Compendium of measures to control Chlamydophila psittaci (formerly Chlamydia psittaci) infection among humans (psittacosis) and pet birds, 2005

Psittacosis, also known as parrot fever and ornithosis, is a bacterial infection of humans that can cause severe pneumonia and other serious health problems. It is caused by Chlamydophila psittaci, formerly known as Chlamydia psittaci. From 1988 through 2003, 935 human cases of psittacosis were reported to the CDC and most resulted from exposure to infected pet birds, usually cockatiels, parakeets, parrots, and macaws. In birds, C. psittaci infection is referred to as avian chlamydiosis. Infected birds shed the bacteria through feces and nasal discharges, and humans become infected from exposure to these materials. This compendium provides information about psittacosis and avian chlamydiosis to public health officials, physicians, veterinarians, the pet bird industry, and others concerned with controlling these diseases and protecting public health. The recommendations in this compendium provide standardized procedures for controlling avian chlamydiosis in birds, a vital step to protecting human health. This document will be reviewed and revised as necessary.     

Enigmatic psittacine chlamydiosis: results of serotesting and isolation attempts, 1978 through 1983, and considerations for the future

From 1978 through 1983, chlamydiosis was diagnosed by isolation of Chlamydia psittaci from various types of psittacine birds. The organism was isolated from 126 (30.4%) of 414 tissue specimens, with the percentages ranging from 12.5% (budgerigars) to 42.8% (cockatiels), excluding 2 parakeets with 1 isolation (50%). From 1,035 cloacal swab/feces specimens, 51 (4.9%) isolations were made, ranging from 1.4% from African grays (1 of 70) to 27.8% from lovebirds (5 of 18). Positive direct microscopic examination of stained (Gimenez method) tissue impressions correlated with positive isolation at a rate of 79.2% and those found negative by direct examination had a correlation of 87.5%. Direct complement-fixation testing was done on 3,485 sera. Forty-six were unsatisfactory for testing due to their being anticomplementary or reacting with control antigen. The distribution of titers ranged from 2,008 (57.6%) at 8 to 76 (2.2%) at greater than or equal to 256. In serotests and isolation attempts from the same bird, there was 42.8% agreement between titers greater than or equal to 32 and positive isolation. One cockatiel with a complement-fixation titer of 16 yielded a positive isolation, whereas other types of birds with a less than or equal to 16 titer were negative.     

Feather-picking psittacines: histopathology and species trends

Histologic findings are described for 408 feather-picking or self-mutilating psittacines with the use of biopsies from clinically affected and unaffected skin. Inflammatory skin disease was diagnosed in 210 birds, and traumatic skin disease was diagnosed in 198 birds. Criteria used for the diagnosis of inflammatory skin disease included the presence of perivascular inflammation in the superficial or deep dermis of clinically affected and unaffected sites. The primary histologic criteria for the diagnosis of traumatic skin disease were superficial dermal scarring with or without inflammation in the affected sites and an absence of inflammation in the unaffected sites. The inflammatory cells associated with the lesions were typically lymphocytes and occasionally plasma cells, histiocytes, and granulocytes. A preponderance of inflammatory skin disease was seen in macaws (Ara spp.) and Amazon parrots (Amazona spp.). A preponderance of traumatic skin disease was seen in cockatoos (Cacatua spp.) and African grey parrots (Psittacus erithacus). The prevalence of each was approximately equal in several other species, including conures (Aratinga and Pyrrhura spp.), eclectus parrots (Eclectus roratus), quaker parrots (Myiopsitta monachus), cockatiels (Nymphicus hollandicus), parakeets (Cyanorhamphus and Psittacula spp.), and caiques (Pionites spp.). No geographic or gender-based trends were identified. These findings could be helpful for identifying and treating birds with feather-picking disorders.     

Catarrhal proventriculitis associated with a filamentous organism in pet birds.

