Susceptibility Test Methods: Mycobacteria, Nocardia, and Other Actinomycetes

Gail L. Woods; Shou-Yean Grace Lin; Edward P. Desmond

doi:10.1128/9781555817381.ch76

Chapter 76 : Susceptibility Test Methods: Mycobacteria, Nocardia, and Other Actinomycetes

Authors: Gail L. Woods, Shou-Yean Grace Lin, Edward P. Desmond

Content Type: Reference

Publication Year: 2015

Category: Clinical Microbiology

Book DOI: 10.1128/9781555817381

Chapter DOI: 10.1128/9781555817381.ch76

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Abstract:

This chapter has four major sections. First is a brief review of antimicrobial agents used to treat mycobacterial infections. This is followed by a discussion of methods used to test susceptibility of Mycobacterium tuberculosis complex to first- and second-line agents. Methods described are agar proportion, rapid broth systems, broth microdilution, and molecular techniques, which are being used with increasing frequency. The next topic is susceptibility testing of nontuberculous mycobacteria by broth microdilution, focusing on Mycobacterium avium complex, Mycobacterium kansasii, Mycobacterium marinum, and the rapidly growing mycobacteria. The last section covers susceptibility testing of Nocardia species by broth microdilution and includes a brief discussion of other aerobic actinomycetes.

Citation: Woods G, Lin S, Desmond E. 2015. Susceptibility Test Methods: Mycobacteria, Nocardia, and Other Actinomycetes, p 1356-1378. In Jorgensen J, Pfaller M, Carroll K, Funke G, Landry M, Richter S, Warnock D (ed), Manual of Clinical Microbiology, Eleventh Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817381.ch76

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References

/content/book/10.1128/9781555817381.mcm11.ch76

1. World Health Organization. 2008. New Laboratory Diagnostic Tools for Tuberculosis Control. World Health Organization, Geneva, Switzerland.

2. World Health Organization. 2008. Guidelines for the Programmatic Management of Drug-Resistant Tuberculosis. WHO/HTM/TB/2008.402. World Health Organization, Geneva, Switzerland.

3. Lawn SD,, Mwaba P,, Bates M,, Piatek A,, Alexander H,, Marais BJ,, Cuevas LE,, McHugh TD,, Zijenah L,, Kapata N,, Abubakar I,, Hoelscher M,, Hemish ZA,, Migliori BB,, Kim Pl,, Mauerer M,, Schito M,, Zumla A. 2003. Advances in tuberculosis diagnostics: the Xpert MTB/RIF assay and future prospects for a point-of-care test. Lancet Infect Dis 13: 349– 361.

4. LoBue P,, Sizemore C,, Castro KG. 2009. Plan to combat extensively drug-resistant tuberculosis: recommendations of the Federal tuberculosis task force. MMWR Recommend Rep 58( RR-03): 1– 43.

5. Centers for Disease Control and Prevention. 2006. Revised definition of extensively drug-resistance tuberculosis. MMWR Morb Mortal Wkly Rep 55: 1176.

6. Mitnick CD,, McGee B,, Peloquin CA. 2009. Tuberculosis pharmacotherapy: strategies to optimize patient care. Expert Opin Pharmacother 10: 381– 401.

7. Moore DA,, Evans CAW,, Gilman RH,, Caviedes L,, Coronel J,, Vivar A,, Sanchez E,, Pinedo Y,, Saravia JC,, Salazar C,, Oberhelman R,, Hollm-Delgado M-G,, LaChira D,, Escombe AR,, Friedland JS. 2007. Microscopic-observation drug-susceptibility assay for the diagnosis of TB. N Engl J Med 355: 1539– 1550.

8. Minion J,, Leung E,, Menzies D,, Pai M. 2010. Microscopic-observation drug susceptibility and thin layer agar assays for the detection of drug resistant tuberculosis: a systematic review and meta-analysis. Lancet Infect Dis 10: 688– 698.

9. Griffith DE,, Aksamit T,, Brown-Elliott B,, Catanzaro A,, Daley C,, Gordin F,, Holland SM,, Horsburgh R,, Huitt G,, Iademarco MF,, Iseman M,, Olivier K,, Ruoss S,, von Reyn CF,, Wallace RJ,, Winthrop K. 2007. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med. 175: 367– 416.

10. Griffith DE,, Aksamit TR. 2012. Therapy of refractory nontuberculous mycobacterial lung disease. Curr Opin Infect Dis 2: 218– 227.

11. Clinical and Laboratory Standards Institute. 2011. Susceptibility Testing of Mycobacteria, Nocardiae, and Other Aerobic Actinomycetes; Approved Standard, 2nd ed. CLSI Document M24-2A. Clinical and Laboratory Standards Institute, Wayne, PA.

12. Wade MM,, Zang Y. 2004. Mechanisms of drug resistance in Mycobacterium tuberculosis. Front Biosci 9: 975– 994.

13. Vilcheze C,, Jacobs WR. 2007. The mechanism of isoniazid killing: clarity through the scope of genetics. Annu Rev Microbiol 61: 35– 50.

14. Inderlied CB,, Nash KA,. 2005. Antimycobacterial agents: in vitro susceptibility testing and mechanisms of action and resistance, p 155– 225. In Lorian V ( ed.), Antibiotics in Laboratory Medicine. Lippincott Williams & Wilkins, Philadelphia, PA.

15. Winder FG,. 1982. Mode of action of the antimycobacterial agents and associated aspects of the molecular biology of the mycobacteria, p 353– 438. In Ratledge C,, Stanford J ( ed.), The Biology of the Mycobacteria, vol. 1. Physiology, Identification and Classification. Academic Press, Inc., New York, NY.

16. Winder FG,, Collins PB. 1969. The effect of isoniazid on nicotinamide nucleotide concentrations in tubercle bacilli. Am Rev Respir Dis 100: 101– 103.

