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Laboratory Diagnosis and Antimicrobial Susceptibility Testing of Nontuberculous Mycobacteria

  • Barbara A. Brown-Elliott
Chapter
Part of the Respiratory Medicine book series (RM)

Abstract

This chapter discusses principles and methods for the laboratory identification of nontuberculous mycobacteria (NTM) beginning with biochemical and chemotaxonomic methods [high-performance liquid chromatography (HPLC), thin-layer chromatography (TLC), and gas-liquid chromatography (GLC)] which have widely been replaced by the more definitive molecular methods including commercial probe technology, gene sequencing, and more recently mass spectrometry (MS) using the matrix-assisted laser desorption-ionization time-of-flight (MALDI-TOF). The MALDI-TOF-MS currently remains non-validated or beyond the capability of many clinical laboratories to implement into the NTM identification algorithm. As with all molecular methodologies, the creation and maintenance of adequate databases are critical to the success of implementation of these techniques. Notably, only limited gene sequencing (i.e., 16S rRNA gene) has been addressed by the Clinical and Laboratory Standards Institute (CLSI), and strict cutoff values for other genes are currently not available.

Early methods of antimicrobial susceptibility testing (AST) including agar dilution and agar disk diffusion have been replaced by broth microdilution as recommended by the CLSI M24-A guidelines published in 2003, 2011, and, more recently, proposals for revisions for a 2017 document. The CLSI has determined MIC breakpoints for multiple antimicrobials used for treatment of NTM disease and advised specific reporting criteria.

Genomic relatedness/diversity of species and subspecies along with antimicrobial resistance and biological properties such as virulence and pathogenic potential by whole genome sequencing is emerging as an important tool in both the identification and antimicrobial susceptibility of NTM. Currently, however, due to its requirement for bioinformatics and ability to interpret and analyze the sequence data which are not available in most clinical laboratories, the whole genomic approach has only been implemented in specialized research laboratories.

Keywords

Nontuberculous mycobacteria Laboratory Acid-fast bacilli Susceptibility testing Nontuberculous mycobacteria (NTM) Antibiotics Susceptibility testing NTM diagnosis 

Notes

Acknowledgments

The author wishes to thank Richard J. Wallace, Jr. for his expert review of the chapter and Joanne Woodring for her excellent clerical skills.

This chapter is dedicated to my beloved husband, Clyde Elliott, and my dear mother Clifford Brown, who passed away during the preparation of this chapter. They provided constant support and encouragement to me throughout my years in the laboratory.

References

  1. 1.
    Tortoli E. Microbiological features and clinical relevance of new species of the genus Mycobacterium. Clin Microbiol Rev. 2014;27:727–52.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Tortoli E. Impact of genotypic studies on mycobacterial taxonomy: the new mycobacteria of the 1990s. Clin Microbiol Rev. 2003;16:319–54.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Turenne CY, Tschetter L, Wolfe J, Kabani A. Necessity of quality-controlled 16S rRNA gene sequence databases: identifying nontuberculous Mycobacterium species. J Clin Microbiol. 2001;39:3637–48.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Vestal AL. Procedures for the isolation and identification of mycobacteria, vol. 1995. In: US Department of Health E, and Welfare, editor. Washington, DC: United States Government Printint Office; 1969. p. 1–118.Google Scholar
  5. 5.
    Brown-Elliott BA, Wallace RJ Jr. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin Microbiol Rev. 2002;15:716–46.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Wallace RJ Jr, Swenson JM, Silcox VA, Good RC. Disk diffusion testing with polymyxin and amikacin for differentiation of Mycobacterium fortuitum and Mycobacterium chelonei. J Clin Microbiol. 1982;16:1003–6.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Wallace RJ Jr, Wiss K, Bushby MB, Hollowell DC. In vitro activity of trimethoprim and sulfamethoxazole against the nontuberculous mycobacteria. Rev Infect Dis. 1982;4:326–31.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Wallace RJ Jr, Brown BA, Onyi GO. Susceptibilities of Mycobacterium fortuitum biovar. fortuitum and the two subgroups of Mycobacterium chelonae to imipenem, cefmetazole, cefoxitin, and amoxicillin-clavulanic acid. Antimicrob Agents Chemother. 1991;35:773–5.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Wallace RJ Jr, Brown BA, Onyi G. Skin, soft tissue, and bone infections due to Mycobacterium chelonae subspecies chelonae – importance of prior corticosteroid therapy, frequency of disseminated infections, and resistance to oral antimicrobials other than clarithromycin. J Infect Dis. 1992;166:405–12.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Wilson RW, Steingrube VA, Böttger EC, Springer B, Brown-Elliott BA, Vincent V, Jost KC Jr, Zhang Y, Garcia MJ, Chiu SH, Onyi GO, Rossmoore H, Nash DR, Wallace RJ Jr. Mycobacterium immunogenum sp. nov., a novel species related to Mycobacterium abscessus and associated with clinical disease, pseudo-outbreaks, and contaminated metalworking fluids: an international cooperative study on mycobacterial taxonomy. Int J Syst Evol Microbiol. 2001;51:1751–64.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Wallace RJJ, Brown-Elliott BA, Brown J, Steigerwalt AG, Hall L, Woods G, Cloud J, Mann L, Wilson R, Crist C, Jost KC Jr, Byrer DE, Tang J, Cooper J, Stamenova E, Campbell B, Wolfe J, Turenne C. Polyphasic characterization reveals that the human pathogen Mycobacterium peregrinum type II belongs to the bovine pathogen species Mycobacterium senegalense. J Clin Microbiol. 2005;43:5925–35.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Wallace RJ Jr, Bedsole G, Sumter G, Sanders CV, Steele LC, Brown BA, Smith J, Graham DR. Activities of ciprofloxacin and ofloxacin against rapidly growing mycobacteria with demonstration of acquired resistance following single-drug therapy. Antimicrob Agents Chemother. 1990;34:65–70.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Wallace RJ Jr, Silcox VA, Tsukamura M, Brown BA, Kilburn JO, Butler WR, Onyi G. Clinical significance, biochemical features, and susceptibility patterns of sporadic isolates of the Mycobacterium chelonae-like organism. J Clin Microbiol. 1993;31:3231–9.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Clinical and Laboratory Standards Institute. Laboratory detection and identification of mycobacteria; approved guidelines. CLSI document M48-A. 2008.Google Scholar
  15. 15.
    Brown-Elliott BA, Wallace RJ Jr. Enhancement of conventional phenotypic methods with molecular-based methods for the more definitive identification of nontuberculous mycobacteria. Clin Microbiol Newsl. 2012;34:109–15.CrossRefGoogle Scholar
  16. 16.