Catarrhal proventriculitis due to infection by an unidentified organism was diagnosed in 79 of 534 pet birds examined histologically. It was more prevalent in domestic birds (70 cases) than in imported ones (9 cases). A high incidence of the disease was encountered in budgerigars (Melopsittacus undulatus) and it was occasionally found in finches (Poephila gouldiae gouldiae), parakeets (Psittacula Krameri manillensis), Amazona parrots (Amazona aestiva aestiva) and cockatiels (Nymphicus hollandicus). The agent was a large filamentous rod, and was stained positively with Gram, GMS and PAS methods. Histologically, it induced a mild to moderate exudative or proliferative inflammation in the proventriculus. All the cases had an erosion in the gizzard. Ultrastructurally, the organism had a eukaryotic nucleus and three cell-wall layers. Concurrent infections were very common, including adenoviruses (37 cases), giardiasis (31 cases), candidiasis (13 cases), papovaviruses (11 cases) and knemidocoptic mites (11 cases).     

Pharmacokinetics of ceftiofur sodium in exotic and domestic avian species

The pharmacokinetics of ceftiofur sodium were determined in domestic chicks, turkey poults, adult cockatiels ( Nymphicus hollandicus ), and adult orange-winged Amazon parrots ( Amazona amazonica ) after subcutaneous (chicks and turkey poults) and intramuscular (i.m.) dosing (cockatiels and Amazon parrots). Turkey poult data were best fit to a single exponential model with disappearance half-lives ( t _1/2) of 8.6, 7.4 and 5.6 h after doses of 0.12, 0.24 and 0.48 mg ceftiofur free acid equivalents (CFAE)/poult, respectively. Data from chicks were best fit to a biexponential model with primary and secondary half-lives of 2.2 and 7.5, 3.7 and 6.8, and 3.8 and 5.3 h after doses of 0.04, 0.08 and 0.16 mg CFAE/chick, respectively. Cockatiel and Amazon parrot data were best fit to a biexponential model with primary and secondary half-lives of 0.28 and 2.5, and 0.93 and 7.9 h, respectively, after doses of 10 mg CFAE/kg body weight. The maximum concentration ( C _max) and area under the concentration time curve ( AUC ) in chicks and poults were dose-proportional. The C _max for cockatiels was 5.2 μg/mL and for Amazon parrots was 11 μg/mL. Clearance in cockatiels and Amazon parrots were 11.3 and 3.8 mL/min/kg, respectively, and reflected the much greater AUC seen in Amazon parrots. Clearance values of ceftiofur were similar in chicks and Amazon parrots, slightly greater in turkey poults and greatest in cockatiels. These results indicate that pharmacokinetic differences must be considered when establishing dosage regimens for different avian species.     

The occurrence of Cryptococcus neoformans in fecal samples from birds kept in human living areas]

With help of Guizotia creatinine agar (syn. bird seed agar) Cryptococcus (Cr.) neoformans var. neoformans was isolated from 71 (7.7%) of 925 investigated droppings of birds kept within human living area. Cr. neoformans was detected in droppings of 1.2% from 164 psittacines, in droppings of 1.7% from 118 budgerigars and in droppings of 18.4% from (carrier) pigeons. This yeast was not isolated from droppings of 13 small parrots, 10 eclectus parrots, 13 rosellas, 21 cockatiels, 6 Polytelidus sp., 32 Cacatua sp., 13 Carduelis sp., 5 waxbills, 5 starlings, 120 chicken, 9 turkeys, 2 geese, 2 Turdus sp., 1 duck and 1 gull.     

Flow cytometric analysis of nuclear DNA for sex identification in three psittacine species

OBJECTIVE: To evaluate flow cytometric analysis for sex identification in 3 psittacine species, establish reference values for blood cell DNA content for each species, and determine effects of sample storage on DNA content. ANIMALS: 36 orange-winged Amazon parrots, 41 budgerigars, and 39 cockatiels. PROCEDURE: Blood samples were stained and analyzed by use of flow cytometry to measure cellular DNA content. Samples were analyzed immediately after collection and after being stored at 4 C for 48 and 72 hours. RESULTS: Mean DNA content (picograms per cell) was 3.248 for Amazon parrots, 2.702 for budgerigars, and 2.946 for cockatiels; DNA concentrations in samples analyzed immediately overlapped in a male and a female Amazon parrot and among 19 cockatiels. For budgerigars, DNA overlap between sexes was not detected in samples analyzed immediately or after storage for 72 hours. Sex was identified correctly in 94.4% of Amazon parrots, 100% of budgerigars, and 51.3% of cockatiels. For both sexes, DNA content in samples analyzed immediately was significantly different from that of stored samples. CONCLUSIONS AND CLINICAL RELEVANCE: Flow cytometric analysis was accurate for sex identification of Amazon parrots and budgerigars. Sample storage at 4 C for 48 or 72 hours caused variability in DNA content.     

