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Research Article Drug Susceptibility of 33 Reference Strains of Slowly Growing Mycobacteria to 19 Antimicrobial Agents

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Research Article Drug Susceptibility of 33 Reference Strains of Slowly Growing Mycobacteria to 19 Antimicrobial Agents Hindawi BioMed Research International Volume 2017, Article ID 1584658, 13 pages https://doi.org/10.1155/2017/1584658 Research Article Drug Susceptibility of 33 Reference Strains of Slowly Growing Mycobacteria to 19 Antimicrobial Agents Hui Pang,1 Yi Jiang,2,3 and Kanglin Wan2,3 1 Department of Immunology, Changzhi Medical College, Changzhi, Shanxi 046000, China 2State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China 3Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, Hangzhou, Zhejiang 310000, China Correspondence should be addressed to Kanglin Wan; [email protected] Received 23 December 2016; Revised 24 March 2017; Accepted 6 April 2017; Published 20 April 2017 Academic Editor: Frederick D. Quinn Copyright © 2017 Hui Pang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Objectives. Slowly growing mycobacteria (SGM) are prevalent worldwide and cause an extensive spectrum of diseases. Methods. In this study, the antimicrobial susceptibility of 33 reference strains of SGM to 19 antimicrobial agents was tested using a modified microdilution method. Results. Cefmetazole (32/33) and azithromycin (32/33) exhibited the highest antimicrobial activity, and dap- sone (9/33) exhibited the lowest activity against the tested strains. Cefoxitin (30/33), cefoperazone (28/33), and cefepime (28/33) were effective against a high proportion of strains, and macrolides were also highly effective as well as offering the benefit of convenient oral administration to patients. Linezolid (27/33), meropenem (26/33), sulfamethoxazole (26/33), and tigecycline (25/33) showed the highest activity; clofazimine (20/33) and doxycycline (18/33) showed intermediate activity; and rifapentine (13/33), rifabutin (13/33), and minocycline (11/33) showed low antimicrobial activity, closely followed by thioacetazone (10/33) and pasiniazid (10/33), against the tested organisms. According to their susceptibility profiles, the slowly growing species Mycobacterium avium and Mycobacterium simiae were the least susceptible to the tested drugs, whereas Mycobacterium intracellulare, Mycobacterium asiaticum, Mycobacterium scrofulaceum, Mycobacterium szulgai, Mycobacterium branderi,andMycobacterium holsaticum were the most susceptible. Conclusions. In summary, cephalosporins and macrolides, particularly cefmetazole, azithromycin, clarithromycin, and roxithromycin, showed good antimicrobial activity against the reference strains of SGM. 1. Introduction growing species were the first nontuberculous mycobacteria (NTM) to be recognized as causing chronic lung disease Slowly growing mycobacteria (SGM) species are ubiquitous [4, 5], which may bring about diverse infections from minor organisms that are widely distributed in the environment [1], sicknesses to serious widespread disorders [6]. not only in tap water, soil, dust, and food products but also At present, standard therapeutic strategies to treat SGM in domestic and wild animals [2]. SGM form colonies visible infections are lacking. In this study, 19 new antimicrobial tothenakedeyeinmorethan7daysonsubculturemedia[3]. agents were tested against 33 reference SGM pathogens using SGM comprise some common species, such as the Mycobac- a modified broth microdilution method with the aim of iden- terium avium complex (Mycobacterium avium, Mycobacte- tifying optimal schemes according to the Clinical Laboratory rium intracellulare,andMycobacterium chimaera), Mycobac- Standards Institute (CLSI) (USA) [7, 8] and World Health terium kansasii, Mycobacterium haemophilum, Mycobacte- Organization (WHO) [9] guidelines. rium marinum,andMycobacterium ulcerans, in addition to some less common pathogens, such as Mycobacterium scro- 2. Materials and Methods fulaceum, Mycobacterium simiae, Mycobacterium malmoense and Mycobacterium xenopi. Mycobacterium xenopi is largely 2.1. Reference Strains. Thirty-three international reference distributed in Canada and northern Europe [4]. Slowly SGM strains were purchased from Deutsche Sammlung von 2 BioMed Research International Mikroorganismen und Zellkulturen (DSMZ) and the Amer- 3. Results ican Type Culture Collection (ATCC), including Mycobac- terium avium, Mycobacterium intracellulare, Mycobacterium The antimicrobial susceptibility profiles of the 33 SGM refer- shimoidei, Mycobacterium farcinogenes,andMycobacterium ence species to 19 antibacterial agents are presented in Table 1. Cephalosporins including cefoxitin (30/33, 90.91%), cefop- simiae (Table1).Thesestrainswereculturedattheappropriate erazone (28/33, 84.85%), cefmetazole (32/33, 96.97%), and temperatures. cefepime (28/33, 84.85%) exhibited high activity against the tested strains. Macrolide antibiotics including azithromycin 2.2. Antimicrobial Agents. Nineteen chemicals were pur- (32/33, 96.97%), clarithromycin (30/33, 90.91%), and rox- chased from Sigma-Aldrich Company: cefoxitin (FOX), ithromycin (31/33, 93.94%) were also effective against the cefoperazone (CFP), cefmetazole (CMZ), cefepime (FEP), SGM strains. Linezolid (27/33, 81.82%), meropenem (26/33, rifapentine (RPT), rifabutin (RBT), azithromycin (AZM), 78.79%), and sulfamethoxazole (26/33, 78.79%) showed simi- clarithromycin (CLR), roxithromycin (ROX), thioacetazone lar levels of activity against the tested strains, and clofazimine (20/33, 60.61%) inhibited most of the SGM strains. The tetra- (THI), doxycycline (DOX), minocycline (MIN), tigecycline cyclines, doxycycline (18/33, 54.55%), minocycline (11/33, (TIG), meropenem (MEM), clofazimine (CLO), sulfame- 33.33%), and tigecycline (25/33, 75.76%), exhibited different thoxazole (SMZ), pasiniazid (PASI), linezolid (LNZ), and levels of activity against the SGM standard species, whereas dapsone (DAP). All of the antituberculous agents were freshly rifapentine (13/33, 39.39%) and rifabutin (13/33, 39.39%) prepared. showed weak antimicrobial activity against the SGM, as did thioacetazone (10/33, 30.30%), pasiniazid (10/33, 30.30%), 2.3. Drug Susceptibility Test. SGM strains were incubated and dapsone (9/33, 27.27%). using Difco Middlebrook 7H10 Agar (BD company) with The drug susceptibility profiles of the tested organisms 5% oleic acid-albumin-dextrose-catalase (OADC) [8]. The revealed that Mycobacterium avium and Mycobacterium drug sensitivity tests were performed using a cation-adjusted simiae were the least susceptible to the tested drugs, Mueller-Hinton (CAMH) broth microdilution method, with whereas Mycobacterium intracellulare, Mycobacterium asiati- the addition of 5% OADC, according to the CLSI standard cum, Mycobacterium scrofulaceum, Mycobacterium szulgai, Mycobacterium branderi,andMycobacterium holsaticum operating procedure [8]. All of the experiments were per- were the most susceptible (Table 3 and Figure 1). Among the formed in 96-well microplates and repeated. The minimum Mycobacterium avium complex, Mycobacterium avium was inhibitory concentration (MIC) for each antibiotic for each themostresistanttothetesteddrugs,whereasMycobacterium strain was the mean of two experiments. Firstly, the bacterial intracellulare was the most susceptible (Figure 2). Azithromy- suspensions were prepared as follows: bacterial inocula were cin was identified as the most effective antimicrobial agent adjusted with normal saline to a density of a 0.5 McFarland against SGM species among the drugs tested, and dapsone × 7 standard with an inoculum density of approximately 1 10 was the least effective. colony forming units (CFU)/mL; then 50 Lofthebacterial suspension was mixed with 10 mL of CAMH and 5% OADC 4. Discussion broth for a 1 : 200 dilution. Secondly, 100 LofCAMHand 5% OADC medium were added to each well of a 96-well In this study, 19 antimicrobial susceptibility tests were per- microplate, with the exception of the first well of every row formed against 33 SGM organisms by a Microplate Alamar to which 180 Lofmediumanda20Ldrugdilutionwere Blue Assay. The current first-line drugs for the treatment of added. The solution in the first well was successively diluted nontuberculous mycobacteria are capreomycin, clarithromy- into subsequent wells, up to the 11th well. The 12th well cin, and rifampin. And the current second-line drugs for the ineveryrowwasusedasablankcontrol.Finally,100L treatment of nontuberculous mycobacteria are moxifloxacin, of the bacterial dilution was added to all of the wells. The linezolid, amikacin, ciprofloxacin, ethambutol, isoniazid, ultimate volume in each well was 200 L. All of the 96-well rifabutin, streptomycin, and trimethoprim-sulfamethoxazole ∘ microplatesweresealedinaplasticbagandincubatedat37 C. [7]. Our findings indicated that cephalosporins and macrol- The concentrations of sulfamethoxazole, dapsone, cefoxitin, ides, particularly cefmetazole, azithromycin, clarithromycin, cefmetazole, cefoperazone, cefepime, thioacetazone, pasini- androxithromycin,showedeffectiveantimicrobialactivity azid, minocycline, doxycycline, tigecycline, and meropenem against the tested strains. were 0.25–256 g/mL; the concentrations of clarithromycin, In recent studies [4, 11–15], cefoxitin and meropenem azithromycin, roxithromycin, clofazimine, rifapentine, and have been reported to show some activity against Mycobac- rifabutin were 0.03–32 g/mL; and the concentration of terium
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