infection include, but are not limited to, depression, anorexia, weight loss, head tremors, seizures, impaired vision, anisocoria, ataxia, and sudden death.31,40 The University of Minnesota Raptor Center Classifies clinical signs as follows:

Phase 1. Depression, anorexia, weight loss, sleeping, pinching off of blood feathers, elevated white cell count.32,41 Phase 2. In addition to the above, head tremors,

green urates, mental dullness/central blindness,

10 general lack of awareness of surroundings, ataxia, weakness in the legs.32,41

Phase 3. More severe tremors, seizures.32,41

Phalen and Dahlhausen described clinical signs of raptors affected in the Midwest United States as exhibiting clinical signs of decreased appetite, reduced body weight, dull mentation progressing to regurgitation, anorexia, cachexia, diarrhea, polyuria, biliverdinuria, recumbency, unresponsiveness to external stimuli, seizures, and death within 72 to 120 hours.31,36,37 Antemortem diagnosis of WNV infection can be difficult. A presumptive diagnosis may be made if clinical signs and time of the year (summer and fall months) are consistent with WNV infection; however, many diseases may cause similar clinical signs. Raptors and other species, such as crows, that are sick with WNV may become viremic, and the virus may be detected in the saliva and cloaca by means of polymerase chain reaction (PCR) from oral and cloacal swabs.31,42,43 Hemaglutination inhibition and plaque reduction serum neutralization assays are available; however, the plaque reduction assay is not as readily available as the others. Positive results on all three tests should be interpreted with caution, because circulating antibodies to other flaviviruses may affect the results.44 Demonstration of a rising antibody titer from paired serum samples with the plaque reduction assay would be the most conclusive proof that a raptor was infected with WNV. A rapid antigen-capture wicking assay, the VecTest (Medical Analysis Systems, Camarillo, CA USA) has been used to detect WNV in mosquitoes and corvids.45 Gancz and coworkers45 evaluated the usefulness of this test for the antemortem detection of WNV from oropharyngeal and cloacal swabs in owls and other raptors confirmed as positive by reverse transcriptase polymerase chain reaction (RT-PCR) on kidney or brain tissue. The VecTest appeared to be highly sensitive (100%) for detecting WNV in the oropharyngeal and cloacal swabs of Northern owl species (species with a natural breeding range north of Latitude 48o N), but provided reduced sensitivity for the detection of WNV in Southern owl species and other raptors.45 The results of this project suggest that the VecTest may be a useful screening test for detection of WNV in live birds; however, the result should be interpreted with caution in some owl species and raptors because of the possibility of false-positive test results.45 RT-PCR should be pursued when there is a need for a definitive diagnosis, such as in those cases evaluating the possible threats to humans.46 Additionally, there may be differences in antigen levels

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early in the incubation period or during recovery from infection that may affect the sensitivity of the VecTest.46 The most definitive method for diagnosing WNV in raptors is through necropsy. However, there are significant species-specific differences in the pathogenesis of WNV infection in raptors that warrant submission of numerous tissues. Detection of viral antigen by PCR or by isolation via cell culture may also be used to confirm infection in dead birds. Because of the zoonotic potential of this pathogen, veterinarians and others performing necropsies of birds suspected to have died from WNV should take appropriate precautions, including wearing a mask and goggles to prevent inhalation, ingestion, or conjunctival exposure to the virus and double gloving to reduce exposure through cuts, abrasions, or other sores on the hands.31 Gross pathologic lesions associated with WNV in raptors may include intraosseus hemorrhage of the calvarium or hemorrhage of the meninges or brain, pancreatitis or pancreatic hemorrhage, hemorrhage within the gastrointestinal tract as well as on its serosal surfaces, splenomegaly, and myocardial necrosis.31,47The kidney and brain are the preferred tissues to submit for histopathologic examination; however, microscopic lesions are also common in the spinal cord, heart, pancreas, spleen, skeletal muscle, skin, and thyroid and adrenal glands.31 Lesions include multifocal hemorrhage in the cebellar folia, mild to severe lymphoplasmacytic meningitis, nonsuppurative encephalitis most commonly in the cerebellum and brain stem, mild to severe diffuse lymphoplasmacytic and histiocytic epicarditis, myocarditis, and endocarditis, lymphoplasmacytic pancreatitis, and inflammation within the adrenal gland.31 Myocardial degeneration and mineralization may accompany lesions within the heart.47 Wünschmann and coworkers36,37 described variable pathologic lesions and immunohistochemical findings associated with WNV in two studies involving red-tailed hawks, Cooper’s hawks (Accipiter cooperi), goshawks, and great-horned owls. All species exhibited a similar triad of inflammatory lesions, including lympho-plasmocytic and histiocytic encephalitis, endophthalmitis, and myocarditis.36,37 Inflammatory lesions of the heart, brain, and eye were similar among goshawks, red-tailed hawks, and Cooper’s hawks, but were inconsistent and comparatively milder in owls.36,37 Encephalitis of the cerebrum more severely affected the goshawk, Cooper’s hawk, and red-tailed hawk, whereas lesions in the cerebellum were more severe in great horned owls. Intention tremors noted in the owls were attributed to the

