Nontuberculous Mycobacteria in Cystic Fibrosis

Christopher J. Richards; Kenneth N. Olivier

doi:10.1055/s-0039-1693706

Seminars in Respiratory and Critical Care Medicine, Table of Contents

Semin Respir Crit Care Med 2019; 40(06): 737-750
DOI: 10.1055/s-0039-1693706

Review Article

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Nontuberculous Mycobacteria in Cystic Fibrosis

Christopher J. Richards

¹Division of Pulmonary and Critical Care Medicine, Massachusetts General Hospital, Boston, Massachusetts

,

Kenneth N. Olivier

²Laboratory of Chronic Airway Infection, Pulmonary Branch, Division of Intramural Research, National Heart, Lung, and Blood Institute, Bethesda, Maryland

› Author Affiliations

Abstract

Over the past decade, the incidence of nontuberculous mycobacterial (NTM) infection has been increasing in cystic fibrosis patients. Along with this have come a host of complications and burdens to patients that threaten longevity and quality of life. The two main constituents of NTM pulmonary disease, Mycobacterium avium complex (MAC) and M. abscessus, are notoriously difficult to treat with suboptimal clinical responses and are accompanied by high treatment burdens for patients. This review aims to summarize the current knowledge of NTM epidemiology, pathogenesis, professional society guidelines for diagnosis and treatment, and the efficacy of current management recommendations, with attention to cystic fibrosis patients. We go on to examine drugs of emerging but unknown efficacy in clinical use to provide a comprehensive assessment of the current state of management of NTM for cystic fibrosis patients.

Keywords

cystic fibrosis - nontuberculous mycobacterium - Mycobacterium avium complex - Mycobacterium abscessus - clofazimine - bedaquiline - liposomal amikacin

