From the Mouths of Monkeys: Detection of Mycobacterium tuberculosis Complex DNA From Buccal Swabs of Synanthropic Macaques

American Journal of Primatology

Volumn 74, Issue 7, 2012, Pages 676-686

  Wilbur, Alicia K ^a   Engel, Gregory A ^b   Rompis, Aida ^c   Putra, I G A A ^c   Lee, Benjamin P Y H ^d   Aggimarangsee, Nantiya ^e   Chalise, Mukesh ^f   Shaw, Eric ^g   Oh, Gunwha ^a   Schillaci, Michael A ^h   Jones Engel, Lisa ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Swedish Cherry Hill Family Medicine   (United States)

^c University of Udayana   (Indonesia)

^d National Parks Board   (Singapore)

^e CHIANG MAI UNIVERSITY   (Thailand)

^f TRIBHUVAN UNIVERSITY   (Nepal)

^g GIBRALTAR ORNITHOLOGICAL AND NATURAL HISTORY SOCIETY   (Gibraltar)

^h UNIVERSITY OF TORONTO   (Canada)

Author keywords

Gibraltar; Mycobacterium tuberculosis complex, MTBC; Nepal; Nonhuman primate; Southeast Asia

Indexed keywords

BACTERIAL DNA;

BACTERIUM; DISEASE PREVALENCE; DNA; MOLECULAR ANALYSIS; PARASITE PREVALENCE; PARASITE TRANSMISSION; PATHOGEN; PRIMATE; TUBERCULOSIS;

ANIMAL; ARTICLE; CHEEK; CROSS-SECTIONAL STUDY; GENETICS; GIBRALTAR; HUMAN; INDONESIA; MACACA; MICROBIOLOGY; MOUTH MUCOSA; MYCOBACTERIUM TUBERCULOSIS; NEPAL; PET ANIMAL; POLYMERASE CHAIN REACTION; SINGAPORE; THAILAND; TUBERCULOSIS; ZOO ANIMAL;

ANIMALS; ANIMALS, ZOO; CHEEK; CROSS-SECTIONAL STUDIES; DNA, BACTERIAL; GIBRALTAR; HUMANS; INDONESIA; MACACA; MOUTH MUCOSA; MYCOBACTERIUM TUBERCULOSIS; NEPAL; PETS; POLYMERASE CHAIN REACTION; SINGAPORE; THAILAND; TUBERCULOSIS;

GIBRALTAR; SOUTHEAST ASIA;

MACACA; MYCOBACTERIUM TUBERCULOSIS COMPLEX; PRIMATES;

EID: 84861560761     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.22022     Document Type: Article

References (57)