Infectious Diseases of Birds of Prey

cerebellar lesions.36,37 Additionally, the formation of glial nodules in the cerebellum was the most common characteristic brain lesion in owls with encephalitis.36,37 The chronicity of the lesions in the 4 raptor species was also of special interest. WNV infections appear to be capable of causing a more chronic and fatal disease in red-tailed hawks, Cooper’s hawks, and great horned owls compared with goshawks.36,37 Viral antigen was detected in both studies by immunohistochemistry. In Cooper’s hawks, viral antigen was found, albeit in small amounts, in the heart, cerebrum, and eye, whereas viral antigen was found in the kidney, cerebrum, cerebellum, and eye in red-tailed hawks; in the kidney, heart, and cerebellum of great-horned owls; and in the spleen, heart, cerebellum, cerebrum, and eye of goshawks.36,37 Interestingly, viral antigen was well distributed in the organs of affected goshawks, whereas only small amounts of WNV antigen were present in affected organs in great-horned owls.36,37 Treatment of birds infected with WNV may be unrewarding, because there is no specific treatment available for WNV. Infected raptors may survive if provided appropriate supportive care, including fluid therapy, broad-spectrum antibiotic therapy, and the use of anti-inflammatory medications. Preventive health programs against WNV infections in avian species should focus on reducing exposure to mosquitoes by keeping birds indoors or in enclosures with mosquito-proof screening, eliminating mosquito breeding grounds by removing standing water, using mosquito traps, and carefully spraying to reduce vector numbers.31 Infected birds should be isolated from naive birds in mosquito-free areas and contaminated carcasses incinerated. Currently, there is no vaccine specifically approved for the prevention of WNV infection in avian species; however, the development of vaccines to protect avian species is underway. At present, a WNV vaccine (Fort Dodge Laboratories, Fort Dodge, IA USA) approved for use in equids has been used in avian species. Unfortunately, the efficacy of this vaccine is still unclear. Nusbaum and coworkers48 reported that Chilean flamingos (Phoenicopterus chilensis) and red-tailed hawks vaccinated with 0.2 mL of the killed Fort Dodge product twice over a 3-week period did not mount a detectable humoral response. Presently, The Raptor Center (University of Minnesota, St. Paul, MN USA) recommends using the Fort Dodge vaccine because there are no other alternatives. Their vaccine schedule is as follows: birds ⬎300 g receive 1.0 mL intramuscularly and birds ⬍300 g receive 0.3 to 0.5 mL intramuscularly.32 A second vaccination is given 3 weeks later.32 A third

11 vaccination may be given during those periods when the vectors are at high densities.

Avian Influenza Influenza A virus (family Orthomyxoviridae) has a cosmopolitan distribution. This virus has been recovered from a wide range of avian and mammalian hosts, including humans. The virus has been associated with an epornitic of respiratory disease in mammalian and captive and free-ranging avian species of all ages.26 Influenza A virus has been recovered from Falconiformes, but is more common in free-ranging ducks, shorebirds, and passerines. These birds may serve as reservoirs for the virus.17,26 Transmission of the virus occurs through direct contact with feces, ocular discharge, aerosolization, or from contaminated water. Influenza A viruses are characterized by the hemagglutinin and neuroaminidase proteins found on their surfaces.26 Affected birds may demonstrate mild or inapparent clinical signs when infected by less virulent strains of the virus, whereas highly susceptible avian species affected with the more virulent strains may develop clinical signs leading to death.26 Clinical signs may include mild to severe respiratory signs, depression, anorexia, diarrhea, or edema of the head and neck.26 Infection with highly virulent strains may result in a viremia associated with lymphopenia, damage to endothelial cells, and bleeding disorders.26 Highly pathogenic H5N1 influenza A virus, the same viral strain associated with epidemics in Southeast Asia, was recovered from two crested hawk-eagles (Spizaetus nipalensis) that were smuggled from Thailand into Europe.49 Necropsy of the eagles revealed enteritis in both birds and bilateral pneumonia in one of the eagles.49 Antigenic subtyping as H5N1 was performed by hemagglutination inhibition, and the diagnosis of H5N1 influenza virus was confirmed by nucleotide RTPCR.49 Influenza A virus (H7 serotype) was reported in a saker falcon in Italy.50

Adenovirus Adenoviruses affect a wide range of avian species and have been previously recovered from several raptor species, including a goshawk exhibiting central nervous system signs and death, a merlin, and an American kestrel with hemorrhagic enteritis and anemia before death.17,18,26 Schrenzel and coworkers51 described a 1996 outbreak of adenovirus in a captive raptor breeding facility that resulted in the deaths of young Northern aplomado falcons (Falco femoralis septentrionalis) between 9 and 35 days old and peregrine falcons from 14 to 25 days of age. Affected birds were anorexic, dehydrated, had diarrhea, and

