An Update on Prevalence of Non tuberculosis Mycobacteria in Clinical Samples from 2000 - 2022; A Retrospective Systematic Review and Meta - Analysis

Maryam Arfaatabar¹, Nadia Mohammad Zadeh² and Abbas Salmani^{3* 1}Department of Medical Sciences, Islamic Azad University, Kashan, Iran
²Department of Medicine, Islamic Azad University Tehran Medical Branch, Tehran, Iran
³Department of Medical Sciences, Gerash University of Medical Sciences, Gerash, Iran
^*Correspondence: Abbas Salmani, Department of Medical Sciences, Gerash University of Medical Sciences, Gerash, Iran, Email:

Received: Mar 03, 2022, Manuscript No. JEBMH-22-51710; Editor assigned: Mar 07, 2022, Pre QC No. JEBMH-22-51710; Reviewed: Mar 21, 2022, QC No. JEBMH-22-51710; Revised: May 02, 2022, Manuscript No. JEBMH-22-51710; Published: May 17, 2022, DOI: 10.18410/jebmh/2022/09.09.18

Citation: Arfaatabar M, Zadeh NM, Salmani SA. An Update on Prevalence of Nontuberculosis Mycobacteria in Clinical Samples from 2000 - 2022; A Retrospective Systematic Review and Meta – Analysis. J Evid Based Med Healthc 2022;9(9):17.

Keywords

Non-tuberculosis mycobacteria, Atypical mycobacterium, Rapid growing mycobacterium

Introduction

Non - Tuberculosis Mycobacteria (NTM) are described as mycobacterial pathogens other than Mycobacterium Tuberculosis (MOTT) and Mycobacterium leprae strains. NTMs are a heterogeneous group of bacteria that together cause a fundamental but frequently unvalued global burden of disease.^1,2NTMs are ubiquitous bacteria with a high prevalence in the environment. There is ample evidence that these microorganisms originate from the environment, of note, for the first time in the 1980’s, NTM was identified as a human pathogen.^3,4 Though most NTM are saprophytes but it is reported that one - third of them are related to human diseases.⁵generally, most NTMs 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, NTMs grow in most environments around humans. Since NTMs retrieved from domestic and animal products, and also man - made systems such as medical devices, and drinking water systems, water tanks and shower streams, this may explain the increasing rate of infections mediated by NTMs.^8,9 Infections caused by NTMs are relatively uncommon and often reported in immunocompromised persons.¹⁰

NTMs have certain features similar to M tuberculosis and may cause diseases like M tuberculosis that make the NTMs difficult to differentiate from tuberculosis.¹¹ Nevertheless, NTMs usually do not respond to common Tuberculosis (TB) drug regimens, causing misdiagnosis and poor treatment, especially in low â? resource settings.¹² Current evidence advice that diseases resulting from NTMs are much more prevalent globally than previously believed, and possibly rising in frequency worldwide.¹³

A report from Canada showed that the incidence of the estimated diseases of non - tuberculosis mycobacteria was 150000 cases per year and also according to USA experts opinion, the NTM prevalence is much higher in some cases than tuberculosis.¹⁴ NTMs were classified by Ernest Runyon based on growth rates, colony morphology, and pigmentation in 1959, accordingly, NTMs categorized into 4 groups, rapid growers (I to III groups), and IV group, which are slow growers (SGM).^(15-17)

These organisms cause 4 distinct clinical diseases, including progressive pulmonary disease, superficial lymphadenitis, disseminated diseases, of the skin and soft tissue infections.¹⁸ The subject of NTM is in particular troubling in developing countries owing to limited published information and unsuitable identification. Meta - analysis studies on the prevalence of non - tuberculosis mycobacteria in Iran have been conducted in previous years.

Given that the last meta - analysis in this field conducted in 2016, and that the topic is of great importance and updating the prevalence of NTMs is necessary, we decided to conduct this study from 2000 - 2022. Therefore, this study aimed to investigate the prevalence of non - tuberculosis mycobacteria in clinical samples during 2000 - 2022.¹⁹

Literature Review

Literature Search Strategy

This literature search has conducted by reviewing published studies addressing non - tuberculosis mycobacteria prevalence from clinical samples in Iran according to PRISMA (Preferred reporting items for meta - analyses and systematic reviews) protocol. The search strategy was performed for only the original cross sectional studies in Persian and English published between 1^th January 2000 to 2022 in international electronic databases such as Scopus, PubMed, Web of Science, Google Scholar, and also Iranian electronic databases including Scientific Information Database. The search process was according to the combination of Medical Subject Headings (Mesh) text words such as “ Non - Tuberculosis Mycobacteria ”, “ NTM ”, “ MOTT ”, “ a typical mycobacterium ”, “ RGM ”, “ SGM ” and “ Iran ”. As an example among the different databases, the search strategy strings in PubMed is summarized as follows, Non - tuberculosis Mycobacteria or a typical mycobacterium. It is important to note that all searches have performed in Persian databases with Persian equivalent words with the same strategy. As well, the reference section of the original and review studies was reviewed to find further articles for including in present systematic review and Meta - analysis. All of these searches have completed by two researchers individually.

