A healthy 8-year-old female Micronesian kingfisher was given a thorough physical examination after its mate of 2.5 years died of avian mycobacteriosis. Examination of a heparinized blood sample revealed no abnormalities via CBC and high plasma activity of AST (850 U/L; reference range, 338 to 583 U/L), compared with reference values1 for Micronesian kingfishers. Results of radiography and palpation of the coelomic cavity were normal. Three cloacal swab specimens yielded negative results for acid-fast bacteria, and 3 fecal specimens yielded negative results of bacteriologic culture for mycobacterial organisms. Five months later, an examination of the bird was performed prior to transfer to another zoologic institution. The kingfisher appeared healthy, had normal results of palpation and radiography, and had mild leukopenia (3,000 cells/μL; reference range, 3,274 to 13,112 cells/μL) and hypoalbuminemia (1.2 g/dL; reference range, 1.3 to 2.5 g/dL). A fecal specimen yielded negative results for acid-fast bacteria. On arrival at the zoologic institution 3 weeks later, a quarantine examination with additional examinations for mycobacterial infection was performed because of the bird's history of exposure to an infected bird. The bird weighed 0.056 kg (0.123 lb) and was anesthetized with isoflurane and oxygen via face mask and intubated. Results of physical examination and radiography were normal; mild anemia (Hct, 40%; reference range, 42% to 52%) and high plasma activity of AST (800 U/L) were detected. Fecal floatation yielded negative results for parasites, and a cloacal swab specimen yielded negative culture results for acid-fast bacteria. Hepatic biopsy specimens were collected through a small ventral midline incision, and the bird received enrofloxacin (9 mg/kg [4.1 mg/lb], IM) and LRS (36 mL/kg [16.4 mL/lb], SC). Histologic examination of the liver specimens revealed that 30% to 40% of the liver tissue was replaced by granulomatous inflammation with centrally located histiocytes and scattered peripherally located lymphocytes. Ziehl-Neelsen staining of the liver specimens revealed low numbers of acid-fast bacteria. A presumptive diagnosis of hepatic mycobacteriosis was made, but mycobacterial culture was not performed.
The bird was isolated in quarantine and monitored with noninvasive diagnostic tests including culture of cloacal swabs and feces for acid-fast organisms, radiography, and blood analyses. Four months after the diagnosis of mycobacteriosis, radiography revealed substantial hepatomegaly, and body weight had increased to 0.067 kg (0.147 lb). Examination of blood revealed high total protein concentration (4.8 g/dL; reference range, 2.8 to 4.4 g/dL) and hyperglobulinemia (3.2 g/dL; reference range, 1.1 to 2.7 g/dL). The bird received LRS (30 mL/kg [13.6 mL/lb], SC) and a cloacal swab specimen and bacteriologic culture of feces yielded negative results for acid-fast and mycobacterial organisms, respectively. Twenty-five percent of the bird's body weight was lost during the next 3 weeks. The Hct (52%) was near the upper limit of the reference range, and heterophilia (49%; reference range, 18% to 35%) and monocytosis (13%; reference range, 8% to 12%) were evident, despite total WBC and absolute differential counts within reference ranges. Total protein (7.8 g/dL) and globulin (6.5 g/dL) concentrations were greater than previously measured, and albumin (1.3 g/dL) concentration was near the lower limit of the reference range. There was marked hyperphosphatemia (7.1 mg/dL; reference range, 0.4 to 4.6 mg/dL) and high plasma activity of AST (1,284 U/L). A cloacal swab specimen again yielded negative results for acid-fast organisms.