12 died acutely.51 The cause of death in 62 (56.3%) of 110 aplomado falcons and 6 (5.8%) of 102 peregrine falcons was determined to be a systemic infection with a new species of adenovirus related to the group I avian viruses, serotypes 1 and 4 aviadenovirus.51 In situ hybridization and PCR demonstrated that the virus was epitheliotropic and lymphotropic.51 No other infectious agents or predisposing factors were found in any of the affected falcons. Subsequent to the 1996 outbreak, adenoviral infections resulted in the deaths of orange-breasted falcons (Falco deiroleucus), teita falcons (Falco fasciinucha), a merlin, Vanuatu peregrine (Falco peregrinus nesiotes), and gyrfalcon x peregrine falcon hybrids (Falco rusticolus/peregrinus) in Wyoming, Oklahoma, Minnesota, and California.51,52 In general, the host range for most adenoviruses is limited to one species or closely related species, so it is not unexpected that the virus only affects falcons. Based on serum neutralization antibodies, peregrine falcons appear to be the natural host and primary reservoir for adenovirus.51,52 Seroprevalence testing of wild and captive peregrine falcons demonstrated high seropositivity rates of 80% and 100%, respectively, whereas aplomado falcons had a lower serpopositivity rate of 43% to 57%, respectively.51,52 Other falcon species from tropical or island origins appear highly susceptible to the disease; however, none of these birds were seropositive. Clinical disease was rarely reported in peregrine falcons. Oaks and coworkers52 suggest that the preventive health programs aimed at limiting the spread of adenoviruses in falcon aviaries be based on segregation of carrier and susceptible falcon species.

Fungal Diseases Aspergillosis Aspergillosis is a mycotic disease commonly seen affecting raptors (especially goshawks, gyrfalcons, and red-tailed hawks). Aspergillus fumigatus is the most common etiologic agent, followed in frequency by A. flavus and A. niger.19 Aspergillus species are thought to be ubiquitous, with infections commonly resulting from inhalation of spores from the environment. Infections are considered to occur secondarily to any event that may compromise the host bird’s immune system. Aspergillosis may be classified as an acute form, a tracheal form, a single or series of granulomas (Fig 2) within the respiratory system, or a systemic form.53-55 Clinical signs are usually associated with the respiratory system or organ(s) affected. The most common clinical signs observed with aspergillosis in birds include: dyspnea, change or loss of voice, depression, anorexia, exaggerated respira-

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Figure 2. Aspergillus fumigatus lesions in the lung of a red-tailed hawk. (Courtesy of David A. Bemis, PhD.)

tory effort (“tail bob”), and weight loss or emaciation. Blepharitis and dermatitis have also been reported in a peregrine falcon x gyrfalcon hybrid.56 Early detection and aggressive treatment are required to successfully treat affected birds. Diagnosing aspergillosis requires a thorough history, physical examination, laboratory diagnostics (complete blood count and chemistry panel), radiography, endoscopic and laparoscopic examination of the respiratory tract, protein electrophoresis, serological testing (enzyme-linked immunosorbent assay—The Raptor Center, College of Veterinary Medicine, University of Minnesota, St. Paul, MN USA; Aspergillus antibody and antigen enzyme-linked immunosorbent assay—Division of Comparative Pathology, University of Miami, Miami, FL USA), and fungal culture.57 However, a definitive diagnosis of aspergillosis may be difficult to achieve despite the many diagnostic tests available. Many therapeutic regimens have been proposed to manage this fungal disease, including the use of amphotericin B (1.5 mg/kg intravenously every 8 hours for 3 days; 1.0 mg/kg intratracheally every 8-12 hours; or 0.5 mg/mL sterile water nasal flush), ketoconazole (15 mg/kg orally every 12 hours), miconazole, clotrimazole (0.2 mL equaling 2 mg/kg intratracheally every 24 hours for 5 days or nebulize 1% solution for 30-60 minutes), fluconazole (5-15 mg/kg orally every 12 hours for 14-60 days), and enilconazole and itraconazole (10 mg/kg orally every 24 hours).14,58-61 Di Somma and coworkers61 evaluated the clinical efficacy and safety of voriconazole in the treatment of aspergillosis in falcons and found that treatment resulted in complete clinical resolution of 76% (19/25 falcons) of the cases, partial response in 16% (4/25) of the cases, and that two falcons failed to

Infectious Diseases of Birds of Prey

respond to treatment. Therapy consisted of oral administration of voriconazole by crop gavage at a dose of 10 mg/kg orally every 12 hours (A. Di Somma and T. A. Bailey, personal communication, November, 2005).61,62 Therapy is usually long term with patient response and serologic testing used to monitor progress. However, it must be remembered that the prognosis for successful treatment of aspergillosis is often poor to guarded.

