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Antimicrobial susceptibility pattern in non-tuberculous mycobacteria in Iran: a systematic review

Mycobacteria volume 1, Article number: 2 (2025) Cite this article

Abstract

Background

Non-tuberculous mycobacteria (NTM) are ubiquitous environmental bacteria that can cause a variety of infections in humans, particularly those with underlying lung diseases. These infections are increasing worldwide and their antimicrobial susceptibility has decreased even more than that of tuberculous mycobacteria. Therefore, determining the local antimicrobial susceptibility of NTM can provide appropriate treatment strategies.

Materials and methods

This study, conducted based on the PRISMA statement, is a systematic review to assess non-tuberculous mycobacteria (NTM) prevalence and drug susceptibility patterns in Iran between 2012 and 2023. Data was extracted from various databases and screened for eligibility using the Rayyan app.

Results

Thirteen studies were included with clinical and environmental samples. Most of the studies were tested for antimicrobial susceptibility based on the CLSI broth dilution method. NTM species varied widely in their susceptibility to common antibiotics. They were generally less susceptible to first-line antituberculosis drugs and meropenem, and predominantly sensitive to amikacin and secondly clarithromycin.

Conclusion

Although NTM isolates are widespread in Iran and have increased resistance to common TB drugs, there is no evidence of this in the literature yet. Our systematic review suggests that amikacin is the most effective drug against almost all NTM species common in Iran.

Introduction

Non-tuberculous mycobacteria (NTM) are a diverse group of bacteria found in the environment and have received attention in recent years due to their increased antimicrobial resistance, even surpassing Mycobacterium tuberculosis. NTM causes pulmonary disease in patients with injured airways (e.g. cystic fibrosis [CF], chronic obstructive pulmonary disease [COPD]), suppressed immune system (e.g. age-related, drug-induced, congenital and acquired immunodeficiency syndromes), and gastroesophageal reflux disease (GERD) [1, 2]. The most important diagnostic challenge is the similarity of the appearance of NTM to M. tuberculosis (causative agent of TB) on a microscopic examination of sputum samples from patients with suspected mycobacterial pulmonary disease as a gold standard detection method. This diagnostic challenge is further complicated by the ability of NTM to adapt to and resist treatment with a variety of antibiotics, including those typically effective against tuberculosis [3]. Therefore, knowledge of the drug susceptibility profile of NTM strains is necessary for the appropriate management of NTM-infected patients.

Although several studies have investigated the prevalence and drug susceptibility patterns of NTM in Iran, there is no comprehensive synthesis of the available evidence. A systematic review is needed to obtain an overview of the prevalence and distribution of drug-resistant NTM strains in Iran. Our study builds on previous studies by synthesizing and analyzing all available data on NTM susceptibility patterns in Iran, and it also provides a comprehensive and up-to-date understanding of the current state of drug resistance in NTM strains in this country. The findings of this study will be of interest to clinicians, researchers, and policymakers involved in the diagnosis and management of NTM infections, and will also provide a basis for future research in this field.

Materials and methods

Search strategy

This study was conducted based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [4].

We conducted a comprehensive literature search using PubMed, Scopus, Web of Science, Scientific Information Database (SID), and Magiran to identify relevant studies on the prevalence and drug susceptibility patterns of NTM in Iran. The search was conducted in November 2022 and updated in July 2023 to include articles published between 2012 and 2023.

Our search strategy included both MeSH terms and free-text keywords related to non-tuberculous mycobacteria, prevalence, drug resistance, antimicrobial susceptibility, and atypical mycobacteria. We also searched the reference lists of included studies and relevant systematic reviews for additional studies that might have been missed. We restricted the search to studies published in English or Persian.

The search strategy was developed in consultation with a research librarian, and we used a combination of subject headings and text words to search for relevant studies. We used the latest version of the Rayyan app [5] for screening the titles and abstracts and for the inclusion and exclusion process.

Study selection

We screened the titles and abstracts of all identified articles to determine their eligibility for inclusion. The full text of potentially eligible articles was then reviewed to determine whether they met the following inclusion criteria: being original research (e.g., no case reports, editorials, or reviews), being conducted in Iran and reported in English or Persian, containing data of the drug susceptibility patterns ± prevalence of NTM species, clearly identifying of sample isolation, detection and identification method, samples being taken from humans or environment, using a single standard drug susceptibility testing method and reporting susceptibility rates based on that method. Otherwise, the studies were excluded. Any discrepancies regarding the inclusion of a study were resolved through discussion and consensus among the review authors.

Data extraction

Two reviewers independently extracted data from the included studies using a standardized data extraction form. The following data were extracted: study design, sample size, patient comorbidities, drug susceptibility testing methods, and antimicrobial susceptibility patterns of NTMs to different drugs.