    Soini H, Musser JM. Molecular diagnosis of mycobacteria. Clin Chem. 2001;47:809–14.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Jagielski T, Minias A, van Ingen J, Rastogi N, Brzostek A, Żaczek A, Dziadek J. Methodological and clinical aspects of the molecular epidemiology of Mycobacterium tuberculosis and other mycobacteria. Clin Microbiol Rev. 2016;29:239–90.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Tortoli E, Pecorari M, Fabio G, Messinò M, Fabio A. Commercial DNA probes for mycobacteria incorrectly identify a number of less frequently encountered species. J Clin Microbiol. 2010;48:307–10.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Cook VJ, Turenne CY, Wolfe J, Pauls R, Kabani A. Conventional methods versus 16S ribosomal DNA sequencing for identification of nontuberculous mycobacteria: cost analysis. J Clin Microbiol. 2003;41:1010–5.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Reisner BS, Gatson AM, Woods GL. Use of Gen-Probe AccuProbes to identify Mycobacterium avium complex, Mycobacterium tuberculosis complex, Mycobacterium kansasii, and Mycobacterium gordonae directly from BACTEC TB broth cultures. J Clin Microbiol. 1994;32:2995–8.PubMedPubMedCentralGoogle Scholar
  21. 21.
    LeBrun L, Espinasse F, Poveda JD, Vincent-Levy-Frebault V. Evaluation of nonradioactive DNA probes for identification of mycobacteria. J Clin Microbiol. 1992;30:2476–8.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Goto M, Oka S, Okuzumi K, Kimura S, Shimada K. Evaluation of acridinium-ester-labeled DNA probes for identification of Mycobacterium tuberculosis and Mycobacterium avium-Mycobacterium intracellulare complex in culture. J Clin Microbiol. 1991;29:2473–6.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Brown-Elliott BA, Wallace RJ Jr. Mycobacterium: clinical and laboratory characteristics of rapidly growing mycobacteria. In: Manual of clinical microbiology, vol. 1. 11th ed. Washington, DC: ASM Press; 2015.Google Scholar
  24. 24.
    de Zwaan R, van Ingen J, van Soolingen D. Utility of rpoB gene sequencing for identification of nontuberculous mycobacteria in the Netherlands. J Clin Microbiol. 2014;52:2544–51.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Blauwendraat C, Dixon GLJ, Hartley JC, Foweraker J, Harris KA. The use of a two-gene sequencing approach to accurately distinguish between the species within the Mycobacterium abscessus complex and Mycobacterium chelonae. Eur J Clin Microbiol Infect Dis. 2012;31:1847–53.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Tortoli E, Mariottini A, Mazzarelli G. Evaluation of INNO-LiPA MYCOBACTERIA v2: improved reverse hybridization multiple DNA probe assay for mycobacterial identification. J Clin Microbiol. 2003;41:4418–20.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Simner PJ, Stenger S, Richter E, Brown-Elliott BA, Wallace RJ Jr, Wengenack NL. Mycobacterium: clinical and laboratory characteristics of slowly growing mycobacteria. In: Manual of clinical microbiology, vol. 1. 11th ed. Washington, DC: ASM Press; 2015.Google Scholar
  28. 28.
    Richter E, Rüsch-Gerdes S, Hillemann D. Evaluation of the GenoType Mycobacterium assay for identification of mycobacterial species from cultures. J Clin Microbiol. 2006;44:1769–75.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Russo C, Tortoli E, Menichella D. Evaluation of the new GenoType mycobacterium assay for identification of mycobacterial disease. J Clin Microbiol. 2006;44:334–9.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Quezel-Guerraz NM, Arriaza MM, Avila JA, Sanchez-Yebra R, Martinez-Lirola MJ. Evaluation of the Speed-oligo(R) Mycobacteria assay for identification of Mycobacterium spp. from fresh liquid and solid cultures of human clinical samples. Diagn Microbiol Infect Dis. 2010;68:123–31.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Lara-Oya A, Mendoza-Lopez P, Rodriguez-Granger J, Fernandez-Sanchez AM, Bermudez-Ruiz MP, Toro-Peinado I, Palop-Bornas B, Navarro-Mari JM, Martinez-Lirola MJ. Evaluation of the speed-oligo direct Mycobacterium tuberculosis assay for molecular detection of mycobacteria in clinical respiratory specimens. J Clin Microbiol. 2013;51:77–82.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Hofmann-Thiel S, Turaev L, Alnour T, Drath L, Mullerova M, Hoffmann H. Multi-centre evaluation of the speed-oligo Mycobacteria assay for differentiation of Mycobacterium spp. in clinical isolates. BMC Infect Dis. 2011;11:353–9.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Telenti A, Marchesi F, Balz M, Bally F, Böttger EC, Bodmer T. Rapid identification of mycobacteria to the species level by polymerase chain reaction and restriction enzyme analysis. J Clin Microbiol. 1993;31:175–8.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Steingrube VA, Gibson JL, Brown BA, Zhang Y, Wilson RW, Rajagopalan M, Wallace RJ Jr. PCR amplification and restriction endonuclease analysis of a 65-kilodalton heat shock protein gene sequence for taxonomic separation of rapidly growing mycobacteria [ERRATUM 1995;33:1686]. J Clin Microbiol. 1995;33:149–53.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Devallois A, Goh KS, Rastogi N. Rapid identification of mycobacteria to species level by PCR-restriction fragment length polymorphism analysis of the hsp65 gene and proposition of an algorithm to differentiate 34 mycobacterial species. J Clin Microbiol. 1997;35:2969–73.Google Scholar
  36. 36.
    Dai J, Chen Y, Lauzardo M. Web-accessible database of hsp65 sequences from Mycobacterium reference strains. J Clin Microbiol. 2011;49:2296–303.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Macheras E, Roux A-L, Bastian S, Leão SC, Palaci M, Silvadon-Tardy V, Gutierrez C, Richter E, Rüsch-Gerdes S, Pfyffer G, Bodmer T, Cambau E, Gaillard J-L, Heym B. Multilocus sequence analysis and rpo B sequencing of Mycobacterium abscessus (sensu Lato) strains. J Clin Microbiol. 2011;49:491–9.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Hall L, Doerr KA, Wohlfiel SL, Roberts GD. Evaluation of the MicroSeq System for identification of mycobacteria by 16S ribosomal DNA sequencing and its integration into a routine clinical mycobacteriology laboratory. J Clin Microbiol. 2003;41:1447–53.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Kirschner P, Springer B, Vogel U, Meier A, Wrede A, Kiekenbeck M, Bange FC, Böttger EC. Genotypic identification of mycobacteria by nucleic acid sequence determination: report of a 2 year experience in a clinical laboratory. J Clin Microbiol. 1993;31:2882–9.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Patel JB, Leonard DGB, Pan X, Musser JM, Berman RE, Nachamkin I. Sequence-based identification of Mycobacterium species using the MicroSeq 500 16S rDNA bacterial identification system. J Clin Microbiol. 2000;38:246–51.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Clinical and Laboratory Standards Institute. Interpretive criteria for identification of bacteria and fungi by DNA target sequencing: approved guideline. CLSI document MM18-A. 2008.Google Scholar
  42. 42.