1. Alfonso R, Romero RE, Diaz A, Calderon MN, Urdaneta G, Arce J, Patarroyo ME, Patarroyo MA. 2004. Isolation and identification of mycobacteria in New World primates maintained in captivity. Vet Micro 98:285-295.
2. Amado A, Albuquerque T, Goncalves A, Duarte E, Botelho A, Fernandes T, Bernardino R, Lapao N. 2006. Tuberculosis in mandrills at the Lisbon zoo. Vet Rec 159:643.
3. American Thoracic Society. 2000. Diagnostic standards and classification of tuberculosis in adults and children. Am J Resp Crit Care Med 161:1376-1395.
4. Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, Eiglmeier K, Garnier T, Gutierrez C, Hewinson G, Kremer K, Parsons LM, Pym AS, Samper S, van SD, Cole ST. 2002. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Nat Acad Sci USA 99:3684-3689.
5. Capuano SV, III, Croix DA, Pawar S, Zinovik A, Myers A, Lin PL, Bissel S, Fuhrman C, Klein E, Flynn JL. 2003. Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect Immun 71:5831-5844.
6. CDC. 1993. Tuberculosis in imported nonhuman primates-United States, June 1990-May 1993. Morb Mortal Wkly Rep 42:572-576.
7. Cortes J, Shaw E. 2006. The Gibraltar macaques: management and future. In: Hodges JK, Cortes J, editors. The Barbary macaque: biology, management and conservation. Nottingham: Nottingham University Press. p 185-198.
8. Eisenach KD. 1994. Use of an insertion sequence for laboratory diagnosis and epidemiologic studies of tuberculosis. Ann Emerg Med 24:450-453.
9. Eisenach KD, Sifford MD, Cave MD, Bates JH, Crawford JT. 1991. Detection of Mycobacterium tuberculosis in sputum samples using a polymerase chain reaction. Amer Rev Respir Dis 144:1160-1163.
10. Engel GA, Pizarro M, Shaw E, Cortes J, Fuentes A, Barry P, Lerche N, Grant R, Cohn D, Jones-Engel L. 2008. Unique pattern of enzootic primate viruses in Gibraltar macaques. Emerg Infect Dis 14:1112-1115.
11. Fairbrother R. 1932. Spontaneous diseases observed in 600 monkeys. J Path Bact 35:867-873.
12. Flynn JL, Capuano SV, Croix D, Pawar S, Myers A, Zinovik A, Klein E. 2003. Non-human primates: a model for tuberculosis research. Tuber (Edinb) 83:116-118.
13. Fooden J. 1976. Provisional classifications and key to living species of macaques (primates: Macaca). Folia Primatol (Basel) 25:225-236.
14. Fox H. 1923. Disease in captive wild mammals. Philadelphia, PA: J. B. Lippincott.
15. Fuentes A. 2006. Human culture and monkey behavior: assessing the contexts of potential pathogen transmission between macaques and humans. Am J Primatol 68:880-896.
16. Fuentes A, Gamerl S. 2005. Disproportionate participation by age/sex classes in aggressive interactions between long-tailed macaques (Macaca fascicularis) and human tourists at padangtegal monkey forest, Bali, Indonesia. Am J Primatol 66:197-204.
17. Garcia MA, Bouley DM, Larson MJ, Lifland B, Moorhead R, Simkins MD, Borie DC, Tolwani R, Otto G. 2004. Outbreak of Mycobacterium bovis in a conditioned colony of rhesus (Macaca mulatta) and cynomolgus (Macaca fascicularis) macaques. Comp Med 54:578-584.
18. Gormus BJ, Blanchard JL, Alvarez XH, Didier PJ. 2004. Evidence for a rhesus monkey model of asymptomatic tuberculosis. J Med Primatol 33:134-145.
19. Gutierrez MC, Brisse S, Brosch R, Fabre M, Omais B, Marmiesse M, Supply P, Vincent V. 2005. Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Path 1:e5.
20. Habel K. 1947. Tuberculosis in a laboratory monkey colony: its spread and its control. Am Rev Tuber LV:77-92.
21. Jones-Engel L, Engel GA, Schillaci MA. 2005a. An ethnoprimatological assessment of disease transmission among humans and wild and pet macaques on the Indonesian island of Sulawesi. In: Patterson J, Wallis J, editors. Commensalism and conflict: the primate-human interface. p 196-221.
22. Jones-Engel L, Engel GA, Heidrich J, Chalise M, Poudel N, Viscidi R, Barry PA, Allan JS, Grant R, Kyes R. 2006a. Temple monkeys and health implications of commensalism, Kathmandu, Nepal. Emerg Inf Dis 12:900-906.
23. Jones-Engel L, Engel GA, Schillaci MA, Lee B, Heidrich J, Chalise M, Kyes RC. 2006b. Considering human-primate transmission of measles virus through the prism of risk analysis. Am J Primatol 68:868-879.
24. Jones-Engel L, Engel GA, Schillaci MA, Rompis A, Putra A, Suaryana KG, Fuentes A, Beer B, Hicks S, White R, Wilson B, Allan JS. 2005b. Primate-to-human retroviral transmission in Asia. Emerg Inf Dis 11:1028-1035.
25. Jones-Engel L, Steinkraus KA, Murray SM, Engel GA, Grant R, Aggimarangsee N, Lee BP, May C, Schillaci MA, Somgird C, Sutthipat T, Vojtech L, Zhao J, Linial ML. 2007. Sensitive assays for simian foamy viruses reveal a high prevalence of infection in commensal, free-ranging Asian monkeys. J Virol 81:7330-7337.
26. Kamerbeek J, Schouls L, Kolk A, van AM, van SD, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van EJ. 1997. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microb 35:907-914.
27. Kennard M, Schroeder C, Trask J, Paul J. 1939. A cutaneous test for tuberculosis in primates. Sci New Series 89:442-443.
28. Lerche NW, Yee JL, Capuano SV, Flynn JL. 2008. New approaches to tuberculosis surveillance in nonhuman primates. ILAR 49:170-178.