Full Text

References

References
1 O'Sullivan BP, Freedman SD. Cystic fibrosis. Lancet 2009; 373 (9678): 1891-1904
2 Bobadilla JL, Macek Jr M, Fine JP, Farrell PM. Cystic fibrosis: a worldwide analysis of CFTR mutations--correlation with incidence data and application to screening. Hum Mutat 2002; 19 (06) 575-606
3 Cystic Fibrosis Foundation Patient Registry 2017 Annual Data Report. Bethesda, MD: Cystic Fibrosis Foundation; 2018
4 Kunzelmann K, Schreiber R, Hadorn HB. Bicarbonate in cystic fibrosis. J Cyst Fibros 2017; 16 (06) 653-662
5 Goetz D, Ren CL. Review of Cystic Fibrosis. Pediatr Ann 2019; 48 (04) e154-e161
6 Jennings MT, Flume PA. Cystic fibrosis: translating molecular mechanisms into effective therapies. Ann Am Thorac Soc 2018; 15 (08) 897-902
7 Bernarde C, Keravec M, Mounier J. , et al. Impact of the CFTR-potentiator ivacaftor on airway microbiota in cystic fibrosis patients carrying a G551D mutation. PLoS One 2015; 10 (04) e0124124
8 Bessonova L, Volkova N, Higgins M. , et al. Data from the US and UK cystic fibrosis registries support disease modification by CFTR modulation with ivacaftor. Thorax 2018; 73 (08) 731-740
9 Heltshe SL, Mayer-Hamblett N, Burns JL. , et al; GOAL (the G551D Observation-AL) Investigators of the Cystic Fibrosis Foundation Therapeutics Development Network. Pseudomonas aeruginosa in cystic fibrosis patients with G551D-CFTR treated with ivacaftor. Clin Infect Dis 2015; 60 (05) 703-712
10 Gomez-Pastrana D, Nwokoro C, McLean M, Brown S, Christiansen N, Pao CS. Real-world effectiveness of ivacaftor in children with cystic fibrosis and the G551D mutation [in Spanish]. An Pediatr (Barc) 2019; 90 (03) 148-156
11 Adjemian J, Olivier KN, Prevots DR. Epidemiology of pulmonary nontuberculous mycobacterial sputum positivity in patients with cystic fibrosis in the United States, 2010-2014. Ann Am Thorac Soc 2018; 15 (07) 817-826
12 Nasiri MJ, Haeili M, Ghazi M. , et al. New insights in to the intrinsic and acquired drug resistance mechanisms in mycobacteria. Front Microbiol 2017; 8: 681
13 Parte AC. LPSN - List of Prokaryotic names with Standing in Nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 2018; 68 (06) 1825-1829
14 Hoefsloot W, van Ingen J, Andrejak C. , et al; Nontuberculous Mycobacteria Network European Trials Group. The geographic diversity of nontuberculous mycobacteria isolated from pulmonary samples: an NTM-NET collaborative study. Eur Respir J 2013; 42 (06) 1604-1613
15 Olivier KN, Weber DJ, Wallace Jr RJ. , et al; Nontuberculous Mycobacteria in Cystic Fibrosis Study Group. Nontuberculous mycobacteria. I: multicenter prevalence study in cystic fibrosis. Am J Respir Crit Care Med 2003; 167 (06) 828-834
16 Adjemian J, Olivier KN, Prevots DR. Nontuberculous mycobacteria among patients with cystic fibrosis in the United States: screening practices and environmental risk. Am J Respir Crit Care Med 2014; 190 (05) 581-586
17 Prevots DR, Adjemian J, Fernandez AG, Knowles MR, Olivier KN. Environmental risks for nontuberculous mycobacteria. Individual exposures and climatic factors in the cystic fibrosis population. Ann Am Thorac Soc 2014; 11 (07) 1032-1038
18 Adjemian J, Olivier KN, Seitz AE, Falkinham III JO, Holland SM, Prevots DR. Spatial clusters of nontuberculous mycobacterial lung disease in the United States. Am J Respir Crit Care Med 2012; 186 (06) 553-558
19 Spaulding AB, Lai YL, Zelazny AM. , et al. Geographic distribution of nontuberculous mycobacterial species identified among clinical isolates in the United States, 2009-2013. Ann Am Thorac Soc 2017; 14 (11) 1655-1661
20 Honda JR, Hasan NA, Davidson RM. , et al. Environmental nontuberculous mycobacteria in the Hawaiian Islands. PLoS Negl Trop Dis 2016; 10 (10) e0005068
21 Donohue MJ, Wymer L. Increasing prevalence rate of nontuberculous mycobacteria infections in five states, 2008-2013. Ann Am Thorac Soc 2016; 13 (12) 2143-2150