17. Davis WB,, Weber MM. 1977. Specificity of isoniazid on growth inhibition and competition for an oxidized nicotiniamide adenine dinucleotide regulatory site on the electron transport pathway in Mycobacterium phlei. Antimicrob Agents Chemother 12: 213– 218.

18. Banerjee A,, Dubnau E,, Quemard A,, Balasubramanian V,, Um KS,, Wilson T,, Collins D,, de Lisle G,, Jacobs WR Jr. 1994. inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263: 227– 230.

19. Heym B,, Zhang Y,, Poulet S,, Young D,, Cole ST. 1993. Characterization of the katG gene encoding a catalase-peroxidase required for isoniazid susceptibility of Mycobacterium tuberculosis. J Bacteriol 175: 4255– 4259.

20. Mdluli K,, Sherman DR,, Hickey MJ,, Kreiswirth BN,, Morris S,, Stover CK,, Barry C III. 1996. Biochemical and genetic data suggest that InhA is not the primary target for activated isoniazid in Mycobacterium tuberculosis. J Infect Dis 174: 1085– 1090.

21. Kelley CL,, Rouse DA,, Morris SL. 1997. Analysis of ahpC gene mutations in isoniazid-resistant clinical isolates of Mycobacterium tuberculosis. Antimicrob Agents Chemother 41: 2057– 2058.

22. Sreevatsan S,, Pan X,, Zhang Y,, Deretic V,, Musser JM. 1997. Analysis of the oxyR-ahpC region in isoniazidresistant and -susceptible Mycobacterium tuberculosis complex organisms recovered from diseased humans and animals in diverse localities. Antimicrob Agents Chemother 41: 600– 606.

23. Telenti A,, Honore N,, Bernasconi C,, March J,, Ortega A,, Heym B,, Takiff HE,, Cole ST. 1997. Genotypic assessment of isoniazid and rifampin resistance in Mycobacterium tuberculosis: a blind study at reference laboratory level. J Clin Microbiol 35: 719– 723.

24. Musser JM. 1995. Antimicrobial agent resistance in mycobacteria: molecular genetic insights. Clin Microbiol Rev 8: 496– 514.

25. Van Deun A,, Barrera L,, Bastian I,, Fattorini L,, Hoffmann H,, Kam KM,, Rigouts L,, Rusch-Gerdes S,, Wright A. 2009. Mycobacterium tuberculosis strains with highly discordant rifampin susceptibility test results. J Clin Microbiol 47: 3501– 3506.

26. Benson C. 1997. Critical drug interactions with agents used for prophylaxis and treatment of Mycobacterium avium infections. Am J Med 102: 32– 36.

27. Saito H,, Sato K,, Tomioka H. 1988. Comparative in vitro and in vivo activity of rifabutin and rifampicin against Mycobacterium avium complex. Tubercle 69: 187– 192.

28. Bodmer T,, Zurcher G,, Imboden P,, Telenti A. 1995. Mutation position and type of substitution in the beta-subunit of the RNA polymerase influence in-vitro activity of rifamycins in rifampicin-resistant Mycobacterium tuberculosis. J Antimicrob Chemother 35: 345– 348.

29. Yang B,, Koga H,, Ohno H,, Ogawa K,, Fukuda M,, Hirakata Y,, Maesaki S,, Tomono K,, Tashiro T,, Kohno S. 1998. Relationship between antimycobacterial activities of rifampicin, rifabutin and KRM-1648 and rpoB mutations of Mycobacterium tuberculosis. J Antimicrob Chemother 42: 621– 628. (Erratum, 43:613, 1999.)

30. Masur H. 1993. Recommendations on prophylaxis and therapy for disseminated Mycobacterium avium complex disease in patients infected with the human-immunodeficiency-virus. N Engl J Med 329: 898– 904.

31. Takayama K,, Kilburn JO. 1989. Inhibition of synthesis of arabinogalactan by ethambutol in Mycobacterium smegmatis. Antimicrob Agents Chemother 33: 1493– 1499.

32. Starks A,, Gumusboga A,, Plikaytis BB,, Shinnick TM,, Posey JE. 2009. Mutations at embB codon 306 are an important molecular indicator of ethambutol resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 53: 1061– 1066.

33. Sreevatsan S,, Stockbauer KE,, Pan X,, Kreiswirth BN,, Moghazeh SL,, Jacobs W Jr,, Telenti A,, Musser JM. 1997. Ethambutol resistance in Mycobacterium tuberculosis: critical role of embB mutations. Antimicrob Agents Chemother 53: 1061– 1066.

34. Safi H,, Sayers B,, Hazbon MH,, Alland D. 2008. Transfer of embB codon 306 mutations into clinical Mycobacterium tuberculosis strains alters susceptibility to ethambutol, isoniazid, and rifampin. Antimicrob Agents Chemother 52: 2027– 2034.

35. Sison JP,, Yao Y,, Kemper CA,, Hamilton JR,, Brummer E,, Stevens DA,, Deresinski SC. 1996. Treatment of Mycobacterium avium complex infection: do the results of in vitro susceptibility tests predict therapeutic outcome in humans? J Infect Dis 173: 677– 683.

36. Hoffner SE,, Svenson SB,, Beezer AE. 1990. Microcalorimetric studies of the initial interaction between antimycobacterial drugs and Mycobacterium avium. J Antimicrob Chemother 25: 353– 359.

37. Zhang Y,, Mitchison D. 2003. The curious characteristics of pyrazinamide: a review. Int J Tuberc Lung Dis 7: 6– 21.

38. Jureen P,, Werngren J,, Toro J-C,, Hoffner S. 2008. Pyrazinamide resistance and pncA gene mutations in Mycobacterium tuberculosis. Antimicrob Agents Chemother 52: 1852– 1854.

39. Maus CE,, Plikaytis BB,, Shinnick TM. 2005. Molecular analysis of cross-resistance to capreomycin, kanamycin, amikacin, and viomycin in Mycobacterium tuberculosis. Antimicrob Agents Chemother 49: 3192– 3197.