Limitations

It should be noted that this review is subject to several limitations. Firstly, we only included studies published in English and Persian, which could lead to linguistic biases. Secondly, research is limited to articles published between 2012 and 2023 and we cannot rule out the possibility of relevant studies outside that time frame. Finally, the tool used for quality assessment of included studies (ROBINS-E) is not completely fitting into characteristics of studies included and it is just the most appropriate one (e.g. questions for quality assessment asked in domains 5 and 7 of this tool are not applicable for these studies). Despite these limitations, this review provides valuable information on the prevalence and sensitivity of NTM drugs in Iran, which can inform the development of more effective strategies for preventing and treating NTM infections in this population.

Results

Thirteen articles (11 with only clinical samples, 1 with only environmental samples, and 1 with a mixture of clinical and environmental samples) were included in the systematic review, with sample sizes ranging from 8 to 198 (Fig. 1). Table 1 summarizes the characteristics of the items included in this report. The methods for measuring antimicrobial susceptibility in the 10 studies were based on Clinical and Laboratory Standards Institute (CLSI) guidelines based on the broth microdilution method which is the recommended method for drug susceptibility testing of Mycobacterium tuberculosis and non-Tuberculous mycobacteria. The REMA (REsazurin Microtiter Assay) plate and E-test methods were each used in one study. The use of antimicrobial susceptibility testing methods other than CLSI in two of the thirteen studies does not impact our reported drug susceptibility results, as each standard institution establishes its own cutoff values for resistance, which were consistently applied in those articles to report resistance rates. Quality assessment done by ROBINS-E tool which was the most appropriate one. Results are produced by ROBVIS tool and depicted in Fig. 2 [6].

Fig. 1
figure 1

PRISMA 2020 flow diagram for new systematic reviews which included searches of databases and registers only [4]

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Table 1 Characteristics of studies included in the systematic review
Full size table
Fig. 2
figure 2

Quality assessment of included studies based on ROBINS-E checklist visualized by ROBVIS tool [6]

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Table 2 summarizes an extensive report on the rate of antimicrobial susceptibility of NTM species to different drugs. Sample sources were mainly regional reference laboratories for tuberculosis, patients from major tuberculosis centers, and water sources. M. avium showed the lowest susceptibility to first-line anti-TB drugs, and the highest susceptibility to amikacin, ciprofloxacin, and cefoxitin. M. abcessus showed the lowest susceptibility to meropenem and trimethoprim-sulfamethoxazole and the highest susceptibility to amikacin. M. fortuitum showed the lowest susceptibility to clarithromycin, meropenem, and ciprofloxacin, and the highest susceptibility to trimethoprim-sulfamethoxazole. M. chelonae showed the lowest susceptibility to ciprofloxacin, doxycycline, and trimethoprim-sulfamethoxazole, and the highest susceptibility to amikacin. M. simiae showed the lowest susceptibility to first-line anti-TB drugs and the highest susceptibility to amikacin. M. kansasii showed the lowest susceptibility to isoniazid and the highest susceptibility to amikacin.

Table 2 Antimicrobial susceptibility pattern of different NTM species to various antibiotics (resistance rates in percent)
Full size table

Discussion

This systematic review shows low susceptibility rates to first-line antituberculosis drugs and meropenem. Different susceptibility rates to ciprofloxacin and trimethoprim-sulfamethoxazole. High susceptibility rate to amikacin. Therefore, amikacin is the most effective drug in this review.

Mycobacterium Avium Complex (MAC)

Studies included in our systematic review showed a low incidence of MAC in Iran. However, this number of MAC species were susceptible to clarithromycin, amikacin, and moxifloxacin, and resistant to linezolid, rifampin, and isoniazid. This finding is consistent with the study in Hainan, China [20]. A study from eight Japanese hospitals of 154 isolates collected from patients with MAC-induced pulmonary disease from 2013 to 2014 found a low moxifloxacin susceptibility rate, which is also in agreement with our review [21]. All isolates from the largest MAC study included in our systematic review appeared to be resistant to isoniazid, rifampin, and linezolid making them MDR species [9]. A number of 43 MAC specimens in a study in Wenzhou, China showed high susceptibility to clarithromycin and amikacin, whereas low susceptibility to moxifloxacin and linezolid [22]. Similar results were obtained in a study of 98 MAC strains isolated from 2006 to 2016 at a tertiary center in central Germany [23]. Another study of 108 NTM specimens isolated from respiratory sources during two periods (2003–2007 and 2013–2017) in a major tertiary care center in Lebanon showed high susceptibility to clarithromycin and low susceptibility to moxifloxacin [24]. The results of these studies are consistent with our systematic review, except for the high sensitivity to moxifloxacin in our review. As mentioned above, the low frequency of MAC in Iran leads to the difference between our studies and others.

