Isolation of Mycobacterium tuberculosis from Captive ...

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An adult female red-faced black spider monkey (Ateles paniscus), housed for 2 years in the Parque Estoril Zoo in. Sa˜o Paulo, Brazil, showed apathy. Clinical ...
DISPONÍVEL EM http://online.liebertpub.com/doi/pdf/10.1089/vbz.2010.0070 VECTOR-BORNE AND ZOONOTIC DISEASES Volume 11, Number 5, 2011 ª Mary Ann Liebert, Inc. DOI: 10.1089/vbz.2010.0070

Isolation of Mycobacterium tuberculosis from Captive Ateles paniscus Vivianne Cambuı´ Mesquita Rocha,1 Ca´ssia Yumi Ikuta,1 Marcelo S. Gomes,2 Fausto Quaglia,2 Eliana R. Matushima,1 and Jose´ Soares Ferreira Neto1

Abstract

An adult female red-faced black spider monkey (Ateles paniscus), housed for 2 years in the Parque Estoril Zoo in Sa˜o Paulo, Brazil, showed apathy. Clinical examination revealed discrete emaciation, swelling and induration of lymph nodes, and presence of a mass in the abdominal cavity. Therapies with enrofloxacin, azithromycin, and ceftiofur were ineffective. The animal died after 6 months. Necropsy and histopathology confirmed granulommas in lymph nodes, parietal and visceral pleura, lungs, liver, spleen, and kidneys. Acid-fast bacilli were isolated and identified as Mycobacterium tuberculosis by polymerase chain reaction restriction analysis and Spoligotyping techniques. The zoo personnel and other animals that had had contact with the infected primate were negative to tuberculosis diagnostic procedures, such as sputum exam (baciloscopy) and thorax radiography. It was impossible to determine whether the infection occurred before or after the arrival of the animal to the Parque Estoril Zoo. This is the first report of M. tuberculosis infection in Ateles paniscus, a neotropical primate. Key Words: Ateles paniscus—Mycobacterium tuberculosis—Neotropical primate—Tuberculosis—Zoo.

Introduction

M

ycobacterium tuberculosis causes one of the major human infectious diseases worldwide, and it has also been identified in several other species, including non-human primates (Vervenne et al. 2004). The infection may be transmitted via inhalation or ingestion by contact with other sick animals or humans (Alfonso et al. 2004), especially in captive settings (Vervenne et al. 2004). Although the great incidence of tuberculosis on Old World primates is well known, it is uncommon on South America species (Montali et al. 2001). This article reports a case of tuberculosis in captive Ateles paniscus in a Brazilian zoo. Materials and Methods In July 2007, at the Parque Estoril Zoo, in Sa˜o Paulo, Brazil, an adult female red-faced black spider monkey (A. paniscus) appeared apathetic. After chemical immobilization, the clinical exam revealed discrete emaciation, swelling and induration of submandibular, axillary, and inguinal lymph nodes, and presence of a 5-cm mass in the abdominal cavity. The hemogram showed high leukocytosis by neutrophilia. The animal was treated with enrofloxacin for 7 days, with no

improvement. The abdominal ultrasonography revealed enlargement of the spleen and presence of masses (*4 cm in diameter) with echogenicity compatible to lymph node. The sample punctured from the axillary lymph node was cultured for aerobic and anaerobic bacteria, but the results were negative. In September 2007, the animal was treated with azithromycin for 10 days. Although the animal had a normal appetite, it remained apathetic with enlarged lymph nodes. The right inguinal lymph node was surgically removed for histopathological and bacteriological examinations. The microscopic exams revealed absence of neoplastic cells and negative results for herpes virus and acid-fast bacteria. The azithromycin therapy was extended for another 15 days. A bloody and purulent sample was punctured from the inguinal lymph node to attempt mycobacteria isolation. After ceftiofur and support therapy, despite normal appetite, the animal was still apathetic and prostrate at the end of December, dying in the beginning of January. At necropsy, the animal was emaciated. Lymph nodes hyperplasia and caseous nodules in parietal and visceral pleura, lungs, liver, spleen, and kidneys were observed. Histological sections stained by hematoxilin–eosin were prepared. For bacteriological exams, the lesions fragments were

1

Faculdade de Medicina Veterina´ria e Zootecnia, Universidade de Sa˜o Paulo, Sa˜o Paulo, SP, Brazil. Zoolo´gico do Parque Municipal Estoril, Sa˜o Paulo, SP, Brazil.

2

593

594 homogenized, decontaminated by the Petroff method, inoculated into Stonebrink and Lo¨wenstein-Jensen media, and incubated at 378C up to 90 days (Centro Panamericano de Zoonosis 1973). The acid-fast isolates were identified by the methods of polymerase chain reaction restriction analysis (Telenti et al. 1993) and Spoligotyping (Kamerbeek et al. 1997). Results The microscopic exam showed the massive presence of granulomatous lesions. After 30 days of incubation, acid-fast bacilli tested positive by the Ziehl-Neelsen staining were isolated from all samples and classified as M. tuberculosis complex by polymerase chain reaction restriction analysis and identified as M. tuberculosis by Spoligotyping method. Discussion Seven zoo workers who had had close contact with the infected primate were submitted to sputum exam and thorax radiography. According to the physician who was responsible for the tuberculosis county program, there were no suspicious signs that justified further examination. These results and the animal history indicate two hypotheses: The monkey was already infected, as it was born in another Brazilian zoo and no tuberculin testing was performed when it was transferred to the Parque Estoril Zoo, in 2005; or a tuberculous visitor transmitted the infection to the A. paniscus inside the Parque Estoril Zoo. Although M. tuberculosis infection in non-human primates has been widely reported (Vervenne et al. 2004), this is the first description of tuberculosis in A. paniscus. This report strengthens the need for implementing active surveillance against tuberculosis in the Brazilian zoo environment. Acknowledgment The authors wish to thank FAPESP for financial support.

ROCHA ET AL. Disclosure Statement No competing financial interests exist. References Alfonso, R, Romero, RE, Diaz, A, Calderon, MN, et al. Isolation and identification of mycobacteria in New World primates maintained in captivity. Vet Microbiol 2004; 98:285–295. Centro Panamericano de Zoonosis. Metodos de laborato´rio de micobacteriologia veterinaria para el aislamiento e identification de micobacterias. Buenos Aires (se´rie de monografı´as cientificas y tecnicas, 6), 1973. Kamerbeek, J, Schouls, L, Kolk, A, Van Agterveld, M, et al. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 1997; 35:907–914. Montali, RJ, Mikota, SK, Cheng, LI. Mycobacterium tuberculosis in zoos and wildlife species. Rev Sci Tech 2001; 20:291–303. Telenti, A, Marchesi, F, Balz, M, Bally, F, et al. Rapid identification of mycobacteria to the species level by polymerase chain reaction and restriction enzyme analysis. J Clin Microbiol 1993; 31:175–178. Vervenne, RAW, Jones, SL, van Soolingen, D, van der Laan, T, et al. TB diagnosis in non-human primates: comparison of two interferon-g assays and the skin test for identification of Mycobacterium tuberculosis infection. Vet Immunol Immunopathol 2004; 100:61–71.

Address correspondence to: Ca´ssia Yumi Ikuta Faculdade de Medicina Veterina´ria e Zootecnia Universidade de Sa˜o Paulo Av. Prof Dr Orlando Marques de Paiva 87, Cidade Universita´ria Sa˜o Paulo, SP, 05508-270 Brazil E-mail: [email protected]