Candidiasis Candidiasis, also known as “thrush” or “moniliasis,” is another significant mycotic infection of raptors and is caused by Candida species.2,21 This organism commonly infects the gastrointestinal tract, resulting in either plaque-like lesions on the mucosa of the tongue, pharynx, and crop, or a deep-seated infection of the gastrointestinal tract with or without oral lesions. When not systemically affected, clinical signs associated with candidiasis can include a reluctance to swallow, decreased appetite, vomiting, regurgitation, and depression. Diagnosis of candidiasis is not always easy, because other diseases that affect the mucosal membranes of the upper gastrointestinal tract may present with similar clinical and pathologic signs.63 Diagnosis is usually made by demonstrating Candida species in Gram stains of lesions from the oral cavity, esophagus, cloaca, and feces, or by culture.21 Because candidiasis often occurs as a secondary problem, the possibility of underlying diseases which compromise the immune system or prolonged antibiotic therapy should be considered. Therapy usually consists of nystatin (100,000 units/kg orally every 8-12 hours for 7-10 days, or 200,000-300,000 units/kg orally every 12 hours ⫻ 7-10 days) or fluconazole (2-5 mg/kg orally every 24 hours ⫻ 7-10 days).14,60,63 Itraconazole is usually considered a good choice for antifungal therapy in most fungal diseases; however, in vitro studies demonstrate concentration-dependent, fungistatic activity at two times the minimum inhibitory concentration (MIC) for Candida species. Therefore, itraconazole may not be the best choice for Candida infections in birds.64 It is important to remember that nystatin is not absorbed systemically, and therefore must come in contact with the affected areas of the gastrointestinal tract. For example, treating oral lesion by gavaging nystatin into the crop is ineffective, because the affected areas are bypassed and the nystatin does not come in contact with the lesions. Fluconazole (5-15 mg/kg orally every 12 hours for 14-60 days)14 and itraconazole have also proven effective for the treatment of resistant strains of Candida species.

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Parasitic Diseases Trichomoniasis Trichomoniasis, also called “frounce,” is a protozoal disease caused by Trichomonas gallinae (which affects the upper digestive system and respiratory systems) and T. gallinarium (affects the lower digestive tract), and is of major significance in captive and wild birds of prey.25,65,66 Healthy pigeons (Columba livia) and doves (Zenaidura macroura) often harbor the organism. Infections are often reported in captive raptors fed a diet of freshly killed pigeons and wild raptors that primarily prey on pigeons (goshawks, falcons, and a several species of owls).2,5,67 An epornitic of trichomoniasis was reported along a 110-km strip on the Eastern slope of the Rocky Mountains that affected a variety of avian species, including American kestrels and Eastern screech-owls.67 Affected raptors often develop caseous plaques in and around the oropharynx. However, infections within the nasal cavities, infraorbital sinuses, and the syrinx have also been described.65 Dysphagia is a common finding in affected raptors.2 Diagnosis is based on history, clinical signs, and demonstration of the organisms from swabs of the exudate expressed into saline solution. Supportive care (gavage feeding) and treatment with metronidazole (30-50 mg/kg every 24 hours for 5-7 days) or carnidazole (Spartrix; Wildlife Pharmaceuticals, Inc., Fort Collins, CO USA) (30 mg/kg every 12 hours for 3 days; 20-30 mg/kg orally once or 20 mg/kg orally every 24 hours for 2 days) is often effective.2,14,65 Ueblacker67 reported poor success with dimetridazole in some kestrels and suggested that the poor results with nitro-imidazoles at recommended dosages may likely be due to resistance of trichomonad strains.67

Helminths Many species of endoparasites infest both captive and wild birds of prey.68,69 Nematodes are the most common and include capillarids, ascarids, spirurids, and tracheal and air sac nematodes.68,69 Capillaria species infections are usually asymptomatic; however, heavy infestations may cause diarrhea, anorexia, emaciation, listlessness, and death. Capillaria species may also cause oral lesions similar to those seen with trichomonad infections. Ascarids are also common in raptors and include the genera Ascaridia spp., Porrocaecum spp., and Contracaecum spp. Clinical signs of ascarid infections are similar to those seen with Capillaria spp. infections. Syngamus spp. infections infest the respiratory tract and are often associated with respiratory signs. Coughing, dyspnea, and open-mouth breathing can occur as a result of

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cies, a dose of 1.0 mg/kg subcutaneously (repeated in 7-14 days) may be required.70

Coccidia

Figure 3. Serratospiculum species removed from the air sacs of a gyrfalcon X peregrine falcon hybrid after treatment with ivermectin.