Despite losing weight, the bird was eating well and energetic during the following 3 weeks. The bird survived more than 4 months after the diagnosis of mycobacteriosis; however, while the bird was anesthetized with isoflurane for additional disease monitoring, cardiac arrest occurred and the bird died. Blood was not submitted for analysis. A cloacal swab specimen yielded negative results for acid-fast bacteria, and results of culture were negative, but cytologic examination of a liver swab revealed many acid-fast bacilli. At necropsy, the liver was enlarged (weight, 4 g [7.7% of body weight]) and tan-brown in color. Adipose stores were scant. Histologically, more than 75% of the hepatic tissue was replaced by rounded clusterings of histiocytes that contained occasional foci of lymphocytes. Histiocytes formed linear aggregations in the perivascular parenchyma. Many foamy macrophages with intracytoplasmic bacilli were in the spleen. The bone marrow had high cellularity because of numerous myeloid cells and occasional foamy macrophages. Use of Ziehl-Neelsen staining confirmed the presence of acid-fast bacilli in macrophages in all areas of histiocytic inflammation. Mycobacterium simiae complex was cultured from the liver by use of liquid culture mediaa,b and confirmed via HPLC.b
A 5-year-old female Micronesian kingfisher appeared healthy until acute onset of dyspnea, lethargy, and weakness. Despite thin body condition (body weight, 0.058 kg [0.128 lb], the coelomic cavity was distended and firm. Blood analysis revealed heterophilia (8,280 cells/μL; reference range, 585 to 4,587 cells/μL), band heterophils (240 cells/μL; reference range, 0 cells/μL), and toxic changes. Plasma biochemical analysis was limited to 2 tests because of sample volume. Uric acid concentration was high (23 mg/dL; reference range, 4 to 18 mg/dL), and albumin concentration (1.2 g/dL) was low. The bird received enrofloxacin (5 mg/kg [2.3 mg/lb], IM) and LRS (17 mL/kg [7.7 mL/lb], SC). The following day, dyspnea was evident at rest, and the bird was placed in an oxygen chamber in preparation for fine-needle aspiration of the middle portion of the coelomic cavity. Cytologic examination of the aspirate revealed findings suggestive of granulomatous coelomitis, and the bird was anesthetized with isoflurane for exploratory surgery. The liver was markedly large, friable, and tan, and a liver lobe was resected. The bird died during the procedure.
At necropsy, the liver was pale tan with a grainy white pattern and was enlarged (weight, 3 g [6% of body weight]). Histologic examination revealed that approximately 5% of the liver parenchyma consisted of hepatocytes and approximately 95% was composed of macrophages. Similar macrophage infiltrates were also detected in the spleen, bone marrow, lungs, and mesovarium. Ziehl-Neelsen staining was used to detect acid-fast bacilli in macrophages in areas of histiocytic inflammation in the liver, lungs, and mesovarium. Bacteriologic culture of liver yielded M simiae complex at the same laboratory and by use of the same techniques as for the first bird of this report.
The bird had been housed with a male for 3.5 years prior to death. To screen for mycobacteria in this mate, the bird was evaluated immediately and 9 months and 13 months after the death of the female. Evaluations included blood analyses, radiography, cloacal swab specimens, and liver biopsies, and all results were unremarkable. Thirty months after death of its mate, the male bird was healthy and had results of blood analyses that were within reference ranges.
A 6.5-year-old, 0.059-g (0.130-lb) male Micronesian kingfisher had progressive episodes of open-mouth breathing during a 1-month period. The coelomic cavity became enlarged, and an intracoelomic mass was palpable. Isoflurane anesthesia was used to facilitate diagnostic procedures. Ultrasonography and contrast radiography performed with diatrizoate meglumine administered via gavage revealed displacement of the gastrointestinal tract, suggesting that the mass was the liver. A CBC revealed mild anemia and marked leukocytosis (31,700 cells/μL) with heterophilia (21,239 cells/μL) and monocytosis (4,121 cells/μL). Band heterophils were detected but not counted. Plasma biochemical analyses revealed hyperproteinemia (5.9 g/dL), hyperglobulinemia (4.6 g/dL), and high activity of AST (1,754 U/L). A left lateral laparotomy was performed, and the liver was enlarged and tan in color; 2 biopsy specimens were collected. Enrofloxacin (15.7 mg/kg [7.14 mg/lb], PO, q 12 h) was prescribed. Histologic examination revealed diffuse histiocytic hepatitis with many acid-fast bacteria. Approximately 90% of the liver was composed of macrophages and giant cells; euthanasia was performed because of the poor prognosis.
At necropsy, the bird was in poor body condition with a markedly swollen, pale tan liver (weight, 16 g) that compressed the other coelomic organs (Figure 1). The spleen was also enlarged and pale tan. Histologic examination revealed that the liver, spleen, and pancreas were almost entirely effaced by macrophage and multinucleated giant cell infiltrates and only scant remnants of parenchymal cells remained (Figure 2). Perivascular and interstitial infiltrates of macrophages and giant cells were also evident in the lungs and kidneys. Fites acid-fast staining revealed many acid-fast bacilli within macrophages in all areas of histiocytic inflammation. The final histopathologic diagnosis was multifocal chronic active histiocytic inflammation with intracellular acid-fast bacteria. Mycobacterium simiae complex was cultured from the liver and spleen on liquidc,d and solid culture mediad,e and confirmed via HPLC.d
Postmortem photograph of a Micronesian kingfisher infected with Mycobacterium simiae complex. The liver (L) is massively enlarged and pale. H = Heart. Bar=2cm.
