Drug treatment combined with BCG vaccination reduces disease reactivation in guinea pigs infected with Mycobacterium tuberculosis

Vaccine

Volumn 30, Issue 9, 2012, Pages 1572-1582

  Shang, Shaobin ^a   Shanley, Crystal A ^a   Caraway, Megan L ^a   Orme, Eileen A ^a   Henao Tamayo, Marcela ^a   Hascall Dove, Laurel ^a   Ackart, David ^a   Orme, Ian M ^a   Ordway, Diane J ^a   Basaraba, Randall J ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

BCG vaccination; Drug therapy; Guinea pig; Tuberculosis

Indexed keywords

BCG VACCINE; ISONIAZID; PYRAZINAMIDE; RIFAMPICIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; BCG VACCINATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DRUG EFFICACY; EXPERIMENTAL GUINEA PIG; EXTRAPULMONARY TUBERCULOSIS; FEMALE; LEUKOCYTE COUNT; LONG TERM SURVIVAL; LUNG GRANULOMA; LUNG TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POSTPRIMARY TUBERCULOSIS; PRIORITY JOURNAL; SINGLE DRUG DOSE; TREATMENT DURATION;

ANIMALS; BCG VACCINE; COMBINED MODALITY THERAPY; FEMALE; GRANULOMA; GUINEA PIGS; ISONIAZID; LUNG; MYCOBACTERIUM TUBERCULOSIS; PYRAZINAMIDE; RIFAMPIN; TUBERCULOSIS;

EID: 84856795736     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.12.114     Document Type: Article

References (49)

