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Single-Nucleotide Polymorphism-Based Differentiation and Drug Resistance Detection in Mycobacterium Tuberculosis from Isolates Or Directly from Sputum C

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Single-Nucleotide Polymorphism-Based Differentiation and Drug Resistance Detection in Mycobacterium Tuberculosis from Isolates Or Directly from Sputum C CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector ORIGINAL ARTICLE 10.1111/j.1469-0691.2004.01034.x Single-nucleotide polymorphism-based differentiation and drug resistance detection in Mycobacterium tuberculosis from isolates or directly from sputum C. Arnold1, L. Westland1,2, G. Mowat3, A. Underwood1, J. Magee3 and S. Gharbia1 1Genomics, Proteomics and Bioinformatics Unit, Centre for Infections, Health Protection Agency, London, UK, 2Hogeschool van Utrecht, Faculteit Natuur & Techniek, Institute of Life Sciences and Chemistry, Utrecht, The Netherlands and 3Regional Centre for Mycobacteriology, Health Protection Agency Newcastle Laboratory, Newcastle, UK ABSTRACT The rapid technique of pyrosequencing was used to examine 123 samples (in the form of DNA extracts and inactivated sputum) of Mycobacterium spp. Of 99 Mycobacterium tuberculosis samples investigated for single-nucleotide polymorphisms (SNPs), 68% of isoniazid-resistant isolates analysed had an AGC fi ACC mutation in katG at codon 315, resulting in the Ser fi Thr substitution associated previously with isoniazid resistance. Of the rifampicin-resistant isolates, 92% showed SNPs in rpoB at codons 516, 531 or 526. Inactivated sputum samples and DNA extracts could both be analysed by pyrosequencing, and the method was able to differentiate rapidly between the closely related species of the M. tuberculosis complex (M. tuberculosis, Mycobacterium bovis, Mycobacterium africanum, Mycobacterium canetti and Mycobacterium microti), except between M. tuberculosis, M. canetti and one of two M. africanum strains. This low-cost, high-throughput technique could be used as a rapid screen for drug resistance and as a replacement for some of the time-consuming tests used currently for species identification. Keywords Antibiotic susceptibility testing, identification, Mycobacterium tuberculosis complex, pyrosequencing, resistance Original Submission: 5 April 2004; Revised Submission: 2 September 2004; Accepted: 11 September 2004 Clin Microbiol Infect 2005; 11: 122–130 amikacin, and fluoroquinolones such as ofloxacin INTRODUCTION and ciprofloxacin, are used as second-line agents. It has been estimated that one-third of the global Drug resistance in M. tuberculosis occurs fol- population is infected with Mycobacterium tuber- lowing spontaneous mutation in target genes culosis, with c. 9 million cases of active tubercu- such as katG, rpoB and inhA [3]. The mechanisms losis (TB) and > 2 million deaths occurring each and the dominant mutations resulting in the drug year [1,2]. These numbers are increasing, as is the resistance profiles have been well-documented number of individuals infected with strains resist- [3–5]. Isoniazid resistance is often associated with ant to first-line anti-TB drugs. In the UK, the mutation in a gene encoding catalase-peroxidase current first-line treatment is a 2-month course of (katG), most frequently a Ser315Thr mutation [6]. isoniazid, rifampicin and pyrazinamide, often Rifampicin inhibits transcription by binding to with the addition of ethambutol, followed by the RNA polymerase b-subunit, encoded by the isoniazid and rifampicin for a further 4–6 months. rpoB gene [7], with resistance resulting from Aminoglycosides such as streptomycin and mutations in the rifampicin resistance-determin- ing region of rpoB, an 81-bp region encoding amino-acids 507–533. The most common (70%) Corresponding author and reprint requests: C. Arnold, mutations are at codons 526 and 531, and Genomics, Proteomics and Bioinformatics Unit, Health Pro- tection Agency, 61 Colindale Avenue, London NW9 5HT, UK are associated with high levels of resist- E-mail: [email protected] ance (> 100 mg ⁄ L). Less frequent mutations, Ó 2004 Copyright by the European Society of Clinical Microbiology and Infectious Diseases Arnold et al. Single-nucleotide polymorphisms in M. tuberculosis 123 particularly in codon 516, are associated with members of the genus Mycobacterium, and spe- lower levels of resistance. The fluoroquinolones cifically the M. tuberculosis complex (MTBC), were considered to be alternative drugs, as they using a composite assay of these three genes. prevent transcription and cell division by sup- As public health intervention strategies and pressing DNA supercoiling [8]. DNA gyrase, transmission models may also benefit from the encoded by gyrAB, catalyses negative supercoil- interpretation of data in the context of phyloge- ing of DNA. Mutations in the short quinolone netically relevant genetic frameworks (geno- resistance-determining region and at