inflammation or obstruction of the trachea/bronchi.2,68,69 The filariid nematode Serratospiculum amaculata (Fig 3) has been reported in various species of falcons, including prairie falcons, peregrine falcons, gyr falcons, hybrid falcons, bald eagles, and Cooper’s hawks.68-70 Hawkins and coworkers71 reported an atypical parasitic migration and necrotizing sacral myelitis due to S. amaculata in a prairie falcon.71 Diagnosis of helminthes larvae, is often accomplished by demonstration of ova, larvae, or adult worms within the feces, or in other areas of the gastrointestinal tract. It must be kept in mind that fecal analysis will often reveal ova from parasites that originate from prey consumed by raptors. These must be differentiated from parasites actually infecting the gastrointestinal tract of the raptor. Additionally, serial fecal examinations are recommended, because one negative fecal examination does not necessarily indicate that the bird of prey is free of parasites. There are a variety of antiparasitic agents that can be used to eliminate nematodes, including ivermectin, fenbendazole, levamisole, mebendazole, and piperazine. Fenbendazole may also be used to treat some trematodes and cestodes. However, fenbendazole was suspected as the cause of death of 6 white-backed vultures (Gyps africanus), one lappetfaced vulture (Torgos tracheliotus), and one marabou stork (Leptoptilos crumeniferus) after oral administration in feed at a dose of 47 to 60 mg/kg for 3 days.72 Fenbendazole is also suspected as the cause of death in a North American goshawk (dose unknown) (M. P. Jones, unpublished data, November, 2005). Ivermectin can be administered orally, intramuscularly, or subcutaneously at a dose of 0.2 to 0.4 mg/ kg. For certain parasites, such as Serratospiculum spe-

Coccidian parasites that affect raptors include Caryospora spp., Cryptosporidium spp., Eimeria spp., Frenkelia spp., Sarcocystis spp., and Toxoplasma gondii. Most coccidia are considered to be nonpathogenic in raptors; however, coccidia more commonly affect young raptors or those with a compromised immune system. Clinical signs are usually vague but may include lethargy, depression, diarrhea (with or without blood in the stool), poor body condition, weight loss, or even death. Diagnosis is usually accomplished by demonstrating oocysts in the feces or the organisms in tissue. Therapy for coccidial infestations include sulfadimethoxine (Albon; Pfizer Animal Health, Exton, PA USA) at 25 to 55 mg/kg orally, once daily for 3 to 7 days) (pyrimethamine (Daraprim; Catalytica Pharmaceuticals, Inc., Greenville, NC USA) at 0.5 mg/kg orally, twice daily for 14 to 28 days (especially effective against toxoplasmosis, atoxoplasmosis, and sarcocystis), or toltrazuril (Baycox; Bayer, Leverkusen, Germany) at 7 mg/kg orally, once daily for 2 to 3 days.14

Hemoparasites Leukocytozoon species and Hemoproteus species are seen in both captive and wild birds of prey and may be found in large numbers within the bloodstream with no apparent clinical signs.2,69 Another hemoparasite, Plasmodium spp., is seen in a wide range of avian hosts; however, they are most commonly seen in gyrfalcons and snowy owls (Nyctea scandiaca).2,5 In these species, Plasmodium spp. is of clinical significance and may result in signs of depression, weight loss, labored respiratory effort, anemia, and decreased appetite. Mosquitoes serve as the primary vector for these hemoparasites, and passerines are generally considered to serve as reservoirs.2 Diagnosis is based on clinical signs and the demonstration of the organisms in red blood cells. Note that intraerythocytic gametocytes of Plasmodium spp. and Hemoproteus spp. may appear very similar and can be difficult to distinguish from one another. Treatment of Plasmodium spp. infestations consists of supportive care (fluid therapy, blood transfusions, and diphenhydramine [Benadryl; Elkins-Fin, Inc., Cherry Hill, NJ USA] or steroids if indicated) and the administration of chloroquine (Aralen; Sanofi Winthrop Pharmaceuticals, New York, NY USA) in combination with primaquine. Chloroqine is given initially (the parenteral form is preferred in acute disease states) at 20 mg/kg, then the dose is lowered (10

Infectious Diseases of Birds of Prey

mg/kg orally) for the 6-, 18-, and 24-hour treatments. In addition to the chloroquine, oral primaquine (1 mg/kg) is given every 24 hours for 2 days.1,73 This regimen is repeated as necessary at weekly intervals for 3 to 5 weeks to prevent relapses. Once the bird is stable, a preventive regime of chloroquine (10 mg/kg orally) and primaquine (1 mg/ kg) is given weekly.73 Other treatment regimes include mefloquine HCl (Lariam; Roche Laboratories, Nutley, NJ USA) 30 mg/kg PO given at 0, 12, 24, 48, and 72 hours then weekly for 6 months,73 or quinacrine (Atabrine; Sanofi Winthrop Pharmaceuticals, New York, NY USA) at a dose of 5 to 10 mg/kg intramuscularly once daily for 7 days. Resistance to blood parasites in raptors is generally attributed to genetics or geographic location, although the age of the bird, virulence or strain of the parasite, and level of stress the raptor is experiencing may also play roles in the pathogenesis of blood parasites.74,75 Forrester and coworkers75 reported that the prevalence of Hemoproteus and Leukocytozoon infections in captive raptors was higher than the prevalence in free-flying raptors, suggesting that captive raptors may be more stressed, more immunocompromised, less likely to be able to rid themselves of infection, and therefore more likely to develop low-grade chronic infections than their wild counterparts.75

References 1.

2. 3.

4. 5. 6. 7. 8.

9. 10.