40. Finken M,, Kirschner P,, Meier A,, Wrede A,, Böttger EC. 1993. Molecular basis of streptomycin resistance in Mycobacterium tuberculosis: alterations of the ribosomal protein S12 gene and point mutations within a functional 16S ribosomal RNA pseudoknot. Mol Microbiol 9: 1239– 1246.

41. Nair J,, Rouse DA,, Bai GH,, Morris SL. 1993. The rpsL gene and streptomycin resistance in single and multiple drug-resistant strains of Mycobacterium tuberculosis. Mol Microbiol 10: 521– 527.

42. Dukes CS,, Sugarman J,, Cegielski JP,, Lallinger GJ,, Mwakyusa DH. 1992. Severe cutaneous hypersensitivity reactions during treatment of tuberculosis in patients with HIV infection in Tanzania. Trop Geogr Med 44: 308– 311.

43. Andreis K,, Verhasselt P,, Guillemont J,, Gohleman HW,, Neefs JM,, Winkler H,, Van Gestel J,, Timmerman P,, Zhu M,, Lee E,, Williams P,, De Chaffoy D,, Huitric E,, Hoffner S,, Cambau E,, Truffot-Pernot C,, Lounis N,, Jarlier V. 2005. A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307: 223– 227.

44. Diacon AH,, Pym A,, Grosbusch M,, Patientia R,, Rustomjeee R,, Page-Shipp L,, Pistorius C,, Krause R,, Bogoshi M,, Churchyard G,, Venter A,, Allen J,, Palomino JC,, DeMarez T,, van Heeswijk RPG,, Lounis N,, Meyvisch P,, Verbeek J,, Parys W,, de Beule K,, Andries K,, McNeeley DF. 2009. The diarylquinoline TMC207 for multidrug-resistant tuberculosis. N Engl J Med 360: 2397– 2405.

45. Cohen J. 2013. Approval of novel TB drug celebrated—with restraint. Science 339: 130.

46. Segala E,, Sougakoff W,, Nevejans-Chauffor A,, Jarlier V,, Petrella S. 2012. New mutations in the mycobacterial ATP synthase: new insights into the binding of the dairylquinoline TMC207 to the ATP synthase C-ring structure. Antimicrob Agents Chemother 56: 2326– 2334.

47. Huitric E,, Verhasselt P,, Koul A,, Andries K,, Hoffner S,, Andersson DI. 2010. Rates and mechanisms of resistance development in Mycobacterium tuberculosis to a novel diarylquinoline ATP synthase inhibitor. Antimicrob Agents Chemother 54: 1022– 1028.

48. Heifets L,, Simon J,, Pham V. 2005. Capreomycin is active against non-replicating M tuberculosis. Ann Clin Microbiol Antimicrob 4: 6.

49. Maus CE,, Plikaytis BB,, Shinnick TM. 2005. Mutation of tlyA confers capreomycin resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 49: 572– 577.

50. Havlir DV,, Dube MP,, Sattler FR,, Forthal DN,, Kemper CA,, Dunne MW,, Parenti DM,, Lavelle JP,, White A,, Witt MD,, Bozzette SA,, McCutchan JA,, the California Collaborative Treatment Group. 1996. Prophylaxis against disseminated Mycobacterium avium complex with weekly azithromycin, daily rifabutin, or both. N Engl J Med 335: 392– 398.

51. Pierce M,, Crampton S,, Henry D,, Heifets L,, LaMarca A,, Montecalvo M,, Wormser GP,, Jablonowski H,, Jemsek J,, Cynamon M,, Yangco BG,, Notario G,, Craft JC. 1996. A randomized trial of clarithromycin as prophylaxis against disseminated Mycobacterium avium complex infection in patients with advanced acquired immunodeficiency syndrome. N Engl J Med 335: 384– 391.

52. Meier A,, Kirschner P,, Springer B,, Steingrube VA,, Brown BA,, Wallace RJ Jr,, Böttger EC. 1994. Identification of mutations in 23S rRNA gene of clarithromycin-resistant Mycobacterium intracellulare. Antimicrob Agents Chemother 38: 381– 384.

53. Nash KA,, Inderlied CB. 1995. Genetic basis of macrolide resistance in Mycobacterium avium isolated from patients with disseminated disease. Antimicrob Agents Chemother 39: 2625– 2630.

54. Wallace R Jr,, Meier A,, Brown BA,, Zhang Y,, Sander P,, Onyi GO,, Böttger EC. 1996. Genetic basis for clarithromycin resistance among isolates of Mycobacterium chelonae and Mycobacterium abscessus. Antimicrob Agents Chemother 40: 1676– 1681.

55. Koletar SL,, Berry AJ,, Cynamon MH,, Jacobson J,, Currier JS,, MacGregor RR,, Dunne MW,, Williams OJ. 1999. Azithromycin as treatment for disseminated Mycobacterium avium complex in AIDS patients. Antimicrob Agents Chemother 43: 2869– 2872.

56. Amsden GW. 1996. Erythromycin, clarithromycin, and azithromycin: are the differences real? Clin Ther 18: 56– 72.

57. Bozeman L,, Burman W,, Metchock B,, Welch L,, Weiner M,, the Tuberculosis Trials Consortium. 2005. Fluoroquinolone susceptibility among Mycobacterium tuberculosis isolates from the United States and Canada. J Infect Dis 40: 386– 391.

58. Young LS,, Berlin OG,, Inderlied CB. 1987. Activity of ciprofloxacin and other fluorinated quinolones against mycobacteria. Am J Med 82: 23– 26.

59. Ginsburg AS,, Grosset JH,, Bishai WR. 2003. Fluoroquinolones, tuberculosis, and resistance. Lancet Infect Dis 3: 432– 442.