    Brown BA, Springer B, Steingrube VA, Wilson RW, Pfyffer GE, Garcia MJ, Menendez MC, Rodriguez-Salgado B, Jost KC Jr, Chiu SH, Onyi GO, Bottger EC, Wallace RJ Jr. Mycobacterium wolinskyi sp. nov. and Mycobacterium goodii sp. nov., two new rapidly growing species related to Mycobacterium smegmatis and associated with human wound infections: a cooperative study from the International Working Group on Mycobacterial Taxonomy. Int J Syst Bacteriol. 1999;49:1493–511.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Tortoli E. Phylogeny of the genus Mycobacterium: many doubts, few certainties. Infect Genet Evol. 2012;12:827–31.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Adékambi T, Colson P, Drancourt M. rpoB-based identification of nonpigmented and late pigmented rapidly growing mycobacteria. J Clin Microbiol. 2003;41:5699–708.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Ben Salah I, Adekambi T, Raoult D, Drancourt M. rpoB sequence-based identification of Mycobacterium avium complex species. Microbiology. 2008;154:3715–23.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Kim B-J, Lee SH, Lyu MA, Kim SJ, Bai GH, Chae GT, Kim EC, Cha CY, Kook YH. Identification of mycobacterial species by comparative sequence analysis of the RNA polymerase gene (rpoB). J Clin Microbiol. 1999;37:1714–20.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Lee H, Bang H-E, Bai G-H, Cho S-N. Novel polymorphic region of the rpoB gene containing Mycobacterium species-specific sequences and its use in identification of mycobacteria. J Clin Microbiol. 2003;41:2213–8.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Tortoli E. Standard operating procedure for optimal identification of mycobacteria using 16S rRNA gene sequences. Stand Genomic Sci. 2010;3:145–52.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Ringuet H, Akoua-Koffi C, Honore S, Varnerot A, Vincent V, Berche P, Gaillard JL, Pierre-Audigier C. hsp65 sequencing for identification of rapidly growing mycobacteria. J Clin Microbiol. 1999;37:852–7.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Turenne CY, Semret M, Cousins DV, Collins DM, Behr MA. Sequencing of hsp65 distinguishes among subsets of the Mycobacterium avium complex. J Clin Microbiol. 2006;44:433–40.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Nash KA, Brown-Elliott BA, Wallace RJ Jr. A novel gene, erm(41), confers inducible macrolide resistance to clinical isolates of Mycobacterium abscessus but is absent from Mycobacterium chelonae. Antimicrob Agents Chemother. 2009;53:1367–76.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Kim H-Y, Kim B-J, Kook Y, Yun Y-J, Shin JH, Kook YH. Mycobacterium massiliense is differentiated from Mycobacterium abscessus and Mycobacterium bolletii by erythromycin ribosome methyltransferase gene (erm) and clarithromycin susceptibility patterns. Microbiol Immunol. 2010;54:347–53.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Koh WJ, Jeon K, Lee NY, Kim B-J, Kook Y-H, Lee S-H, Park Y-K, Kim CK, Shin SJ, Huitt GA, Daley CL, Kwon OJ. Clinical significance of differentiation of Mycobacterium massiliense from Mycobacterium abscessus. Am J Respir Crit Care Med. 2011;183:405–10.PubMedCrossRefGoogle Scholar
  54. 54.
    Nash KA, Andini N, Zhang Y, Brown-Elliott BA, Wallace RJ Jr. Intrinsic macrolide resistance in rapidly growing mycobacteria. Antimicrob Agents Chemother. 2006;50:3476–8.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Nash KA. Intrinsic macrolide resistance in Mycobacterium smegmatis is conferred by a novel erm gene, erm(38). Antimicrob Agents Chemother. 2003;47:3053–60.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Nash DR, Wallace RJ Jr, Steingrube VA, Udou T, Steele LC, Forrester GD. Characterization of beta-lactamases in Mycobacterium fortuitum including a role in beta-lactam resistance and evidence of partial inducibility. Am Rev Respir Dis. 1986;134:1276–82.Google Scholar
  57. 57.
    Brown-Elliott BA, Vasireddy S, Vasireddy R, Iakhiaeva E, Howard ST, Nash KA, Parodi N, Strong A, Gee M, Smith T, Wallace RJ Jr. Utility of sequencing the erm(41) gene in isolates of Mycobacterium abscessus subsp. abscessus with low and intermediate clarithromycin MICs. J Clin Microbiol. 2015;53:1211–5; ERRATUM J Clin Microbiol 1254:1172, April 2016.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Brown-Elliott BA, Hanson K, Vasireddy S, Iakhiaeva E, Nash KA, Vasireddy R, Parodi N, Smith T, Gee M, Strong A, Baker A, Cohen S, Muir H, Slechta ES, Wallace RJ Jr. Absence of a functional erm gene in isolates of Mycobacterium immunogenum and the Mycobacterium mucogenicum group, based on in vitro clarithromycin susceptibility. J Clin Microbiol. 2015;53:875–8.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Adékambi T, Drancourt M. Dissection of phylogenetic relationships among nineteen rapidly growing mycobacterium species by 16S rRNA, hsp65, sodA, recA, and rpoB gene sequencing. Int J Syst Evol Microbiol. 2004;54:2095–105.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Park H, Jang H, Kim J, Chung B, Chang CL, Park SK, Song S. Detection and identification of mycobacteria by amplification of the internal transcribed spacer regions with genus- and species-specific PCR primers. J Clin Microbiol. 2000;38:4080–5.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Macheras E, Roux A-L, Ripoll F, Sivadon-Tardy V, Gutierrez C, Gaillard J-L, Heym B. Inaccuracy of single-target sequencing for discriminating species of the Mycobacterium abscessus group. J Clin Microbiol. 2009;47:2596–600.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Adékambi T, Raoult D, D M. Mycobacterium barrassiae sp. nov., a Mycobacterium moriokaense group species associated with chronic pneumonia. J Clin Microbiol. 2006;44:3493–8.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Roth A, Reischl U, Streubel A, Naumann L, Kroppenstedt RM, Habicht M, Fischer M, Mauch H. Novel diagnostic algorithm for identification of mycobacteria using genus-specific amplification of the 16S-23S rRNA gene spacer and restriction endonucleases. J Clin Microbiol. 