The American Journal of Medicine
Volume 121, Issue 10 , Pages 835-844 , October 2008

Extensively Drug-resistant Tuberculosis

  • Miguel G. Madariaga, MD

      Affiliations

    • Section of Infectious Diseases, University of Nebraska Medical Center, Omaha
    • Corresponding Author InformationRequests for reprints should be addressed to Miguel G. Madariaga, MD, Section of Infectious Diseases, University of Nebraska Medical Center, 988106 Nebraska Medical Center, Omaha, NE 68198-8106
  • ,
  • Umesh G. Lalloo, MBChB, MD, FCCP

      Affiliations

    • Nelson Mandela School of Medicine, University of Kwa Zulu Natal, Durban, South Africa
  • ,
  • Susan Swindells, MBBS

      Affiliations

    • Section of Infectious Diseases, University of Nebraska Medical Center, Omaha

References 

  1. Gandhi NR, Moll A, Sturm AW, et al. Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet. 2006;368:1575–1580
  2. Shah NS, Wright A, Bai GH, et al. Worldwide emergence of extensively drug-resistant tuberculosis. Emerg Infect Dis. 2007;13:380–387
  3. Centers for Disease Control and Prevention (CDC). Emergence of Mycobacterium tuberculosis with extensive resistance to second-line drugs—worldwide, 2000-2004. MMWR Morb Mortal Wkly Rep. 2006;55:301–305
  4. Centers for Disease Control and Prevention (CDC). Notice to readers: revised definition of extensively drug-resistant tuberculosis. MMWR Morb Mortal Wkly Rep. 2005;55:1576
  5. Friedland G. Confronting the catastrophe of M/XDR TB. Presented at: 15th Conference on Retroviruses and Opportunistic Infections, February 3-6, 2008; Boston, Massachusetts.
  6. Bateman C. XDR-TB or not XDR-TB? (That is the question). S Afr Med J. 2007;97:318–322
  7. Kam KM, Yip CW. Surveillance of Mycobacterium tuberculosis susceptibility to second-line drugs in Hong Kong, 1995-2002, after the implementation of DOTS-plus. Int J Tuberc Lung Dis. 2004;8:760–766
  8. Khuê PM, Truffot-Pernot C, Texier-Maugein J, Jarlier V, Robert J. A 10-year prospective surveillance of Mycobacterium tuberculosis drug resistance in France 1995-2004. Eur Respir J. 2007;30:937–944
  9. Toungoussova OS, Mariandyshev AO, Bjune G, Caugant DA, Sandven P. Resistance of multidrug-resistant strains of Mycobacterium tuberculosis from the Archangel oblast, Russia, to second-line anti-tuberculosis drugs. Eur J Clin Microbiol Infect Dis. 2005;24:202–206
  10. Prammananan T, Arjratanakool W, Chaiprasert A, et al. Second-line drug susceptibilities of Thai multidrug-resistant Mycobacterium tuberculosis isolates. Int J Tuberc Lung Dis. 2005;9:216–219
  11. Masjedi MR, Fadaizadeh L, Taghizadeh Asl R. Notification of patients with tuberculosis detected in the private sector, Tehran, Iran. Int J Tuberc Lung Dis. 2007;11:882–886
  12. World Health Organization. Anti-tuberculosis Drug Resistance in the World: Report No. 4. Geneva, Switzerland: World Health Organization http://www.who.int/tb/publications/2008/drs_report4_26feb08.pdfAccessed April 11, 2008
  13. World Health Organization. Countries with XDR-TB confirmed cases as of February 2008. Geneva, Switzerland: World Health Organization http://www.who.int/tb/challenges/xdr/xdrmap_26feb08_en.pdfAccessed April 11, 2008
  14. Tuberculosis Division International Union Against Tuberculosis and Lung Disease. Tuberculosis bacteriology—priorities and indications in high prevalence countries: position of the technical staff of the Tuberculosis Division of the International Union Against Tuberculosis and Lung Disease. Int J Tuberc Lung Dis. 2005;9:355–361