22 Meier A, Heifets L, Wallace Jr RJ. , et al. Molecular mechanisms of clarithromycin resistance in Mycobacterium avium: observation of multiple 23S rDNA mutations in a clonal population. J Infect Dis 1996; 174 (02) 354-360
23 Bar-On O, Mussaffi H, Mei-Zahav M. , et al. Increasing nontuberculous mycobacteria infection in cystic fibrosis. J Cyst Fibros 2015; 14 (01) 53-62
24 Thomson R, Donnan E, Konstantinos A. Notification of nontuberculous mycobacteria: an Australian perspective. Ann Am Thorac Soc 2017; 14 (03) 318-323
25 De Groote MA, Pace NR, Fulton K, Falkinham III JO. Relationships between Mycobacterium isolates from patients with pulmonary mycobacterial infection and potting soils. Appl Environ Microbiol 2006; 72 (12) 7602-7606
26 Fujita K, Ito Y, Hirai T. , et al. Genetic relatedness of Mycobacterium avium-intracellulare complex isolates from patients with pulmonary MAC disease and their residential soils. Clin Microbiol Infect 2013; 19 (06) 537-541
27 Malcolm KC, Caceres SM, Honda JR. , et al. Mycobacterium abscessus displays fitness for fomite transmission. Appl Environ Microbiol 2017; 83 (19) 83
28 Fletcher LA, Chen Y, Whitaker P, Denton M, Peckham DG, Clifton IJ. Survival of Mycobacterium abscessus isolated from people with cystic fibrosis in artificially generated aerosols. Eur Respir J 2016; 48 (06) 1789-1791
29 Caskey S, Moore JE, Rendall JC. In vitro activity of seven hospital biocides against Mycobacterium abscessus: implications for patients with cystic fibrosis. Int J Mycobacteriol 2018; 7 (01) 45-47
30 Sniadack DH, Ostroff SM, Karlix MA. , et al. A nosocomial pseudo-outbreak of Mycobacterium xenopi due to a contaminated potable water supply: lessons in prevention. Infect Control Hosp Epidemiol 1993; 14 (11) 636-641
31 Bennett SN, Peterson DE, Johnson DR, Hall WN, Robinson-Dunn B, Dietrich S. Bronchoscopy-associated Mycobacterium xenopi pseudoinfections. Am J Respir Crit Care Med 1994; 150 (01) 245-250
32 Gubler JG, Salfinger M, von Graevenitz A. Pseudoepidemic of nontuberculous mycobacteria due to a contaminated bronchoscope cleaning machine. Report of an outbreak and review of the literature. Chest 1992; 101 (05) 1245-1249
33 Conger NG, O'Connell RJ, Laurel VL. , et al. Mycobacterium simae outbreak associated with a hospital water supply. Infect Control Hosp Epidemiol 2004; 25 (12) 1050-1055
34 Camargos P, Le Bourgeois M, Revillon Y. , et al. Lung resection in cystic fibrosis: a survival analysis. Pediatr Pulmonol 2008; 43 (01) 72-76
35 Sermet-Gaudelus I, Le Bourgeois M, Pierre-Audigier C. , et al. Mycobacterium abscessus and children with cystic fibrosis. Emerg Infect Dis 2003; 9 (12) 1587-1591
36 Bryant JM, Grogono DM, Greaves D. , et al. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 2013; 381 (9877): 1551-1560
37 Yan J, Kevat A, Martinez E. , et al. Investigating transmission of Mycobacterium abscessus amongst children in an Australian cystic fibrosis centre. J Cyst Fibros 2019 (e-pub ahead of print). Doi: 10.1016/j.jcf.2019.02.011
38 Aitken ML, Limaye A, Pottinger P. , et al. Respiratory outbreak of Mycobacterium abscessus subspecies massiliense in a lung transplant and cystic fibrosis center. Am J Respir Crit Care Med 2012; 185 (02) 231-232
39 Tettelin H, Davidson RM, Agrawal S. , et al. High-level relatedness among Mycobacterium abscessus subsp. massiliense strains from widely separated outbreaks. Emerg Infect Dis 2014; 20 (03) 364-371
40 Zelazny AM, Root JM, Shea YR. , et al. Cohort study of molecular identification and typing of Mycobacterium abscessus, Mycobacterium massiliense, and Mycobacterium bolletii. J Clin Microbiol 2009; 47 (07) 1985-1995
41 Mougari F, Amarsy R, Veziris N. , et al. Standardized interpretation of antibiotic susceptibility testing and resistance genotyping for Mycobacterium abscessus with regard to subspecies and erm41 sequevar. J Antimicrob Chemother 2016; 71 (08) 2208-2212
42 Brown-Elliott BA, Vasireddy S, Vasireddy R. , et al. 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 (04) 1211-1215
