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Firoozeh F, Firoozeh A, Salmani A. An Update on the Prevalence of Nontuberculous Mycobacteria in Clinical Samples in Iran during 2000-2022: A Systematic Review and Meta-Analysis. mljgoums 2023; 17 (3) :22-31
URL: http://mlj.goums.ac.ir/article-1-1491-en.html
1- Department of Microbiology, Islamic Azad University of Damghan, Damghan, Iran
2- Mashhad Uni Meed Sci , arez90fir89@yahoo.com
3- Gerash Uni Med Sci
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Nontuberculosis mycobacteria (NTM) are described as mycobacterial pathogens other than
Mycobacterium tuberculosis (MOTT) and Mycobacterium leprae strains. They are a heterogeneous group of bacteria that cause a fundamental but frequently unvalued global burden of disease (1, 2).  These ubiquitous bacteria have a high prevalence in the environment. There is ample evidence that these microorganisms originate from the environment. In the 1980s, NTM was identified as a human pathogen (3, 4). Although most NTM are saprophytes, one-third of them are related to human diseases (5).  Generally, most NTM are aerobic, immotile bacteria with a firm and dense cell wall (6).  The thickness of NTM cell wall functions as a natural protective shield against disinfectants and antibiotics (7). Therefore, NTM grow in most environments around humans. The increasing rate of infections caused by NTMs may be related to the presence of  NTMs in domestic and animal products, medical devices, drinking water systems, water tanks, and shower streams (8).
Infections caused by NTM are relatively uncommon and often reported in immunocompromised persons (9).  Certain features of NTM are similar to M. tuberculosis that make NTM difficult to differentiate (10). Nevertheless, NTM usually do not respond to common tuberculosis (TB) drug regimens, causing misdiagnosis and poor treatment, especially in low-resource settings (11). Current evidence advises that diseases resulting from NTM are much more prevalent globally than previously believed, and possibly rising in frequency worldwide (12). A report from Canada showed that the incidence of NTM was 150,000 cases per year (13).
In 1959, Ernest Runyon classified NTM based on growth rates, colony morphology, and pigmentation (14). Accordingly, NTM were categorized into four groups: rapid growers (groups I to III) and slow growers (group IV) (15, 16).  Slowly growing species (SGM) typically require more than 7 days before colonies become visible on solid media, while rapidly growing species (RGM) form colonies on selective media within 2–5 days (17). These organisms cause four distinct clinical diseases, including progressive pulmonary disease, superficial lymphadenitis, disseminated diseases of the skin, and soft tissue infections (17).
The subject of NTM is particularly troubling in developing countries owing to limited published information and unsuitable identification. Meta-analysis studies on the prevalence of NTM have been previously conducted in Iran. Given that the last meta-analysis on this subject dates back to 2016 (18), this study aimed to investigate the prevalence of NTM in clinical samples during 2000-2022.

This systematic review and meta-analysis was conducted by reviewing published studies on the prevalence of NTM among clinical samples in Iran. The study was carried out according to Preferred Reporting Items for Meta-Analyses and Systematic Reviews (PRISMA) protocol. The search was performed only for original cross-sectional studies in Persian and English that have been published between January 2000 and 2022 in international electronic databases, such as Scopus, PubMed, Web of Science, Google Scholar, and Scientific Information Database, IranMedex, Magiran, and IranDoc. The search process was according to the combination of Medical Subject Headings (MeSH) text words such as “non-tuberculosis mycobacteria”, “NTM”, “MOTT”, “atypical mycobacterium”, “RGM”, “SGM”, and “Iran”.
As an example among the different databases, the search strategy strings in PubMed are summarized as follows; Non-tuberculosis Mycobacteria (MeSH Terms) OR atypical mycobacterium (MeSH Terms) OR NTM (Title/Abstract), MOTT (MeSH Terms)) AND (rapid-growing mycobacterium (MeSH Terms) OR RGM (Title/Abstract)), AND (slow-growing
Mycobacterium (MeSH Terms), OR SGM (Title/Abstract)). All searches were performed in Persian databases with Persian equivalent words with the same strategy. In addition, the reference section of the original and review studies was screened to find further articles for inclusion in the present systematic review and meta-analysis. All of these searches have completed by two researchers individually.