  15. Centers for Disease Control and Prevention (CDC). Health advisory (Investigation of U.S. traveler with extensively drug resistant tuberculosis). Atlanta, GA: CDC http://www2a.cdc.gov/HAN/ArchiveSys/ViewMsgV.asp?AlertNum=00262Accessed April 11, 2008
  16. Centers for Disease Control and Prevention (CDC). Extensively drug-resistant tuberculosis—United States, 1993-2006. MMWR Morb Mortal Wkly Rep. 2007;56:250–253
  17. Iseman MD. Extensively drug-resistant Mycobacterium tuberculosis: Charles Darwin would understand. Clin Infect Dis. 2007;45:1415–1416
  18. Andrews JR, Shah NS, Gandhi N, Moll T, Friedland G Tugela Ferry Care and Research (TF CARES) Collaboration. Multidrug-resistant and extensively drug-resistant tuberculosis: implications for the HIV epidemic and antiretroviral therapy rollout in South Africa. J Infect Dis. 2007;196(Suppl 3):S482–S490
  19. Wells CD, Cegielski JP, Nelson LJ, et al. HIV infection and multidrug-resistant tuberculosis: the perfect storm. J Infect Dis. 2007;196(Suppl 1):S86–S107
  20. Havlir DV, Barnes PF. Tuberculosis in patients with human immunodeficiency virus infection. N Engl J Med. 1999;340:367–373
  21. Small PM, Shafer RW, Hopewell PC, et al. Exogenous reinfection with multidrug-resistant Mycobacterium tuberculosis in patients with advanced HIV infection. N Engl J Med. 1993;328:1137–1144
  22. Toossi Z. Virological and immunological impact of tuberculosis on human immunodeficiency virus type 1 disease. J Infect Dis. 2003;188:1146–1155
  23. Whalen C, Horsburgh CR, Hom D, Lahart C, Simberkoff M, Ellner J. Accelerated course of human immunodeficiency virus infection after tuberculosis. Am J Respir Crit Care Med. 1995;151:129–135
  24. Raviglione MC, Smith IM. XDR tuberculosis—implications for global public health. N Engl J Med. 2007;356:656–659
  25. Kapp C. XDR tuberculosis spreads across South Africa. Lancet. 2007;369:729
  26. Madariaga MG, Jalali Z, Swindells S. Clinical utility of interferon gamma assay in the diagnosis of tuberculosis. J Am Board Fam Med. 2007;20:540–547
  27. Pai M, Riley LW, Colford JM. Interferon-gamma assays in the immunodiagnosis of tuberculosis: a systematic review. Lancet Infect Dis. 2004;4:761–776
  28. Luetkemeyer AF, Charlebois ED, Flores LL, et al. Comparison of an interferon-gamma release assay with tuberculin skin testing in HIV-infected individuals. Am J Respir Crit Care Med. 2007;175:737–742
  29. Joh JS, Lee CH, Lee JE, et al. The interval between initiation of anti-tuberculosis treatment in patients with culture-positive pulmonary tuberculosis and receipt of drug-susceptibility test results. J Korean Med Sci. 2007;22:26–29
  30. Perkins MD, Cunningham J. Facing the crisis: improving the diagnosis of tuberculosis in the HIV era. J Infect Dis. 2007;196(Suppl 1):S15–S27
  31. Caviedes L, Lee TS, Gilman RH, et al. Rapid, efficient detection and drug susceptibility testing of Mycobacterium tuberculosis in sputum by microscopic observation of broth cultures (The Tuberculosis Working Group in Peru). J Clin Microbiol. 2000;38:1203–1208
  32. Moore DA, Evans CA, Gilman RH, et al. Microscopic-observation drug-susceptibility assay for the diagnosis of TB. N Engl J Med. 2006;355:1539–1550
  33. Arias M, Mello FCQ, Pavon A, et al. Clinical evaluation of the microscopic-observation drug-susceptibility assay for detection of tuberculosis. Clin Infect Dis. 2007;44:674–680
  34. Sethi S, Sharma S, Sharma SK, et al. Drug susceptibility of Mycobacterium tuberculosis to primary antitubercular drugs by nitrate reductase assay. Indian J Med Res. 2004;120:468–471
