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Nontuberculous Mycobacteria from Gene Sequences to Clinical Relevance PDF hosted at the Radboud Repository of the Radboud University Nijmegen The following full text is a publisher's version. For additional information about this publication click this link. http://hdl.handle.net/2066/52929 Please be advised that this information was generated on 2021-10-07 and may be subject to change. Nontuberculous Mycobacteria From Gene Sequences to Clinical Relevance Jakko van Ingen Nontuberculous mycobacteria from gene sequences to clinical relevance Printing of this thesis was financially supported by: KNCV Tuberculosefonds Hain Lifescience Innogenetics bioMérieux BD Europe J. van Ingen Nontuberculous mycobacteria; from gene sequence to clinical relevance Thesis Radboud University Nijmegen Medical Centre, Nijmegen, the Netherlands, with summary in Dutch; 348 pages. © 2009 ISBN/EAN: 978-90-9024581-2 Print: Ipskamp Drukkers B.V., Enschede Design & Layout: M.K.P. Poll & J. van Ingen Photographs: J. van Ingen & H.M.H. Braakman Cover: Sher Dor Madrassa, Samarkand, Uzbekistan No part of this book may be reproduced in any form without written permission of the author. Nontuberculous mycobacteria from gene sequences to clinical relevance Een wetenschappelijke proeve op het gebied van de Medische Wetenschappen Proefschrift ter verkrijging van de graad van doctor aan de Radboud Universiteit Nijmegen op gezag van de rector magnificus, prof. mr. S.C.J.J. Kortmann volgens besluit van het college van decanen in het openbaar te verdedigen op maandag 21 september 2009, om 15.30 uur precies door Jakobus van Ingen, geboren op 14 juni 1979 te Kesteren Promotor: Prof. dr. P.N.R. Dekhuijzen Copromotores: Dr. M.J. Boeree Dr. D. van Soolingen Manuscriptcommissie: Prof. dr. J. W. M. van der Meer (voorzitter) Prof. dr. P. E. Verweij Prof. C. L. Daley (University of Colorado, Denver, Colorado) Sweet to ride forth at evening from the wells When shadows pass gigantic on the sand, And softly through the silence beat the bells Along the Golden Road to Samarkand. We travel not for trafficking alone: By hotter winds our fiery hearts are fanned: For lust of knowing what should not be known We make the Golden Journey to Samarkand. James Elroy Flecker, Golden Journey to Samarkand (1913) Table of Contents Chapter 1: General introduction 11 Chapter 2: Clinical relevance of isolation of nontuberculous 33 mycobacteria in the Netherlands 2.1 The clinical relevance of nontuberculous mycobacteria isolated in 35 the Nijmegen-Arnhem region, the Netherlands 2.2 Mycobacterium xenopi clinical relevance and determinants, the 47 Netherlands 2.3 Clinical relevance of Mycobacterium simiae in pulmonary samples 57 2.4 Clinical relevance of Mycobacterium szulgai in the Netherlands 65 2.5 Clinical Mycobacterium conspicuum isolation from two 75 immunocompetent patients in the Netherlands 2.6 Clinical relevance of Mycobacterium malmoense isolation in the 79 Netherlands 2.7 Relevance of Mycobacterium chelonae and Mycobacterium 89 abscessus isolation in 95 patients 2.8 Impact of new American Thoracic Society diagnostic criteria on 101 management of nontuberculous mycobacterial infection 2.9 The changing pattern of clinical Mycobacterium avium isolation 103 in the Netherlands 2.10 Otomastoiditis caused by nontuberculous mycobacteria, the 111 Netherlands Chapter 3: Nontuberculous mycobacterial disease in patients treated 119 for rheumatic disease 3.1 Pulmonary Mycobacterium szulgai infection and treatment in a 121 patient receiving anti-tumor necrosis factor therapy 3.2 Mycobacterial disease in patients with rheumatic disease 131 Chapter 4: How can we improve treatment outcome in nontuberculous 147 mycobacterial disease? 4.1 In vitro drug susceptibility of 2275 clinical nontuberculous 149 Mycobacterium strains of 49 species in the Netherlands 4.2 In vitro activity of thioridazine against mycobacteria 161 4.3 Surgery for nontuberculous mycobacterial lung disease: Strike in 165 time Chapter 5: The burden of unidentifiable mycobacteria in a national 177 reference laboratory 5.1 Re-analysis of 178 previously unidentifiable Mycobacterium 179 isolates in the Netherlands from the 1999-2007 period 5.2 Mycobacterium noviomagense sp. nov.; clinical relevance 189 evaluated in 17 patients 5.3 Proposal to elevate Mycobacterium avium complex ITS sequevar 199 MAC-Q to Mycobacterium vulneris sp. nov. 5.4 Mycobacterium mantenii sp. nov.; A novel pathogenic slowly 211 growing scotochromogenic Mycobacterium species Chapter 6: Inter- and intraspecies genetic divergence and its relation 223 to mycobacterial taxonomy and virulence 6.1 Intraspecies genetic divergence in nontuberculous mycobacteria 225 6.2 The Region of Difference 1 in nontuberculous Mycobacterium 239 species adds a phylogenetic and taxonomical character 6.3 Presence of