New approaches to tuberculosis surveillance in nonhuman primates

ILAR Journal

Volumn 49, Issue 2, 2008, Pages 170-178

  Lerche, Nicholas W ^a,b   Yee, JoAnn L ^c   Capuano, Saverio V ^d   Flynn, Joanne L ^e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF WISCONSIN   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Diagnosis; Nonhuman primates; Screening tests; Surveillance; Tuberculosis

Indexed keywords

GAMMA INTERFERON; TUBERCULIN;

BLOOD ANALYSIS; CELLULAR IMMUNITY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST; ENZYME LINKED IMMUNOSPOT ASSAY; HEALTH CARE COST; HEALTH SURVEY; IMMUNE RESPONSE; IMMUNOASSAY; IN VITRO STUDY; LABORATORY DIAGNOSIS; MEDICAL TECHNOLOGY; MULTIANTIGEN PRINT IMMUNOASSAY; MULTIPLEX MICROBEAD IMMUNOASSAY; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIMATE; PROTEIN SECRETION; RAPID TEST LATERAL FLOW IMMUNOASSAY; RELIABILITY; REVIEW; SCREENING; SENSITIVITY AND SPECIFICITY; TUBERCULIN TEST; TUBERCULOSIS; ANIMAL; ARTICLE; MASS SCREENING; METHODOLOGY; REPRODUCIBILITY;

ANIMALIA; MAMMALIA; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS COMPLEX; PRIMATES;

ANIMALS; MASS SCREENING; PRIMATES; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TUBERCULOSIS;

EID: 48949120110     PISSN: 10842020     EISSN: None     Source Type: Journal    
DOI: 10.1093/ilar.49.2.170     Document Type: Review

References (52)