The two main genetic mutations that make MAC clinically drug-resistant are the 23s rRNA gene for macrolides and the 16s rRNA gene for amikacin [25]. However, this resistance was not related to mutations in gyrA, gyrB, or VNTR genotypes [21]. Additionally, another study also confirmed that these mutations were not attributed to moxifloxacin resistance after assessing 105 MAC or MABC isolates, including 72 moxifloxacin-resistant strains [26].

Non-MAC mycobacteria

RGM

Mycobacterium abscessus complex (MABC)

Similar to our study, a study on 373 Non-Tuberculous Mycobacteria in Patients with Suspected Pulmonary Tuberculosis in Hainan Island, China between 2014 and 2021 represented low levels of susceptibility (about 10%) of MABC to ciprofloxacin, imipenem, moxifloxacin, doxycyclin, trimethoprim-sulfamethoxazole, and tobramycin [20]. In our study, MABC showed 70–100% resistance to clarithromycin As shown in a study conducted in Korea, in which 83% of MABC subspecies were resistant to this drug [27]. Another study of 67 MABC strains isolated from patients with skin and soft tissue infections at a tertiary teaching hospital in Taiwan from 2012 to 2016 showed high susceptibility to cefoxitin, amikacin, and clarithromycin (5–30%). Studies included in our systematic review showed high susceptibility to cefoxitin and amikacin (93–97%), but low susceptibility to clarithromycin (0–30%) [28]. A study conducted on 43 MABC isolates from respiratory samples in Shanghai, China from 2014 to 2018 showed high susceptibility to amikacin and cefoxitin and low susceptibility to clarithromycin and doxycycline. This is completely consistent with the results of our review except imipenem which had a high susceptibility rate in the Shanghai study contrary to its low susceptibility rate in our review [29]. Our major included study on MABC shows similar periods and isolated sources to other studies around the world. Therefore, the differences should be due to differences in antibiotic consumption patterns in each society.

Maycobacterium fortuitum

In southern and eastern China, a study of 51 M. fortuitum samples isolated from major TB-specialized hospitals from 2012 to 2014 showed high susceptibility to moxifloxacin and amikacin; Intermediate susceptibility to meropenem, cefoxitin, and imipenem; And low susceptibility to linezolid, clarithromycin, and tobramycin. Based on our study, the results are broadly consistent with our systematic review, except for moderate susceptibility to clarithromycin and linezolid and high susceptibility to tobramycin [30]. Isolates of our included studies had been mostly obtained from TB patients which is similar to the study of China. However, a number of studies on M. fortuitum included in our review had been isolated from water sources. The implementation period of major studies was 2010–2014 and 2019–2022. This may be the reason for the difference in resistivity.

IGM

M. simiae

In our review, M. simiae demonstrated high susceptibility to amikacin, intermediate susceptibility to clarithromycin and moxifloxacin, and low susceptibility to linezolid, imipenem, first-line anti-TB drugs, streptomycin, kanamycin, trimethoprim-sulfamethoxazole, and doxycycline. In a study of 108 NTM specimens isolated from respiratory sources during two periods (2003–2007 and 2013–2017) in a major tertiary care center in Lebanon, M. simiae showed low susceptibility to rifampin, ethambutol, ciprofloxacin, rifabutin, linezolid, moxifloxacin, and cotrimoxazole, and high susceptibility to amikacin and clarithromycin [24]. Another study on 103 M. simiae isolates from respiratory sources at a tertiary care center in Lebanon between 2004 and 2016 showed high susceptibility to clarithromycin and amikacin and low susceptibility to trimethoprim-sulfamethoxazole and moxifloxacin [31]. The results are similar to those of our review, except for the median susceptibility rate for clarithromycin in our systematic review. Differences in treatment regimens may explain the moderate susceptibility to clarithromycin in our review, in contrast to the low susceptibility in Lebanon, as the differences between isolates were negligible. Furthermore, these different susceptibility rates may be due to water contamination by this microorganism [15, 32, 33]. The main mutated genes that strongly influence the reduction of antimicrobial susceptibility in M. simiae are the rrl gene (clarithromycin resistance) and gyrA and gyrB (moxifloxacin resistance) [8, 9].