Duplicates were initially identified and eliminated after entering all the recognized studies into a self-created database. After that, the articles were assessed by two reviewers (AF and AS) by screening titles, abstracts, topics, and finally full texts. At each level, the reviewers independently screened the articles and finally merged their conclusions. Discrepancies were resolved by discussion before finalizing the records for the next level. In case of disagreements, a third assessor was assigned to make a decision. Finally, the studies were assessed for eligibility before the final selection.
We included studies that met the following eligible inclusion criteria: (1) original data, (2) studies on the prevalence of NTM, and (3) studies with accepted standard methods including growth in Lowenstein-Jensen media containing p-nitrobenzoate or thiophene-carboxylic acid hydrazide, growth rate, pigment production, growth at 42 °C and 44 °C, tellurite reduction, arylsulfatase activity, tween hydrolysis, nitrate reduction, catalase, urease, tolerance to the NaCl 5%, and molecular methods such as PCR-RFLP (PRA hsp65), sequencing of hsp, PCR and sequencing of 16s rRNA, multiplex allele-specific PCR (MAS-PCR), Line Probe Assay (LPA), PCR and sequencing rpoB gene, sequencing erm gen, multilocus sequence analysis of 16S rRNA, rpoB, and ITS genes. Reviews, case reports, and conference abstracts were excluded. , studies not performed according to the accepted standard methods.
The studies’ quality was assessed using the criteria specified in Critical Appraisal Skills Programmed checklists (www.casp-UK) (19). This assessment is based on answers to 10 questions designed for each study. If any query data was available, the answer was ‘yes’. In case of doubt or lack of appropriate answer, the answer was ‘no’ or ‘cannot tell’. Based on the number of questions answered "yes", the studies were classified into three categories: good (score of 8-10), moderate (score of 6-8), and poor (score of <6) (20).  Finally, weakly scored studies were not enrolled in the study.
In this review, two researchers independently extracted the data including the first author, study’s time, publication time, geographic location, NTM, methods, and mean age of patients. Meta-analysis was conducted for determining the prevalence of NTM at 95% confidence interval (CI) by comprehensive meta-analysis (V2.0, Biostat, Englewood, NJ, USA).
Random effect model was used and tested with Cochran’s Q test and I2 to determine the possibility of heterogeneity between studies. Egger weighted regression test was applied for the statistical assessment of publication bias, and p-values less than 0.05 were considered statistically significant. In addition, funnel plot was used to evaluate publication bias in the studies.

As shown in figure 1, 1,078 articles were retrieved through database searches. After excluding 452 duplicate articles, 626 studies were assessed, 201 of which were removed because of title or abstract irrelevance. Next, 425 full texts were evaluated for content and method. Finally, 26 eligible studies were systematically reviewed and analyzed.
The characteristics of the included studies are summarized in table 1. The mean age of patients positive for NTM was between 11 and 80 years.  Geographic locations included Tehran, Kashan, Khuzestan, Tabriz, Yazd, Golestan, Kermanshah, Mashhad, and Hormozgan (Table 1).  
All included studies used conventional methods for the detection of mycobacteria. These methods were growth in Lowenstein-Jensen media containing p-nitrobenzoate or thiophene-carboxylic acid hydrazide, growth rate, pigment production, growth at 42 °C and 44 °C, tellurite reduction, arylsulfatase activity, tween hydrolysis, nitrate reduction, catalase, urease, and tolerance to the NaCl 5%. The majority of NTM were isolated from respiratory and bronchoalveolar lavage samples.
Our review showed that the prevalence of NTMs in positive mycobacterial cultures varied from 0.1 to 72.7%. As shown in table 2 and figure 2, the combined prevalence of NTM in clinical samples was 4.5% (95% Cl: 3.1-6.5, Q = 1562.7, Z = 15.2, I2 =98.4, and p=0.00).