esat-6 and cfp-10 genes does not lead to phagolysosome 245 translocation of Mycobacterium szulgai Chapter 7: Nontuberculous mycobacteria in other geographical areas 253 7.1 Clinical relevance of nontuberculous mycobacteria, Oman 255 7.2 Mycobacterium riyadhense sp. nov.; a non-tuberculous species 261 identified asMycobacterium tuberculosis complex by a commercial line-probe assay 7.3 Nontuberculous mycobacteria in Vietnam; more than 269 confounders of culture-based TB diagnosis 7.4 Invasive disease caused by nontuberculous mycobacteria in HIV- 273 infected patients, Tanzania Chapter 8: Discussion, conclusions and strategies for future research 281 Chapter 9: Summary 319 Chapter 10: Nederlandstalige samenvatting 327 Dankwoord 337 Biography 343 List of publications 345 Chapter 1 General Introduction General Introduction Chapter 1 12 Chapter 1 Chapter 1: General Introduction A historical perspective In the years following the ground-breaking discovery of Mycobacterium tuberculosis by Robert Koch in 1882, similar mycobacteria were isolated from a wide variety of animal and environmental sources. At the time, these were all considered “atypical M. tuberculosis”.1 In the following decades, it became evident that the genus Mycobacterium comprises three separate parts: I) the Mycobacterium tuberculosis complex, causative agents of tuberculosis in humans and animals, II) M. leprae, the causative agent of leprosy, and III) the “atypical” mycobacteria. From the 1950’s on, the pathogenicity of these “atypical” mycobacteria to humans was increasingly recognized.1 This recognition followed a key publication by Buhler and Pollack,2 in which they described two cases of pulmonary disease similar to tuberculosis, but caused by what they called the “yellow bacillus”. The “yellow bacillus” was named after its production of a bright yellow pigment after exposure to light; this species is today known as M. kansasii. In addition to “atypical pulmonary tuberculosis”, specific diseases were attributed to the “atypical” mycobacteria, including pediatric cervical lymphadenitis and skin disease by M. marinum (swimming pool granuloma) and M. ulcerans (Buruli ulcer).1 At the time, it was often suggested that these “atypical” mycobacteria had arisen in some way as a result of the introduction of chemotherapy for tuberculosis, with streptomycin, isoniazid and para- aminosalicylic acid.3 Various attempts were even made to create “atypical” mycobacteria, by repeated in vitro exposure of M. tuberculosis to various drugs; although drug resistance, a hallmark feature of “atypical” mycobacteria, could be induced, the resulting strains were still M. tuberculosis.3 Just four years after Buhler and Pollack, the first cases of disease caused by “atypical” mycobacteria were recorded in the Netherlands. Manten reported three patients who had been admitted to a sanatorium on a clinical and radiological suspicion of tuberculosis. All their sputum samples grew the “yellow bacillus” on culture, in large quantities.4 The increasing recognition of their ability to cause human disease led to a long discussion on the correct nomenclature of the “atypical” mycobacteria. Different authors in different periods have proposed the names anonymous mycobacteria, environmental mycobacteria, atypical mycobacteria, opportunist mycobacteria, mycobacteria other than tubercle bacilli (MOTT) and nontuberculous mycobacteria.1 As these mycobacteria make up the majority of species within the genus Mycobacterium, the term “atypical” is debatable. Moreover, many of these mycobacteria are no longer anonymous and there is no evidence that they are environmental or opportunistic pathogens by definition. Hence, we prefer the term nontuberculous mycobacteria (NTM) and it will be used throughout this thesis. 13 General Introduction Chapter 1 To facilitate structured clinical and taxonomical study, Runyon proposed a classification of NTM into four major groups, based on growth rate and colony pigmentation, in his seminal 1959 review.3 His bacteriological classification, which remained in use until the wide-scale application of molecular techniques, is summarized in Table 1. Table 1: Classification of nontuberculous mycobacteria according to Runyon3 Group Characteristics Important species I Slow growth; Pigmentation after M. kansasii, M. szulgai, exposure to light (Photochromogens) M. simiae II Slow growth; Pigmentation without M. scrofulaceum, M. xenopi, light exposure (Scotochromogens) M. gordonae III Slow growth; No pigmentation (Non- M. avium, M. intracellulare, chromogens) M. malmoense IV Rapid growers M. fortuitum, M. abscessus, M. chelonae Much of the early research in the Netherlands also focused on the classification of mycobacteria based on bacteriological features. Coster made an important contribution with his animal
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