43 Bastian S, Veziris N, Roux AL. , et al. Assessment of clarithromycin susceptibility in strains belonging to the Mycobacterium abscessus group by erm(41) and rrl sequencing. Antimicrob Agents Chemother 2011; 55 (02) 775-781
44 Koh WJ, Jeon K, Lee NY. , et al. Clinical significance of differentiation of Mycobacterium massiliense from Mycobacterium abscessus . Am J Respir Crit Care Med 2011; 183 (03) 405-410
45 Rollet-Cohen V, Roux AL, Le Bourgeois M. , et al. Mycobacterium bolletii lung disease in cystic fibrosis. Chest 2019; S0012-3692(19)30747-0
46 Kadota T, Matsui H, Hirose T. , et al. Analysis of drug treatment outcome in clarithromycin-resistant Mycobacterium avium complex lung disease. BMC Infect Dis 2016; 16: 31
47 Jönsson BE, Gilljam M, Lindblad A, Ridell M, Wold AE, Welinder-Olsson C. Molecular epidemiology of Mycobacterium abscessus, with focus on cystic fibrosis. J Clin Microbiol 2007; 45 (05) 1497-1504
48 Malcolm KC, Caceres SM, Pohl K. , et al. Neutrophil killing of Mycobacterium abscessus by intra- and extracellular mechanisms. PLoS One 2018; 13 (04) e0196120
49 Bernut A, Herrmann JL, Kissa K. , et al. Mycobacterium abscessus cording prevents phagocytosis and promotes abscess formation. Proc Natl Acad Sci U S A 2014; 111 (10) E943-E952
50 Bernut A, Dupont C, Ogryzko NV. , et al. CFTR protects against Mycobacterium abscessus infection by fine-tuning host oxidative defenses. Cell Reports 2019; 26 (07) 1828-1840.e4
51 Ravnholt C, Kolpen M, Skov M. , et al. The importance of early diagnosis of Mycobacterium abscessus complex in patients with cystic fibrosis. APMIS 2018; 126 (12) 885-891
52 Griffith DE, Aksamit T, Brown-Elliott BA. , et al; ATS Mycobacterial Diseases Subcommittee; American Thoracic Society; Infectious Disease Society of America. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med 2007; 175 (04) 367-416
53 Miwa S, Shirai M, Toyoshima M. , et al. Efficacy of clarithromycin and ethambutol for Mycobacterium avium complex pulmonary disease. A preliminary study. Ann Am Thorac Soc 2014; 11 (01) 23-29
54 Griffith DE, Brown BA, Girard WM, Griffith BE, Couch LA, Wallace Jr RJ. Azithromycin-containing regimens for treatment of Mycobacterium avium complex lung disease. Clin Infect Dis 2001; 32 (11) 1547-1553
55 Kim EY, Chi SY, Oh IJ. , et al. Treatment outcome of combination therapy including clarithromycin for Mycobacterium avium complex pulmonary disease. Korean J Intern Med (Korean Assoc Intern Med) 2011; 26 (01) 54-59
56 Sim YS, Park HY, Jeon K, Suh GY, Kwon OJ, Koh WJ. Standardized combination antibiotic treatment of Mycobacterium avium complex lung disease. Yonsei Med J 2010; 51 (06) 888-894
57 Kwak N, Park J, Kim E, Lee CH, Han SK, Yim JJ. Treatment outcomes of Mycobacterium avium complex lung disease: a systematic review and meta-analysis. Clin Infect Dis 2017; 65 (07) 1077-1084
58 Floto RA, Olivier KN, Saiman L. , et al; US Cystic Fibrosis Foundation and European Cystic Fibrosis Society. US Cystic Fibrosis Foundation and European Cystic Fibrosis Society consensus recommendations for the management of non-tuberculous mycobacteria in individuals with cystic fibrosis. Thorax 2016; 71 (Suppl. 01) i1-i22
59 Morimoto K, Namkoong H, Hasegawa N. , et al; Nontuberculous Mycobacteriosis Japan Research Consortium. Macrolide-resistant Mycobacterium avium complex lung disease: analysis of 102 consecutive cases. Ann Am Thorac Soc 2016; 13 (11) 1904-1911
60 Mojica JE, Richards CJ, Husseini JS, Hariri LP. Case 40-2018: a 47-year-old woman with recurrent sinusitis, cough, and bronchiectasis. N Engl J Med 2018; 379 (26) 2558-2565
61 Griffith DE, Brown-Elliott BA, Langsjoen B. , et al. Clinical and molecular analysis of macrolide resistance in Mycobacterium avium complex lung disease. Am J Respir Crit Care Med 2006; 174 (08) 928-934
