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An Outbreak of Chlamydophila psittaci in an outdoor colony of Magellanic penguins (Spheniscus magellanicus).

Abstract: An outbreak of Chlamydophila psittaci occurred in an outdoor colony of 63 Magellanic penguins (Spheniscus magellanicus) at the San Francisco Zoo. Affected penguins presented with inappetence, lethargy, and light green urates. Hematologic and serum biochemical findings were consistent with chronic inflammation. Penguins did not respond to initial supportive and antimicrobial therapy, and 3 died. Necropsy results of the 3 birds revealed hepatomegaly and splenomegaly, and histologic lesions included necrotizing hepatitis, splenitis, and vasculitis. Chlamydophila psittaci infection was confirmed by results of Gimenez staining, immunohistochemistry, and tissue polymerase chain reaction assay. As additional birds continued to present with similar clinical signs, the entire colony of penguins was prophylactically treated with a 30-day minimum course of doxycycline, administered orally or intramuscularly or as a combination of both. Despite treatment, 9 additional penguins died during a 3-month period. Pathologic results from these birds revealed renal and visceral gout (n = 4), cardiac insufficiency (n = 2), sepsis from a suspected esophageal perforation (n = 2), and no gross lesions (n = 1). During the outbreak, 4 birds presented with seizures, 5 developed dermatitis, and nearly 90% of birds in the colony showed severe keratoconjunctivitis, believed to be related to drug therapy with doxycycline. We report the clinical and pathologic features of Chlamydophila psittaci infection in an outdoor colony of penguins and the associated challenges of treatment.

Key words: avian chlamydiosis, dermatitis, keratoconjunctivitis, Chlamydophila psittaci, doxycycline, avian, Magellanic penguins, Spheniscus magellanicus

Clinical Report

Since 1984, the San Francisco Zoo has housed a successful breeding colony of Magellanic penguins (Spheniscus magellanicus) in an outdoor exhibit. The colony has to date successfully hatched and raised 182 chicks and comprised, at the time of this report, 63 penguins. The outdoor exhibit consists of an island (133 [m.sup.2]) surrounded entirely by a pool of water (340 [m.sup.3]). The pool is filled with a combination of city and groundwater and is emptied and refilled once weekly for thorough cleaning. The primary diet is herring that are handfed to each bird twice daily. Penguins receive nutritional supplements consisting of salt tablets (15 grain PO 3 times/wk), thiamine (500 mg PO 6 times/wk), vitamin E (600 IU PO 3 times/wk), and multivitamins (1 tablet PO q56h) (Vita-Zu Bird Tablet, PMI Nutrition International, LLC, St Louis, MO, USA). Because of a preventive medicine program based on periodic antifungal and antimalarial prophylactic treatments and mosquito control within the colony, aspergillosis and malaria had not been disease concerns in recent years. Additionally, no confirmed cases of West Nile Virus have been identified at the San Francisco Zoo.

In January 2005, 9 penguins presented with acute lethargy, inappetence or anorexia, and light green urates. The birds were hospitalized and initially treated with a protocol of force-feeding, subcutaneous fluids, primaquine (3.75 mg with chloroquine 50 mg PO q24h) and fluconazole (100 mg PO q12-24h). Blood samples were initially collected from each bird for a complete blood cell count (CBC), serum biochemical analysis, Aspergillus titer, serum protein electrophoresis, and West Nile virus polymerase chain reaction (PCR) and serologic testing (Table 1). Aerobic and anaerobic cultures of cloacal swab samples were also performed (Table 1). Based on the clinical presentations, histories, and diagnostic test results, enrofloxacin (15 mg/kg PO q12-24h) (Baytril, Bayer HealthCare LLC, Shawnee Mission, KS, USA) was added to the treatment regime.

