Previous Article | Next Article 
Journal of Clinical Microbiology, April 1998, p. 1101-1102, Vol. 36, No. 4
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Mycobacterium tuberculosis Infection in
a Green-Winged Macaw (Ara chloroptera): Report with Public
Health Implications
Rita M.
Washko,1,2
Heidi
Hoefer,3
Timothy E.
Kiehn,4,*
Donald
Armstrong,5
Guy
Dorsinville,2 and
Thomas R.
Frieden2,6
Epidemic Intelligence Service, Division of
Field Epidemiology,1 and
Division of
Tuberculosis Elimination, National Center for Prevention
Services,6 Centers for Disease Control and
Prevention, Atlanta, Georgia;
Bureau of Tuberculosis
Control, New York City Department of Health, New York, New
York2;
Animal Medical Center, New
York, New York3; and
Microbiology
Service, Department of Clinical
Laboratories,4 and
Infectious Disease
Service, Department of Medicine,5 Memorial
Sloan-Kettering Cancer Center, New York, New York
Received 2 September 1997/Returned for modification 9 December
1997/Accepted 30 December 1997
 |
ABSTRACT |
Mycobacterium tuberculosis was isolated from the
eyelid, skin, tongue, and lungs of a green-winged macaw (Ara
chloroptera). Two persons living in the same household were
culture positive for pulmonary tuberculosis 3 to 4 years before
tuberculosis was diagnosed in the bird. Although humans have not been
shown to acquire tuberculosis from birds, an infected bird may be a
sentinel for human infection.
 |
TEXT |
Although Mycobacterium
tuberculosis primarily causes disease in humans, many animals are
reported to be susceptible to infection, including primates, swine,
cattle, sheep, goats, dogs, cats, and elephants (3, 8).
Infection with M. tuberculosis in birds is rare. Psittacine
birds (principally the parrot family) are the only avian species known
to become infected with M. tuberculosis, presumably due to
close contact with tuberculous owners. There are four reports of
infection in Amazon parrots: one each in a mealy parrot (1),
a yellow-naped parrot (10), and a red-lored parrot
(2) and one in an Amazon parrot which was not further identified (4). All of the parrots presented with cutaneous growths on the head and neck and had localized granulomas in the eye
and retrobulbar tissues, the sinuses and nares, and the oral cavity.
Two parrots were found to have systemic infections at necropsy (1,
4). The birds had no known contact with humans with tuberculosis.
This report describes disseminated M. tuberculosis disease
in another psittacine bird, a green-winged macaw, and notes a possible human source of the infection. This report has implications for public
health in that human-to-bird and, possibly, bird-to-human transmission
of tuberculosis could create a perpetual reservoir of untreated
tuberculosis.
Case report.
An adult, imported green-winged macaw (Ara
chloroptera) had been ill for several months with progressive
eyelid swelling, intermittent diarrhea, occasional loud respiratory
sounds, listlessness, and poor feeding. The bird had lived in a
multiple-person household in New York City for at least 6 years.
Several months prior to the presentation described here the bird had
been evaluated for tachypnea by a veterinarian. At that time, specimens
from facial lesions were positive for acid-fast bacilli on microscopic
examination, but culturing was not performed. The owner was advised to
euthanatize the bird but chose not to do so.
The bird presented in April 1995 to the Animal Medical Center with
multiple nodules on the eyelids and conjunctivae of both eyes as well
as on the unfeathered areas of the face and head. The oral cavity
contained numerous small white nodules on the tongue, choana, and
glottis. The bird was moderately thin and had a cardiac murmur. Blood
tests revealed a moderate leukocytosis, a mildly elevated aspartate
aminotransferase level, and a marked elevation in the beta globulin
level as determined by plasma protein electrophoresis. Radiographs
revealed enlarged cardiac and hepatic silhouettes.
Microbiology.
Acid-fast bacilli were seen in auramine
acid-fast stains of biopsied tissue from the eyelid, tongue, and skin.
Specimens were processed and inoculated into BACTEC 12B broth bottles
(Becton Dickinson, Diagnostic Instrument Systems, Sparks, Md.) and onto Middlebrook 7H11 agar plates (Becton Dickinson Microbiology Systems, Cockeysville, Md.). In approximately 2 weeks, cultures were positive and the organism was identified as M. tuberculosis by
conventional biochemical tests, including niacin production, nitrate
reduction, and growth on thiophene-2-carboxylic acid hydrazide medium.
A DNA probe for M. tuberculosis complex was positive
(GenProbe, San Diego, Calif.). A standardized IS6110-based
Southern blot hybridization protocol was used to determine the genotype
of the isolate. Restriction fragment length polymorphism analysis
revealed a three-banded pattern that is the most common pattern in New York City. The organism was susceptible when tested by the radiometric antimicrobial susceptibility test system (BACTEC) to ethambutol, isoniazid, pyrazinamide, rifampin, and streptomycin.
Epidemiology.
Review of the New York City tuberculosis
registry and hard copies of Department of Health records revealed that
two people with a history of culture-confirmed pulmonary tuberculosis
resided at the address listed for the bird's owner. They had extensive contact with the bird while they were potentially infectious, including
placing food between their lips for the bird to grasp. The first person
had drug-treatable tuberculosis diagnosed in 1991 and did not adhere to
treatment but ultimately completed treatment while incarcerated. The
second person's disease was diagnosed in January 1992, but the isolate
was not tested for antimicrobial susceptibility. The patient completed
a full course of antituberculosis treatment.
After the bird's diagnosis, the two household members previously
treated for tuberculosis underwent repeat evaluation, including chest
radiographs and sputum cultures. All results were negative. Two other
household members, who were known to have positive tuberculin skin
tests, had normal chest radiographs. Three people who came in contact
with the bird at the veterinarian's office were later noted to have no
response to tuberculin skin testing.