62 Lee SH, Yoo HK, Kim SH. , et al. The drug resistance profile of Mycobacterium abscessus group strains from Korea. Ann Lab Med 2014; 34 (01) 31-37
63 Jeon K, Kwon OJ, Lee NY. , et al. Antibiotic treatment of Mycobacterium abscessus lung disease: a retrospective analysis of 65 patients. Am J Respir Crit Care Med 2009; 180 (09) 896-902
64 Lam DL, Kapnadak SG, Godwin JD, Kicska GA, Aitken ML, Pipavath SN. Radiologic computed tomography features of Mycobacterium abscessus in cystic fibrosis. Clin Respir J 2018; 12 (02) 459-466
65 Moore EH. Atypical mycobacterial infection in the lung: CT appearance. Radiology 1993; 187 (03) 777-782
66 Martiniano SL, Sontag MK, Daley CL, Nick JA, Sagel SD. Clinical significance of a first positive nontuberculous mycobacteria culture in cystic fibrosis. Ann Am Thorac Soc 2014; 11 (01) 36-44
67 van Ingen J, Aksamit T, Andrejak C. , et al; for NTM-NET. Treatment outcome definitions in nontuberculous mycobacterial pulmonary disease: an NTM-NET consensus statement. Eur Respir J 2018; 51 (03) 1800170
68 Asgrimsson V, Gudjonsson T, Gudmundsson GH, Baldursson O. Novel effects of azithromycin on tight junction proteins in human airway epithelia. Antimicrob Agents Chemother 2006; 50 (05) 1805-1812
69 Cory TJ, Birket SE, Murphy BS. , et al. Impact of azithromycin treatment on macrophage gene expression in subjects with cystic fibrosis. J Cyst Fibros 2014; 13 (02) 164-171
70 Schögler A, Kopf BS, Edwards MR. , et al. Novel antiviral properties of azithromycin in cystic fibrosis airway epithelial cells. Eur Respir J 2015; 45 (02) 428-439
71 Mayer-Hamblett N, Retsch-Bogart G, Kloster M. , et al; OPTIMIZE Study Group. Azithromycin for early pseudomonas infection in cystic fibrosis. The OPTIMIZE Randomized Trial. Am J Respir Crit Care Med 2018; 198 (09) 1177-1187
72 Saiman L, Marshall BC, Mayer-Hamblett N. , et al; Macrolide Study Group. Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA 2003; 290 (13) 1749-1756
73 Samson C, Tamalet A, Thien HV. , et al. Long-term effects of azithromycin in patients with cystic fibrosis. Respir Med 2016; 117: 1-6
74 Murray TS, Egan M, Kazmierczak BI. Pseudomonas aeruginosa chronic colonization in cystic fibrosis patients. Curr Opin Pediatr 2007; 19 (01) 83-88
75 Mogayzel Jr PJ, Naureckas ET, Robinson KA. , et al; Cystic Fibrosis Foundation Pulmonary Clinical Practice Guidelines Committee. Cystic Fibrosis Foundation pulmonary guideline. pharmacologic approaches to prevention and eradication of initial Pseudomonas aeruginosa infection. Ann Am Thorac Soc 2014; 11 (10) 1640-1650
76 Gibson PG, Yang IA, Upham JW. , et al. Effect of azithromycin on asthma exacerbations and quality of life in adults with persistent uncontrolled asthma (AMAZES): a randomised, double-blind, placebo-controlled trial. Lancet 2017; 390 (10095): 659-668
77 Banerjee D, Honeybourne D, Khair OA. The effect of oral clarithromycin on bronchial airway inflammation in moderate-to-severe stable COPD: a randomized controlled trial. Treat Respir Med 2004; 3 (01) 59-65
78 Martinez FJ, Curtis JL, Albert R. Role of macrolide therapy in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 2008; 3 (03) 331-350
79 Yates B, Murphy DM, Forrest IA. , et al. Azithromycin reverses airflow obstruction in established bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2005; 172 (06) 772-775
80 Poletti V, Casoni G, Chilosi M, Zompatori M. Diffuse panbronchiolitis. Eur Respir J 2006; 28 (04) 862-871
81 Altenburg J, de Graaff CS, Stienstra Y. , et al. Effect of azithromycin maintenance treatment on infectious exacerbations among patients with non-cystic fibrosis bronchiectasis: the BAT randomized controlled trial. JAMA 2013; 309 (12) 1251-1259
82 Valery PC, Morris PS, Byrnes CA. , et al. Long-term azithromycin for Indigenous children with non-cystic-fibrosis bronchiectasis or chronic suppurative lung disease (Bronchiectasis Intervention Study): a multicentre, double-blind, randomised controlled trial. Lancet Respir Med 2013; 1 (08) 610-620