Despite treatment, 3 birds died and gross postmortem and histopathologic findings revealed lesions consistent with avian chlamydiosis (Table 1). A Gimenez stain performed on sections from the 3 birds revealed minute magenta bodies in the cytoplasm of inflammatory cells, consistent with elementary bodies of Chlamydophila psinaci (Figs 1 and 2). Immunohistochemistry results for C psittaci were positive in 1 bird (Fig 2). Additionally, results of tissue PCR analysis for C psittaci confirmed the diagnosis of avian chlamydiosis in all 3 penguins. Multiple diagnostic testing methods for C psittaci were performed on a subset of the remaining penguins of the colony, including PCR analysis of choanal/cloacal/fecal swabs, environmental swabs, and whole blood samples, as well as serologic testing by direct complement fixation (DCF) and elementary body agglutination (EBA) (Table 1). Results were consistent with a colony-wide exposure to, shedding of, and environmental contamination with C psittaci. Testing by EBA was discontinued because results were suggestive of low test sensitivity. Overall, rising or persistently elevated titers were not demonstrated in the colony by subsequent monthly serologic testing over a 3-month period.

All penguins were considered exposed to C psittaci and were, therefore, prophylactically treated. Quarantine protocols were established to protect the other birds in the collection as well as the zoo personnel caring for the penguins (environmental cleaning, coveralls/slickers, masks, caps, gloves, boots, and foot baths). The entire flock was treated with oral doxycycline hyclate to reduce shedding and treat clinical cases. An equal dose of doxycycline for all the birds was determined based on their average weight (weight range, 3-6 kg). An initial dosage of 100 mg/bird PO q24h (dosage range, 17-33 mg/kg) was administered. That dose was then doubled to 200 mg because of inconsistent initial treatment response. However, two-thirds of the colony experienced clinical side effects after 5 days, primarily inappetence, and the dose was reduced to 100 mg/bird. In the birds that remained inappetent at that dose or for birds with further episodes of anorexia, a long-lasting injectable form of doxycycline (50-75 mg/kg IM q7d) was given in alternate sites in combination with subcutaneous fluid administration. The overall treatment was given for 30 days minimum, with 18 birds receiving a combination of oral and injectable doxycycline. Fluconazole (100 mg PO q24h) was also given to the birds prophylactically to prevent opportunistic fungal infection, (1,2) and avian malarial prophylaxis was also maintained. Because of the differences in appetite and, therefore, consistency of medicating, each penguin finished the doxycycline treatment at different times.

During the outbreak and the treatment period, 4 birds presented with seizures, 2 of which died and were submitted for necropsy and histopathologic examination (Table 1). Additionally, 50 birds showed severe keratoconjunctivitis (Fig 3) with serous to purulent conjunctival exudate, chemosis, and variable degrees of corneal edema. The eyes were treated topically with a saline eyewash followed by the application of an ophthalmic lubricant. For these birds, PCR testing and cytologic examination of conjunctival swab samples were negative for C psinaci (Table 1). In the 7 additional penguins that subsequently died during the outbreak, tissue samples of conjunctiva and salt glands were also submitted for histopathologic examination (Table 1). Five birds with ocular lesions also presented with varying severity of dermatitis along the legs and dorsal feet after completing the doxycycline treatment protocol. They were treated with nonsteroidal anti-inflammatory drugs, either ketoprofen (2 mg/kg IM PRN) (Ketofen, Fort Dodge Animal Health, Fort Dodge, IA, USA) or carprofen (2 mg/kg PO q12h) (Rimadyl, Pfizer Animal Health, Exton, PA, USA) and topical zinc oxide. Histologic examination of biopsy samples from the feet of the most-affected penguin revealed severe ulceroproliferative dermatitis with superficial bacterial colonies (Table 1). The dermatitis resolved over an average of 3-4 weeks after beginning treatments.


Complete blood cell counts, protein electrophoresis, and Aspergillus antibody titers were repeated at 1 and 2 months after initiating treatment in 16 penguins. Random fecal samples collected periodically from the exhibit and 2 environmental swab samples were submitted for C psittaci PCR testing. The CBC results consistently showed moderate leukocytosis despite treatment. Although aspergillosis was not confirmed or supported by radiographs or necropsy results in the 12 birds that died, laboratory test results raised the suspicion of fungal infections and the frequency of fluconazole administration was increased to twice daily. All random fecal sample results were PCR positive for C psittaci and remained so 2 weeks into the doxycycline treatment of the colony, after which the results were negative. To date, there have been no further positive results of fecal, choanal, or cloacal samples. The zoo continues to randomly test fecal samples from birds housed on the island.