1. Marsh B.J., von Reyn C.F., Edwards J., Ristola M.A., Bartholomew C., Brindle R.J., et al. The risks and benefits of childhood bacille Calmette-Guerin immunization among adults with AIDS. International MAC study groups. AIDS 1997, 11(5):669-672.
2. Trunz B.B., Fine P., Dye C. Effect of BCG vaccination on childhood tuberculous meningitis and miliary tuberculosis worldwide: a meta-analysis and assessment of cost-effectiveness. Lancet 2006, 367(9517):1173-1180.
3. Fine P.E. Variation in protection by BCG: implications of and for heterologous immunity. Lancet 1995, 346(8986):1339-1345.
4. Beresford B., Sadoff J.C. Update on research and development pipeline: tuberculosis vaccines. Clin Infect Dis 2010, 50(Suppl. 3):S178-S183.
5. Basaraba R.J., Dailey D.D., McFarland C.T., Shanley C.A., Smith E.E., McMurray D.N., et al. Lymphadenitis as a major element of disease in the guinea pig model of tuberculosis. Tuberculosis (Edinburgh) 2006, 86(5):386-394.
6. Irwin S.M., Goodyear A., Keyser A., Christensen R., Troudt J.M., Taylor J.L., et al. Immune response induced by three Mycobacterium bovis BCG substrains with diverse regions of deletion in a C57BL/6 mouse model. Clin Vaccine Immunol 2008, 15(5):750-756.
7. Ordway D., Henao-Tamayo M., Shanley C., Smith E.E., Palanisamy G., Wang B., et al. Influence of Mycobacterium bovis BCG vaccination on cellular immune response of guinea pigs challenged with Mycobacterium tuberculosis. Clin Vaccine Immunol 2008, 15(8):1248-1258.
8. Lagranderie M., Ravisse P., Marchal G., Gheorghiu M., Balasubramanian V., Weigeshaus E.H., et al. BCG-induced protection in guinea pigs vaccinated and challenged via the respiratory route. Tubercle Lung Dis 1993, 74(1):38-46.
9. Ahmad Z., Klinkenberg L.G., Pinn M.L., Fraig M.M., Peloquin C.A., Bishai W.R., et al. Biphasic kill curve of isoniazid reveals the presence of drug-tolerant: not drug-resistant, Mycobacterium tuberculosis in the guinea pig. J Infect Dis 2009, 200(7):1136-1143.
10. Lenaerts A.J., Hoff D., Aly S., Ehlers S., Andries K., Cantarero L., et al. Location of persisting mycobacteria in a Guinea pig model of tuberculosis revealed by r207910. Antimicrob Agents Chemother 2007, 51(9):3338-3345.
11. Smith D.W., Balasubramanian V., Wiegeshaus E. A guinea pig model of experimental airborne tuberculosis for evaluation of the response to chemotherapy: the effect on bacilli in the initial phase of treatment. Tubercle 1991, 72(3):223-231.
12. Ulrichs T., Lefmann M., Reich M., Morawietz L., Roth A., Brinkmann V., et al. Modified immunohistological staining allows detection of Ziehl-Neelsen-negative Mycobacterium tuberculosis organisms and their precise localization in human tissue. J Pathol 2005, 205(5):633-640.
13. Barclay W.R., Ebert R.H., Le Roy G.V., Manthei R.W., Roth L.J. Distribution and excretion of radioactive isoniazid in tuberculous patients. J Am Med Assoc 1953, 151(16):1384-1388.
14. Manthei R.W., Roth L.J., Barclay W.R., Ebert R.H. The distribution of C14 labeled isoniazid in normal and infected guinea pigs. Arch Int Pharmacodyn Ther 1954, 98(2):183-192.
15. Barry C.E., Boshoff H.I., Dartois V., Dick T., Ehrt S., Flynn J. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 2009, 7(12):845-855.
16. Gomez J.E., McKinney J.D. M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis (Edinburgh) 2004, 84(1-2):29-44.
17. Manabe Y.C., Bishai W.R. Latent Mycobacterium tuberculosis-persistence: patience, and winning by waiting. Nat Med 2000, 6(12):1327-1329.
18. Klinkenberg L.G., Sutherland L.A., Bishai W.R., Karakousis P.C. Metronidazole lacks activity against Mycobacterium tuberculosis in an in vivo hypoxic granuloma model of latency. J Infect Dis 2008, 198(2):275-283.
19. Timm J., Post F.A., Bekker L.G., Walther G.B., Wainwright H.C., Manganelli R., et al. Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. Proc Natl Acad Sci U S A 2003, 100(24):14321-14326.
20. Ryan G.J., Hoff D.R., Driver E.R., Voskuil M.I., Gonzalez-Juarrero M., Basaraba R.J., et al. Multiple M. tuberculosis phenotypes in mouse and guinea pig lung tissue revealed by a dual-staining approach. PLoS One 2010, 5(6):e11108.
21. Saunders B.M., Orme I.M., Basaraba R.J. Immunopathology of tuberculosis. Handbook of tuberculosis: immunology and cell biology 2008, 245-278. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim. S.H.E. Kaufmann, W.J. Britton (Eds.).
22. Dhillon J., Mitchison D.A. Influence of BCG-induced immunity on the bactericidal activity of isoniazid and rifampicin in experimental tuberculosis of the mouse and guinea-pig. Br J Exp Pathol 1989, 70(1):103-110.
23. Guirado E., Gil O., Caceres N., Singh M., Vilaplana C., Cardona P.J. Induction of a specific strong polyantigenic cellular immune response after short-term chemotherapy controls bacillary reactivation in murine and guinea pig experimental models of tuberculosis. Clin Vaccine Immunol 2008, 15(8):1229-1237.
24. Shang S., Shanley C.A., Caraway M.L., Orme E.A., Henao-Tamayo M., Hascall-Dove L., et al. Activities of TMC207: rifampin, and pyrazinamide against Mycobacterium tuberculosis infection in guinea pigs. Antimicrob Agents Chemother 2011, 55(1):124-131.