codon 94 of types) based on SNPs [14,15], a pyrosequencing gyrA overcome the DNA gyrase-blocking action assay to determine genotype was also developed. of fluoroquinolones [8]. These three composite high-throughput assays, A rapid screening system for these mutations designed to be used on sputum samples and among isolates of M. tuberculosis is essential. A cultures in the early stages of growth to deter- sequence-based method, rather than a DNA mine resistance profile, species and genotype, migration or a hybridisation approach, is ideal were applied to three groups of M. tuberculosis for the development of a fast, accurate and high- isolates to determine their utility in public health throughput system, as this will aid in the identi- microbiology. fication of alternative mutations in the regions analysed, as well as those characterised previ- MATERIALS AND METHODS ously. The present study investigated the possi- bility of detecting the most common mutations Samples by pyrosequencing, a short-read (c. 30–50 bp) In total, 123 samples of mycobacteria were studied, of which 98 sequencing technique based on the quantitative were M. tuberculosis nucleic acid extracts. detection of pyrophosphate released following Group 1 comprised 72 M. tuberculosis DNA extracts from three northwest London hospitals [16]. Seven (9.7%) of these nucleotide incorporation into a growing DNA extracted isolates were isoniazid-resistant (Table 1). There chain. The technology has also been used previ- were six epidemiologically related groups of isolates (100 ously for single-nucleotide polymorphism (SNP) and 203; 113 and 128; 129 and 264; 139 and 140; 232, 251, detection [9]. 252 and 253; 1085 and 1086). Group 2 comprised 20 M. tuberculosis DNA extracts and The slow-growing nature of M. tuberculosis seven inactivated sputum samples containing M. tuberculosis means that several weeks can elapse before the from northeast England (Newcastle) (Table 1). Fourteen of the susceptibility profile of an isolate is known and extracted isolates were isoniazid- or isoniazid- and rifampicin- appropriately guided anti-TB chemotherapy can resistant. The sputum samples, containing > 90 bacilli ⁄ field, were inactivated by boiling in 1 M NaOH for 10 min following be put in place. Although genotypic testing cannot dithiothreitol liquefaction (Sputasol; Oxoid, Basingstoke, UK). wholly replace phenotypic methods for the detec- Four of these samples yielded isoniazid-resistant M. tubercu- tion of antibiotic resistance, as not all mechanisms losis isolates. A further four sputum samples contained of action (and therefore specific mutations) are mycobacterial species other than those causing TB, i.e., known for the different drugs used, a molecular M. avium complex, M. malmoense and M. chelonae, which were isoniazid-resistant. screen capable of use on primary clinical samples Group 3 comprised 24 DNA extracts from 11 different to detect most mutations associated with resist- Mycobacterium spp. (Table 2) obtained from K. Kremer ance could be invaluable. This study therefore (National Institute of Public Health and the Environment, assessed pyrosequencing as a high-throughput, Bilthoven, The Netherlands) [17]. cost-effective genotypic screen for M. tuberculosis isoniazid resistance in which common mutations Primer design associated with resistance were detected in spu- Amplification and pyrosequencing primers were designed by tum samples and early cultures. visual comparison and confirmed with the use of on-line Speciation of mycobacteria has been attempted software (http://www.pyrosequencing.com). The sequence of M. tuberculosis H37Rv, ATCC 27294, was used as an in-silico previously by sequencing all or part of the 16S template. Pyrosequencing primers were designed to detect rRNA gene [10], but this approach has failed to resistance or species-associated SNPs (Fig. 1). Two of the delineate this highly conserved genus. Other regions analysed (katG 463 and gyrA 95) were control regions regions of the genome that are useful for myco- that were not associated with drug resistance, but were associated with genotype assignation of M. tuberculosis [14], bacterial speciation include rpoB [11,12] and gyrB namely: CTG ⁄ ACC = genotype I; CGG ⁄ ACC = genotype II; [13]. Therefore, the present study also assessed and CGG ⁄ AGC = genotype III (Table 1). pyrosequencing as a rapid test for identifying Ó 2004 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 122–130 124 Clinical Microbiology and Infection, Volume 11 Number 2, February 2005 Table 1. Strain information for Mycobacterium tuberculosis isolates in groups 1 and 2: resistance profile, single-nucleotide polymorphism profile and genotype katG 315 rpoB 516 rpoB 526 rpoB 531 gyrA 94 Identifier Resistance (WT = AGC) (WT = GAC) (WT = CAC) (WT = TCG) (WT = GAC) katG 463 gyrA 95 Genogroup Northwest London isolates (DNA extracts) WT profile 1 104, 124, 125, 126, WT AGC
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