A total of 12 birds died during the outbreak. The first 3 deaths were the only fatalities confirmed to be caused by systemic infection with C psittaci. Additional diagnoses that were confirmed by necropsy and histopathologic examination were visceral gout, myocardial degeneration and insufficiency, and severe esophagitis (Table 1).

In an attempt to identify potential environmental or toxicologic factors promoting this outbreak of avian chlamydiosis, multiple areas of the penguins' exhibit were sampled. Among the samples analyzed were the pool water, the supply of fish used as food, and the algae found in the pool. Fish samples were submitted to the California Animal Health and Food Safety Laboratory System, Davis Laboratory, University of California, Davis (CA, USA) for metals, organochlorine insecticide, and polychlorobiphenyls analysis (Table 1). Pool water and algae samples were also submitted for analysis for microcystins, which are hepatotoxic peptides produced by certain strains of freshwater cyanobacteria, to the Wright State University, Department of Biological Sciences, Process Development Center for Biomolecules (Dayton, OH, USA) (Table 1). Chronic ingestion of microcystins has been associated with hepatic and gastrointestinal disorders (W. Carmichael, oral communication, March 2010). (3,4) A liver sample from one of the deceased penguins was also submitted for microcystin analysis by enzyme-linked immunosorbent assay (ELISA), results of which were negative (Table 1). (5) Further toxicologic testing was performed on tissues from 2 penguins that were submitted to the California Animal Health and Food Safety Laboratory System, Davis Laboratory, for vitamin E, heavy metal, vitamin A, and selenium levels (Table 1). Overall, environmental and food testing failed to identify potential, predisposing factors for the emergence of C psittaci in this penguin colony.


In this report, we document the first occurrence, to our knowledge, of an outbreak of C psittaci in a captive colony of penguins and the challenges of its management. Confirmation of infection was difficult and multiple testing modalities were used for the diagnosis, management, and follow-up, including histopathologic examination, histochemical staining, immunohistochemistry, PCR testing of different biological samples, and serologic testing by EBA and DCF. Environmental and dietary exposures to a variety of toxins were also investigated. A 30-day minimum course of doxycycline was found effective in treating the colony, even though several adverse effects were encountered.

Common medical problems diagnosed in penguin colonies maintained in zoologic collections are aspergillosis, avian malaria, bumblefoot, and vital encephalitis. (6-12) Avian chlamydiosis is a contagious, zoonotic, systemic, and occasionally fatal disease caused by the obligate intracellular bacteria C psittaci. Chlamydophila psittaci occurs worldwide, and multiple chlamydial disease outbreaks have been reported in commercial, pet, and wild birds. (13-15) Published reports indicate that birds from more than 400 avian species from 30 orders, including Sphenisciformes, have tested positive by C psittaci antigen or antibody testing. (16) Positive titers have been documented in free-ranging penguins, including rockhopper penguins (Eudyptes chrysocome), emperor penguins (Aptenodytes forsteri), a gentoo penguin (Pygoscelis papua), an Adelie penguin (Pygoscelis adeliae), and Galapagos penguins (Spheniscus mendiculus). (17,18) However, clinical disease and management have not been reported in captive penguins, to our knowledge.