2000;38:1094–104.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Mohamed AM, Kuyper DJ, Iwen PC, Ali HH, Bastola DR, Hinrichs SH. Computational approach involving use of the internal transcribed spacer 1 region for identification of Mycobacterium species. J Clin Microbiol. 2005;43:3811–2817.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Frothingham R, Wilson KH. Molecular phylogeny of the Mycobacterium avium complex demonstrates clinically meaningful divisions. J Infect Dis. 1994;169:305–12.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Frothingham R, Wilson KH. Sequence-based differentiation of strains in the Mycobacterium avium complex. J Bacteriol. 1993;175:2818–25.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Kim H-Y, Kook Y, Yun Y-J, Park CG, Lee NY, Shim TS, Kim B-J, Kook Y-H. Proportions of Mycobacterium massiliense and Mycobacterium bolletii in Korean Mycobacterium chelonae-Mycobacterium abscessus group isolates. J Clin Microbiol. 2008;46:3384–90.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Bao JR, Master RN, Schwab DA, Clark RB. Identification of acid-fast bacilli using pyrosequencing analysis. Diagn Microbiol Infect Dis. 2010;67:234–8.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Heller LC, Jones M, Widen RH. Comparison of DNA pyrosequencing with alternative methods for identification of mycobacteria. J Clin Microbiol. 2008;46:2092–4.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Tuohy MJ, Hall GS, Sholtis M, Procop GW. Pyrosequencing as a tool for the identification of common isolates of Mycobacterium sp. Diagn Microbiol Infect Dis. 2005;51:245–50.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Arnold C, Barrett A, Cross L, Magee JG. The use of rpoB sequence analysis in the differentiation of Mycobacterium abscessus and Mycobacterium chelonae: a critical judgement in cystic fibrosis? Clin Microbiol Infect. 2012;18:E131–3.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Buckwalter SP, Olson SL, Connelly BJ, Lucas BC, Rodning AA, Walchak RC, Deml SM, Wohlfiel SL, Wengenack NL. Evaluation of matrix-assisted laser desorption ionization-time of flight mass spectrometry for identification of Mycobacterium species, Nocardia species, and other aerobic actinomycetes. J Clin Microbiol. 2016;54:376–84.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Saleeb PG, Drake SK, Murray PR, Zelazny AM. Identification of mycobacteria in solid-culture media by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol. 2011;49:1790–4.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Rodríguez-Sánchez B, Ruiz-Serrano MJ, Ruiz A, Timke M, Kostrzewa M, Bouza E. Evaluation of MALDI biotyper mycobacterial library v3.0 for identification of nontuberculous mycobacteria. J Clin Microbiol. 2016;54:1144–7.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Hettick JM, Kashon ML, Slaven JE, Ma Y, Simpson JP, Siegel PD, Mazurek GN, Weissman DN. Discrimination of intact mycobacteria at the strain level: a combined MALDI-TOF MS and biostatistical analysis. Proteomics. 2006;6:6416–25.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Lefmann M, Honsich C, Böcker S, Storm N, von Wintzingerode F, Schlötelburg C, Moter A, van den Boom D, Göbel UB. Novel mass spectrometry-based tool for genotypic identification of mycobacteria. J Clin Microbiol. 2004;42:339–46.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Lotz A, Gerroni A, Beretti J-L, Dauphin B, Carbonnelle E, Guet-Revillet H, Veziris N, Heym B, Jarlier V, Gaillard J-L, Pierre-Audigier C, Frapy E, Berche P, Nassif X, Bille E. Rapid identification of mycobacterial whole cells in solid and liquid culture media by matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Clin Microbiol. 2010;48:4481–6.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Tan N, Sampath R, Abu Saleh OM, Tweet MS, Jevremovic D, Alniemi S, Wengenack NL, Sampathkumar P, Badley AD. Disseminated Mycobacterium chimaera infection after cardiothoracic surgery. Open Forum Infect Dis. 2016;3:1–3.Google Scholar
  79. 79.
    Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33:2233–9.PubMedPubMedCentralGoogle Scholar
  80. 80.
    Wallace RJ Jr, Zhang Y, Brown-Elliott BA, Yakrus MA, Wilson RW, Mann L, Couch L, Girard WM, Griffith DE. Repeat positive cultures in Mycobacterium intracellulare lung disease after macrolide therapy represent new infections in patients with nodular bronchiectasis. J Infect Dis. 2002;186:266–73.CrossRefGoogle Scholar
  81. 81.
    Zhang Y, Yakrus MA, Graviss EA, Williams-Bouyer N, Turenne C, Kabani A, Wallace RJ Jr. Pulsed-field gel electrophoresis study of Mycobacterium abscessus isolates previously affected by DNA degradation. J Clin Microbiol. 2004;42:5582–7.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Howard ST, Newman KL, McNulty S, Brown-Elliott BA, Vasireddy R, Bridge L, Wallace RJ Jr. Insertion site and distribution of a genomic island conferring DNA phosphorothioation in the Mycobacterium abscessus complex. Microbiology. 2013;159:2323–32.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Hector JSR, Pang Y, Mazurek GH, Zhang Y, Brown BA, Wallace RJ Jr. Large restriction fragment patterns of genomic Mycobacterium fortuitum DNA as strain-specific markers and their use in epidemiologic investigation of four nosocomial outbreaks. J Clin Microbiol. 1992;30:1250–5.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Lai KK, Brown BA, Westerling JA, Fontecchio SA, Zhang Y, Wallace RJ Jr. Long-term laboratory contamination by Mycobacterium abscessus resulting in two pseudo-outbreaks: recognition with use of random amplified polymorphic DNA (RAPD) polymerase chain reaction. Clin Infect Dis. 1998;27:169–75.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Brown-Elliott BA, Wallace RJ Jr. Nontuberculous mycobacteria. In: Mayhall CG, editor. Hospital epidemiology and infection control. 4th ed. Philadelphia: Lippincott Williams & Wilkins; 2012. p. 593–608.Google Scholar
  86. 86.