Increasing incidence of megabacteriosis in canaries (Serinus canarius domesticus)

A total of 312 post-mortem examinations of 178 canaries (Serinus canarius domesticus), 40 parakeets (Melopsittacus undulatus, Nymphicus hollandicus) and 94 parrots (Amazona aestiva, Psitaccus erithacus) were conducted at the Birds and Rabbits Service of the University of Liège, Belgium. After a detailed gross examination, tissue samples were collected for virological and/or bacteriological and/or parasitological examination to complete the diagnosis. In all cases, a microscopic examination of the proventricular mucus layer was undertaken for the detection of the anamorphic ascomycetous yeast Macrorhabdus ornithogaster, which causes the non-zoonotic but important disease in cage birds known as megabacteriosis. At the time of death, megabacteriosis was diagnosed respectively in 28% of canaries and 22.5% of budgerigars (P value for Fisher's exact test=0.5576), but was not diagnosed in parrots (P value for Fisher's exact test <0.0001). The incidence of megabacteriosis significantly increases along the years (P value for chi2 test <0.0001, Cramer's coefficient=0.3405). The most common gross lesions seen at necropsy of the 59 megabacteriosis cases was proventricular dilatation (86.1%). All the birds diagnosed as typical megabacteriosis cases were free of Salmonella spp. infections and of any parasitic infections. Four megabacteriosis cases (three canaries, one parakeet) were not included in statistical analysis as salmonellosis, pseudotuberculosis, coccidiosis and chlamydophilosis were diagnosed concomitantly in these birds. With the exception of megabacteriosis, the most frequent causes of death were protozoan (coccidiosis, lankesterellosis) infections (18.4%) and salmonellosis (17.1%) in canaries, and psittacosis (31.5%) and viral hepatitis (26.3%) in parakeets. In parrots, the most common causes of death were psittacosis (28.6%) and aspergillosis (28.5%).     

Survey of clinical psittacine bird sera for Salmonella typhimurium agglutinins.

Of 2407 serum samples from various kinds of psittacine birds submitted for Chlamydia serology, 2343 (97.4%) were negative, 25 (1.0%) were equivocal, and 39 (1.6%) were positive for Salmonella typhimurium agglutinins. In additional serum samples from two groups of African gray parrots, the prevalence of agglutinins was 0.0% (0/38) in the Timneh variety and 24.0% (6/25) in the Congo variety. In sera from one macaw, one cockatoo, and one Amazon parrot, which were negative for chlamydial antibody activity, there were strongly reactive agglutinins for S. typhimurium. Two Amazon parrots had antibody activity against Salmonella and Chlamydia antigens.     

Vaccination of calves with a modified bacterin or oil-in-water emulsion containing alkali-detoxified Salmonella typhimurium lipopolysaccharide

Twenty-six clinically normal colostrum-fed dairy calves were allotted to 5 groups. Calves of groups 1 and 2 served as nonvaccinated controls and were challenge-exposed with variable numbers of organisms. Group-3 calves were vaccinated SC with a modified Salmonella typhimurium bacterin. The bacterin was composed of killed acid-hydrolyzed S typhimurium G30/C21 (Re-mutant) whole cells coated with alkali-hydrolyzed S typhimurium LT-2 lipopolysaccharide, as antigen, and monophosphoryl lipid A, as adjuvant. Calves of groups 4 and 5 were vaccinated with a 2% mineral oil-in-water emulsion containing lipopolysaccharide as antigen and monophosphoryl lipid A and trehalose 6-6'-dimycolate as adjuvants. Calves of groups 3-5 were vaccinated at 2 weeks of age and again at 4 or 6 weeks of age. Adverse reactions were not observed after vaccination. Calves were challenge-exposed orally at 6 or 8 weeks of age with 1.5 X 10(11) (groups 1 and 4), or 3.0 X 10(11) (groups 2, 3, and 5) colony-forming units of S typhimurium UCD 108-11. Mortality after challenge exposure was 2 of 5 group-1 calves; 4 of 5 group-2 calves; 5 of 6 group-3 calves; 1 of 5 group-4 calves; and 4 of 5 group-5 calves. Statistical difference between calves of similarly challenge-exposed groups was not evident, indicating failure of either vaccine to protect calves of this age from oral challenge exposure with virulent S typhimurium.     