The 3 zoo penguins that had confirmed avian chlamydiosis by histopathologic testing were originally from other zoologic institutions before their arrival at the San Francisco Zoo. Additionally, some penguins that were wild caught may have been latently infected with C psittaci before the outbreak. Common reservoirs of C psittaci in the United States include sea gulls (Laridae), ducks (Anatidae), herons (Ardeidae), egrets (Ardeidae), pigeons (Columba livia), blackbirds (Icteridae), grackles (Quiscalus species), house sparrows (Passer domesticus), and killdeers (Charadrius vociferus). (14) Chlamydial strains are very host specific, and although mild to moderate clinical signs are seen in the natural host, severe and fatal diseases may be observed in secondary hosts. (13) Modes and dynamics of transmission in wild birds are largely unknown but are suspected to occur by a relatively simple process, such as oral transmission. (13) Gulls and pigeons are frequent uninvited guests on Penguin Island (San Francisco Zoo) and these free-ranging birds may have introduced C psittaci to the colony. During the outbreak reported here, prophylactic measures were initiated to minimize shedding, disease transmission, and development of carrier status by the birds.

In addition, several factors may influence the susceptibility to infection and disease. Environmental changes and concurrent infections may activate persistent infections and increase susceptibility to avian chlamydiosis. (13,15) The pathogenesis and infection cycle of C psittaci have been reviewed elsewhere and should be consulted for more detailed information. (l,13-15,19,20) The typical colony size of Penguin Island (San Francisco Zoo) has historically been 50-55 birds. Before the outbreak, the colony population was 63 birds. Overpopulation on the island may have increased stress in the colony and could have led to activation of latent C psittaci infections. (1) In addition, this outbreak occurred during breeding season, a normally stressful time for captive penguins. The colony went through a normal, although delayed a few weeks, breeding season. Other environmental factors that may have promoted the emergence of clinical avian chlamydiosis in this colony were investigated by water quality and toxicologic analysis, but none could be identified. The water sample tested was positive for microcystins, and several potential microcystin-producing cyanobacteria were identified. No data are available, to our knowledge, on the toxicity of microcystins in penguins but, as in other species, chronic ingestion could cause low-level liver and gastrointestinal insults. However, one penguin liver sample was negative for the presence of microcystins, and no histologic findings consistent with microcystin toxicosis could be found. Finally, most of the birds that died were either older or originated outside the San Francisco Zoo. Of the 12 birds that succumbed to disease, all but one was older than 14 years. Of the deceased birds, 5 were wild caught in 1984, 2 were hatched at the San Francisco zoo, and 5 were hatched at other institutions.

Gross and histologic lesions in 3 of the penguins were typical of avian chlamydiosis. (1,13,14) Chlamydial antigen was identified by immunohistochemistry in the lesions, and a PCR assay on hepatic tissue identified DNA from C psittaci. The antemortem diagnosis of avian chlamydiosis can be challenging and has never been documented in captive penguins, to our knowledge. In this outbreak, the diagnosis was confirmed based on histopathologic results from the dead penguins. Multiple testing was also instituted in an attempt to further investigate the epidemiology of the outbreak and to establish reference values for this colony of Magellanic penguins (Table 1). The fecal PCR testing was useful to determine shedding status and to identify potentially infected birds because positive results were seen until colony-wide treatment with doxycycline was instituted. Blood samples were tested by PCR assay in 34 birds, and only one result was found positive. Negative blood PCR results can occur in birds undergoing antimicrobial treatments. (21) Serologic testing of blood samples by DCF and EBA was also performed, and results were generally questionable in differentiating between exposure and infection during this outbreak. Direct complement fixation can be useful as a diagnostic test for exposure to C psittaci because it is specific for immunoglobulin (Ig) Y/IgG antibodies, indicative of the chronic phase of disease. (21) Nearly all the penguins had a positive titer. Conversely, EBA testing measures IgM antibodies, which are indicators of acute infection. (21) However, EBA was considered a test of low sensitivity in this outbreak, with positive results in only 5 birds. As with the DCF test, the value of the EBA for diagnosing avian chlamydiosis has not been determined in penguins, to our knowledge. To better interpret and diagnose chlamydiosis outbreaks, further work is required to establish accurate antemortem diagnostic screening protocols for penguins.