    Griffith DE, Brown-Elliott BA, Langsjoen B, Zhang Y, Pan X, Girard W, Nelson K, Caccitolo J, Alvarez J, Shepherd S, Wilson R, Graviss EA, Wallace RJ Jr. Clinical and molecular analysis of macrolide resistance in Mycobacterium avium complex lung disease. Am J Respir Crit Care Med. 2006;174:928–34.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Wallace RJ Jr, Zhang Y, Brown BA, Dawson D, Murphy DT, Wilson R, Griffith DE. Polyclonal Mycobacterium avium complex infections in patients with nodular bronchiectasis. Am J Respir Crit Care Med. 1998;158:1235–44.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Zelazny AM, Root JM, Shea YR, Colombo RE, Shamputa IC, Stock F, Conlan SS, McNulty S, Brown-Elliott BA, Wallace RJ Jr, Olivier KN, Holland SM, Sampaio EP. Cohort study of molecular identification and typing of Mycobacterium abscessus, Mycobacterium massiliense and Mycobacterium bolletii. J Clin Microbiol. 2009;47:1985–95.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Cangelosi GA, Freeman RJ, Lewis KN, Livingston-Rosanoff D, Shah KS, Milan SJ, Goldberg SV. Evaluation of a high-throughput repetitive-sequence-based PCR system for DNA fingerprinting of Mycobacterium tuberculosis and Mycobacterium avium complex strains. J Clin Microbiol. 2004;42:2685–93.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Zhang Y, Rajagopalan M, Brown BA, Wallace RJ Jr. Randomly amplified polymorphic DNA PCR for comparison of Mycobacterium abscessus strains from nosocomial outbreaks. J Clin Microbiol. 1997;35:3132–9.PubMedPubMedCentralGoogle Scholar
  91. 91.
    Sax H, Bloemberg G, Hasse B, Sommerstein R, Kohler P, Achermann Y, Rössle M, Falk V, Kuster SP, Böttger EC, Weber R. Prolonged outbreak of Mycobacterium chimaera infection after open-chest heart surgery. Clin Infect Dis. 2015;61:67–75.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Sommerstein R, Rüegg C, Kohler P, Bloemberg G, Kuster SP, Sax H. Transmission of Mycobacterium chimaera from heater-cooler units during cardiac surgery despite an ultraclean air ventilation system. Emerg Infect Dis. 2016;22:1008–14.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Inagaki T, Nishimori K, Yagi T, Ichikawa K, Moriyama M, Nakagawa T, Shibayama T, Uchiya K-I, Nikai T, Ogawa K. Comparison of a variable-number tandem-repeat (VNTR) method for typing Mycobacterium avium with mycobacterial interspersed repetitive-unit-VNTR and IS1245 restriction fragment length polymorphism typing. J Clin Microbiol. 2009;47:2156–64.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Wallace RJ Jr, Iakhiaeva E, Williams M, Brown-Elliott BA, Vasireddy S, Vasireddy R, Lande L, Peterson D, Sawicki J, Kwait R, Tichenor W, Turenne C, Falkinham JO III. Absence of Mycobacterium intracellulare and the presence of Mycobacterium chimaera in household water and biofilm samples of patients in the U.S. with Mycobacterium avium complex respiratory disease. J Clin Microbiol. 2013;51:1747–52.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Iakhiaeva E, Howard S, Brown-Elliott BA, McNulty S, Falkinham JO III, Newman K, Williams M, Kwait R, Lande L, Vasireddy R, Turenne C, Wallace RJ Jr. Variable number tandem-repeat (VNTR) analysis of respiratory and household water biofilm isolates of “Mycobacterium avium subspecies hominissuis” with establishment of a PCR database. J Clin Microbiol. 2016;54:891–901.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Iakhiaeva E, McNulty S, Brown-Elliott BA, Falkinham JO III., Williams MD, Vasireddy R, Wilson RW, Turenne C, Wallace RJ Jr. Mycobacterial interspersed repetitive-unit-variable-number tandem-repeat (MIRU-VNTR) genotyping of Mycobacterium intracellulare for strain comparison with establishment of a PCR database. J Clin Microbiol. 2013;51:409–16.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Wong YL, Ong CS, Ngeow YF. Molecular typing of Mycobacterium abscessus based on tandem-repeat polymorphism. J Clin Microbiol. 2012;50:3084–8.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Machado GE, Matsumoto CK, Chimara E, da Silva Duarte F, de Freitas D, Palaci M, Hadad DJ, Batista KV, Lopes LML, Ramos JP, Campos CE, Caldas PC, Heym B, Leão SC. Multilocus sequence typing scheme versus pulsed-field gel electrophoresis for typing Mycobacterium abscessus isolates. J Clin Microbiol. 2014;52:2881–91.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Sampaio JL, Chimara E, Ferrazoli L, da Silva Telles MA, Del Guercio VM, Jericó ZV, Miyashiro K, Fortaleza CM, Padoveze MC, Leão SC. Application of four molecular typing methods for analysis of Mycobacterium fortuitum group strains causing post-mammaplasty infections. Clin Microbiol Infect. 2006;12:142–9.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Sampaio JL, Viana-Niero C, de Freitas D, Höfling-Lima AL, Leão SC. Enterobacterial repetitive intergenic consensus PCR is a useful tool for typing Mycobacterium chelonae and Mycobacterium abscessus isolates. Diagn Microbiol Infect Dis. 2006;55:107–18.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE, 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, Jagels K, Krogh A, McLean J, Moule S, Murphy L, Olivier K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 1998;393:537–44.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Kohler P, Kuster SP, Bloemberg G, Schulthess B, Frank M, Tanner FC, Rössle M, Böni C, Falk V, Wilhelm MJ, Sommerstein R, Achermann Y, Ten Oever J, Debast SB, Wolfhagen MJHM, Bravo Bruinsma GJB, Vos MC, Bogers A, Serr A, Beyersdorf F, Sax H, Böttger EC, Weber R, van Ingen J, Wagner D, Hasse B. Healthcare-associated prosthetic heart valve, aortic vascular graft, and disseminated Mycobacterium chimaera infections subsequent to open heart surgery. Eur Heart J. 2015;36:2745–53.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Choo SW, Wong YL, Tan JL, Ong CS, Wong GJ, Ng KP, Ngeow YF. Annotated genome sequence of Mycobacterium massiliense strain M154, belonging to the recently created taxon Mycobacterium abscessus subsp. bolletii comb. nov. J Bacteriol. 2012;194:4778.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Ngeow YF, Wee WY, Wong YL, Tan JL, Ongi CS, Ng KP, Choo SW. Genomic analysis of Mycobacterium abscessus strain M139, which has an ambiguous subspecies taxonomic position. J Bacteriol. 2012;194:6002–3.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Ngeow YF, Wong YL, Lokanathan N, Wong GJ, Ong CS, Ng KP, Choo SW. Genomic analysis of Mycobacterium massiliense strain M115, an isolate from human sputum. J Bacteriol. 2012;194:4786.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Ngeow YF, Wong YL, Tan JL, Arumugam R, Wong GJ, Ong CS, Ng KP, Choo SW. Genome sequence of Mycobacterium massiliense M18, isolated from a lymph node biopsy specimen. J Bacteriol. 2012;194:4125.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Tettelin H, Sampaio EP, Daugherty SC, Hine E, Riley DR, Sadzewicz L, Sengamalay N, Shefchek K, Su Q, Tallon LJ, Conville P, Olivier KN, Holland SM, Fraser CM, Zelazny AM. Genomic insights into the emerging human pathogen Mycobacterium massiliense. J Bacteriol. 2012;194:5450.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Chan J, Halachev M, Yates E, Smith G, Pallen M. Whole-genome sequence of the emerging pathogen Mycobacterium abscessus strain 47J26. J Bacteriol. 2012;194:549.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Tortoli E, Kohl TA, Brown-Elliott BA, Trovato A, Cardoso Leao S, Garcia MJ, Vasireddy S, Turenne CY, Griffith DE, Philley JV, Balden R, Campana S, Cariani L, Colombo C, Taccetti G, Teri A, Niemann S, Wallace RJ Jr, Cirillo DM. Emended description of Mycobacterium abscessus, Mycobacterium abscessus subsp. abscessus and Mycobacterium abscessus subsp. bolletii and designation of Mycobacterium abscessus subsp. massiliense subsp. comb. nov. Int J Syst Evol Microbiol. 2016;66:4471–9.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Woods GL, Brown-Elliott BA, Desmond EP, Hall GS, Heifets L, Pfyffer GE, Ridderhof JC, Wallace RJ Jr., Warren NG, Witebsky FG. Susceptibility testing of mycobacteria, norcardiae, and other aerobic actinomycetes; approved standard. NCCLS document M24-A. 2003.Google Scholar
  111. 111.