Investigation of Japanese quail (Coturnix japonica) as a pharmacokinetic model for cockatiels (Nymphicus hollandicus) and Poicephalus parrots via comparison of the pharmacokinetics of a single intravenous injection of oxytetracycline hydrochloride

The purpose of this study was to determine whether Japanese quail (Coturnix japonica) would serve as a pharmacokinetic animal model for two small companion parrots: cockatiels (Nymphicus hollandicus) and Poicephalus parrots. Oxytetracycline (OTC) was the pharmacologic agent chosen for this study as it is eliminated primarily by renal glomerular filtration and undergoes minimal metabolism. A single intravenous injection of 20 mg/kg oxytetracycline hydrochloride was administered to the three study groups and blood samples were obtained at 5, 10, 15, and 30 min post-OTC injection as well as 1, 2, 4, 8, 12 and 24 h post-OTC injection. Quantification of plasma OTC was accomplished using a standardized microbial inhibition assay. Naïve-pooled data (NPD) analysis of the plasma concentration–time profile of OTC best fit a two-compartment open model for all three avian species. Noncompartmental analysis of the mean data yielded the following parameters for quail, cockatiels and Poicephalus parrots respectively: λ_z = 3.14, 4.57, 3.71 h; AUC = 38.9, 42.7, 49.6 μg·h/mL; and Cl = 514, 468, 403 mL/h/kg. Based on the similarity of these pharmacokinetic parameters, it appears that quail could be used as a model species to predict the appropriate OTC dosing regimen for small psittacine birds. A bootstrap procedure was also applied to these sparse data sets for both compartmental and noncompartmental analysis. The bootstrap procedure allowed for the calculation of variability of parameters; however, the estimates of the parameters were very similar to those calculated using the NPD and the data mean values.     

Tissue distribution of psittacid herpesviruses in latently infected parrots, repeated sampling of latently infected parrots and prevalence of latency in parrots submitted for necropsy.

Psittacid herpesvirus-1 (PsHV-1) is the cause of an acute fatal disease in parrots and is implicated as the cause of papillomatous lesions of the digestive tract. Not all infections cause disease and some parrots are infected asymptomatically. Latently infected parrots are potential sources for virus dissemination. Tissues from parrots that died spontaneously with a history of coming from flocks where a PsHV-1 outbreak had occurred were examined for PsHV-1 DNA. Fourteen of 16 parrots examined were infected with at least 1 variant of PsHV-1; of these 13 (93%) had viral DNA in either or both the oral and cloacal mucosa, suggesting that most latently infected parrots could be detected by sampling these sites. Nine of 9 parrots shown to be infected 5 years prior to this study were positive again on repeat sampling and were infected with the same virus genotype. Opportunistic sampling of parrots submitted for diagnostic necropsy indicated that the prevalence of PsHV-1 in parrots in the sampled population was approximately 9.3%. PsHV-1 genotypes 1, 2, and 3 were found in these birds, but genotype 4 was not. Six necropsy specimens were found to be infected with two PsHV-1 genotypes and it was concluded that infection with one serotype did not protect against infection with another. Psittacid herpesvirus 2 (PsHV-2) was identified in 4 African grey parrots and a blue and gold macaw. Prior to this study PsHV-2 had only been found in African grey parrots.     

Prevalence and epizootiology of equine salmonellosis.