Clinical sequelae from either avian chlamydiosis or the doxycycline treatment were numerous and included prolonged anorexia, seizures, keratoconjunctivitis, and dermatitis of the dorsum of feet. Seizures have been reported with avian chlamydiosis (1,19) and may have been caused by other diseases in these penguins as suggested by the postmortem results. In the birds with keratoconjunctivitis, laboratory tests did not demonstrate the presence of C psittaci in the ophthalmic samples submitted. Considering these birds were under treatment, these could have been false-negative results. Keratoconjunctivitis is a frequent presentation of avian chlamydiosis in other bird species. (1,15,22) In humans, doxycycline has been associated with photosensitivity reactions, but that side effect has infrequently been reported in birds. (2) It was difficult to determine whether the infection or the doxycycline treatment was responsible for these ocular signs. However, the leg dermatitis was likely caused by photosensitization induced by the doxycycline. Interestingly, all 5 birds affected with dermatitis were either 1 or 2 years old. These birds accounted for one-third of the birds within this age range in which increased skin susceptibility was suspected. Additionally, 2 other penguins died from severe esophagitis and suspected sepsis from esophageal perforations. Many of the sickest birds were either being tube fed or force fed fish daily. Oral doxycycline has also been implicated in causing severe esophagitis and strictures in animals from retention of pills or capsules sticking on the wall of the esophagus. (2,23,24) A combination of local irritation from the doxycycline capsules as well as potential physical trauma from force feeding may have contributed to these 2 deaths. Nevertheless, the 30-day treatment with doxycycline appeared effective at improving the colony clinically as well as in halting the shedding of the organism.

In conclusion, the diagnosis and treatment of avian chlamydiosis in a penguin colony of 63 birds presented challenges, particularly because of the zoonotic potential of the organism. Zoo veterinarians should be aware of C psittaci as a potential disease problem in penguins, and avian chlamydiosis should be included in the differential diagnosis of any sick penguin. Avian chlamydiosis testing should also be part of the general health screening of penguins before exchange between zoologic institutions. In this report, we also highlight the need for more-specific and combined testing modalities to confirm avian chlamydiosis in penguins and to differentiate it from other common diseases of similar clinical presentation in birds from this order.

Acknowledgments: We gratefully acknowledge the penguin keepers and hospital staff for their hard work and dedication through those trying times. The San Francisco Zoo wishes to acknowledge Lynn Dustin, VMD, for her generous contribution of numerous vials of injectable doxycycline.


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Jacqueline E. Jencek, DVM, Hugues Beaufrere, Dr Med Vet, Dipl ECZM (Avian), Thomas N. Tully Jr, DVM, MS, Dipl ABVP (Avian), Dipl ECZM (Avian), Michael M. Garner, DVM, Dipl ACVP, Freeland H. Dunker, DVM, and Timothy V. Baszler, DVM, Dipl ACVP

From the San Francisco Zoo, One Zoo Rd, San Francisco, CA 94! 32, USA (Jencek); the Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Skip Bertman Dr, Baton Rouge, LA 70803, USA (Beaufrere, Tully); Northwest ZooPath, 654 W Main, Monroe, WA 98272, USA (Garner); the Steinhart Aquarium, 55 Music Concourse Dr, San Francisco, CA 94118, USA (Dunker); and the Washington Animal Disease Diagnostic Laboratory, College of Veterinary Medicine, Washington State University, Stadium Way and Grimes Way, Pullman, WA 99164, USA (Baszler).
Table 1. Diagnostic tests performed on clinical and environmental
samples during an outbreak of avian chlamydiosis in  a colony of
63 Magellanic penguins. Diagnostic tests performed are presented
in chronologic order. Follow-up and subsequent screening testing
are not reported.