60. Dorman SE,, Johnson JL,, Goldberg S,, Muzanye G,, Padayatchi N,, Bozeman L,, Heilig CM,, Bernardo J,, Choudhri S,, Grosset JH,, Guy E,, Guyadeen P,, Leus MC,, Maltas G,, Menzies D,, Nuermberger EL,, Villarino M,, Vernon A,, Chaisson RE. 2009. Substitution of moxifloxacin for isoniazid during intensive phase treatment of pulmonary tuberculosis. Am J Respir Crit Care Med 180: 273– 280.

61. Revel Viravau V,, Truong QC,, Moreau N,, Jarlier V,, Sougakoff W. 1996. Sequence analysis, purification, and study of inhibition by 4-quinolones of the DNA gyrase from Mycobacterium smegmatis. Antimicrob Agents Chemother 40: 2054– 2061.

62. Takiff HE,, Salazar L,, Guerrero C,, Philipp W,, Huang WM,, Kreiswirth B,, Cole ST,, Jacobs W Jr,, Telenti A. 1994. Cloning and nucleotide sequence of Mycobacterium tuberculosis gyrA and gyrB genes and detection of quinolone resistance mutations. Antimicrob Agents Chemother 38: 773– 780.

63. Berning SE,, Madsen L,, Iseman MD,, Peloquin CA. 1995. Long-term safety of ofloxacin and ciprofloxacin in the treatment of mycobacterial infections. Am J Respir Crit Care Med 151: 2006– 2009.

64. Tasneen R,, Tyagi S,, Williams K,, Grosset J,, Nuermberger E. 2008. Enhanced bactericidal activity of rifampin and/or pyrazinamide when combined with PA-824 in a murine model of tuberculosis. Antimicrob Agents Chemother 52: 3664– 3668.

65. Koh WJ,, Kwon OJ,, Gwak H,, Chung JW,, Cho SN,, Kim WS,, Shim TS. 2009. Daily 300 mg dose of linezolid for the treatment of intractable multidrug-resistant and extensively drug-resistant tuberculosis. J Antimicrob Chemother 64: 388– 391.

66. Ntziora F,, Falagas ME. 2007. Linezolid for the treatment of patients with mycobacterial infections: a systematic review. Int J Tuberc Lung Dis 11: 606– 611.

67. Canetti G,, Fox W,, Khomenko A,, Mahler HT,, Menon NK,, Mitchison DA,, Rist N,, Smelev NA. 1969. Advances in techniques of testing mycobacterial drug sensitivity, and the use of sensitivity tests in tuberculosis control programs. Bull World Health Organ 41: 21– 43.

68. Canetti G,, Froman S,, Grosset J,, Hauduroy P,, Lagerova M,, Mahler HT,, Meissner G,, Mitchison DA,, Sula L. 1963. Mycobacteria: laboratory methods for testing drug sensitivity and resistance. Bull World Health Organ 29: 565– 578.

69. Russel WR,, Middlebrook G. 1961. Chemotherapy of Tuberculosis. Charles C. Thomas, Springfield, IL.

70. Kubica GP,, Dye WE. 1967. Laboratory Methods for Clinical and Public Health Mycobacteriology. U.S. Government Printing Office, Washington, DC.

71. Canetti G. 1965. Present aspects of bacterial resistance in tuberculosis. Am Rev Respir Dis 92: 687– 702.

72. Howard WL,, Maresh F,, Mueller EE,, Yanitelli SA,, Woodruff GF. 1949. The role of pulmonary cavitation in the development of bacterial resistance to streptomycin. Am Rev Tuberc 59: 391– 401.

73. Howlett HS,, O’Connor JB,, Sadusk JF,, Swift JE,, Beardsley FA. 1949. Sensitivity of tubercle bacilli to streptomycin: the influence of various factors upon the emergence of resistant strains. Am Rev Tuberc 59: 402– 414.

74. David HL. 1970. Probability distribution of drug-resistant mutants in unselected populations of Mycobacterium tuberculosis. Appl Microbiol 20: 810– 814.

75. Crofton J,, Mitchison DA. 1948. Streptomycin resistance in pulmonary tuberculosis. Br Med J 2: 1009– 1015.

76. Pyle M. 1947. Relative number of resistant tubercle bacilli in sputa of patients before and during treatment with streptomycin. Proc Mayo Clin 22: 465– 473.

77. Mitchison DA. 1979. Basic mechanisms of chemotherapy. Chest 76( Suppl): 771– 781.

78. Burman WJ. 1997. The value of in vitro drug activity and pharmacokinetics in predicting the effectiveness of antimycobacterial therapy: a critical review. Am J Med Sci 313: 355– 363.

79. Kent PT,, Kubica GP. 1985. Public Health Mycobacteriology—a Guide for the Level III Laboratory. U.S. Department of Health and Human Services, Centers for Disease Control, Atlanta, GA.

80. Bergmann JS,, Woods GL. 1997. Mycobacterial growth indicator tube for susceptibility testing of Mycobacterium tuberculosis to isoniazid and rifampin. Diagn Microbiol Infect Dis 27: 153– 156.

81. Lin S-YG,, Desmond E,, Bonato D,, Gross W,, Siddiqui S. 2009. Multicenter evaluation of BACTEC MGIT 960 system for second-line drug susceptibility testing of Mycobacterium tuberculosis complex. J Clin Microbiol 47: 3630– 3634.

82. Rodrigues C,, Jani J,, Shenai S,, Thakker P,, Siddiqui S,, Mehta A. 2008. Drug susceptibility testing of Mycobacterium tuberculosis against second-line drugs using the Bactec MGIT 960 system. Int J Tuberc Lung Dis 12: 1449– 1455.

83. Rusch-Gerdes S,, Pfyffer GE,, Casal M,, Chadwick M,, Siddiqui S. 2006. Multicenter laboratory validation of the Bactec MGIT 960 techniques for testing susceptibilities of Mycobacterium tuberculosis to classical second-line drugs and new antimicrobials. J Clin Microbiol 44: 688– 692.

84. Tenover FC,, Crawford JT,, Huebner RE,, Geiter LJ,, Horsburgh CR,, Good RC. 1993. The resurgence of tuberculosis: is your laboratory ready? J Clin Microbiol 31: 767– 770.