Citation: Journal of the American Veterinary Medical Association 230, 10; 10.2460/javma.230.10.1524
Postmortem photograph of a Micronesian kingfisher infected with Mycobacterium simiae complex. The liver (L) is massively enlarged and pale. H = Heart. Bar=2cm.
Citation: Journal of the American Veterinary Medical Association 230, 10; 10.2460/javma.230.10.1524
Postmortem photograph of a Micronesian kingfisher infected with Mycobacterium simiae complex. The liver (L) is massively enlarged and pale. H = Heart. Bar=2cm.
Citation: Journal of the American Veterinary Medical Association 230, 10; 10.2460/javma.230.10.1524
Photomicrographs of a portion of the liver from a Micronesian kingfisher infected with M simiae complex. A—Notice that a thin remnant of hepatocytes (H) remains between massive sheets of foamy macrophages (M). H&E stain; bar = 100 μm. B—Notice that a thin remnant of hepatocytes (H) remains between sheets of macrophages containing numerous acid-fast bacteria (Mb). Fites acid-fast stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 10; 10.2460/javma.230.10.1524
Photomicrographs of a portion of the liver from a Micronesian kingfisher infected with M simiae complex. A—Notice that a thin remnant of hepatocytes (H) remains between massive sheets of foamy macrophages (M). H&E stain; bar = 100 μm. B—Notice that a thin remnant of hepatocytes (H) remains between sheets of macrophages containing numerous acid-fast bacteria (Mb). Fites acid-fast stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 10; 10.2460/javma.230.10.1524
Photomicrographs of a portion of the liver from a Micronesian kingfisher infected with M simiae complex. A—Notice that a thin remnant of hepatocytes (H) remains between massive sheets of foamy macrophages (M). H&E stain; bar = 100 μm. B—Notice that a thin remnant of hepatocytes (H) remains between sheets of macrophages containing numerous acid-fast bacteria (Mb). Fites acid-fast stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 230, 10; 10.2460/javma.230.10.1524
A 2.5-year-old 0.06-kg (0.13-lb) female Micronesian kingfisher was fluffed and slightly lethargic. Results of a CBC indicated leukocytosis (13,600 cells/μL) with monocytosis (3,944 cells/μL); plasma biochemical analysis was not performed. Enrofloxacin (5 mg/kg [2.3 mg/lb], PO, q 12 h for 14 days) was administered, and 3 weeks later, results of physical examination, radiography, and monocyte count were unremarkable, although high plasma activity of AST (673 U/L) was detected. No acid-fast bacteria were seen in a cloacal smear specimen. Five weeks later, leukocytosis (13,600 cells/μL) with lymphocytosis (8,840 cells/μL; reference range, 688 to 7,044 cells/μL) was detected, although the bird did not have clinical signs of disease. Four months later, the bird was fluffed, had signs of depression, and was unable to fly to its perch. The bird was thin (weight, 0.056 kg despite having a distended coelomic cavity and palpable hepatomegaly. Examination of a fecal sample revealed many acid-fast bacteria. Because of the bird's distress, it was placed in an oxygen chamber; blood was not collected. The bird died overnight.