29. Lin PL, Rodgers M, Smith L, Bigbee M, Myers A, Bigbee C, Chiosea I, Capuano SV, Fuhrman C, Klein E, Flynn JL. 2009. Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infec Immun 77:4631-4642.
30. Machotka S, Chapple F, Stookey J. 1975. Cerebral tuberculosis in a rhesus monkey. J Am Vet Med Assoc 167:648-650.
31. Martin J. 1968. Tuberculosis if the spine (Pott's disease) in a rhesus monkey (Macaca mulatta). J Am Vet Med Assoc 153:914-917.
32. Martino M, Hubbard GB, Schlabritz-Loutsevitch N. 2007. Tuberculosis (Mycobacterium tuberculosis) in a pregnant baboon (Papio cynocephalus). J Med Primatol 36:108-112.
33. McHugh TD, Newport LE, Gillespie SH. 1997. IS6110 homologs are present in multiple copies in mycobacteria other than tuberculosis-causing mycobacteria. J Clin Microbio 35:1769-1771.
34. Michel AL, Coetzee ML, Keet DF, Mare L, Warren R, Cooper D, Bengis RG, Kremer K, van HP. 2009. Molecular epidemiology of Mycobacterium bovis isolates from free-ranging wildlife in South African game reserves. Vet Microb 133:335-343.
35. Michel A, Venter L, Espie I, Coetzee M. 2003. Mycobacterium tuberculosis infections in eight species at the National Zoological Gardens of South Africa, 1991-2001. J Zoo Wild Med 34:364-370.
36. Morton WR, Agy MB, Capuano SV, Grant RF. 2008. Specific pathogen-free macaques: definition, history, and current production. ILAR 49:137-144.
37. Motzel S, Lell J, Pouch W, Ngai D, Middleton M, Nolan T, Klein H. 1995. Polymerase chain reaction as a method to aid in diagnosis of Mycobacterium tuberculosis in a colony of cynomolgus monkeys [abstract]. Lab Anim Sci 45:453-454.
38. Panarella M, Bimes R. 2010. A naturally occurring outbreak of tuberculosis in a group of imported Cynomolgus monkeys (Macaca fascicularis). J Am Assoc Lab Anim Sci 49:221-225.
39. Rocha V, Ikuta C, Gomes MS, Quaglia F, Matsushima ER, Neto J. 2011. Isolation of Mycobacterium tuberculosis from captive Ateles paniscus. Vec Born Zoo Dis 11:593-594.
40. Rock F, Landi M, Meunier L, Morris T, Rolf L, Warnick C, McCreedy B, Hughes H. 1995. Diagnosis of a case of Mycobacterium tuberculosis in a cynomolgus (Macaca fascicularis) monkey colony by polymerase chain reaction and enzyme-linked immunosorbent assay. Lab Anim Sci 45:315-319.
41. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor: CSHL Press.
42. Sapolsky RM, Else JG. 1987. Bovine tuberculosis in a wild baboon population-epidemiologic aspects. J Med Primatol 16:229-235.
43. Schillaci MA, Jones-Engel L, Engel GA, Kyes RC. 2006. Exposure to human respiratory viruses among urban performing monkeys in Indonesia. Am J Trop Med Hyg 75:716-719.
44. Schillaci MA, Jones-Engel L, Engel GA, Paramastri Y, Iskandar E, Wilson B, Allan JS, Kyes RC, Watanabe R, Grant R. 2005. Prevalence of enzootic simian viruses among urban performance monkeys in Indonesia. Trop Med Int Heal 10:1305-1314.
45. Sha JC, Gumert MD, Lee B, Fuentes A, Chan S, Jones-Engel L. 2009. Status of the long-tailed macaque (Macaca fascicularis) in Singapore and implications for management. Biodiv Conser 18:2909-2926.
46. Singh P, Singla L, Gupta M, Sharma S, Sharma D. 2009. Epidemiology and chemotherapy of parasitic infections in wild omnivores in the Mahendra Choudhury zoological Park, Chhat Bir, Punjab. J Threaten Taxa 1:62-64.
47. Stockinger DE, Roellich KM, vogel KW, Eiffert KL, Torrence AE, Prentice JL, Stephens KG, Wallis CK, Hotchkiss CE, Murnane RD. 2011. Primary hepatic Mycobacterium tuberculosis complex infection with terminal dissemination in a pig-tailed macaque (Macaca nemestrina). J Am Assoc Lab Animal Sci 50:258-262.
48. Tarara R, Suleman M, Sapolsky R, Wabomba M, Else J. 1985. Tuberculosis in wild olive baboons, Papio cynocephalus anubis (Lesson), in Kenya. J Wild Dis 21:137-140.
49. Une Y, Mori T. 2007. Tuberculosis as a zoonosis from a veterinary perspective. Comp Immunol 30:425.
50. van Bogaert L, Innes J. 1962. Neurologic diseases of apes and monkeys. In: Innes J, Saunders LZ, editors. Comparative neuropathology. New York: Academic Press. pp 108-112.
51. Vervenne RAW, Jones SL, van Soolingen D, van der Laan T, Peter A, Heidt PJ, Thomas AW, Langermans JAM. 2004. TB diagnosis in non-human primates: comparison of two interferon-gamma assays and the skin test for identification of Mycobacterium tuberculosis infection. Vet Immunol Immunopath 100:61-71.
52. West C, Vainisi S, Vygantas C, Beluhan F. 1981. Intraocular granulomas associated with tuberculosis in primates. J Am Vet Med Assoc 179:1240-1244.
53. WHO. 2009. Global tuberculosis control-epidemiology, strategy, financing. WHO Report 2009. Geneva: World Health Organization. p 1-28.
54. Wolfe ND, Escalante AA, Karesh WB, Kilbourn A, Spielman A, Lal AA. 1998. Wild primate populations in emerging infectious disease research: the missing link? Emerg Infect Dis 4:149-158.
55. Young JS, Gormley E, Wellington EM. 2005. Molecular detection of Mycobacterium bovis and Mycobacterium bovis BCG (Pasteur) in soil. Appl Environ Microbio 71:1946-1952.
56. Zumpe D, Silberman MS, Michael RP. 1980. Unusual outbreak of tuberculosis due to Mycobacterium bovis in a closed colony of rhesus monkeys (Macaca mulatta). Lab Anim Sci 30:237-240.
57. Gibson S. 1998. Bacterial and mycotic diseases: non-human primates in biomedical research. San Diego: Academic Press. p 59-110.