Redig PT: Falconiformes (vultures, hawks, falcons, secretary bird), in Fowler ME (ed): Zoo and Wild Animal Medicine (ed 5). St. Louis, MO, Saunders/ Elsevier Science, Inc., 2005, pp 150-161 Redig PT: Medical Management of Birds of Prey. St. Paul, MN, The Raptor Center, University of Minnesota, 1993 Remple JD: Raptor bumblefoot: a new treatment technique, in Redig PT, Cooper JE, et al (eds): Raptor Biomedicine. Minneapolis, MN, University of Minnesota Press, 1993, pp 154-159 Deem SL: Infectious and parasitic diseases of raptors. Compendium 21:329-337, 1999 Cooper JE: Veterinary Aspects of Captive Birds of Prey (supplement). Sal, Gloucestershire, UK, Standfast Press, 1985 Halliwell WH: Bumblefoot infections in birds of prey. J Zoo Anim Med 6:8-10, 1975 Fitzgerald SD, Simmons HA, Cooley TM: Clinical Challenge. J Zoo Wildl Med 35:251-254, 2004 Portaels F, Realini L, Bauwens L, et al: Mycobacteriosis caused by Mycobacterium genavense in birds kept in a zoo: 11-year survey. J Clin Microbiol 34:319-323, 1996 Tell LA, Woods L, Crome RL: Mycobacteriosis in birds. Rev Sci Tech Off Int Epizoot 20:180-203, 2001 Heidenreich M: Bacterial, chlamydial and mycoplasmal diseases, in Birds of Prey: Medicine and Manage-

15

11.

12. 13.

14. 15. 16.

17.

18. 19.

20.

21.

22. 23. 24.

25.

26. 27.

ment. Malden, MA, Blackwell Science, 1997, pp 114-124 Gerlach H: Bacteria, in Ritchie BW, Harrison BJ, Harrison LR (eds): Avian Medicine: Principles and Applications. Lake Worth, FL, Wingers Publishing, Inc, 1994, pp 949-983 Hoenerhoff M, Kiupel M, Sikarskie J, et al: Mycobacteriosis in an American bald eagle (Haliaeetus leucocephalus). J Wild Dis 48:437-441, 2004 Lumeij JT, Dorrestein GM, Stam JWE, et al: Observations on tuberculosis in raptors, in Cooper JE, Greenwood A (eds): Recent Advances in the Study of Raptor Diseases. Keighly, UK, Chiron Publications, 1980, pp 137-139 Pollock C, Carpenter JW, Antinoff N: Birds, in Carpenter JW (ed): Exotic Animal Formulary (ed 3). St. Louis, MO, Elsevier Inc, 2005, pp 133-344 Samour J: Toxicology, in Samour J (ed): Avian Medicine. Philadelphia, PA, Mosby, 2000, pp 180-193 Graham DL, Halliwell WH: Viral diseases of birds of prey, in Fowler ME (ed): Zoo and Wild Animal Medicine. Philadelphia, PA, WB Saunders, 1986, pp 408-413 Gerlach H: Viruses, in Ritchie BW, Harrison BJ, Harrison LR (eds): Avian Medicine: Principles and Applications. Lake Worth, FL, Wingers Publishing, 1994, pp 862-948 Wernery U: Viral diseases, in Samour J (ed): Avian Medicine. Philadelphia, PA, Mosby, 2000, pp 264-275 Moyer RW, Arif BM, Black DN, et al: Poxviridae, in Van Regenmortel MJV, Fauquet CM, Bishop DHL (eds): Virus Taxonomy, Seventh report of the International Committee on Taxonomy of Viruses. New York, NY, San Diego, CA, Academic Press, 2000, pp 137-157 Tae-Joong K, Schnitzlein WM, McAloose D, et al: Characterization of an avianpox virus isolated from an Andean condor (Vultur gryphus). Vet Microbiol 96:237-246, 2003 Krone O, Essbauer S, Wibbelt G, et al: Avipoxvirus infection in peregrine falcons (Falco peregrinus) from a reintroduction programme in Germany. Vet Rec 154:110-113, 2004 Bolte A, Meurer J, Kaleta EF: Avian host spectrum of avipoxvirus. Avian Pathol 28:415-432, 1999 Morishita TY, Itchon CS, Brooks DL: Herpesvirus infections in raptorial birds, in Proc Assoc Avian Vet 1994; 69-75 Gough RE, Capua I, Wernery U: Herpesvirus infections in raptors, in Lumeij JT, Remple JD, Redig PT, et al (eds): Raptor Biomedicine III. Lake Worth, FL, Zoological Education Network, Inc., 2000, pp 9-11 Remple JD: Considerations on the production of a safe and efficacious falcon herpesvirus vaccine, in Lumeij JT, Remple JD, Redig PT, et al (eds): Raptor Biomedicine III. Lake Worth, FL, Zoological Education Network, Inc., 2000, pp 9-11 Ritchie BW (ed): Avian Viruses Function and Control. Lake Worth, FL, Wingers Publishing, 1995 Manvell RT, Wernery U, Alexander DJ, et al: Newcastle disease (Avian PMV-1) viruses in raptors, in Lumeij JT, Remple JD, Redig PT, Lierz M, Cooper JE (eds): Raptor Biomedicine III Including Bibliography of Diseases of Birds of Prey. Lake Worth, FL, Zoological Education Network, 2000

Jones

16 28. 29.