  35. Montoro E, Lemus D, Echemendia M, Martin A, Portaels F, Palomino JC. Comparative evaluation of the nitrate reduction assay, the MTT test, and the resazurin microtitre assay for drug susceptibility testing of clinical isolates of Mycobacterium tuberculosis. J Antimicrob Chemother. 2005;55:500–505
  36. Martin A, Palomino JC, Portaels F. Rapid detection of ofloxacin resistance in Mycobacterium tuberculosis by two low-cost colorimetric methods: resazurin and nitrate reductase assays. J Clin Microbiol. 2005;43:1612–1616
  37. De Logu A, Uda P, Pellerano ML, Pusceddu MC, Saddi B, Schivo ML. Comparison of two rapid colorimetric methods for determining resistance of Mycobacterium tuberculosis to rifampin, isoniazid, and streptomycin in liquid medium. Eur J Clin Microbiol Infect Dis. 2001;20:33–39
  38. Yajko DM, Madej JJ, Lancaster MV, et al. Colorimetric method for determining MICs of antimicrobial agents for Mycobacterium tuberculosis. J Clin Microbiol. 1995;33:2324–2327
  39. Palomino JC, Martin A, Camacho M, Guerra H, Swings J, Portaels F. Resazurin microtiter assay plate: simple and inexpensive method for detection of drug resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother. 2002;46:2720–2722
  40. Martin A, Portaels F, Palomino JC. Colorimetric redox-indicator methods for the rapid detection of multidrug resistance in Mycobacterium tuberculosis: a systematic review and meta-analysis. J Antimicrob Chemother. 2007;59:175–183
  41. Morcillo N, Di Giulio B, Testani B, Pontino M, Chirico C, Dolmann A. A microplate indicator-based method for determining the susceptibility of multidrug-resistant Mycobacterium tuberculosis to antimicrobial agents. Int J Tuberc Lung Dis. 2004;8:253–259
  42. Martin A, Camacho M, Portaels F, Palomino JC. Resazurin microtiter assay plate testing of Mycobacterium tuberculosis susceptibilities to second-line drugs: rapid, simple, and inexpensive method. Antimicrob Agents Chemother. 2003;47:3616–3619
  43. Pai M, Kalantri S, Pascopella L, Riley LW, Reingold AL. Bacteriophage-based assays for the rapid detection of rifampicin resistance in Mycobacterium tuberculosis: a meta-analysis. J Infect. 2005;51:175–187
  44. Banaiee N, Bobadilla-del-Valle M, Riska PF, et al. Rapid identification and susceptibility testing of Mycobacterium tuberculosis from MGIT cultures with luciferase reporter mycobacteriophages. J Med Microbiol. 2003;52:557–561
  45. Albert H, Trollip AP, Seaman T, et al. Evaluation of a rapid screening test for rifampicin resistance in re-treatment tuberculosis patients in the Eastern Cape. S Afr Med J. 2007;97:858–863
  46. Telenti A, Honoré N, Bernasconi C, et al. Genotypic assessment of isoniazid and rifampin resistance in Mycobacterium tuberculosis: a blind study at reference laboratory level. J Clin Microbiol. 1997;35:719–723
  47. Piatek AS, Telenti A, Murray MR, et al. Genotypic analysis of Mycobacterium tuberculosis in two distinct populations using molecular beacons: implications for rapid susceptibility testing. Antimicrob Agents Chemother. 2000;44:103–110
  48. Mokrousov I, Otten T, Filipenko M, et al. Detection of isoniazid-resistant Mycobacterium tuberculosis strains by a multiplex allele-specific PCR assay targeting katG codon 315 variation. J Clin Microbiol. 2002;40:2509–2512
  49. Hillemann D, Rüsch-Gerdes S, Richter E. Evaluation of the GenoType MTBDR plus assay for rifampin and isoniazid susceptibility testing of Mycobacterium tuberculosis strains and clinical specimens. J Clin Microbiol. 2007;45:2635–2640
  50. Traore H, van Deun A, Shamputa IC, Rigouts L, Portaels F. Direct detection of Mycobacterium tuberculosis complex DNA and rifampin resistance in clinical specimens from tuberculosis patients by line probe assay. J Clin Microbiol. 2006;44:4384–4388