According to funnel plot, publication bias was visually found among the included studies (Figure 3). Egger’s weighted regression test results also suggested the presence of bias in the studies (p=0.6). Therefore, there is a possibility of publication bias due to the existence of small studies included in this review.
As reported in table 2, the most common SGM among NTM species were Mycobacterium simiae [35.8% (95% CI 16.4-44.4)], Mycobacterium intracellulare [19% (95% CI 8.7-28.3)], and Mycobacterium kansasii [13.4% (95% CI 7.3-24.3)], while Mycobacterium fortuitum [24.6% (95% CI 12.9-46.7)], Mycobacterium terrae [18.5 % (95% CI 11.5-29.2)], and Mycobacterium gastri [15.9%(95% CI6.0-41.2)] were the most prevalent RGM among NTM species.
Table 1-Characteristics of the studies included in the review
First author (reference) Time of study Date of publication Location Sample size NTM Number (%) Identification methods Mean age of patient (years)
Derakhshani Nejad(40) 2003-11 2014 Tehran 8322 124 Conventional tests,
57 ±18.9  
Heidari(41) 2007-8 2009 Tehran 371 43 Conventional tests,
Nasiri(42) 2010-12 2014 Tehran 6426 9 Conventional tests,
Javid(43) 2007- 8 2009 Golestan 104 17 Conventional tests,
14 ≤65  
Shafipour(44) 2010-11 2013 Golestan 336 16 Conventional tests 44 ±23.3  
Moghtaderi(45) 2000-10 2011 Tabriz 235 15 Conventional tests -  
Heidar Nejad(46) 2001 2001 Tabriz 165 10 Conventional tests 44.01±18.23  
2002- 4 2006 Sistan- Baluchestan 210 59 Conventional tests 20 ≤60  
Naderi(48) 2003- 4 2006 Sistan-
150 20 Conventional tests -  
Namaei (49) 2002 2003 R.Khorasan 1700 8 Conventional tests -  
Hashemi-Shahraki (50) 2008-12 2014 Khuzestan 2313 92 Conventional tests,
2009-12 2013 khuzestan 190 23 Conventional tests,
Khosravi(52) 2007-8 2009 Khuzestan 150 8 Conventional tests
Yazdi(53) 2009-10 2012 Yazd 32 1 Conventional tests  
Zilaee(54) 2012-15 2016 Kashan 106 4 PRA hsp65 -  
Nour-Neamatollahie(55) 2011-13 2017 Tehran 10,377 59 PCR-RFLP (PRA hsp65 50.9 ± 7.6  
Nasiri(56) 2014-16 2018 Tehran 410 56 PCR-RFLP (PRA hsp65) 50.9 ± 7.6  
Nasiri(57) 2016-17 2018 Tehran 230 12 hsp 65- PRA, sequencing
of 16S rRNA, rpoB, and ITS genes
Irandoost(58) 2014-16 2018 Tehran 6800 64 PRA and sequencing of hsp65 -  
Aghajani(59) 2011-19 2019 Tehran 15829 591 hsp65- PRA, sequencing
16S rRNA, rpoB
50.7 ±18.4
Mortazavi(60) 2015-17 2019 Tehran 478 53 hsp65-PRA, sequencing
16S rRNA, rpoB
43.4 ±15.7  
Davari(61) 2013-15 2018 Tehran 520 61 Multilocus sequence
analysis of 16S rRNA,
2rpoB, and ITS genes
49.6 ± 16.6
Karami-Zarandi(62) 2017-19 2019 Tehran 5061 60 LPA, PCR and
sequencing 16s rRNA
Khosravi(63) 2016-18 2018 Khuzestan
55 40 PCR and sequencing rpoB gene, sequencing erm gene 47.4 ±19.9  
Ayoubi(64) 2011- 18 2021 Tehran 15771 658 (RFLP)-PCR of a hsp65 fragment, Nested-PCR -  
Shafipour(65) 2016-18 2021 Gorgan 2994 12 Conventional tests, PCR(16S rRNA gene) 59.9 ± 16.9
Subgroups Number of studies Heterogeneity test Egger’s test Random model
Prevalence (95% CI) Z p Q p I t p
Combined NTM 26 4.5(3.1-6.5) 15.2 0.00 1562.7 0.00 98.4 0.5 0.6
Slowly growing mycobacteria
M. simiae 25 35.8(16.4-44.4) 2.5 0.01 102.3 0.00 93.1 3.1 0.01
M. kansasii 22 13.4(7.3-24.3) 5.1 0.00 64.1 0.00 87.5 0.6 0.5
M. gordonae 13 6.6(0.6-17.5) 3.6 0.00 31.5 0.00 90.4 1.4 0.27