85. Inderlied CB,, Nash KA,. 1996. Antimycobacterial agents: in vitro susceptibility testing, spectra of activity, mechanisms of action and resistance, and assays for activity in biologic fluids, p 127– 175. In Lorian V ( ed.), Antibiotics in Laboratory Medicine, 4th ed. The Williams & Wilkins Co., Baltimore, MD.

86. Heifets LB. 1991. Drug Susceptibility in the Chemotherapy of Mycobacterial Infections, p. 212. CRC Press, Inc., Boca Raton, FL.

87. Pfyffer GE,, Palicova F,, Rüsch-Gerdes S. 2002. Testing of susceptibility of Mycobacterium tuberculosis to pyrazinamide with the nonradiometric BACTEC MGIT 960 system. J Clin Microbiol 40: 1670– 1674.

88. Pfyffer GE,, Welscher HM,, Kissling P,, Cieslak C,, Casal MJ,, Gutierrez J,, Rüsch-Gerdes S. 1997. Comparison of the Mycobacteria Growth Indicator Tube (MGIT) with radiometric and solid culture for recovery of acid-fast bacilli. J Clin Microbiol 35: 364– 368.

89. Hawkins JE,. 1984. Drug susceptibility testing, p 177– 193. In Kubica GP,, Wayne LG ( ed), The Mycobacteria: a Sourcebook, part A. Marcel Dekker, Inc., New York, NY.

90. Madison B,, Robinson-Dunn B,, George I,, Gross W,, Lipman H,, Metchock B,, Sloutsky A,, Washabaugh G,, Mazurek G,, Ridderhof J. 2002. Multicenter evaluation of ethambutol susceptibility testing of Mycobacterium tuberculosis by agar proportion and radiometric methods. J Clin Microbiol 40: 3976– 3979.

91. Bémer P,, Palicova F,, Rüsch-Gerdes S,, Siddiqi SH,, Drugeon HB,, Pfyffer GE. 2002. Multicenter evaluation of fully-automated BACTEC Mycobacteria Growth Indicator Tube 960 System for susceptibility testing of Mycobacterium tuberculosis. J Clin Microbiol 40: 150– 154.

92. Kruuner A,, Yates MD,, Drobniewski FA. 2006. Evaluation of MGIT 960-based antimicrobial testing and determination of critical concentrations of first- and second-line antimicrobial drugs with drug-resistant clinical strains of Mycobacterium tuberculosis. J Clin Microbiol 44: 811– 818.

93. Rüsch-Gerdes S,, Domehl C,, Nardi G,, Gismondo MR,, Welscher HM,, Pfyffer GE. 1999. Multicenter evaluation of the mycobacteria growth indicator tube for testing susceptibility of Mycobacterium tuberculosis to first-line drugs. J Clin Microbiol 37: 45– 48.

94. Scarparo C,, Ricordi P,, Ruggiero G,, Piccoli P. 2004. Evaluation of the fully automated BACTEC MGIT 960 System for testing susceptibility of Mycobacterium tuberculosis to pyrazinamide, streptomycin, isoniazid, rifampin, and ethambutol and comparison with the radiometric BACTEC 460TB. J Clin Microbiol 42: 1109– 1114.

95. Horne DJ,, Pinto LM,, Arentz M,, Lin S-YG,, Desmond E,, Flores LL,, Steingart KR,, Minion J. 2013. Diagnostic accuracy and reproducibility of WHO-endorsed phenotypic drug susceptibility testing methods for first-line and second-line anti-tuberculosis drugs: a systematic review and meta-analysis. J Clin Microbiol 51: 393– 401.

96. Martin A,, von Groll A,, Fissette K,, Palomino JC,, Varaine F,, Portaels F. 2008. Rapid detection of Mycobacterium tuberculosis resistance to second-line drugs by use of the manual Mycobacterium Growth Indicator Tube system. J Clin Microbiol 46: 3952– 3956.

97. Chedore P,, Bertucci L,, Wolfe J,, Sharma M,, Jamieson F. 2010. Potential for erroneous results indicating resistance when using the Bactec MGIT 960 system for testing susceptibility of Mycobacterium tuberculosis to pyrazinamide. J Clin Microbiol 48: 300– 301.

98. Chiang LS,, Yew WW,, Zhang Y. 2011. Pyrazinamide susceptibility testing in Mycobacterium tuberculosis: a systematic review with meta-analysis. Antimicrob Agents Chemother 55: 4499– 4505.

99. Piersimoni C,, Mustazzolu A,, Giannoni F,, Bornigia S,, Gherardi G,, Fattorini L. 2013. Prevention of false resistance results obtained in testing the susceptibility of Mycobacterium tuberculosis to pyrazinamide with the BACTEC MGIT 960 system using a reduced inoculum. J Clin Microbiol 51: 291– 294.

100. Simons SO,, van Ingen J,, van der Laan T,, Mulder A,, Dekhuijzen PNR,, Broere MJ,, van Soolingen D. 2012. Validation of pncA gene sequencing in combination with the Mycobacterial Growth Indicator Tube method to test susceptibility of Mycobacterium tuberculosis to pyrazinamide. J Clin Microbiol 50: 428– 434.

101. Bergmann JS,, Woods GL. 1998. Evaluation of the ESP culture system II for testing susceptibilities of Mycobacterium tuberculosis isolates to four primary antituberculous drugs. J Clin Microbiol 36: 2940– 2943.

102. Ruiz P,, Zerolo FJ,, Casal MJ. 2000. Comparison of susceptibility testing of Mycobacterium tuberculosis using the ESP culture system II with that using the BACTEC method. J Clin Microbiol 38: 4663– 4664.

103. Espasa M,, Salvadó M,, Vincente E,, Tudó G,, Alcaide R,, Coll P,, Martin-Casabona N,, Torra M,, Fontanals D,, González-Martin J. 2012. Evaluation of the VersaTREK system compared to the Bactec MGIT 960 system for first-line drug susceptibility testing of Mycobacterium tuberculosis. J Clin Microbiol 50: 488– 491.