  51. Hoek KG, Gey van Pittius NC, Moolman-Smook H, et al. Fluorometric assay for testing rifampin susceptibility of Mycobacterium tuberculosis complex. J Clin Microbiol. 2008;46:1369–1373
  52. Reid A, Scano F, Getahun H, et al. Towards universal access to HIV prevention, treatment, care, and support: the role of tuberculosis/HIV collaboration. Lancet Infect Dis. 2006;6:483–495
  53. Partners in Health. The PIH Guide to the Medical Management of Multidrug-Resistant Tuberculosis. Boston, MA: PIH http://www.pih.org/inforesources/pihguide-mdrtb.htmlAccessed April 11, 2008
  54. World Health Organization. Guidelines for the Programmatic Management of Drug-Resistant Tuberculosis. Geneva, Switzerland: WHO; 2006;Available at: http://whqlibdoc.who.int/publications/2006/9241546956_eng.pdf. Accessed April 11, 2008
  55. Francis J Curry National Tuberculosis Center and California Department of Health. Drug-resistant tuberculosis: a survival guide for clinicians. San Francisco: Francis J. Curry National Tuberculosis Center; 2008;Available at http://www.nationaltbcenter.edu/drtb/docs/MDRTB_Web_Mar08.pdf. Accessed August 14, 2008
  56. Dickinson JM, Mitchison DA. Experimental models to explain the high sterilizing activity of rifampin in the chemotherapy of tuberculosis. Am Rev Respir Dis. 1981;123:367–371
  57. Nathanson E, Lambregts-van Weezenbeek C, Rich ML, et al. Multidrug-resistant tuberculosis management in resource-limited settings. Emerg Infect Dis. 2006;12:1389–1397
  58. Tsukamura M. Drug-resistance test for kanamycin and cross resistance problem in Mycobacterium tuberculosis with special reference to kanamycin, streptomycin, and viomycin. J Antibiot (Tokyo). 1959;12:189–191
  59. McClatchy JK, Kanes W, Davidson PT, Moulding TS. Cross-resistance in M. tuberculosis to kanamycin, capreomycin and viomycin. Tubercle. 1977;58:29–34
  60. Nuermberger EL, Yoshimatsu T, Tyagi S, et al. Moxifloxacin-containing regimens of reduced duration produce a stable cure in murine tuberculosis. Am J Respir Crit Care Med. 2004;170:1131–1134
  61. Burman WJ, Goldberg S, Johnson JL, et al. Moxifloxacin versus ethambutol in the first 2 months of treatment for pulmonary tuberculosis. Am J Respir Crit Care Med. 2006;174:331–338
  62. Spigelman MK. New tuberculosis therapeutics: a growing pipeline. J Infect Dis. 2007;196(Suppl 1):S28–S34
  63. Okwera A, Johnson JL, Vjecha MJ, et al. Risk factors for adverse drug reactions during thiacetazone treatment of pulmonary tuberculosis in human immunodeficiency virus infected adults. Int J Tuberc Lung Dis. 1997;1:441–445
  64. Daley CL. Treatment and clinical outcome of patients infected with an MDR/XDR strain. Presented at: 38th Union World Conference on Lung Health, November 8-12, 2007, Cape Town, South Africa.
  65. Drobac PC, del Castillo H, Sweetland A, et al. Treatment of multidrug-resistant tuberculosis during pregnancy: long-term follow-up of 6 children with intrauterine exposure to second-line agents. Clin Infect Dis. 2005;40:1689–1692
  66. Drobac PC, Mukherjee JS, Joseph JK, et al. Community-based therapy for children with multidrug-resistant tuberculosis. Pediatrics. 2006;117:2022–2029
  67. Lounis N, Veziris N, Chauffour A, Truffot-Pernot C, Andries K, Jarlier V. Combinations of R207910 with drugs used to treat multidrug-resistant tuberculosis have the potential to shorten treatment duration. Antimicrob Agents Chemother. 2006;50:3543–3547