M. intracellulare 13 19(8.7-28.3) 17.4 0.00 2.7 0.4 0.00 2.2 0.15
M. avium complex 12 10.3(1.6-18.1) 14.8 0.00 1.7 0.45 0.00 0.65 0.63
M. szulgai 23 9.1 (3.2-28.1) 2.1 0.00 1.1 0.00 0.00 0.00 0.03
Rapid growing mycobacteria
M. fortuitum 24 24.6(12.9-46.7) 2.2 0.02 152.3 0.00 94 2.1 0.06
M. abscessus 12 10.6(4.3-11.8) 9.1 0.00 2.1 0.00 0.00 1 0.31
M. chelonae 11 6.8(3.8-11.7) 10.7 0.00 2.2 0.31 12.4 1 0.01
M.thermoresistibile 10 2.95(1.4-8.1) 7.2 0.00 0.76 0.00 0.00 0.00 0.00
M. terrae 19 18.5 (11.5-29.2) 8.1 0.00 0.00 0.00 0.00 0.00 0.00
M. gastri 23 15.9 (6.0-41.2) 6.4 0.00 1.4 0.00 0.00 0.00 0.00

Figure 2- Forest plot of the meta-analysis of epidemiology of NTM in clinical samples from Iran

Figure 3-Funnel plot of the meta-analysis of epidemiology of NTM in clinical samples from Iran
Since many studies do not consider infections caused by NTMs as a public health problem, there is not enough data about these microorganisms and their frequency distribution, at least in Middle Eastern and third-world countries. This has made developing infection control strategies challenging (21).
Our review showed that the prevalence of NTM in clinical samples varied from 0.1 to 72.7%.  As mentioned in the results, the majority of NTM were isolated from respiratory and bronchoalveolar lavage samples. These findings emphasize the importance of identifying NTM from suspected pulmonary TB patients (22).  In line with our findings, a study from Saudi Arabia reported that pulmonary (54.7%) and bronchial lavage/wash (22.1%) specimens were predominant (23). The difference in the prevalence of NTM in the studies reviewed in our survey might be due to the difference in the molecular techniques used in each study, the geographic region, types of clinical specimens, laboratory personnel skills, sanitation, and living conditions (4).
We showed that the combined prevalence of NTM isolated from clinical samples in Iran was 4.5% during 2000-2022. Because the manifestations of NTM and TB are similar and all NTM are acid-fast and cannot be segregated by phenotypic methods, NTM may be mistaken for TB. Moreover, diseases caused by NTM typically do not respond to anti-TB drugs (24). Furthermore, in some cases, patients with multi-drug resistant TB were in fact infected with NTM (25).
Reports should be interpreted with caution because it is often challenging to determine whether NTM are the real source of infection (1). In line with our results, the study from Saudi Arabia reported a prevalence rate of 1.4% for NTM (23). Studies by Pokam et al. (12) and Aliyu et al. (11) in Nigeria reported prevalence rates of 16.5% and 15%, respectively. However, higher prevalence rates were reported in studies from Canada (33%) and the Netherlands (25%) (26, 27).  A systematic review and meta-analysis published by Nasiri et al. in 2015 reported a pooled prevalence rate of 10.2% in Iran, which is higher than the rate found in our study (11.2%). This could be related to the source of NTM because our study was focused on clinical samples, but the mentioned study was focused on suspected TB patients (18). In recent years, the reports of NTM have been rising, mainly because of the active search for NTM species, improvements in culture methods (28), and most importantly, the use of sensitive molecular techniques (22, 29).