    Griffith DE, Aksamit T, Brown-Elliott BA, 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 Jr, Winthrop K. An official ATS/IDSA statement: diagnosis, treatment and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med. 2007;175:367–416.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Brown-Elliott BA, Nash KA, Wallace RJ Jr. Antimicrobial susceptibility testing, drug resistance mechanisms, and therapy of infections with nontuberculous mycobacteria. Clin Microbiol Rev. 2012;25:545–82.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Clinical and Laboratory Standards Institute. Susceptibility testing of mycobacteria, nocardiae, and other aerobic actinomycetes: approved standard—second edition. CLSI document M24-A2. 2011.Google Scholar
  114. 114.
    Forbes BA, Banaiee N, Beavis KG, Brown-Elliott BA, Della Latta P, Elliott LB, Hall GS, Hanna B, Perkins MD, Siddiqi SH, Wallace RJ Jr., Warren NG. Laboratory detection and identification of mycobacteria; approved guideline. CLSI document M48-A. 2008.Google Scholar
  115. 115.
    Vasireddy R, Vasireddy S, Brown-Elliott BA, Wengenack NL, Eke UA, Benwill JL, Turenne C, Wallace RJ Jr. Mycobacterium arupense, Mycobacterium heraklionense, and a newly proposed species, “Mycobacterium virginiense” sp. nov., but not Mycobacterium nonchromogenicum, as species of the Mycobacterium terrae complex causing tenosynovitis and osteomyelitis. J Clin Microbiol. 2016;54:1340–51.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Brown-Elliott BA, Iakhiaeva E, Griffith DE, Woods GL, Stout JE, Wolfe CR, Turenne CY, Wallace RJ Jr. In vitro activity of amikacin against isolates of Mycobacterium avium complex with proposed MIC breakpoints and finding of a 16S rRNA gene mutation in treated isolates. J Clin Microbiol. 2013;51:3389–94. ERRATUM J Clin Microbiol 3352:1311, 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Wallace RJ Jr, Meier A, Brown BA, Zhang Y, Sander P, Onyi GO, Bottger EC. Genetic basis for clarithromycin resistance among isolates of Mycobacterium chelonae and Mycobacterium abscessus. Antimicrob Agents Chemother. 1996;40:1676–81.PubMedPubMedCentralGoogle Scholar
  118. 118.
    Wallace RJ Jr, Hull SI, Bobey DG, Price KE, Swenson JM, Steele L, Christensen L. Mutational resistance as the mechanism of acquired drug resistance to aminoglycosides and antibacterial agents in Mycobacterium chelonae: Evidence based on plasmid analysis, mutational frequencies, and aminoglycoside modifying enzyme assays. Am Rev Respir Dis. 1985;132:409–16.PubMedPubMedCentralGoogle Scholar
  119. 119.
    Nash KA, Inderlied CB. Genetic basis of macrolide resistance in Mycobacterium avium isolated from patients with disseminated disease. Antimicrob Agents Chemother. 1995;39:2625–30.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    van Ingen J, Egelund EF, Levin A, Totten SE, Boeree MJ, Mouton JW, Aarnoutse RE, Heifets LB, Peloquin CA, Daley CL. The pharmacokinetics and pharmacodynamics of pulmonary Mycobacterium avium complex disease treatment. Am J Respir Crit Care Med. 2012;186:559–65.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Wallace RJ Jr, Swenson JM, Silcox VA. The rapidly growing mycobacteria: characterization and susceptibility testing. Antimicrob Newsl. 1985;2:85–92.CrossRefGoogle Scholar
  122. 122.
    Stone MS, Wallace RJ Jr, Swenson JM, Thornsberry C, Christensen LA. Agar disk elution method for susceptibility testing of Mycobacterium marinum and Mycobacterium fortuitum complex to sulfonamides and antibiotics. Antimicrob Agents Chemother. 1983;24:486–93.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Biehle JR, Cavalieri SJ, Saubolle MA, Getsinger LJ. Evaluation of Etest for susceptibility testing of rapidly growing mycobacteria. J Clin Microbiol. 1995;33:1760–4.PubMedPubMedCentralGoogle Scholar
  124. 124.
    Fabry W, Schmid EN, Ansorg R. Comparison of the E test and a proportion dilution method for susceptibility testing of Mycobacterium kansasii. Chemotherapy. 1995;41:247–52.PubMedCrossRefPubMedCentralGoogle Scholar
  125. 125.
    Fabry W, Schmid EN, Ansorg R. Comparison of the E test and a proportion dilution method for susceptibility testing of Mycobacterium avium complex. J Med Microbiol. 1996;44:227–30.PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Jarboe E, Stone BL, Burman WJ, Wallace RJ Jr, Brown BA, Reves RR, Wilson ML. Evaluation of a disk diffusion method for determining susceptibility of Mycobacterium avium complex to clarithromycin. Diagn Microbiol Infect Dis. 1998;30:197–203.PubMedCrossRefPubMedCentralGoogle Scholar
  127. 127.
    Woods GL, Bergmann JS, Witebsky FG, Fahle GA, Boulet B, Plaunt M, Brown BA, Wallace RJ Jr, Wanger A. Multisite reproducibility of Etest for susceptibility testing of Mycobacterium abscessus, Mycobacterium chelonae, and Mycobacterium fortuitum. J Clin Microbiol. 2000;38:656–61.PubMedPubMedCentralGoogle Scholar
  128. 128.