30.

31. 32.

33. 34. 35. 36.

37.

38.

39.

40. 41.

42.

43. 44.

45.

Wernery U: Viral diseases, in Samour JH (ed): Avian Medicine. London, UK, Mosby, 2000, pp 264-275 West Nile virus: statistics, surveillance and control. Available at: http://www.cdc.gov/ncidod/dvbid/ westnile/surv&control.htm. Accessed October 21, 2005. Jerzak G, Bernard KA, Kramer LD, et al: Genetic Variation in West Nile Virus from naturally infected mosquitoes and birds suggest quasispecies structure and strong purifying selection. J Gen Virol 86:21752183, 2005 Phalen DN, Dahlhausen B: West Nile virus. Sem Avian Exotic Pet Med 13:67-78, 2004 Facts about West Nile Virus, University of Minnesota Raptor Center. Available at: http://www.raptor.cvm. umn.edu/content.asp?page⫽9002. Accessed October 21, 2005. Gibbs SEJ, Ellis AE, Mead DG, et al: West Nile virus detection in the organs of naturally infected blue jays (Cyanocitta cristata). J Wildl Dis 41:354-362, 2005 McLean RG, Ubico SR, Docherty DE, et al: West Nile virus transmission and ecology in birds. Ann NY Acad Sci 951:54-57, 2001 Komar N: West Nile virus encephalitis. Revue Sci Tech 19:166-176, 2000 Wünschmann A, Shivers J, Bender J, et al: Pathologic and immunohistochemical findings in goshaws (Accipiter gentilis) and great horned owls (Bubo virginianus) naturally infected with West Nile virus. Avian Dis 49:252-259, 2005 Wünschmann A, Shivers J, Bender J, et al: Pathologic findings in red-tailed hawks (Buteo jamaicensis) and Cooper’s hawks (Accipiter cooperi) naturally infected with West Nile virus. Avian Dis 49:570-580, 2004 Sardelis MR, Turell MJ, Dohm DJ, et al: Vector Competence of Selected North American Culex and Coquillettidia Mosquitoes for West Nile Virus. Emerg Infect Dis [serial online], 2004. Available at: http:// www.cdc.gov/ncidod/eid/vol7no6/sardelis.htm. Accessed October 21, 2005. Tesh RB, Siirin M, Guzman H, et al: Persistent West Nile virus infection in the golden hamster: studies on its mechanism and possible implications for other Flavivirus infections. J Infect Dis 192:287-295, 2005 Malkinson M, Banet C: The role of birds in the ecology of West Nile virus in Europe and Africa. Curr Top Microbiol Immun 267:309-322, 2001 Rapid antigen capture assay to detect West Nile virus in dead corvids. Available at: http://www.raptor. cvm.umn.edu/img/assets/16863/West_Nile-Raptor_ Release_Article.pdf. Accessed October 21, 2005. Lindsay R, Barker I, Hayar G, et al: Rapid antigen capture assay to detect West Nile virus in dead corvids. Emerg Infect Dis [serial online], 2003. Available at: http://www.cdc.gov/ncidod/EID/vo19no11/030318.htm, 2003. Accessed October 21, 2005. Komar N, Laniciotti R, Bowen R, et al: Detection of West Nile virus in oral and cloacal swabs collected from bird carcasses. Emerg Inf Dis 8:741-742, 2003 Johnson AJ, Langevin S, Wolff KL, et al: Detection of anti-West Nile virus immunoglobulin M in chicken serum by an enzyme-linked immunosorbent assay. J Clin Microbiol 41:2002-2007, 2003 Gancz AY, Campbell DG, Barker IK, et al: Detecting

46.

47.

48.

49. 50. 51. 52. 53. 54.

55. 56.

57. 58.

59. 60. 61.

62.

63.