SGM

Mycobacterium kansasii

Multidrug therapy for M. kansasii consists of rifampin, isoniazid, and ethambutol. Although the susceptibility of M. kansasii to these drugs was expected to be higher, studies included in our systematic review reported low to moderate susceptibility rates to these drugs; with the highest rate for isoniazid. Thus, second-line drugs such as amikacin, ciprofloxacin, linezolid, moxifloxacin, doxycyxline, and trimethoprim-sulfamethoxazole can be tested [34]. We noted some contradictory results. For instance, the resistance rate of M. kansasii to isoniazid was highest in studies N03, N06, and N07, whereas studies N01 and N11 showed no resistance to this drug. A study of 85 samples of M. kansasii isolated in Poland between 2000 and 2015 showed high susceptibility rates to amikacin, rifampin, trimethoprim-sulfamethoxazole, and moxifloxacin; This is similar to the results of our systematic review. In this study, susceptibility to ethambutol, ciprofloxacin, and clarithromycin was low. However, our study showed that the sensitivity to these drugs was moderate to high. [35]. Another study of 69 M. kansasii isolates in Brazil showed high susceptibility to clarithromycin, moxifloxacin, and amikacin, and low susceptibility to ciprofloxacin and ethambutol. This is consistent with the results of our review. The only difference was a high sensitivity rate for trimethoprim-sulfamethoxazole in the systematic review, which was low in the Brazilian study [36]. In China, a study of 60 M. kansasii isolates showed low susceptibility to ciprofloxacin and ethambutol, which is inconsistent with our study. However, the high susceptibility rates to amikacin, rifampin, and moxifloxacin are similar to the results of our systematic review [37]. The difference may be due to the fact that a significant number of isolates from our included studies belong to study N01, which had been performed on water isolates. Another reason could be various frequency and treatment regimens in different geographical areas. The main mutated genes that strongly influence the reduction of antimicrobial susceptibility in M. simiae are the rrl gene (clarithromycin resistance), rpoB (rifampin resistance), gyrA, and gyrB (moxifloxacin resistance) [9].

Conclusion

Our systematic review suggests that amikacin is the most effective drug against almost all NTM species common in Iran. Despite being a major concern, the reduced susceptibility rate to first-line anti-TB drugs in NTM species may be a clue in the clinical field to suspect NTM in patients with the diagnosis of TB when the patients are unresponsive to anti-TB treatment. The low susceptibility rates to carbapenems are a concern since they are used in cases of multi-drug resistant (MDR) and extensively drug-resistant (XDR) TB. The emergence of resistance to trimethoprim-sulfamethoxazole is a warning that we should reduce the frequency of using broad-spectrum antibiotics to treat NTM. The results of our systematic review were negatively affected by limited access to antibiotic susceptibility data (especially for MAC), particularly on the low susceptibility drugs' side. Therefore, it may be more refined in the future as more data on sensitivity becomes available.

Data availability

No datasets were generated or analysed during the current study.

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Acknowledgements

The authors would like to thank the Clinical Research Development Unit (CRDU) of Loghman Hakim Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran for their help and support in conducting this study.

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Author notes

  1. Shahrzad Shahrokhi Nejad and Ibrahim Bahrami Mianrood contributed equally to this work.

Authors and Affiliations

  1. Infectious Diseases and Tropical Medicine Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Shahrzad Shahrokhi Nejad, Ibrahim Bahrami Mianrood, Farid Javandoust Gharehbagh & Ilad Alavi Darazam

  2. Department of Infectious Diseases and Tropical Medicine, Loghman Hakim Hospital, Shahid Beheshti University of Medical Sciences, Makhsoos St, South Kargar Ave, Tehran, Iran

    Shahrzad Shahrokhi Nejad, Ibrahim Bahrami Mianrood & Ilad Alavi Darazam

  3. Department of Microbiology, Faculty of Medicine, Urmia University of Medical Sciences, Urmia, Iran

    Lida Lotfollahi

  4. Research Center for Antibiotic Stewardship and Antimicrobial Resistance, Imam Khomeini Hospital Complex, Tehran University of Medical Sciences, Tehran, Iran

    Ilad Alavi Darazam

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  1. Shahrzad Shahrokhi Nejad
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Contributions

Data curation, Ibrahim Bahrami Mianrood and Shahrzad Shahrokhi; methodology, Ilad Alavi Darazam; validation, Ilad Alavi Darazam; investigation, Ibrahim Bahrami Mianrood and Shahrzad Shahrokhi; data curation, Ibrahim Bahrami Mianrood and Shahrzad Shahrokhi; writing—original draft preparation, Ibrahim Bahrami Mianrood and Shahrzad Shahrokhi; writing—review and editing, Farid Javandoust Gharabagh and Lida Lotfollahi; supervision, Ilad Alavi Darazam; All authors have read and agreed to the published version of the manuscript.

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Correspondence to Ilad Alavi Darazam.

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Nejad, S.S., Mianrood, I.B., Gharehbagh, F.J. et al. Antimicrobial susceptibility pattern in non-tuberculous mycobacteria in Iran: a systematic review. Mycobacteria 1, 2 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s44350-024-00001-2

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s44350-024-00001-2

Keywords

Mycobacteria

ISSN: 3004-9555

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