83 Wong C, Jayaram L, Karalus N. , et al. Azithromycin for prevention of exacerbations in non-cystic fibrosis bronchiectasis (EMBRACE): a randomised, double-blind, placebo-controlled trial. Lancet 2012; 380 (9842): 660-667
84 Renna M, Schaffner C, Brown K. , et al. Azithromycin blocks autophagy and may predispose cystic fibrosis patients to mycobacterial infection. J Clin Invest 2011; 121 (09) 3554-3563
85 Levy I, Grisaru-Soen G, Lerner-Geva L. , et al. Multicenter cross-sectional study of nontuberculous mycobacterial infections among cystic fibrosis patients, Israel. Emerg Infect Dis 2008; 14 (03) 378-384
86 Binder AM, Adjemian J, Olivier KN, Prevots DR. Epidemiology of nontuberculous mycobacterial infections and associated chronic macrolide use among persons with cystic fibrosis. Am J Respir Crit Care Med 2013; 188 (07) 807-812
87 Cogen JD, Onchiri F, Emerson J. , et al. Chronic azithromycin use in cystic fibrosis and risk of treatment-emergent respiratory pathogens. Ann Am Thorac Soc 2018; 15 (06) 702-709
88 Moon SM, Park HY, Kim SY. , et al. Clinical characteristics, treatment outcomes, and resistance mutations associated with macrolide-resistant Mycobacterium avium complex lung disease. Antimicrob Agents Chemother 2016; 60 (11) 6758-6765
89 Jhun BW, Yang B, Moon SM. , et al. Amikacin inhalation as salvage therapy for refractory nontuberculous mycobacterial lung disease. Antimicrob Agents Chemother 2018; 62 (07) 62
90 Olivier KN, Shaw PA, Glaser TS. , et al. Inhaled amikacin for treatment of refractory pulmonary nontuberculous mycobacterial disease. Ann Am Thorac Soc 2014; 11 (01) 30-35
91 Peloquin CA, Berning SE, Nitta AT. , et al. Aminoglycoside toxicity: daily versus thrice-weekly dosing for treatment of mycobacterial diseases. Clin Infect Dis 2004; 38 (11) 1538-1544
92 Malinin V, Neville M, Eagle G, Gupta R, Perkins WR. Pulmonary deposition and elimination of liposomal amikacin for inhalation and effect on macrophage function after administration in rats. Antimicrob Agents Chemother 2016; 60 (11) 6540-6549
93 Caimmi D, Martocq N, Trioleyre D. , et al. Positive effect of liposomal amikacin for inhalation on Mycobacterium abcessus in cystic fibrosis patients. Open Forum Infect Dis 2018; 5 (03) ofy034
94 Handelsman JA, Nasr SZ, Pitts C, King WM. Prevalence of hearing and vestibular loss in cystic fibrosis patients exposed to aminoglycosides. Pediatr Pulmonol 2017; 52 (09) 1157-1162
95 Griffith DE, Eagle G, Thomson R. , et al; CONVERT Study Group. Amikacin liposome inhalation suspension for treatment-refractory lung disease caused by Mycobacterium avium complex (CONVERT): a prospective, open-label, randomized study. Am J Respir Crit Care Med 2018 (e-pub ahead of print). Doi: 10.1164/rccm.201807-1318OC
96 Pryjma M, Burian J, Kuchinski K, Thompson CJ. Antagonism between front-line antibiotics clarithromycin and amikacin in the treatment of Mycobacterium abscessus infections is mediated by the whiB7 gene. Antimicrob Agents Chemother 2017; 61 (11) 61
97 Nessar R, Reyrat JM, Murray A, Gicquel B. Genetic analysis of new 16S rRNA mutations conferring aminoglycoside resistance in Mycobacterium abscessus . J Antimicrob Chemother 2011; 66 (08) 1719-1724
98 Woods GL. Performance Standards for Susceptibility Testing of Mycobacteria, Nocardia spp., and Other Aerobic Actinomycetes. Wayne, PA: Clinical and Laboratory Standards Institute; 2018
99 Brown-Elliott BA, Iakhiaeva E, Griffith DE. , et al. 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 (10) 3389-3394
100 McGuffin SA, Pottinger PS, Harnisch JP. Clofazimine in nontuberculous mycobacterial infections: a growing niche. Open Forum Infect Dis 2017; 4 (03) ofx147
101 Murashov MD, LaLone V, Rzeczycki PM. , et al. The physicochemical basis of clofazimine-induced skin pigmentation. J Invest Dermatol 2018; 138 (03) 697-703