Feces from 1,451 horses entering a veterinary hospital over a 13-month period were cultured for salmonella. A total of 46 horses (3.2%) yielded 1 or more salmonella-positive fecal cultures. Twenty horses were found to be excreting salmonella in the feces on admission, and 5 of these later had severe diarrhea associated with enteric salmonellosis. Abdominal surgery and other severe stresses were associated with all cases of severe enteric salmonellosis. Serotypes of salmonella isolated included Salmonella agona (15), S anatum (14), S typhimurium (7), S typhimurium var copenhagen (4), S infantis (2), S montevideo (1), S meleagridis (1), S drypool (1), and an unnamed Salmonella serotype (1). Seven deaths were attributed to 4 serotypes (S typhimurium, 3; S anatum, 2; S typhimurium var copenhagen, 1; and S montevideo, 1). A marked seasonal incidence is isolations was found with isolations highest in later summer to early fall and lowest in the spring. It was also found that horses can shed salmonella intermittently, and a minimal of 5 consecutive negative fecal cultures is recommended before considering a horse not to be infected with salmonella.     

Ocular teratoid medulloepithelioma in a northern red-shouldered macaw: case report and literature review

A 4-mo-old northern red-shouldered macaw (Diopsittaca nobilis) was admitted to the veterinary hospital of the Arruda Câmara Zoo, in the State of Paraiba, Brazil, for investigation of an orbital mass. Given rapid progression and lack of response to treatment, the bird was euthanized, and an autopsy was performed. Histologically, the mass consisted of a retrobulbar invasive tumor characterized by tubular and rosette-like structures, with interspersed heteroplastic tissues, such as aggregates of neuroglial cells and islands of hyaline cartilage. The tumor was immunopositive for pancytokeratin, GFAP, NSE, and S100. These findings were compatible with an ocular teratoid medulloepithelioma, a neoplasm best described in humans but also reported rarely in young cockatiels and African Grey parrots.     

Efficacy of acyclovir against herpesvirus infection in Quaker parakeets.

We evaluated the efficacy of acyclovir against experimentally induced herpesvirus infection (Pacheco's parrot disease) in Quaker parakeets. Thirty-two of 40 birds were challenge-exposed with 0.1 ml of a suspension of herpesvirus (10(4) median cell culture infective doses [CCID50]) given IM. Treatment with acyclovir was started 24 hours later and was continued for 7 days. The birds were allotted to 5 groups of 8 birds each. There was a considerable difference in mortality between groups 1-5. Of 8 bird in each group, 6 died in group 1 (control), 1 died in group 2 (gavage), 3 died in group 3 (low dose, IM), 4 died in group 4 (high dose, IM), and none died in group 5 (contact controls). There was a significant (P = 0.023) difference in mortality between groups 1 and 2, thus the oral form of acyclovir administered by gavage was the most efficacious therapeutic regimen. Clinical signs and death occurred after discontinuation of acyclovir in groups 2 and 3, whereas the mean time of death for the control group was 6 days after challenge exposure. Herpesvirus was recovered by inoculation of chick embryo cell culture with pooled tissue suspensions from all birds that died. Histologic evidence of herpesvirus infection was found in most birds that died, with the control group having the most severe lesions. Surviving Quaker parakeets were transferred to cages with seronegative Quaker parakeets with no known exposure to herpesvirus. There have been no deaths attributable to herpesvirus infection in a period exceeding 2 years.     

Thyrotropin stimulation test for evaluation of thyroid function in psittacine birds

Serum thyroid hormone concentrations were determined before and after thyrotropin (thyroid stimulating hormone [TSH]) stimulation in caged psittacine birds to determine whether the TSH stimulation test could be used to evaluate thyroid function in this class of birds. The mean (+/- SD) resting thyroxine concentrations (ng/ml) for the species studied were: cockatoos, 13.63 +/- 6.53 (n = 6); Amazon parrots, 8.19 +/- 6.90 (n = 8); scarlet macaws, 1.34 +/- 0.51 (n = 9); blue and gold macaws, 3.41 +/- 1.78 (n = 8); African gray parrots, 1.42 +/- 0.44 (n = 6); conures, 1.76 +/- 0.77 (n = 5); and cockatiels, 11.83 +/- 6.76 (n = 3). The mean (+/- SD) thyroxine concentrations (ng/ml) 4 to 6 hours after TSH stimulation were 35.10 +/- 13.16, 27.40 +/- 15.93, 6.46 +/- 3.10, 12.36 +/- 6.34, 9.30 +/- 2.90, 13.50 +/- 7.71, and 39.0 +/- 5.66, respectively. Serum tri-iodothyronine concentration did not increase significantly after TSH stimulation. The results demonstrated that the TSH stimulation test can be used to evaluate thyroid function in caged psittacine birds.     