104. Barnard M,, Albert H,, Coetzee G,, O’Brien R,, Bosman ME. 2008. Rapid molecular screening for multidrug-resistant tuberculosis in a high-volume public health laboratory in South Africa. Am J Respir Crit Care Med 177: 787– 792.

105. Choi JH,, Lee KW,, Kang HR,, Hwang YI,, Jang S,, Kim DG,, Kim CH,, Hyun IG,, Shin TR,, Park SM,, Lee MG,, Lee CY,, Park YB,, Jung KS. 2010. Clinical efficacy of direct DNA sequencing analysis on sputum specimens for early detection of drug-resistant Mycobacterium tuberculosis in a clinical setting. Chest 137: 393– 400.

106. Hillemann D,, Rusch-Gerdes S,, Richter E. 2009. Feasibility of the GenoType MTBDRsl assay for fluoroquinolone, amikacin-capreomycin, and ethambutol resistance testing of Mycobacterium tuberculosis strains and clinical specimens. J Clin Microbiol 47: 1767– 1772.

107. Lin SY,, Probert W,, Lo M,, Desmond E. 2004. Rapid detection of isoniazid and rifampin resistance mutations in Mycobacterium tuberculosis complex from cultures or smear-positive sputa by use of molecular beacons. J Clin Microbiol 42: 4204– 4208.

108. Ling DI,, Zwerling AA,, Pai M. 2008. Rapid diagnosis of drug-resistant TB using line probe assays; from evidence to policy. Expert Rev Respir Med 2: 583– 588.

109. Migliori GB,, Matteelli A,, Cirillo D,, Pai M. 2008. Diagnosis of multidrug-resistant tuberculosis and extensively drug-resistant tuberculosis: current standards and challenges. Can J Infect Dis Med Microbiol 19: 169– 172.

110. Lin S-YG,, Rodwell TC,, Victor TC,, Rider EC,, Pham L,, Catanzaro A,, Desmond EP. 2014. Pyrosequencing for rapid detection of extensively drug-resistant tuberculosis in clinical isolates and clinical specimens. J Clin Microbiol 52: 475– 482.

111. Palomino JC. 2009. Molecular detection, identification, and drug-resistance detection in Mycobacterium tuberculosis. FEMS Immunol Med Microbiol 2009: 1– 9.

112. Piatek AS,, Telenti A,, Murray MR,, El-Hajj H,, Jacobs WR Jr,, Kramer FR,, Alland D. 2000. Genotypic analysis of Mycobacterium tuberculosis in two distinct populations using molecular beacons: implications for rapid susceptibility testing. Antimicrob Agents Chemother 44: 103– 110.

113. Hall L,, Jude KP,, Clark SL,, Dionne K,, Merson R,, Boyer A,, Parrish NM,, Wengenack NL. 2012. Evaluation of the Sensititre Myco TB plate for susceptibility testing of the Mycobacterium tuberculosis complex against first- and second-line agents. J Clin Microbiol 50: 3732– 3734.

114. Martin A,, Portaels F,, Palomino JC. 2007. Colorimetric redox-indicator methods for the rapid detection of multidrug resistance in Mycobacterium tuberculosis: a systematic review and meta-analysis. J Antimicrob Chemother 59: 175– 183. http://jac.oxfordjournals.org/content/59/2/175.full.pdf+html.

115. Martin A,, Paasch F,, Docx S,, Fissette K,, Imperiale B,, Ribón W,, González LA,, Werngren J,, Engström A,, Skenders G,, Juréen P,, Hoffner S,, Del Portillo P,, Morcillo N,, Palomino JC. 2011. Multicentre laboratory validation of the colorimetric redox indicator (CRI) assay for the rapid detection of extensively drug-resistant (XDR) Mycobacterium tuberculosis. J Antimicrob Chemother 66: 827– 833.

116. World Health Organization. 2011. Non-commercial culture and drug-susceptibility testing methods for screening patients at risk for multidrug-resistant tuberculosis 2011. http://whqlibdoc.who.int/publications/2011/9789241501 620_eng.pdf

117. Ruiz M,, Torres MJ,, Llanos AC,, Arroyo A,, Palomares JC,, Aznar J. 2004. Direct detection of rifampin-and-isoniazid-resistant Mycobacterium tuberculosis in auramine-rhodamine-positive sputum specimens by real-time PCR. J Clin Microbiol 42: 1585– 1589.

118. Diggle MA,, Clarke SC. 2004. Pyrosequencing (TM)—sequencing typing at the speed of light. Mol Biotechnol 28: 129– 138.

119. Rinder H,, Feldmann K,, Tortoli E,, Grosset J,, Casal M,, Richter E,, Rifai M,, Jarlier V,, Vaquero M,, Rüsch-Gerdes S,, Cambau E,, Gutierrez J,, Loscher T. 1999. Culture-independent prediction of isoniazid resistance in Mycobacterium tuberculosis by katG gene analysis directly from sputum samples. Mol Diagn 4: 145– 152.

120. Campbell PJ,, Morlock GP,, Sikes RD,, Dalton TL,, Metchock B,, Starks AM,, Hooks DP,, Cowan L,, Plikaytis BB,, Posey JE. 2011. Molecular detection of mutations associated with first- and second-line drug resistance compared with conventional drug susceptibility testing of Mycobacterium tuberculosis. Antimicrob Agents Chemother 55: 2032– 2041.

121. Bravo LTC,, Tuohy MJ,, Ang C,, Destura RV,, Mendoza M,, Procop GW,, Gordon SM,, Hall GS,, Shrestha NK. 2009. Pyrosequencing for rapid detection of Mycobacterium tuberculosis resistance to rifampin, isoniazid, and fluoroquinolones. J Clin Microbiol 47: 3985– 3990.