At necropsy, the bird was cachexic and had a markedly distended and firm coelomic cavity. The liver occupied approximately 80% of the coelomic cavity and was firm and pale tan with a few mottled red regions on the capsular surface. The enlarged liver compressed coelomic organs including the heart, intestinal tract, air sacs, and oviduct. The spleen was diffusely tan and firm, similar to the liver. Histologic examination revealed that approximately 90% of the hepatic parenchyma was replaced by infiltrates of macrophages and scattered multinucleated giant cells. Similar macrophage and giant cell infiltrates were evident in the spleen (replacing 40% of the splenic parenchyma), and mild infiltrates were evident in the lungs, adrenal glands, ventriculus, and small intestine. Pale basophilic slender bacilli were observed within macrophages in multiple tissues, and acid-fast staining revealed bacilli in the liver and ventriculus. Bacteriologic culture of a liver sample by use of liquidf and solide culture media yielded M simiae complexg; identity of the bacterium was confirmed via HPLC.b
Discussion
To the authors' knowledge, this is the first report of infection with M simiae complex in Micronesian kingfishers. Results of a recent study2 suggest that Mycobacterium avium and Mycobacterium intracellulare infections are rarely caused by direct or indirect bird-to-bird transmission and that exposure is most likely from an environmental source. It is unknown whether agents in the M simiae complex are transmitted in a similar manner. Three of the 4 infected birds in the present report had previous exposure to another kingfisher infected with a mycobacterium. The first and third kingfisher described in this report both had mates with histologic evidence of avian mycobacteriosis, and the fourth kingfisher in this report was the offspring of a male kingfisher with histologic evidence of avian mycobacteriosis. Mycobacterial infection in the 4 studied kingfishers was initially suspected on the basis of acid-fast staining and histopathologic changes in the liver and other organs. Definitive diagnosis was made via mycobacterial culture of liver and HPLC analysis of the isolates, which had trimodal mycolic acid profiles of mycobacteria closely related to M simiae. Mycobacterial nomenclature and phylogenetic relationships change frequently as new diagnostic and genetic tests become available. The National Jewish Medical and Research Center, which performed bacteriologic culture of one of the kingfisher samples, defined M simiae complex as including M simiae, Mycobacterium lentiflavum, Mycobacterium triplex, and Simiae-avium-like organisms, which is supported by other publications.3,4 At the time of the cases reported here, no generally accepted laboratory method for differentiating the species within the complex was available. However, recent work with HPLC, gas-liquid chromatography, DNA hybridization, 16S rRNA, and hsp65 gene sequencing indicates that M simiae, Mycobacterium genavense, M lentiflavum, M triplex, and a novel mycobacterium designated Mycobacterium sherrisii sp nov are genetically distinct but phylogenetically related.5 Of these 5 closely related mycobacteria, only M genavense has been previously reported in birds, to the authors' knowledge.6–9 Our review of the literature indicated that infections with M lentiflavum or M sherrisii sp nov have not been diagnosed in veterinary species, whereas M triplex has been found in fish10 and M simiae in monkeys,11–14 mice,12 and a domestic cat.15 Although M genavense is closely related to these mycobacteria, the laboratories in the present study were unable to culture M genavense, detect it by use of blood culture systems, or identify its characteristic profile via HPLC.16 Therefore, the 4 kingfishers were considered to have negative results for M genavense and positive results for M simiae complex, which is important because none of the other bacteria in the M simiae complex have previously been detected in Micronesian kingfishers or other avian species.
The mycobacteria in the M simiae complex are considered nontuberculous mycobacteria and are present in the environment as saprophytes.17,18 M simiae has been found in sphagnum,19 feces of healthy humans,20 and water.21–23 Nontuberculous mycobacteria are opportunistic pathogens with variable pathogenicity. A national study by the CDC found that 21% of M simiae isolates were associated with disease,24 immunocompromised individuals were more at risk,13,25–27 and there has been an increase in infections in certain geographic regions.26,28,29
Most published information on avian mycobacteriosis concerns M avium subsp avium (hereafter referred to as M avium), M intracellulare, and M genavense.6,30–33 A diagnosis of mycobacteriosis is a stepwise process, and a review of diagnostic testing has been published.1 Veterinarians must combine clinical signs and results of blood tests, radiography, laparoscopy, biopsy, cytology, culture, and advanced laboratory testing.6 The infected kingfishers reported here had typical clinical signs of avian mycobacteriosis of slowly progressive decline.6,30,32,34,35 Avian mycobacteriosis often causes hepatomegaly6,33,36 as seen in all 4 birds reported here, although none had typical radiographic bony lesions.6 There are no pathognomonic hematologic or biochemical findings associated with avian mycobacteriosis. Birds infected with M avium may have leukocytosis, heterophilia, monocytosis, or no WBC abnormalities despite clinical disease or mild to moderate anemia.6,30,32-35,37,38 Some infected birds may have high activities of AST,33 and plasma protein concentrations are variable.30,31,33,34,37 In a study of zoo birds, an arbitrary total WBC count of ≥ 18,000 cells/μL was used to suggest the possibility of mycobacteriosis.37 This critical value would not have been an accurate indicator of infection with M simiae complex in the birds reported here because only one of the WBC counts exceeded that value. Excluding that particular WBC count, the range of values was 3,000 to 13,600 cells/μL, which was similar to the reference range for Micronesian kingfishers.1 Therefore, mycobacteriosis caused by M simiae complex cannot be ruled out on the basis of the WBC count. Similar to M avium,33 high AST activity values can be detected in animals infected with M simiae complex, and because creatine phosphokinase values are often not abnormal, this may be attributed to liver damage.39
Hepatosplenomegaly is a common finding on necropsy of birds infected with M avium6,32 and was seen in all 4 affected kingfishers. Similar to lesions caused by other types of mycobacterial infection, organomegaly caused by M avium infection can be the result of granuloma formation, histiocytic inflammation, or amyloid deposition6,30; the granulomatous form is the most common. In contrast, organomegaly in the 4 birds reported here was caused by histiocytic inflammation; the pathogenesis of this lesion was unclear. In a report36 of M avium infection in a Micronesian kingfisher, hepatomegaly associated with histiocytic inflammation was observed. Thus, a histiocytic inflammatory response and associated organomegaly may be a unique response of Micronesian kingfishers to mycobacterial infection.