1. Affronti LF, Fife EH, Grow L. 1973. Serodiagnostic test for tuberculosis. Am Rev Respir Dis 107:822-825.
2. Amor YB, Shashkina E, Johnson S, Bifani PJ, Kurepina N, Kreiswirth B, Bhattacharya S, Spencer J, Rendon A, Catanzaro A, Gennaro ML. 2005. Immunological characterization of novel secreted antigens of Mycobacterium tuberculosis. Scand J Immunol 61:139-146.
3. Andersen P, Munk ME, Pollock JM, Doherty TM. 2000. Specific immune-based diagnosis of tuberculosis. Lancet 356:1099-1104.
4. Brammer DW, O'Rourke CM, Heath LA, Chrisp CE, Peter GK, Hofnig GL. 1995. Mycobacterium kansasii infection in squirrel monkeys (Saimiri sciureus). J Med Primatol 24:231-235.
5. Brusasca PN, Peters RL, Motzel SL, Klein HJ, Gennaro ML. 2003. Antigen recognition by serum antibodies in non-human primates experimentally infected with Mycobacterium tuberculosis. Comp Med 53:165-172.
6. Butler TM, Brown BG, Dysko RC, Ford EW, Hoskins DE, Klein HJ, Levin JL, Murray KA, Rosenberg DP, Southers JL, Swensen RB. 1995. Medical management. In: Bennet BT, Abee CR, Henrickson R, eds. Nonhuman Primates in Biomedical Research. San Diego: Academic Press. p 257-334.
7. Capuano SV 3rd, 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.
8. CDC. 1991. Update: Nonhuman primate importation. MMWR 40:684-685, 691.
9. CDC. 1993. Tuberculosis in imported nonhuman primates: United States, June 1990-May 1993. MMWR 42:572-576.
10. Chaparas SD, Hedrick SR, Clark RG, Garman R. 1970. Comparison of the lymphocyte transformation test with the tuberculin test in rhesus monkeys and chimpanzees. Am J Vet Res 31:1437-1441.
11. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eilmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagles K, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandram MA, Rogers J, Rutter S, Seeger K, Skelton K, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544.
12. Collins HL, Kaufmann SH. 2001. The many faces of host responses to tuberculosis. Immunology 103:1-9.
13. Corcoran KD, Thoen CO. 1991. Application of an enzyme immunoassay for detecting antibodies in sera of Macaca fascicularis naturally exposed to Mycobacterium tuberculosis. J Med Primatol 20:404-408.
14. Davidow A, Kanaujia GV, Shi L, Kaviar J, Guo XS, Kaplan G, Menzies D, Gennaro ML. 2005. Antibody profiles characteristic of Mycobacterium tuberculosis infection state. Infect Immun 73:6846-6851.
15. Detjen AK, Keil T, Roll S, Hauer B, Mauch H, Wahn U, Magdorf K. 2007. Interferon-gamma release assays improve the diagnosis of tuberculosis and nontuberculosis mycobacterial disease in children in a country with low incidence of tuberculosis. Clin Infect Dis 45:322-328.
16. Fletcher HA. 2007. Correlates of immune protection from tuberculosis. Curr Mol Med 7:319-325.
17. Flynn JL, Chan J. 2001. Tuberculosis: Latency and reactivation. Infect Immun 69: 4195-4201.
18. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178:2249-2254.
19. Garcia MA, Bouley DM, Larson MJ, Lifland B, Moorehead R, Simkins MD, Borie DC, Tolwani R, Otto G. 2004a. Outbreak of Mycobacterium bovis in a conditioned colony of rhesus (Macaca mulatta) and cynomolgus (Macaca fascicularis) macaques. Comp Med 54:578-584.
20. Garcia MA, Yee J, Bouley DM, Moorhead R, Lerche NW. 2004b. Diagnosis of tuberculosis in macaques, using whole-blood in vitro interferon-gamma (PRIMAGAM) testing. Comp Med 54:86-92.
21. Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, Pryor M, Duthoy S, Grondin S, Lacroix C, Monsempe C, Simon S, Harris B, Atkin R, Doggett K, Mayes R, Keating L, Wheeler PR, Parkhill J, Barrell BG, Cole ST, Gordon SV, Hewinson RG. 2003. The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci U S A 100:7877-7882.
22. Gibson S. 1998. Bacterial and Mycotic Diseases: Non-human Primates in Biomedical Research. San Diego: Academic Press. p 59-110.
23. Goodwin BT, Jerome CP, Bullock BC. 1988. Unusual lesion morphology and skin test reaction for Mycobacterium avium complex in macaques. Lab Anim Sci 38:20-24.
24. Gormus BJ, Blanchard JL, Alvarez XH, Didier PJ. 2004. Evidence for a rhesus monkey model of asymptomatic tuberculosis. J Med Primatol 33:134-145.
25. Greenwald R, Lyashchenko K, Esfandiari J, Gibson S, Didier P, McCombs C, Stutzman L. 2007. Prima-TB STAT-PAKTM assay, a novel rapid test for tuberculosis in nonhuman primates [Abstract #182]. Am J Primatol 69(Suppl 1):120.
26. Harboe M, Oettinger T, Wiker HG, Rosenkrands I, Andersen P. 1996. Evidence for occurrence of the ESAT-6 protein in Mycobacterium tuberculosis and virulent Mycobacterium bovis and for its absence in Mycobacterium bovis BCG. Infect Immun 64:16-22.
27. Heywood R, Medd RK, Street AE. 1970. The early clinical diagnosis of tuberculosis in baboons. Br Vet J 126:372-382.