Genetics of resistance to Salmonella typhimurium in newly hatched chicks

1. A survey of inbred and partially inbred lines of chickens showed pronounced differences in mortality following challenge of the newly hatched chicks with Salmonella typhimurium. Lines W, 6(1) and N were highly resistant to challenge, whereas lines C and 15I were highly susceptible. 2. This difference in susceptibility was observed with a range of 5 strains of S. typhimurium of different degrees of virulence and also following both oral and intramuscular challenge. 3. The inheritance of resistance was studied in detail by examining a series of crosses between the susceptible line C and resistant line W. The pattern of mortality in crosses and back-crosses between these lines indicated resistance is dominant and was consistent with the inheritance of a dominant autosomal resistance gene. 4. There was no evidence of maternal effects in these crosses, and no evidence of association with the major histocompatability complex.     

Use of refractometry for determination of psittacine plasma protein concentration

Background: Previous studies have demonstrated both poor and good correlation of total protein concentrations in various avian species using refractometry and biuret methodologies. Objectives: The purpose of the current study was to compare these 2 techniques of total protein determination using plasma samples from several psittacine species and to determine the effect of cholesterol and other solutes on refractometry results. Methods: Total protein concentration in heparinized plasma samples without visible lipemia was analyzed by refractometry and an automated biuret method on a dry reagent analyzer (Ortho 250). Cholesterol, glucose, and uric acid concentrations were measured using the same analyzer. Results were compared using Deming regression analysis, Bland–Altman bias plots, and Spearman's rank correlation. Results: Correlation coefficients (r) for total protein results by refractometry and biuret methods were 0.49 in African grey parrots (n=28), 0.77 in Amazon parrots (20), 0.57 in cockatiels (20), 0.73 in cockatoos (36), 0.86 in conures (20), and 0.93 in macaws (38) (P≤.01). Cholesterol concentration, but not glucose or uric acid concentrations, was significantly correlated with total protein concentration obtained by refractometry in Amazon parrots, conures, and macaws (n=25 each, P<.05), and trended towards significance in African grey parrots and cockatoos (P=.06). Conclusions: Refractometry can be used to accurately measure total protein concentration in nonlipemic plasma samples from some psittacine species. Method and species‐specific reference intervals should be used in the interpretation of total protein values.     

Identification of Chlamydophila pneumoniae in an emerald tree boa, Corallus caninus.

Tissues were evaluated from emerald tree boas, Corallus caninus, from a collection in which chlamydiosis was diagnosed. To determine the strain of chlamydia infecting these snakes, tissue samples from 5 frozen snakes were tested by a quantitative TaqMan polymerase chain reaction (PCR) test and a PCR sequence analysis test. Of the 22 samples tested, 9 were categorized as either positive or weakly positive with the TaqMan test, and 6 yielded an amplicon using a serial PCR test that amplified a portion of the 23S ribosomal RNA gene. A PCR product suitable for sequencing was obtained from the heart of one of the snakes. Sequence analysis showed that the snake had been infected with Chlamydophila pneumoniae. These findings show that C. pneumoniae can infect emerald tree boas, broadening the range of reptiles known to be infected by this primarily human pathogen.     

Multiple drug-resistant Salmonella typhimurium DT104 and DT104b isolated in bobwhite quail (Colinus virginianus)

Multiple drug-resistant Salmonella typhimurium, definitive type (DT) 104 and DT104b, were isolated in three separate hunting preserve bobwhite quail (Colinus virginianus) outbreaks. The cases involved 4-day-old and 3-wk-old quail with increased mortality of 5%-8.6%, respectively. Postmortem lesions included emaciation, distended abdomens, and dark colon contents, which were gaseous and fluid in consistency. Salmonella typhimurium isolated from the intestines and/or livers was resistant to ampicillin, chloramphenicol, sulfonamides, and tetracycline. The isolate involving the 3-wk-old quail was phage typed as S. typhimurium DT104. The isolates involving the two cases of 4-day-old quail were phage typed as S. typhimurium DT104b.