122. Jureen P,, Engstrand L,, Eriksson S,, Alderborn A,, Krabbe M,, Hoffner SE. 2006. Rapid detection of rifampin resistance in Mycobacterium tuberculosis by pyrosequencing technology. J Clin Microbiol 44: 1925– 1929.

123. Engstrom A,, Morcillo N,, Imperiale B,, Hoffner SE,, Jureen P. 2012. Detection of first- and second-line drug resistance in Mycobacterium tuberculosis clinical isolates by pyrosequencing. J Clin Microbiol 50: 2026– 2033.

124. Garcia-Sierra N,, Lacoma A,, Prat C,, Haba L,, Maldonado J,, Ruiz-Manzano J,, Gavin P,, Samper S,, Ausina V,, Dominguez J. 2011. Pyrosequencing for rapid molecular detection of rifampin and isoniazid resistance in Mycobacterium tuberculosis strains and clinical specimens. J Clin Microbiol 49: 3683– 3686.

125. Halse TA,, Edwards J,, Cunningham PL,, Wolfgang WJ,, Dumas NB,, Escuyer VE,, Musser KA. 2010. Combined real-time PCR and rpoB gene pyrosequencing for rapid identification of Mycobacterium tuberculosis and determination of rifampin resistance directly in clinical specimens. J Clin Microbiol 48: 1182– 1188.

126. Zhao J-R,, Bai Y-J,, Wang Y,, Zhang Q-H,, Luo M,, Yan X-J. 2005. Development of a pyrosequencing approach for rapid screening of rifampin, isoniazid and ethambutol-resistant Mycobacterium tuberculosis. Int J Tuber Lung Dis 9: 328– 332.

127. Koser CU,, Bryant JM,, Becq J,, Torok ME,, Ellington MJ,, MA Marti-Renom,, Carmichael AJ,, Parkhill J,, Smith GP,, Peacock SJ. 2013. Whole-genome sequencing for rapid susceptibility testing of M tuberculosis. N Engl J Med 369: 290– 292.

128. O’Riordan P,, Schwab U,, Logan S,, Cooke G,, Wilkinson RJ,, Davidson RN,, Bassett P,, Wall R,, Pasvol G,, Flanagan KL. 2008. Rapid molecular detection of rifampicin resistance facilitates early diagnosis and treatment of multidrug-resistant tuberculosis: case control study. PLoS ONE 3: e3173.

129. Banerjee R,, Allen J,, Lin S-YG,, Westenhouse J,, Desmond E,, Schecter GF,, Scott C,, Raftery A,, Mase S,, Watt JP,, Flood J. 2010. Rapid drug susceptibility testing with a molecular beacon assay is associated with earlier diagnosis and treatment of multidrug-resistant tuberculosis in California. J Clin Microbiol 48: 3779– 3781.

130. Kiet VS,, Lan NTN,, An DD,, Dung NH,, Hoa DV,, van Vinh Chau N,, Chinh NT,, Farrar J,, Caws M. 2010. Evaluation of the MTBDRsl test for detection of second-line-drug resistance in Mycobacterium tuberculosis. J Clin Microbiol 48: 2934– 2939.

131. Huang W-L,, Chi T-L,, Wu M-H,, Jou R. 2011. Performance assessment of the GenoType MTBDRsl Test and DNA sequencing for detection of second-line and ethambutol drug resistance among patients infected with multidrug-resistant Mycobacterium tuberculosis. J Clin Microbiol 49: 2502– 2508.

132. Alonso M,, Palacios JJ,, Herranz M,, Penedo A,, Menendez A,, Bouza E,, Garcia de Viedrna D. 2011. Isolation of Mycobacterium tuberculosis strains with a silent mutation in rpoB leading to potential misassignment of resistance category. J Clin Microbiol 49: 2688– 2690.

133. Boehme CC,, Nabeta P,, Hillernann D,, Nicol MP,, Shenai S,, Krapp F,, Allen J,, Tahirli R,, Blakemore R,, Rustomjee R,, Milovic A,, Jones M,, O’Brien SM,, Persing DH,, Ruesch-Gerdes S,, Gotuzzo E,, Rodrigues C,, Alland D,, Perkins MD. 2010. Rapid molecular detection of tuberculosis and rifampin resistance. N Engl J Med 363: 1005– 1015.

134. Kasperbauer SH,, Daley CL. 2008. Diagnosis and treatment of infections due to Mycobacterium avium complex. Semin Respir Care Med 29: 569– 576.

135. Chaisson RE,, Benson CA,, Dube MP,, Heifets LB,, Korvick JA,, Elkin S,, Smith T,, Craft JC,, Sattler FR,, the AIDS Clinical Trials Group Protocol 157 Study Team. 1994. Clarithromycin therapy for bacteremic Mycobacterium avium complex disease. Ann Intern Med 121: 905– 911.

136. Brown-Elliott BA,, Iakhiaeva E,, Griffith DE,, Woods G,, Stout JE,, Wolfe CR,, Turenne C,, Wallace RJ Jr. 2013. In vitro activity of amikacin against isolates of Mycobacterium avium complex with proposed MIC breakpoints and finding of a 16S gene mutation in treated isolates. J Clin Microbiol 51: 3389– 3394.

137. Clinical and Laboratory Standards Institute. 2014. Performance Standards for Antimicrobial Susceptibility Testing; 24th Informational Supplement. CLSI Document M100-S24. Clinical and Laboratory Standards Institute, Wayne, PA.

138. Griffith DE,, Brown-Elliott BA,, Wallace RJ Jr. 2003. Thrice-weekly clarithromycin-containing regimen for treatment of Mycobacterium kansasii lung disease: results of a preliminary study. Clin Infect Dis 37: 736– 743.

139. Bernard EM,, Edwards FF,, Kiehn TE,, Brown ST,, Armstrong D. 1993. Activities of antimicrobial agents against clinical isolates of Mycobacterium haemophilum. Antimicrob Agents Chemother 37: 2323– 2326.