102 Ferro BE, Meletiadis J, Wattenberg M. , et al. Clofazimine prevents the regrowth of Mycobacterium abscessus and Mycobacterium avium type strains exposed to amikacin and clarithromycin. Antimicrob Agents Chemother 2015; 60 (02) 1097-1105
103 Yang B, Jhun BW, Moon SM. , et al. Clofazimine-containing regimen for the treatment of Mycobacterium abscessus lung disease. Antimicrob Agents Chemother 2017; 61 (06) e02052-e16
104 Field SK, Cowie RL. Treatment of Mycobacterium avium-intracellulare complex lung disease with a macrolide, ethambutol, and clofazimine. Chest 2003; 124 (04) 1482-1486
105 Moran GJ, Fang E, Corey GR, Das AF, De Anda C, Prokocimer P. Tedizolid for 6 days versus linezolid for 10 days for acute bacterial skin and skin-structure infections (ESTABLISH-2): a randomised, double-blind, phase 3, non-inferiority trial. Lancet Infect Dis 2014; 14 (08) 696-705
106 Lee EY, Caffrey AR. Thrombocytopenia with tedizolid and linezolid. Antimicrob Agents Chemother 2017; 62 (01) 62
107 Winthrop KL, Ku JH, Marras TK. , et al. The tolerability of linezolid in the treatment of nontuberculous mycobacterial disease. Eur Respir J 2015; 45 (04) 1177-1179
108 Brown-Elliott BA, Wallace Jr RJ. In vitro susceptibility testing of tedizolid against nontuberculous Mycobacteria. J Clin Microbiol 2017; 55 (06) 1747-1754
109 Wallace Jr RJ, Brown-Elliott BA, Ward SC, Crist CJ, Mann LB, Wilson RW. Activities of linezolid against rapidly growing mycobacteria. Antimicrob Agents Chemother 2001; 45 (03) 764-767
110 Tang YW, Cheng B, Yeoh SF, Lin RTP, Teo JWP. Tedizolid activity against clinical Mycobacterium abscessus complex isolates-an in vitro characterization study. Front Microbiol 2018; 9: 2095
111 Kim SY, Jhun BW, Moon SM. , et al. Genetic mutations in linezolid-resistant Mycobacterium avium complex and Mycobacterium abscessus clinical isolates. Diagn Microbiol Infect Dis 2019; 94 (01) 38-40
112 Koul A, Dendouga N, Vergauwen K. , et al. Diarylquinolines target subunit c of mycobacterial ATP synthase. Nat Chem Biol 2007; 3 (06) 323-324
113 Hards K, Robson JR, Berney M. , et al. Bactericidal mode of action of bedaquiline. J Antimicrob Chemother 2015; 70 (07) 2028-2037
114 Worley MV, Estrada SJ. Bedaquiline: a novel antitubercular agent for the treatment of multidrug-resistant tuberculosis. Pharmacotherapy 2014; 34 (11) 1187-1197
115 Brown-Elliott BA, Wallace Jr RJ. In vitro susceptibility testing of bedaquiline against Mycobacterium abscessus complex. Antimicrob Agents Chemother 2019; 63 (02) 63
116 Li B, Ye M, Guo Q. , et al. Determination of MIC distribution and mechanisms of decreased susceptibility to bedaquiline among clinical isolates of Mycobacterium abscessus . Antimicrob Agents Chemother 2018; 62 (07) 62
117 Brown-Elliott BA, Philley JV, Griffith DE, Thakkar F, Wallace Jr RJ. In vitro susceptibility testing of bedaquiline against Mycobacterium avium complex. Antimicrob Agents Chemother 2017; 61 (02) 61
118 Philley JV, Wallace Jr RJ, Benwill JL. , et al. Preliminary results of bedaquiline as salvage therapy for patients with nontuberculous mycobacterial lung disease. Chest 2015; 148 (02) 499-506
119 Svensson EM, Murray S, Karlsson MO, Dooley KE. Rifampicin and rifapentine significantly reduce concentrations of bedaquiline, a new anti-TB drug. J Antimicrob Chemother 2015; 70 (04) 1106-1114
120 Ruth MM, Sangen JJN, Remmers K. , et al. A bedaquiline/clofazimine combination regimen might add activity to the treatment of clinically relevant non-tuberculous mycobacteria. J Antimicrob Chemother 2019; 74 (04) 935-943
121 Soroka D, Dubée V, Soulier-Escrihuela O. , et al. Characterization of broad-spectrum Mycobacterium abscessus class A β-lactamase. J Antimicrob Chemother 2014; 69 (03) 691-696
122 Wallace Jr RJ, Swenson JM, Silcox VA, Bullen MG. Treatment of nonpulmonary infections due to Mycobacterium fortuitum and Mycobacterium chelonei on the basis of in vitro susceptibilities. J Infect Dis 1985; 152 (03) 500-514