Because avian mycobacteria are often present within the gastrointestinal tract, feces should be collected for acid-fast staining and bacteriologic culture. Sensitivity of these tests may improve as the disease progresses and may be enhanced by collecting feces on sequential days to account for intermittent shedding.40 Of the cloacal and fecal smears submitted from the kingfishers, only 1 yielded positive results for acid-fast bacteria; that smear was obtained within 24 hours of death when the bird had advanced disease. Conversely, the first kingfisher of this report had histologic evidence of mycobacteria, was monitored aggressively for mycobacterial shedding, and had negative results for acid-fast bacteria in cloacal swab specimens (n = 4) and mycobacterial cultures of feces (2) during 5 months of screening after diagnosis. Although fecal testing has been successful in experimental avian mycobacteriosis,40 it was not helpful in the Micronesian kingfishers reported here; examination for hepatomegaly and bacteriologic culture of liver biopsy specimens were more informative.
Once a mycobacterial isolate is obtained via bacteriologic culture of appropriate tissues, a variety of laboratory techniques such as HPLC, genetic sequencing of 16S rRNA, or DNA-DNA hybridization are available to identify the species of mycobacteria.5,41–44 Disagreements are evident in the clinical microbiology literature regarding which testing methods are best. However, because mycolic acids of bacterial cell walls are species specific, HPLC is a rapid, accurate, and cost-effective method for identifying mycobacterial species16,41,43,44 and was used to diagnose infection with M simiae complex in liver tissues obtained at necropsy from the kingfishers reported here.
At the time of this report, only 80 Micronesian kingfishers were in captivity; therefore, infection with M simiae complex was diagnosed in 5% (4 of 80) of the captive population. This is important from a conservation standpoint because the Guam subspecies of the Micronesian kingfisher is extinct in the wild and captive propagation programs are used to help repatriate the species. We recommend that a bird with a suspected infection be quarantined for 1 year and noninvasive testing, such as use of cloacal swab specimens and feces for culture of acid-fast organisms, radiography, and blood analyses, be performed quarterly; liver biopsy for histologic examination and culture should be performed at 6 months and 1 year. Treatment of mycobacteriosis in birds is rarely pursued.6
Although we were unable to identify the particular mycobacterial agent within the M simiae complex responsible for the disease processes reported here, results indicated that the M simiae complex was pathogenic in Micronesian kingfishers. Additional studies are warranted to determine whether M simiae, M lentiflavum, M triplex, or M sherrisii sp nov can individually cause disease in birds as has been reported with M genavense. Because nontuberculous mycobacteria are often environmental contaminants, it is proposed that wild birds are less likely to become infected than captive birds. Additional research is needed to determine whether other veterinary species, and birds in particular, are susceptible to the agents grouped together as the M simiae complex.
ABBREVIATIONS
| AST | Aspartate aminotransferase |
| LRS | Lactated Ringer's solution |
| HPLC | High-performance liquid chromatography |
BACTEC 12B media and BACTEC 460 system, Becton, Dickinson & Co, Franklin Lakes, NJ.
Focus Technologies, Cypress, Calif.
BACTEC 71 media, Becton, Dickinson & Co, Franklin Lakes, NJ.
National Jewish Medical and Research Center, Denver, Colo.
Lowenstein-Jensen media, Hardy Diagnostics, Santa Monica, Calif.
7H9 Middlebrook media and MGIT 960 system, Becton, Dickinson & Co, Franklin Lakes, NJ.
Sekot Laboratory, Miami, Fla.
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