West Nile virus in owls and raptors by an antigen-capture assay. Emerg Infect Dis 10:22042206, 2004 Stone WB, Okoniewski JC, Therrien JE, et al: VecTest as a diagnostic and surveillance tool for West Nile virus in dead birds. Emerg Infect Dis 10:2175-2181, 2004 Steele KE, Linn MJ, Schoepp RJ, et al: Pathology of fatal West Nile virus infection in native and exotic birds during the 1999 outbreak in New York City, New York. Vet Pathol 37:208-224, 2000 Nusbaum KE, Wright JC, Johnston WB, et al: Absence of humoral response in flamingos and redtailed hawks to experimental vaccination with a killed West Nile virus vaccine. Avian Dis 47:750-752, 2003 Van Borm S, Thomas I, Hanquet G, et al: Highly pathogenic H5N1 Influenza virus in smuggled Thai eagles, Belgium. Emerg Infect Dis 11:702-705, 2005 Magnino S, Fabbi M, Moreno A, et al: Avian influenza virus (H7 serotype) in a saker falcon in Italy. Vet Rec 17:740, 2000 Schrenzel M, Oaks JL, Rotstein D, et al: Characterization of a new species of adenovirus in falcons. J Clin Microbiol 43:3402-3413, 2005 Oaks JL, Schrenzel M, Rideout, et al: Isolation and epidemiology of falcon adenovirus. J Clin Microbiol 43:3414-3420, 2005 Deem SL: Fungal diseases of birds of prey. Vet Clin North Am (Exotic Anim Pract) 6:363-376, 2003 Bauk L: Mycoses, in Ritchie BW, Harrison BJ, Harrison LR (eds): Avian Medicine: Principles and Applications. Lake Worth, FL, Wingers Publishing, 1994, pp 997-1006 Redig PT: Avian aspergillosis, in Fowler ME (ed): Zoo and Wild Animal Medicine. Current Therapy 3. Philadelphia, PA, WB Saunders, 1993, pp 178-181 Abrams GA, Paul-Murphy J, Ramer JC, et al: Aspergillus blepharitis and dermatitis in a peregrine falcongyrfalcon hybrid (Falco peregrinus x Falco rusticolus). J Avian Med Surg 15:114-120, 2001 Jones MP: The diagnosis of aspergillosis in birds. Sem Avian Exotic Pet Med 9:52-58, 2000 Redig PT: Mycotic infections of birds of prey, in Fowler ME (ed): Zoo and Wild Animal Medicine. Philadelphia, PA, W.B. Saunders Company, 1986, pp 420-424 Jones MP, Orosz SE, Cox SK, et al: Pharmacokinetic disposition of itraconazole in red-tailed hawks (Buteo jamaicensis). J Avian Med Surg 14:15-22, 2000 Orosz SE: Antifungal drug therapy in avian species. Vet Clin North Am (Exotic Anim Pract) 6:337-350, 2003 Di Somma A, Bailey TA, Silvanose C, et al: The use of voriconazole for the treatment of aspergillosis in falcons. Proc Societa’ Italiana Veterinari Animali Esotici, Rome, Italy, 2004 Langenberg JA: Emerging antifungals and the use of voriconazole with amphotericin to treat aspergillus. Proceedings of the Annual Conference of the Association of Avian Veterinarians, New Orleans, LA, August, 2004, pp 21-24 Samour JH, Naldo JL: Diagnosis and therapeutic management of candidiasis in falcons in Saudi Arabia. J Avian Med Surg 16:129-132, 2002

Infectious Diseases of Birds of Prey 64. 65. 66. 67.

68.

69.

Groll AH, Piscitelli SC, Walsh TJ: Antifungal pharmacodynamics: concentration-effect relationships in vitro and in vivo. Pharmacotherapy 21:133S-485S, 2001 Samour JH, Naldo JL: Diagnosis and therapeutic management of trichomoniasis in falcons in Saudi Arabia. J Avian Med Surg 17:136-143, 2003 Zucca P: Protozoa, in Samour JH (ed): Avian Medicine. Philadelphia, PA, Mosby, 2000, pp 225-231 Ueblacker SN: Trichomoniasis in American kestrels (Falco sparverius) and Eastern screech-owls (Otus asio), in Lumeij JT, Remple JD, Redig PT, et al (eds): Raptor Biomedicine III. Lake Worth, FL, Zoological Education Network, 2000, pp 59-63 Smith SA: Diagnosis and treatment of helminths in birds of prey, in Redig PT, Cooper JE, Remple JD, et al (eds): Raptor Biomedicine. Minneapolis, MN, The University of Minnesota Press, 1993, pp 21-27 Lacina D, Bird DM: Endoparasites of raptors—a review and an update, in Lumeij JT, Remple JD, Redig PT, et al (eds): Raptor Biomedicine III. Lake Worth, FL, Zoological Education Network, 2000, pp 65-99

17 70. 71.

72.

73. 74. 75.

Samour JH, Naldo J: Serratospiculumin captive falcons in the Middle East: a review. J Avian Med Surg 15:2-9, 2001 Hawkins MG, Couto S, Tell LA, et al: Atypical parasitic migration and necrotizing sacral myelitis due to Serratospiculoides amaculata in a prairie falcon (Falco mexicanus). Avian Dis 45:276-283, 2001 Bonar CJ, Lewandowski AH, Schaul J: Susptected fenbendazole toxicosis in two vulture species (Gyps africanus, Torgos tracheliotus) and marabou storks (Leptoptilos crumeniferus). J Avian Med Surg 17:16-19, 2003 Joseph V: Emergency care of raptors. Vet Clin North Am (Exotic Anim Pract) 1:77-98, 1998 Ziman M, Colagross-Schouten A, Griffey S, et al: Haemoptroteus spp. and Leukocytozoon spp. in captive raptor populations. J Wildl Dis 40:137-140, 2004 Forrester DJ, Sam TR, Foster JR, et al: Blood parasite of raptors in Florida. J Raptor Res 28:226-231, 1994