123 Lavollay M, Dubée V, Heym B. , et al. In vitro activity of cefoxitin and imipenem against Mycobacterium abscessus complex. Clin Microbiol Infect 2014; 20 (05) O297-O300
124 Lefebvre AL, Le Moigne V, Bernut A. , et al. Inhibition of the β-lactamase Bla_Mab by avibactam improves the in vitro and in vivo efficacy of imipenem against Mycobacterium abscessus . Antimicrob Agents Chemother 2017; 61 (04) 61
125 Pandey R, Chen L, Manca C. , et al. Dual β-lactam combinations highly active against Mycobacterium abscessus complex in vitro . MBio 2019; 10 (01) 10
126 Rahme C, Butterfield JM, Nicasio AM, Lodise TP. Dual beta-lactam therapy for serious Gram-negative infections: is it time to revisit?. Diagn Microbiol Infect Dis 2014; 80 (04) 239-259
127 Kaushik A, Ammerman NC, Lee J. , et al. In vitro activity of the new β-lactamase inhibitors relebactam and vaborbactam in combination with β-lactams against Mycobacterium abscessus complex clinical isolates. Antimicrob Agents Chemother 2019; 63 (03) 63
128 Deshpande D, Srivastava S, Chapagain ML. , et al. The discovery of ceftazidime/avibactam as an anti-Mycobacterium avium agent. J Antimicrob Chemother 2017; 72 (Suppl. 02) i36-i42
129 Miller C, McMullin B, Ghaffari A. , et al. Gaseous nitric oxide bactericidal activity retained during intermittent high-dose short duration exposure. Nitric Oxide 2009; 20 (01) 16-23
130 Deppisch C, Herrmann G, Graepler-Mainka U. , et al. Gaseous nitric oxide to treat antibiotic resistant bacterial and fungal lung infections in patients with cystic fibrosis: a phase I clinical study. Infection 2016; 44 (04) 513-520
131 Yaacoby-Bianu K, Gur M, Toukan Y. , et al. Compassionate nitric oxide adjuvant treatment of persistent mycobacterium infection in cystic fibrosis patients. Pediatr Infect Dis J 2018; 37 (04) 336-338
132 Bentur L, Gur M, Ashkenazi M. , et al. Pilot study to test inhaled nitric oxide in cystic fibrosis patients with refractory Mycobacterium abscessus lung infection. J Cyst Fibros 2019 (pub ahead of print). Doi: 10.1016/j.jcf.2019.05.002
133 Kakasis A, Panitsa G. Bacteriophage therapy as an alternative treatment for human infections. A comprehensive review. Int J Antimicrob Agents 2019; 53 (01) 16-21
134 Chanishvili N. Bacteriophages as therapeutic and prophylactic means: summary of the Soviet and post Soviet experiences. Curr Drug Deliv 2016; 13 (03) 309-323
135 Casey E, van Sinderen D, Mahony J. In vitro characteristics of phages to guide ‘real life’ phage therapy suitability. Viruses 2018; 10 (04) 10
136 Dedrick RM, Guerrero-Bustamante CA, Garlena RA. , et al. Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus . Nat Med 2019; 25 (05) 730-733
137 Ward R, Carroll WD, Cunningham P. , et al. Radiation dose from common radiological investigations and cumulative exposure in children with cystic fibrosis: an observational study from a single UK centre. BMJ Open 2017; 7 (08) e017548
138 Grasemann H, Ciet P, Amin R. , et al. Changes in magnetic resonance imaging scores and ventilation inhomogeneity in children with cystic fibrosis pulmonary exacerbations. Eur Respir J 2017; 50 (02) 50
139 Altes TA, Johnson M, Fidler M. , et al. Use of hyperpolarized helium-3 MRI to assess response to ivacaftor treatment in patients with cystic fibrosis. J Cyst Fibros 2017; 16 (02) 267-274
140 Wielpütz MO, von Stackelberg O, Stahl M. , et al. Multicentre standardisation of chest MRI as radiation-free outcome measure of lung disease in young children with cystic fibrosis. J Cyst Fibros 2018; 17 (04) 518-527
141 Bader TR, Semelka RC, Pedro MS, Armao DM, Brown MA, Molina PL. Magnetic resonance imaging of pulmonary parenchymal disease using a modified breath-hold 3D gradient-echo technique: initial observations. J Magn Reson Imaging 2002; 15 (01) 31-38
142 Chung JH, Huitt G, Yagihashi K. , et al. Proton magnetic resonance imaging for initial assessment of isolated Mycobacterium avium complex pneumonia. Ann Am Thorac Soc 2016; 13 (01) 49-57