25. Ordway D.J., Shanley C.A., Caraway M.L., Orme E.A., Bucy D.S., Hascall-Dove L., et al. Evaluation of standard chemotherapy in the guinea pig model of tuberculosis. Antimicrob Agents Chemother 2010, 54(5):1820-1833.
26. Ordway D., Palanisamy G., Henao-Tamayo M., Smith E.E., Shanley C., Orme I.M., et al. The cellular immune response to Mycobacterium tuberculosis infection in the guinea pig. J Immunol 2007, 179(4):2532-2541.
27. Hummler H.D., Pohlandt F., Franz A.R. Pulse oximetry during low perfusion caused by emerging pneumonia and sepsis in rabbits. Crit Care Med 2002, 30(11):2501-2508.
28. Grover A., Taylor J., Troudt J., Keyser A., Arnett K., Izzo L., et al. Kinetics of the immune response profile in guinea pigs after vaccination with Mycobacterium bovis BCG and infection with Mycobacterium tuberculosis. Infect Immun 2009, 77(11):4837-4846.
29. Basaraba R.J., Smith E.E., Shanley C.A., Orme I.M. Pulmonary lymphatics are primary sites of Mycobacterium tuberculosis infection in guinea pigs infected by aerosol. Infect Immun 2006, 74(9):5397-5401.
30. Tan B.T., Ekelaar F., Luirink J., Rimmelzwaan G., De Jonge A.J., Scheper R.J. Production of monoclonal antibodies defining guinea pig T-cell surface markers and a strain 13 Ia-like antigen: the value of immunohistological screening. Hybridoma 1985, 4(2):115-124.
31. Takizawa M., Chiba J., Haga S., Asano T., Yamazaki T., Yamamoto N., et al. Novel two-parameter flow cytometry (MIL4/SSC followed by MIL4/CT7) allows for identification of five fractions of guinea pig leukocytes in peripheral blood and lymphoid organs. J Immunol Methods 2006, 311(1-2):47-56.
32. Hart I.J., Schafer H., Scheper R.J., Stevenson G.T. Subpopulations of guinea-pig T lymphocytes defined by isoforms of the leucocyte common antigen. Immunology 1992, 77(3):377-384.
33. Haverson K., Bailey M., Higgins V.R., Bland P.W., Stokes C.R. Characterization of monoclonal antibodies specific for monocytes: macrophages and granulocytes from porcine peripheral blood and mucosal tissues. J Immunol Methods 1994, 170(2):233-245.
34. Kraal G., Shiamatey-Koolma R., Hoffer M., Baker D., Scheper R. Histochemical identification of guinea-pig macrophages by monoclonal antibody MR-1. Immunology 1988, 65(4):523-528.
35. Wilcox C.E., Baker D., Butter C., Willoughby D.A., Turk J.L. Differential expression of guinea pig class II major histocompatibility complex antigens on vascular endothelial cells in vitro and in experimental allergic encephalomyelitis. Cell Immunol 1989, 120(1):82-91.
36. Palanisamy G.S., Smith E.E., Shanley C.A., Ordway D.J., Orme I.M., Basaraba R.J. Disseminated disease severity as a measure of virulence of Mycobacterium tuberculosis in the guinea pig model. Tuberculosis (Edinburgh) 2008.
37. Turner O.C., Basaraba R.J., Orme I.M. Immunopathogenesis of pulmonary granulomas in the guinea pig after infection with Mycobacterium tuberculosis. Infect Immun 2003, 71(2):864-871.
38. Via L.E., Lin P.L., Ray S.M., Carrillo J., Allen S.S., Eum S.Y., et al. Tuberculous granulomas are hypoxic in guinea pigs: rabbits, and nonhuman primates. Infect Immun 2008, 76(6):2333-2340.
39. Ahmad Z., Fraig M.M., Pinn M.L., Tyagi S., Nuermberger E.L., Grosset J.H., et al. Effectiveness of tuberculosis chemotherapy correlates with resistance to Mycobacterium tuberculosis infection in animal models. J Antimicrob Chemother 2011, 66(7):1560-1566.
40. Cardona P.J., Amat I., Gordillo S., Arcos V., Guirado E., Diaz J., et al. Immunotherapy with fragmented Mycobacterium tuberculosis cells increases the effectiveness of chemotherapy against a chronical infection in a murine model of tuberculosis. Vaccine 2005, 23(11):1393-1398.
41. Ha S.J., Jeon B.Y., Youn J.I., Kim S.C., Cho S.N., Sung Y.C. Protective effect of DNA vaccine during chemotherapy on reactivation and reinfection of Mycobacterium tuberculosis. Gene Ther 2005, 12(7):634-638.
42. Basaraba R.J., Izzo A.A., Brandt L., Orme I.M. Decreased survival of guinea pigs infected with Mycobacterium tuberculosis after multiple BCG vaccinations. Vaccine 2006, 24(3):280-286.
43. Palanisamy G.S., DuTeau N., Eisenach K.D., Cave D.M., Theus S.A., Kreiswirth B.N., et al. Clinical strains of Mycobacterium tuberculosis display a wide range of virulence in guinea pigs. Tuberculosis (Edinburgh) 2009, 89(3):203-209.
44. Canetti G. The tubercle bacillus in the pulmonary lesion of man 1955, Springer Publishing, Inc., New York.
45. Kara I., Yeler D., Yeler H., Ay S. Panoramic radiographic appearance of massive calcification of tuberculous lymph nodes. J Contemp Dental Pract 2008, 9(6):108-114.
46. Warmelink I., ten Hacken N.H., van der Werf T.S., van Altena R. Correlation between serum tumor necrosis factor alpha levels and clinical severity of tuberculosis. Braz J Infect Dis 2008, 12(3):226-233.
47. Ly L.H., Russell M.I., McMurray D.N. Cytokine profiles in primary and secondary pulmonary granulomas of Guinea pigs with tuberculosis. Am J Respir Cell Mol Biol 2008, 38(4):455-462.
48. Warmelink I., ten Hacken N.H., van der Werf T.S., van Altena R. Weight loss during tuberculosis treatment is an important risk factor for drug-induced hepatotoxicity. Br J Nutr 2011, 105(3):400-408.
49. Basaraba R.J. Experimental tuberculosis: the role of comparative pathology in the discovery of improved tuberculosis treatment strategies. Tuberculosis (Edinb) 2008, 88(Suppl. 1):S35-S47.