    Woods GL, Bergmann JS, Witebsky FG, Fahle GA, Wanger A, Boulet B, Plaunt M, Brown BA, Wallace RJ Jr. Multisite reproducibility of results obtained by the broth microdilution method for susceptibility testing of Mycobacterium abscessus, Mycobacterium chelonae, and Mycobacterium fortuitum. J Clin Microbiol. 1999;37:1676–82.PubMedPubMedCentralGoogle Scholar
  129. 129.
    Fernandez-Roblas R, Martin-de-Hijas NZ, Fernandez-Martinez AI, et al. In vitro activities of tigecycline and 10 other antimicrobials against nonpigmented rapidly growing mycobacteria. Antimicrob Agents Chemother. 2008;52:4184–6.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Brown BA, Wallace RJ Jr, Onyi GO. Activities of the glycylcyclines N, N-dimethylglycylamido-minocycline and N, N-dimethylglycylamido-6-demethyl-6-deoxytetracycline against Nocardia spp. and tetracycline-resistant isolates of rapidly growing mycobacteria. Antimicrob Agents Chemother. 1996;40:874–8.PubMedPubMedCentralGoogle Scholar
  131. 131.
    Brown BA, Wallace RJ Jr, Onyi GO, De Rosas V, Wallace RJ III. Activities of four macrolides, including clarithromycin, against Mycobacterium fortuitum, Mycobacterium chelonae, and M. chelonae-like organisms. Antimicrob Agents Chemother. 1992;36:180–4.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Turenne CY, Wallace RJ Jr, Behr MA. Mycobacterium avium in the postgenomic era. Clin Microbiol Rev. 2007;20:205–29.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    van Ingen J, Turenne C, Tortoli E, Wallace RJ Jr, Brown-Elliott BA. A Definition of the Mycobacterium avium complex for taxonomic and clinical purposes. IJSEM. 2018. In Press.Google Scholar
  134. 134.
    Babady NE, Hall L, Abbenyi AT, Eisberner JJ, Brown-Elliott BA, Pratt CJ, McGlasson MC, Beierle KD, Wohlfiel SL, Deml SM, Wallace RJ Jr, Wengenack NL. Evaluation of Mycobacterium avium complex clarithromycin susceptibility testing using SLOMYCO sensititre panels and JustOne strips. J Clin Microbiol. 2010;48:1749–52.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Brown BA, Wallace RJ Jr, Onyi GO. Activities of clarithromycin against eight slowly growing species of nontuberculous mycobacteria, determined by using a broth microdilution MIC system. Antimicrob Agents Chemother. 1992;36:1987–90.PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Eisenberg E, Barza M. Azithromycin and clarithromycin. Curr Clin Top Infect Dis Chest. 1994;14:52–79.Google Scholar
  137. 137.
    Brown-Elliott BA, Crist CJ, Mann LB, Wilson RW, Wallace RJ Jr. In vitro activity of linezolid against slowly growing nontuberculous mycobacteria. Antimicrob Agents Chemother. 2003;47:1736–8.PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Woods GL, Williams-Bouyer N, Wallace RJ Jr, Brown-Elliott BA, Witebsky FG, Conville PS, Plaunt M, Hall G, Aralar P, Inderlied C. Multisite reproducibility of results obtained by two broth dilution methods for susceptibility testing of Mycobacterium avium complex. J Clin Microbiol. 2003;41:627–31.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    van Ingen J, Boeree MJ, van Soolingen D, Mouton JW. Resistance mechanisms and drug susceptibility testing of nontuberculous mycobacteria. Drug Resist Updat. 2012;15:149–61.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Meier A, Heifets L, Wallace RJ Jr, Zhang Y, Brown BA, Sander P, Böttger EC. Molecular mechanisms of clarithromycin resistance in Mycobacterium avium: observation of multiple 23S rDNA mutations in a clonal population. J Infect Dis. 1996;174:354–60.CrossRefGoogle Scholar
  141. 141.
    Meier A, Kirschner P, Springer B, Steingrube VA, Brown BA, Wallace RJ Jr, Böttger EC. Identification of mutations in 23S rRNA gene of clarithromycin-resistant Mycobacterium intracellulare. Antimicrob Agents Chemother. 1994;38:381–4.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Nash KA, Inderlied CB. Rapid detection of mutations associated with macrolide resistance in Mycobacterium avium complex. Antimicrob Agents Chemother. 1996;40:1748–50.PubMedPubMedCentralGoogle Scholar
  143. 143.
    Griffith DE, Brown-Elliott BA, Wallace RJ Jr. Thrice-weekly clarithromycin-containing regimen for treatment of Mycobacterium kansasii lung disease: results of a preliminary study. Clin Infect Dis. 2003;37:1178–82.PubMedCrossRefGoogle Scholar
  144. 144.
    Burman WJ, Stone BL, Brown BA, Wallace RJ Jr, Böttger EC. AIDS-related Mycobacterium kansasii infection with initial resistance to clarithromycin. Diagn Microbiol Infect Dis. 1998;31:369–71.PubMedCrossRefPubMedCentralGoogle Scholar
  145. 145.
    Klein JL, Brown TJ, French GL. Rifampin resistance in Mycobacterium kansasii is associated with rpoB mutations. Antimicrob Agents Chemother. 2001;45:3056–8.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Wallace RJ Jr, Dunbar D, Brown BA, Onyi G, Dunlap R, Ahn CH, Murphy DT. Rifampin-resistant Mycobacterium kansasii. Clin Infect Dis. 1994;18:736–43.CrossRefGoogle Scholar
  147. 147.
    Jernigan JA, Farr BM. Incubation period and sources for cutaneous Mycobacterium marinum infection: case report and review of the literature. Clin Infect Dis. 2000;31:439–43.PubMedCrossRefPubMedCentralGoogle Scholar
  148. 148.
    Tortoli E, Piersimoni C, Bacosi D, Bartoloni A, Betti F, Bono L, Burrini C, De Sio G, Lacchini C, Mantella A, Orsi PG, Penati V, Simonetti MT, Böttger EC. Isolation of the newly described species Mycobacterium celatum from AIDS patients. J Clin Microbiol. 1995;33:137–40.PubMedPubMedCentralGoogle Scholar
  149. 149.
    Tortoli E, Piersimoni C, Kirschner P, Bartoloni A, Burrini C, Lacchini C, Mantella A, Muzzi G, Passerini-Tosi C, Penati V, Scarparo C, Simonetti MT, Böttger EC. Characterization of mycobacterial isolates phylogenetically related to, but different from Mycobacterium simiae. J Clin Microbiol. 1997;35:697–702.PubMedPubMedCentralGoogle Scholar
  150. 150.
    MacSwiggan DA, Collins CH. The isolation of M. kansasii and M. xenopi from water systems. Tubercle. 1974;55:291–7.CrossRefGoogle Scholar
  151. 151.