28. Kanaujia GV, Garcia MA, Bouley DM, Peters R, Gennaro ML. 2003. Detection of early secretory antigenic target-6 antibody for diagnosis of tuberculosis in non-human primates. Comp Med 53:602-606.
29. Kanaujia GV, Motzel S, Garcia MA, Andersen P, Gennaro ML. 2004. Recognition of ESAT-6 sequences by antibodies in sera of tuberculous nonhuman primates. Clin Diagn Lab Immunol 11:222-226.
30. Kaufmann AF. 1971. A program for surveillance of nonhuman primate disease. Lab Anim Sci 21:1061-1067.
31. Kennard MA, Schroeder CR, Trask JD, Paul JR. 1939. A cutaneous test for tuberculosis in primates. Science 89:442-443.
32. Khan IH, Ravindran R, Yee JL, Ziman M, Lewinsohn D, Gennaro M, Flynn J, Goulding C, DeReimer K, Lerche NW, Luciw PA. Profiling antibodies to Mycobacterium tuberculosis by multiplex microbead suspension arrays for serodiagnosis of tuberculosis. Clin Vacc Immunol (in press).
33. Lin PL, Pawar S, Myers A, Pegu A, Fuhrman C, Reinhart TA, Capuano SV, Klein E, Flynn JL. 2006. Early events in Mycobacterium tuberculosis infection in cynomolgus macaques. Infect Immun 74:3790-3803.
34. Lyashchenko KP, Singh M, Colangeli R, Gennaro ML. 2000. A multi-antigen print immunoassay for the development of serological diagnosis of infectious diseases. J Immunol Methods 242:91-100.
35. Lyashchenko KP, Greenwald R, Esfandiari K, Olsen JH, Ball R, Dumonceaux G, Dunker F, Buckley C, Richard M, Murray S, Payeur JB, Andersen P, Pollock JM, Mikota S, Miller M, Sofranko D, Waters WR. 2006. Tuberculosis in elephants: Antibody responses to defined antigens of Mycobacterium tuberculosis, potential for early diagnosis, and monitoring of treatment. Clin Vaccine Immunol 13:722-732.
36. Mayall CG, Lamb VA, Coleman PH. 1981. Infection in rhesus (Macaca mulatta) and squirrel (Saimiri sciureus) monkeys due to Mycobacterium tuberculosis phage type B: Outbreak in a primate colony. J Med Primatol 10:302-311.
37. Meya DB, McAdam KP. 2007. The TB pandemic: An old problem seeking new solutions. J Intern Med 261:309-329.
38. Montali RJ, Mikota SK, Cheng LI. 2001. Mycobacterium tuberculosis in zoo and wildlife species. Rev Sci Technol 20:291-303.
39. Motzel SL, Schachner RD, Kornegay RW, Fletcher MA, Kanaya B, Gomez JA, Ngai DT-W, Pouch WJ, Washington MV, Handt LA, Wagner JL, Klein H. 2003. Diagnosis of tuberculosis in nonhuman primates. In: International Perspectives: The Future of Nonhuman Primate Resources. Washington: National Academies Press. p 156-159.
40. Muscoplat CC, Thoen CO, McLaughlin RM, Thoenig JR, Chen AW, Johnson DW. 1975. Comparison of lymphocyte stimulation and tuberculin skin reactivity in Mycobacterium bovis-infected Macaca mulatta. Am J Vet Res 36:699-701.
41. NRC [National Research Council]. 1980. Laboratory Animal Management: Nonhuman Primates. ILAR News XXIII(2-3). Washington: National Academy Press.
42. Pollock JM, Girvin RM, Lightbody KA, Clements RA, Neill SD, Buddle BM, Andersen P. 2000. Assessment of defined antigens for the diagnosis of bovine tuberculosis in skin test-reactor cattle. Vet Record 146:659-665.
43. Richter CB, Lehner NDM, Henrickson RV. 1984. Primates. In: Fox JG, Cohen BJ, Loew FM, eds. Laboratory Animal Medicine. Orlando: Academic Press. p 298-383.
44. Roberts JA, Andrews K. 2008. Nonhuman primate quarantine: Its evolution and practice. ILAR J 49:145-156.
45. Rock FM, Landi MS, Meunier LD, Morris TH, Rolf LL, Warnick CL, McCreedy BJ, Hughes HC. 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.
46. Sapolsky RM, Else JG. 1987. Bovine tuberculosis in a wild baboon populaton: Epidemiologic aspects. J Med Primatol 16:229-235.
47. Soave O, Jackson S, Ghumman JS. 1981. Atypical mcyobacteria as the probable cause of positive tuberculin reactions in squirrel monkeys (Saimiri sciureus). Lab Anim Sci 31:295-296.
48. Staley EC, Southers JL, Thoen CO, Easley SP. 1995. Evaluation of tuberculin testing and measles prophylaxis procedures used in rhesus macaque quarantine/conditioning protocols. Lab Anim Sci 45:125-130.
49. Vervenne RA, Jones SL, Van Soolingen D, Van Der Laan T, Andersen P, Heidt PJ, Thomas AW, Langermans JA. 2004. TB diagnosis in nonhuman primates: Comparison of two interferon-gamma assays and the skin test for identification of Mycobacterium tuberculosis infection. Vet Immunol Immunop 100:61-71.
50. Walsh GP, Tan EV, dela Cruz EC, Abalos RM, Villahermosa LG, Young LG, Cellona RV, Nazzareno JB, Horwitz MA. 1996. The Philippine cynomolgus monkey (Macaca fascicularis) provides a new nonhuman primate model of tuberculosis that resembles human disease. Nat Med 2:430-436.
51. Wang JY, Chou CH, Lee LN, Hsu HL, Jan IS, Hsueh PR, Yang PC, Luh KT. 2007. Diagnosis of tuberculosis by an enzyme-linked immunospot assay for interferon-gamma. Emerg Infect Dis 13:553-558.
52. Wood PR, Jones SL. 2001. BOVIGAM: An in vitro cellular diagnostic test for bovine tuberculosis. Tuberculosis 81:147-155.