  68. Lenaerts AJ, Gruppo V, Marietta KS, et al. Preclinical testing of the nitroimidazopyran PA-824 for activity against Mycobacterium tuberculosis in a series of in vitro and in vivo models. Antimicrob Agents Chemother. 2005;49:2294–2301
  69. Lalloo UG, Naidoo R, Ambaram A. Recent advances in the medical and surgical treatment of multi-drug resistant tuberculosis. Curr Opin Pulm Med. 2006;12:179–185
  70. Panel on Antiretroviral Guidelines for Adults and Adolescents. Guidelines for the Use of Antiretroviral Agents in HIV-1-Infected Adults and Adolescents. Washington, DC: United States Department of Health and Human Services; 2008;Available at: http://aidsinfo.nih.gov/contentfiles/AdultandAdolescentGL.pdf. Accessed April 11, 2008
  71. World Health Organization. Antiretroviral Therapy for HIV Infection in Adults and Adolescents: Recommendations for a Public Health Approach. Geneva, Switzerland: WHO; 2006;Available at: http://www.who.int/hiv/pub/guidelines/artadultguidelines.pdf. Accessed April 11, 2008
  72. World Health Organization. Tuberculosis TB/HIV: A Clinical Manual. Geneva, Switzerland: WHO; 2004;Available at: http://whqlibdoc.who.int/publications/2004/9241546344.pdf. Accessed April 11, 2008
  73. Lawn SD, Myer L, Bekker LG, Wood R. Tuberculosis-associated immune reconstitution disease: incidence, risk factors and impact in an antiretroviral treatment service in South Africa. AIDS. 2007;21:335–341
  74. Breen RA, Swaden L, Ballinger J, Lipman MC. Tuberculosis and HIV co-infection: a practical therapeutic approach. Drugs. 2006;66:2299–2308
  75. Centers for Disease Control and Prevention (CDC). Management of persons exposed to multidrug-resistant tuberculosis. MMWR Recomm Rep. 1992;41(RR-11):61–71
  76. Grode L, Seiler P, Baumann S, et al. Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guérin mutants that secrete listeriolysin. J Clin Invest. 2005;115:2472–2479
  77. Pym AS, Brodin P, Majlessi L, et al. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat Med. 2003;9:533–539
  78. McShane H, Pathan AA, Sander CR, et al. Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat Med. 2004;10:1240–1244
  79. Nicas M. Respiratory protection and the risk of Mycobacterium tuberculosis infection. Am J Ind Med. 1995;27:317–333
  80. World Health Organization. Tuberculosis and Air Travel: Guidelines for Prevention and Control. Geneva, Switzerland: WHO; 2006;Available at: http://www.who.int/tb/publications/2006/who_htm_tb_2006_363.pdf. Accessed April 11, 2008
  81. Singh JA, Upshur R, Padayatchi N. XDR-TB in South Africa: no time for denial or complacency. PLoS Med. 2007;4:e50
  82. Moszynski P. Doctors disagree over detention of patients with extensively drug resistant tuberculosis. BMJ. 2007;334:228
  83. Stop TB Partnership. The global plan to stop TB. Geneva, Switzerland: Stop TB Partnership; 2008;Available at: http://www.stoptb.org/globalplan. Accessed April 11, 2008
  84. World Health Organization, 2007. The five elements of DOTS. Geneva, Switzerland: WHO; 2003;Available at: http://www.who.int/tb/dots/whatisdots/en/index.html. Accessed April 11, 2008
  85. Mitnick C, Bayona J, Palacios E, et al. Community-based therapy for multidrug-resistant tuberculosis in Lima, Peru. N Engl J Med. 2003;348:119–128
  86. World Health Organization. Tuberculosis XDR-TB: the facts. Geneva, Switzerland: WHO; 2008;Available at: http://www.who.int/tb/challenges/xdr/xdrmap_26feb08_en.pdf. Accessed April 11, 2008
  87. Harper C. Tuberculosis, a neglected opportunity?. Nat Med. 2007;13:309–312

PII: S0002-9343(08)00434-8

doi: 10.1016/j.amjmed.2008.04.015

The American Journal of Medicine
Volume 121, Issue 10 , Pages 835-844 , October 2008