    Buchholz UT, McNeill MM, Keyes LE, Good RC. Mycobacterium malmoense infections in the United States, January 1993 through June 1995. Clin Infect Dis. 1998;27:551–8.PubMedCrossRefPubMedCentralGoogle Scholar
  152. 152.
    Heginbothom ML, Lindholm-Levy PJ, Heifets LB. Susceptibilities of Mycobacterium malmoense determined at the growth optimum pH (pH 6.0). Int J Tuberc Lung Dis. 1998;2:430–4.PubMedPubMedCentralGoogle Scholar
  153. 153.
    Ji B, Lefrançois S, Robert J, Chauffour A, Truffot C, Jarlier V. In vitro and in vivo activities of rifampin, streptomycin, amikacin, moxifloxacin, R207910, linezolid, and PA-824 against Mycobacterium ulcerans. Antimicrob Agents Chemother. 2006;50:1921–6.PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    Vadney FS, Hawkins JE. Evaluation of a simple method for growing Mycobacterium haemophilum. J Clin Microbiol. 1985;28:884–5.Google Scholar
  155. 155.
    McBride ME, Rudolph AH, Tschen JA, Cernoch P, Davis J, Brown BA, Wallace RJ Jr. Diagnostic and therapeutic considerations for cutaneous Mycobacterium haemophilum infections. Arch Dermatol. 1991;127:276–7.PubMedCrossRefGoogle Scholar
  156. 156.
    Prammananan T, Sander P, Brown BA, Frischkorn K, Onyi GO, Zhang Y, Böttger EC, Wallace RJ Jr. A single 16S ribosomal RNA substitution is responsible for resistance to amikacin and other 2-deoxystreptamine aminoglycosides in Mycobacterium abscessus and Mycobacterium chelonae. J Infect Dis. 1998;177:1573–81.CrossRefGoogle Scholar
  157. 157.
    Rahman SA, Singh Y, Kohli S, Ahmad J, Ehtesham NZ, Tyagi AK, Hasnain SE. Comparative analyses of nonpathogenic, opportunistic, and totally pathogenic mycobacteria reveal genomic and biochemical variabilities and highlight the survival attributes of Mycobacterium tuberculosis. mBio. 2014;5:e02020–14; ERRATUM mBio 02015;02026(02021):e02343–02014.PubMedPubMedCentralCrossRefGoogle Scholar
  158. 158.
    Stinear TP, Seemann T, Pidot S, Frigui W, Reysset G, Garnier T, Meurice G, Simon D, Bouchier C, Ma L, Tichit M, Porter JL, Ryan L, Johnson PDR, Davies JK, Jenkin GA, Small PLC, Jones LM, Tekaia F, Laval F, Daffé M, Parkhill J, Cole ST. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res. 2007;17:192–300.PubMedPubMedCentralCrossRefGoogle Scholar
  159. 159.
    Bryant JM, Grogono DM, Greaves D, Foweraker J, Roddick I, Inns T, Reacher M, Haworth CS, Curran MD, Harris SR, Peacock SJ, Parkhill J, Floto RA. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet. 2013;381:1551–60.PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Aitken ML, Limaye A, Pottinger P, Whimbey E, Goss GH, Tonelli MR, Cangelosi GA, Ashworth M, Olivier KN, Brown-Elliott BA, Wallace RJ Jr. Respiratory outbreak of Mycobacterium abscessus subspecies massiliense in a lung transplant and cystic fibrosis center. Am J Respir Crit Care Med. 2012;185:231–3.PubMedCrossRefPubMedCentralGoogle Scholar
  161. 161.
    Davidson RM, Hasan N, Reynolds PR, Totten S, Garcia B, Levin A, Ramamoorthy P, Heifets L, Daley CL, Strong M. Genome sequencing of Mycobacterium abscessus isolates from patients in the United States and comparisons to globally diverse clinical strains. J Clin Microbiol. 2014;52:3573–82.PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Duarte RS, Silva Lourenço MC, de Souza Fonseca L, Leão SC, Amorim EDLT, ILL R, Coelho FS, Viana-Niero C, Gomes KM, da Silva MG, de Oliveira Lorena NS, Pitombo MC, Ferreira RMC, de Oliveira Garcia MH, de Oliveira GP, Lupi O, Vilaça BR, Serradas LR, Chebato A, Marques EA, Teixeira LM, Dalcolmo M, Senna SG, Sampaio JLM. Epidemic of postsurgical infections caused by Mycobacterium massiliense. J Clin Microbiol. 2009;47:2149–55.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Leão SC, Matsumoto CK, Carneiro A, Ramos RT, Nogueira CL, Lima JD Jr, Lima KV, Lopes ML, Schneider H, Azevedo VA, Da Costa da Silva A. The detection and sequencing of a broad-host-range conjugative IncP-Ibeta plasmid in an epidemic strain of Mycobacterium abscessus subsp bolletii. PLoS One. 2013;8:e60746.PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Raiol T, Ribeiro GM, Maranhão AQ, Bocca AL, Silva-Pereira I, Junqueira-Kipnis AP, Brigido MM, Kipnis A. Complete genome sequence of Mycobacterium massiliense. J Bacteriol. 2012;194:5455.PubMedPubMedCentralCrossRefGoogle Scholar
  165. 165.
    Kim B-J, Kim B-R, Hong S-H, Seok S-H, Kook Y-H. Complete genome sequence of Mycobacterium massiliense clinical strain Asan 505945, belonging to the type II genotype. Genome Announc. 2013;1:e00429–00413.Google Scholar
  166. 166.
    Tettelin H, Davidson RM, Agrawal S, Aitken ML, Shallom S, Hasan NA, Strong M, de Moura VCN, De Groote MA, Duarte RS, Hine E, Parankush S, Su Q, Daugherty SC, Fraser CM, Brown-Elliott BA, Wallace RJ Jr, Holland SM, Sampaio EP, Olivier KN, Jackson M, Zelazny AM. High-level relatedness among Mycobacterium abscessus subsp. massiliense strains from widely separated outbreaks. Emerg Infect Dis. 2014;20:364–71.PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Brown-Elliott BA, Philley JV, Griffith DE, Thakkar F, Wallace RJ Jr. 2017. In vitro susceptibility testing of bedaquiline against Mycobacterium avium complex. Antimicrob Agents Chemother. In Press.Google Scholar
  168. 168.
    Brown-Elliott BA, Philley JV, Griffith DE, Wallace RJ Jr. Comparison of in vitro susceptibility testing of tedizolid and linezolid against isolates of nontuberculous mycobacteria, 1st ASM-Microbe Meeting, 2016, Boston, MA.Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Microbiology, Mycobacteria/Nocardia Research LaboratoryThe University of Texas Health Science CenterTylerUSA

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