Necropsy.
The bird was seized and euthanatized under the
authority of the New York City Health Code after the owner refused
multiple requests to have the bird euthanatized. Necropsy revealed
miliary granulomatous pneumonia, hepatitis, stomatitis, glossitis,
myocarditis, endocarditis, and conjunctivitis. Acid-fast bacilli were
identified in the lung, liver, and skin lesions. Histopathology
revealed classic tuberculous nodules with a central necrotic core
surrounded by epithelioid macrophages, multinucleated giant cells, and
a fibrous capsule. There was no mineralization. Specimens from the lungs and skin were culture positive for M. tuberculosis,
and the antimicrobial susceptibility and restriction fragment length polymorphism patterns of the postmortem isolates were identical to
those of the antemortem isolates.
Discussion.
Birds can have avian, bovine, and human
tuberculosis. More recently, disseminated disease with the emerging
human pathogen Mycobacterium genavense has been reported for
a variety of birds (5-7, 9). Mycobacterial infections in
nonpsittacine birds are usually caused by the ubiquitous soil and water
organism Mycobacterium avium (3, 8), and the
route of infection is usually the alimentary tract. Most lesions
develop in the intestinal tract, liver, and spleen. Birds only
occasionally suffer from pulmonary M. avium disease.
Parrots suffering from disease caused by
M. tuberculosis
usually present with cutaneous lesions. This report describes a macaw
with active tuberculosis caused by
M. tuberculosis.
Epidemiologic
investigation revealed that two people who lived in the
same house
with the pet bird and who had close respiratory contact with
it
had active tuberculosis 3 to 4 years before diagnosis of
tuberculosis
in the bird. One patient did not adhere to
antituberculosis treatment
for more than 1 year. The bird probably
contracted the disease
from its human housemates. This type of
situation presents public
health implications in that a bird could
acquire multiply drug-resistant
strains, possibly infect other humans,
and even act as a perpetual
reservoir if the bird survives as long as
the one discussed in
this report.
Any parrot with ocular, sinus, oral, or cutaneous nodular lesions
should be considered suspect for
M. tuberculosis infection.
It is imperative from a public health perspective that tissue
be sent
for culture and not only for acid-fast staining. Birds
probably acquire
the infection from humans, but it is not known
if humans can acquire
the infection from birds. However, birds
may be sentinels for human
infection.
 |
FOOTNOTES |
*
Corresponding author. Mailing address: Microbiology
Laboratory, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021. Phone: (212) 639-8181. Fax: (212) 772-9285. E-mail: kiehnt{at}mskcc.org.
 |
REFERENCES |
| 1.
|
Ackerman, L. J.,
S. C. Benbrook, and B. C. Walton.
1974.
Mycobacterium tuberculosis infection in a parrot (Amasona farinosa).
Am. Rev. Respir. Dis.
109:388-390[Medline].
|
| 2.
|
Brown, R.
1990.
Sinus, articular and subcutaneous Mycobacterium tuberculosis infection in a juvenile red-lored Amazon parrot, p. 10-15.
In
Proceedings of the 1990 Annual Conference of the Association of Avian Veterinarians.
|
| 3.
|
Hines, M. E., II,
H. M. Kreeger, and A. J. Herron.
1995.
Mycobacterial infections of animals: pathology and pathogenesis.
Lab. Anim. Sci.
45:334-351[Medline].
|
| 4.
|
Hinshaw, W. R.
1933.
Tuberculosis of human origin in an Amazon parrot.
Am. Rev. Tuberc.
28:273-278.
|
| 5.
|
Hoop, R. K.,
E. C. Böttger,
P. Ossent, and M. Salfinger.
1993.
Mycobacteriosis due to Mycobacterium genavense in six pet birds.
J. Clin. Microbiol.
31:990-993[Abstract/Free Full Text].
|
| 6.
|
Kiehn, T. E.,
H. Hoefer,
E. C. Bottger,
R. Ross,
M. Wong,
F. Edwards,
N. Antinoff, and D. Armstrong.
1996.
Mycobacterium genavense infections in pet animals.
J. Clin. Microbiol.
34:1840-1842[Abstract].
|
| 7.
|
Portaels, F.,
L. Realini,
L. Bauwens,
B. Hirschel,
W. M. Meyers, and W. De Meurichy.
1996.
Mycobacteriosis caused by Mycobacterium genavense in birds kept in a zoo: 11-year survey.
J. Clin. Microbiol.
34:319-323[Abstract].
|
| 8.
|
Quinn, P. J.,
M. E. Carter,
B. Markey, and G. R. Carter.
1994.
Mycobacterium species, p. 156-169.
In
P. J. Quinn, M. E. Carter, B. Markey, and G. R. Carter (ed.), Clinical veterinary microbiology. Mosby-Wolfe, London, England.
|
| 9.
|
Ramis, A.,
L. Ferrer,
A. Aranaz,
E. Liebana,
A. Mateos,
L. Dominguez,
C. Pascual,
J. Fdez-Garayazabal, and M. D. Collins.
1996.
Mycobacterium genavense infection in canaries.
Avian Dis.
40:246-251[Medline].
|
| 10.
|
Woerper, M. S., and W. J. Rosskoph.
1983.
Retro-orbital Mycobacterium tuberculosis infection in a yellow-naped Amazon parrot (Amazona ochrocephala auropalliata), p. 71-76.
In
Proceedings of the 1983 Annual Meeting of the Association of Avian Veterinarians.
|
Journal of Clinical Microbiology, April 1998, p. 1101-1102, Vol. 36, No. 4
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.