140. Brown-Elliott BA,, Wallace RJ Jr. 2002. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin Microbiol Rev 15: 716– 746.

141. Woods GL,, Bergmann JS,, Witebsky FG,, Fahle GA,, Wanger A,, Boulet B,, Plaunt M,, Brown BA,, Wallace RJ Jr. 1999. Multisite reproducibility of results obtained by the broth microdilution method for susceptibility testing of Mycobacterium abscessus, Mycobacterium chelonae, and Mycobacterium fortuitum. J Clin Microbiol 37: 1676– 1682.

142. Agterof MJ,, van der Bruggen T,, Tersmette M,, ter Borg EJ,, van den Bosch JMM,, Biesma DH. 2007. Nocardiosis: a case series and a mini review of clinical and microbiological features. Neth J Med 65: 199– 202.

143. Blaschke AJ,, Bender J,, Byington CL,, Korgenski K,, Daly J,, Petti CA,, Pavia AT,, Ampofo K. 2007. Gordonia species: emerging pathogens in pediatric patients that are identified by 16S ribosomal RNA gene sequencing. Clin Infect Dis 45: 483– 486.

144. Bouza E,, Perez-Parra A,, Rosal M,, Martin-Rabadan P,, Rodriguez-Creixems M,, Marin M. 2009. Tsukamurella: a cause of catheter-related bloodstream infections. Eur J Clin Microbiol Infect Dis 28: 203– 210.

145. Brown-Elliott BA,, Brown J,, Conville PS,, Wallace RJ. 2006. Clinical and laboratory features of the Nocardia spp. based on current molecular taxonomy. Clin Microbiol Rev 19: 259– 282.

146. Jannat-Khah DP,, Halsey ES,, Lasker BA,, Steigerwalt AG,, Hinrikson HP,, Brown JM. 2009. Gordonia araii infection associated with an orthopedic device and review of the literature on medical device-associated Gordonia infections. J Clin Microbiol 47: 499– 502.

147. Sheng WH,, Huang YT,, Chang SC,, Hsueh PR. 2009. Brain abscess caused by Tsukamurella tyrosinosolvens in an immunocompetent patient. J Clin Microbiol 47: 1602– 1604.

148. Verma P,, Brown JM,, Nunez VH,, Morey RE,, Steigerwalt AG,, Pellegrini GJ,, Kessler HA. 2006. Native valve endocarditis due to Gordonia polyisoprenivorans: case report and review of literature of bloodstream infections caused by Gordonia species. J Clin Microbiol 44: 1905– 1908.

149. Waggoner JJ. 2009. First case report of communityacquired pneumonia due to Tsukamurella pulmonis. Ann Intern Med 150: 147– 148.

150. Conville PS,, Brown-Elliott BA,, Wallace RJ,, Witebsky FG,, Koziol D,, Hall GS,, Killian SB,, Knapp CC,, Warshauer D,, Van T,, Wengenack NL,, Deml S,, Woods GL. 2012. Multisite reproducibility of the broth microdilution method for susceptibility testing of Nocardia species. J Clin Microbiol 50: 1270– 1280.

151. Clinical and Laboratory Standards Institute. 2012. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard, 9th ed. CLSI Document M07-A9. Clinical and Laboratory Standards Institute, Wayne, PA.

152. Lee J,, Armstrong DT,, Ssengooba W,, Park JA,, Yu Y,, Mumbowa F,, Namaganda C,, Mboowa G,, Nakayita G,, Armakovitch S,, Chien G,, Cho SN,, Via LE,, Barry CE III,, Ellner JJ,, Alland D,, Doman SE,, Joloba ML. 2014. Sensititre MYCOTB MIC plate for testing Mycobacterium tuberculosis susceptibility to first- and second-line drugs. Antimicrob Agents Chemother 58: 11– 18.

153. Centers for Disease Control and Prevention. 2013. Availability of an assay for detecting Mycobacterium tuberculosis, including rifampin-resistant strains, and consideration for its use—United States, 2013. Morb Mortal Wkly Rep 62( 41): 821– 824.

Tables

Susceptibility Test Methods: Mycobacteria, Nocardia, and Other Actinomycetes

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/content/10.1128/9781555817381.mcm11.ch76.ch76.tab001

TABLE 1

Antimicrobial agents recommended for primary treatment of common mycobacterial infections a

TABLE 1

Antimicrobial agents recommended for primary treatment of common mycobacterial infections a

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TABLE 2

Genes associated with drug resistance in M. tuberculosis

TABLE 2

Genes associated with drug resistance in M. tuberculosis

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TABLE 3

Test concentrations a of antimycobacterial agents against M. tuberculosis complex

TABLE 3

Test concentrations a of antimycobacterial agents against M. tuberculosis complex

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TABLE 4

Guidelines for selection of the dilution of a specimen concentrate prior to inoculation of 7H10 medium for susceptibility testing using the direct method

TABLE 4

Guidelines for selection of the dilution of a specimen concentrate prior to inoculation of 7H10 medium for susceptibility testing using the direct method

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TABLE 5

Antimycobacterial agents, interpretative criteria, and quality control recommendations for testing M. avium complex by broth microdilution

TABLE 5

Antimycobacterial agents, interpretative criteria, and quality control recommendations for testing M. avium complex by broth microdilution

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TABLE 6

Secondary antimycobacterial agents and MIC values indicating resistance for testing M. kansasii and other slowly growing nontuberculous mycobacteria (excluding M. avium complex) a

TABLE 6

Secondary antimycobacterial agents and MIC values indicating resistance for testing M. kansasii and other slowly growing nontuberculous mycobacteria (excluding M. avium complex) a

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TABLE 7

Broth microdilution interpretive criteria for rapidly growing mycobacteria a

TABLE 7

Broth microdilution interpretive criteria for rapidly growing mycobacteria a

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TABLE 8

Broth microdilution breakpoints for Nocardia a

TABLE 8

Broth microdilution breakpoints for Nocardia a