Diagnostic test          Sample        n             Results

CBC, cells/L          Whole blood       9   WBC, 20,000-60,000
                                            (reference range,
                                            6,200-17,800) (a);
                                            relative heterophilia;
                                            toxic heterophils

Serum biochemical     Serum             9   Elevated TP, 6.5-9.0
analysis                                    g/dL (reference range,
                                            4.8-6.8 g/dL) (a)
                                            AST, moderate increase
                                            in 5 birds
                                            Uric acid, moderate
                                            increase in 3 birds

Aspergillus           Serum             9   Negative
species titer

Protein               Serum             9   [gamma] globulins,
electrophoresis,                            1.92-2.01 (reference
g/dL                                        range, 0.51_0.9) (b)
                                            [beta] globulins, 1.5-3.0
                                            (reference range,
                                            0.5-0.99) (b)

West Nile virus
PCR                   Whole blood       9   Negative
SN titer              Serum             9   Negative

Bacterial culture     Cloacal swabs     9   Enterococcus species,
                                            Escherichia coli,
                                            Corynebacterium species,
                                            Proteus mirabilis

psittaci testing
PCR                   Tissues           3   Positive
                      Choanal-         34   Positive

                      Conjunctival     50   Negative
                      Blood            34   1 positive (retested
                                            negative at 3 and 5 wk)
                      Environmental     2   Positive
                      swabs                 1 : 80 (n = 1)
                                            1 : 20 (n = 4)
                                            >1 : 10(n = 38)

EBA (titer)           Serum            43   1 : 64 (n = 38, 2 banked
                                            1 : 16 (n = 5, 1 banked

DCF (titer)           Serum            47   Negative (n = 4, 1 banked

First set of          --                3   Hepatomegaly,
necropsy/                                   splenomegaly, serosal
histopathologic                             petechiae, congested
findings                                    lungs, fibrinonecrotic
                                            splenitis, hepatitis,

Gimenez stain                           3   Positive
Chlamydophila                           1   Positive
psittaci IHC

Second set of         --                9   Severe visceral gout
necropsy/                                   (n = 4), moderate
histopathologic                             myocardial degeneration
findings                                    (n = 1), severe
                                            esophagitis with
                                            perforation (n = 2),
                                            severe ulcerative and
                                            conjunctivitis with focal
                                            ulcerative keratitis
                                            (n = 5)

Histopathology        Skin (feet)       1   Severe ulceroproliferative
(biopsy)                                    dermatitis with keratin,
                                            cellular crusts and
                                            superficial bacterial
Metals (As, Cd, Cu, FeFood (fish)      NA   Negative
Mn, Mo, Pb, Zn)       Tissues           2   Negative
Organochlorine        Food (fish)      NA   Negative
PCB                   Food (fish)      NA   Negative
Microbiology          Pool water,      NA   Potential microcystin-
testing               algae                 producing cyanobacteria
Microcystin           Pool water,      NA   4.87 (reference range,
(ELISA), [micro]g/L   algae                 [less than or equal to] 1)
                      Liver             1   Negative
Vitamins E, A;        Tissues           2   Negative (no toxic levels)
Se, Pb, Hg

Abbreviations: CBC, complete blood cell count; WBC, white blood cell
count; TP, total protein; AST, aspartate aminotransferase; PCR,
polymerase chain reaction; EBA, elementary body agglutination; DCF,
direct complement fixation; IHC, immunohistochemistry; ELISA,
enzyme-linked immunosorbent assay; SN, serum neutralization; As,
arsenic; Cd, cadmium; Cu, copper; Fe, iron; Hg, mercury; Mn,
 manganese; Mo, molybdenum; Pb, lead; Zn, zinc; PCB,
polychlorobiphenyls; NA, not applicable; Se, selenium.

(a) International Species Information System (reference ranges,
March 2002). ISIS Web site. Accessed on
March 2, 2011.

(b) Avian and Wildlife Laboratory, University of Miami, Miller School
of Medicine, Miami, FL 33136, USA.

(c) Wright State University, Department of Biological Sciences,
Process Development Center for Biomolecules, Dayton, OH 45435, USA.
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Title Annotation:Clinical Reports
Author:Jencek, Jacqueline E.; Beaufrere, Hugues; Tully, Thomas N., Jr.; Garner, Michael M.; Dunker, Freelan
Publication:Journal of Avian Medicine and Surgery
Article Type:Clinical report
Geographic Code:1USA
Date:Dec 1, 2012
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