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Volume 21, Number 3—March 2015
Letter

Disseminated Mycobacterium tuberculosis in Imported Sooty Mangabey, Thailand

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To the Editor: Tuberculosis caused by bacteria of the Mycobacterium tuberculosis complex affects humans and various species of captive and free-living wildlife (1). In addition, M. tuberculosis has been used experimentally in many different species of Old World monkeys as part of the attempt to establish a suitable model for human tuberculosis (2). We report a case of disseminated tuberculosis caused by M. tuberculosis Spoligotype International Type (SIT) 52 in a recently imported sooty mangabey (Cercocebus atys) from South Africa to Thailand.

A juvenile male sooty mangabey was imported from South Africa to Thailand in September 2009. Within 1 week, while in quarantine, convulsion and salivation developed in the mangabey, and it died suddenly. This animal, along with another mangabey and 4 mustached guenons (Cercopithecus cephus), was imported from its native Africa to Thailand for the pet trade. Complete histories of the second mangabey and the mustached guenons were not available.

A complete necropsy of the dead sooty mangabey was conducted, and full histopathologic and microbiological analysis was performed. At necropsy, the mangabey was emaciated, with no subcutaneous and abdominal fat tissues. Disseminated granulomas (up to 2 cm) were observed throughout the carcass, including the lungs, liver, spleen, kidneys, multiple lymph nodes (hilar, mediastinal, mesenteric, splenic, hepatic, renal, and pancreatic), and the ileum. The lung was also multifocally adhered to the thoracic wall and pleural diaphragm.

Histologically, the granulomas in all tissues examined demonstrated similar histopathologic features, characterized by a central core of caseous necrosis and surrounded by an unorganized rim of mixed inflammatory cells, including neutrophils, lymphocytes, plasma cells, and epithelioid macrophages. Numerous acid-fast bacilli were present in the cytoplasm of the epithelioid macrophages and in the necrotic area of all tissues. Acid-fast bacilli were isolated and classified as M. tuberculosis on the basis of 1-tube multiplex PCR (3) and sequencing of 16S rRNA gene results. Spoligotyping revealed that the M. tuberculosis isolate belonged to SIT 52.

The international wildlife trade had been reported to be a major source of imported zoonoses, particularly tuberculosis, in nonhuman primates (48). In the mangabey reported here, fulminant tuberculosis was diagnosed within 1 week after it arrived in Thailand, during the 21-day quarantine period. The granulomas were morphologically similar to the histopathologic description of tuberculosis lesions of experimentally infected cynomolgus macaques (Macaca fascicularis), which demonstrated lesions as early as 3 weeks after infection, with a gradual increase in severity (2). Previously, East African–Indian lineage (9) and Beijing spoligotype (SIT 1) accounted for most M. tuberculosis isolates in Thailand (10). In nonhuman primates in Thailand, M. tuberculosis complex had been detected at rates of up to 50% (5 positive samples from 10 test samples) by PCR from buccal swabs in long-tailed macaque (Macaca fascicularis) (1). M. tuberculosis belonging to SIT 52 observed in this case has been primarily isolated from countries in Africa (9). Only 1 case of M. tuberculosis belonging to SIT 52 that caused tuberculous meningitis was reported in a human in Thailand (10), but that case was not related to the case reported here. Our finding of a relatively novel spoligotype of M. tuberculosis in an animal destined for the pet trade underscores the need for intensive testing of and extended quarantine for all imported nonhuman primates to prevent the spread of newly isolated M. tuberculosis (4,7,8).

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Acknowledgments

We thank Areeya Disrattakit and Nampung Makao for their excellent technical assistance and Eric Lombardini and Roongroje Thanawongnuwech for their critical suggestions on this manuscript.

This report was financially supported by Grants for Development of New Faculty Staff, Ratchadaphiseksomphot Endowment Fund, Chulalongkorn University.

The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article, and no competing financial interests exist.

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Sawang KesdangsakonwutComments to Author , Angkana Sommanustweechai, and Angkana Chaiprasert

Author affiliations: Chulalongkorn University, Bangkok, Thailand (S. Kesdangsakonwut); Ministry of Public Health, Muang Nonthaburi, Thailand (A. Sommanusweechai); Mahidol University, Bangkok (A. Chaiprasert)

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References

  1. Wilbur  AK, Engel  GA, Rompis  A. A Putra IG, Lee BP, Aggimarangsee N, et al. From the mouths of monkeys: detection of Mycobacterium tuberculosis complex DNA from buccal swabs of synanthropic macaques. Am J Primatol. 2012;74:676–86. PubMed
  2. Lin  PL, Pawar  S, Myers  A, Pegu  A, Fuhrman  C, Reinhart  TA, Early events in Mycobacterium tuberculosis infection in cynomolgus macaques. Infect Immun. 2006;74:3790803 and. DOIPubMed
  3. Chaiprasert  A, Prammananan  T, Tingtoy  N, Na-Ubol  P, Srimuang  S, Samerpitak  K, One-tube multiplex PCR method for rapid identification of Mycobacterium tuberculosis. Southeast Asian J Trop Med Public Health. 2006;37:494502 .PubMed
  4. Panarella  ML, Bimes  RS. A naturally occurring outbreak of tuberculosis in a group of imported cynomolgus monkeys (Macaca fascicularis). J Am Assoc Lab Anim Sci. 2010;49:2215 .PubMed
  5. Centers for Disease Control and Prevention. Tuberculosis in imported nonhuman primates—United States, June 1990–May 1993. MMWR Morb Mortal Wkly Rep. 1993;42:5726 .PubMed
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  7. Shipley  ST, Coksaygan  T, Johnson  DK, McLeod  CG Jr, DeTolla  LJ. Diagnosis and prevention of dissemination of tuberculosis in a recently imported rhesus macaque (Macaca mulatta). J Med Primatol. 2008;37(Suppl 1):204 and. DOIPubMed
  8. Engel  GA, Wilbur  AK, Westmark  A, Horn  D, Johnson  J, Jones-Engel  L. Naturally acquired Mycobacterium tuberculosis complex in laboratory pig-tailed macaques. Emerg Microb Infect. 2012;1:e30.
  9. Brudey  K, Driscoll  JR, Rigouts  L, Prodinger  WM, Gori  A, Al-Hajoj  SA, Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol. 2006;6:23 and.PubMed
  10. Yorsangsukkamol  J, Chaiprasert  A, Prammananan  T, Palittapongarnpim  P, Limsoontarakul  S, Prayoonwiwat  N. Molecular analysis of Mycobacterium tuberculosis from tuberculous meningitis patients in Thailand. Tuberculosis (Edinb). 2009;89:3049 and. DOIPubMed

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Cite This Article

DOI: 10.3201/eid2103.131785

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Table of Contents – Volume 21, Number 3—March 2015

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Sawang Kesdangsakonwut, Department of Pathology, Faculty of Veterinary Science, Chulalongkorn University, Henri Dunant Rd, Pathumwan, Bangkok 10330, Thailand

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Page created: February 18, 2015
Page updated: February 18, 2015
Page reviewed: February 18, 2015
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
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