Here, we detected a combined prevalence rate of 4.5% in clinical specimens, which is similar to the rate reported by Khaledi et al. in Iran in 2016 (2). Subgroup analysis in our review showed that the combined prevalence of M. simiae (35.8%), M. intracellulare (19%), and M. kansasii (13.4%) was highest among SGM, while M. fortuitum (24.6%), M. terrae (18.5%), and M. gastri (15.9%) were the most prevalent RGM. Evidence suggests that RGM species are among the most predominant NTM associated with nosocomial infections (40). As described by previous reports, tap water, dialysis water provided from tap water, drinking water, shower water, and piped water systems in clinical settings are the common sources of NTM-related nosocomial infections (30). In addition, RGM are relatively resistant to standard disinfectants such as chlorine, alkaline glutaraldehydes, and antimicrobial agents compared to M. tuberculosis; thus, their eradication is more difficult (31).
In line with our study, a previous review on the distribution of NTM species among environmental and clinical samples in the Middle East reported that 58.7% of isolates were SGM and 41.2% were RGM. This study also reported similar prevalence rates for SGM (56.4%) and RGM (44.6%) in Iran (21). Moreover, this study reported M. fortuitum (60.1%) as the most prevalent RGM isolated from clinical specimens in the Middle East (30). M. fortuitum was detected in 71.9%, 54.4%, 46.6%, and 48.9% of RGM isolates from Iran, Saudi Arabia, Turkey, and Pakistan, respectively (6). Other reports from Iran’s neighboring countries (Saudi Arabia and Kuwait) also found M. fortuitum as the predominant isolate (23, 32). The proportion of RGM in pulmonary diseases from Iran and other Asian countries is much higher than in European and North American countries (18, 22, 33). For example, studies from the Netherlands and the United States reported a prevalence rate of 3% and 5% for RGM, respectively (26, 34).
In our study, M. simiae was found as the most predominant SGM among NTM isolates. This finding is in agreement with the results of previous reviews from Iran (18, 22). On the contrary, in developed countries, M. avium complex has been described as the most common NTM species (35).  It is noteworthy to mention that M. simiae is an endemic SGM in Iran. It is often not distinguishable from TB complex due to its similar clinical and radiologic manifestations as well as the lack of response to anti-TB drugs (36). Therefore, it is recommended to consider M. simiae in cases where anti-TB treatment does not respond (37). The spread of diseases caused by mycobacteria, especially respiratory diseases, and the possible inappropriate treatment imposes a lot of costs on both patients and health systems. Nevertheless, most laboratories do not have accurate diagnostic criteria for NTM owing to the lack of appropriate equipment and qualified experts (1). In recent studies, the increased use of molecular methods has increased the accuracy of NTM diagnosis (38). National TB reference laboratories necessitate standardizing existing protocols for the identification of NTM in Middle Eastern countries (21, 39). Thus, given the rising importance of NTM, quick and precise identification of NTM is of great importance for active management strategy against NTM Infections (21). The main limitation of the present study was that studies published in languages other than English and Persian have not been included in the analysis. Another limitation was that the protocol of this systematic review and meta-analysis was not registered in a standard platform like Cochrane or Prospero.
In summary, our findings indicate a relatively high combined prevalence of NTM in clinical samples in Iran.  Some of these species such as M. simiae can have clinical and radiologic manifestations similar to those of TB and are resistant to anti-TB drugs. Therefore, standardizing the use of molecular methods for the detection of NTM seems necessary. 
The authors received no financial support for the research, authorship, and/or publication of this article.
Ethics approvals and consent to participate
Not applicable.
The authors declare that there is no conflict of interest regarding the publication of this article.
Research Article: Systematic Review | Subject: Others
Received: 2022/03/2 | Accepted: 2022/06/6 | Published: 2023/05/21 | ePublished: 2023/05/21

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