Isolation of Mycobacterium tuberculosis from Captive Ateles paniscus

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 São 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 homogenized, decontaminated by the Petroff method, inoculated into Stonebrink and Löwenstein-Jensen media, and incubated at 37°C 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.