Inclusion and Exclusion Criteria

We included studies that met the following eligible inclusion criteria: (1) original data have addressed, (2) studies presented the prevalence of NTMs, (3) accepted standard methods (e.g. growth in Lowensteine Jensen (LJ) media containing P – Nitro Benzoate (PNB) or Thiophene - Carboxylic Acid Hydrazide (TCH), 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 %), or molecular methods such as PCR - RFLP (PRA hsp 65), sequencing of hsp, PCR and sequencing of 16s rRNA, multiplex allele -specific polymerase chain reaction (MAS - PCR), Line Probe Assay (LPA), PCR and sequencing rpoB gene, sequencing germ gen, multilocus sequence analysis of 16S rRNA, rpoB, and ITS genes were used. Reviews, case reports, and conference abstracts, studies have been described in languages other than English or Persian, studies not performed according to the accepted standard methods. Studies published before 2000 and studies did not address the prevalence of NTMs were excluded.

Quality Assessment

The studies quality has assessed using the criteria specified in Critical Appraisal Skills Programmed checklists.²⁰ this assessment has based on the answers to ten questions designed for each study. If any query data was available, the answer scored as ‘yes’. In case of doubt or lack of appropriate answer, it was categorized, as no or cannot tell. Based on the number of questions answered “Yes” the studies were classified into three categories: strong (8 - 10), medium (6 - 8) and weak (< 6).²¹ finally, weak studies did not obtain approval for this study.

DataExtraction

In this review, two researchers extracted the data independently, shared the extracted data, and then included in the data extraction form. They would seek help from another researcher if there were differences in data extraction. Extracted data included first author, study’s time, publication time, geographic location, NTM, methods, and Mean age of patients.

Statistical Analysis

Meta - analysis was conducted for calculating the prevalence of NTM and its 95 % confidence interval (95 % CI) by Comprehensive Meta - analysis Random effect models was used and tested with Cochran’s Q test, and I₂ to determine the possibility of heterogeneity between studies. As well as Egger weighted regression test was applied to a statistical assessment of publication bias and p < 0.05 was considered statistically significant. In addition to this method, funnel plot was also used to evaluate publication bias in the studies.

Results

According to the flow diagram of Figure 1, 1078 articles were recognized through searching databases, then, 452 duplicate articles were excluded, 626 studies were assessed, 201 articles were removed because their title or abstract were not relevant. Then, 425 full texts evaluated, and 399 studies with justified reasons (studies with the lack of sufficient data, missed data, unclear data, defect in reporting data, and non - use of suitable statistical analysis for data analysis, studies with no standard methods, reference standard not met, studies with the lack of outcomes).

The remaining 26 eligible studies systematically reviewed and analyzed. The characteristics of the included studies summarized in Table 1. The mean age of positive patients for NTMs was between 11 - 80 year. Geographic location 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 including (e.g. growth in Lowensteine Jensen (LJ) media containing P - Nitrobenzoate (Pnb) or Thiophene - Carboxylic Acid Hydrazide (TCH), 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 BAL samples.

Overall Effects

Combined prevalence of non - tuberculosis mycobacteria in clinical samples our review showed that the prevalence of NTMs in positive mycobacterial cultures varied from 0.1 - 72.7 % in included studies. As shown in Figure 2 and Table 2, the combined prevalence of NTMs in clinical samples was 4.5 %( 95 % Cl: 3.1 - 6.5), Q = 1562.7 and Z = 15.2, I₂ = 98.4, and p = 0.00.

Sources of Heterogeneity

A funnel plot is a plot used for effect size against sample size or some other indicator related to precision of the estimate. According to Funnel plot publication bias was visually found amongst included studies (Figure 3), because 95 % of studies didn’t lie within the two limit lines (inside funnel). If no bias was observe, it was symmetrical about the correct population effect size and got narrower as the sample size enlarged. Egger’s weighted regression test can recognize small - study effects and not tell if publication bias occurs. When we used, similarly, the findings suggesting the presence of bias in the studies (p = 0.6). Therefore, there is a probably publication bias in studies included due to small studies.

Sub Group Analysis For Slow Growing Mycobacteria and Rapid Growing Mycobacteria Species: As reported in Table 2, "M. simiae (35.8 % [95 % CI 16.4 - 44.4]), "M. intracellulare (19 % [95 % CI 8.7 - 28.3]), and "M. kansasii (13.4 % [95 % CI 7.3 - 2 4.3]) were the most common NTM species among SGM, while "M. fortuitum (24.6 % [95 % CI 12.9 - 46.7]), M. terrae (18.5 % [95 % CI 11.5 - 29.2), and "M. gastri (15.9 % [95 % CI 6.0 - 41.2]) were the most prevalent NTM species among Rapidly Growing Mycobacteria (RGM).

Discussion

For our knowledge, many studies do not address non - tuberculosis mycobacteria as a public health problem, and physicians and microbiologists do not know much about their infection. Therefore, there is not much data about these microorganisms and their frequency distribution at least in Middle Eastern and third world countries and this has created a particular challenge to infection control Strategies.²² Our review showed that the prevalence of NTMs in clinical samples varied from 0.1 - 72.7 % in included studies. As mentioned in the results, the majority of NTM were isolated from respiratory and BAL samples. These findings emphasize the importance of identifying NTM from suspected pulmonary TB patients.²³ In line with our findings, a study from Saudi Arabia reported that pulmonary specimens were predominant sputum 52 (54.7 %) and bronchial lavage / wash - 21 (22.1 %).²⁴ The difference in the prevalence of non - tuberculosis mycobacteria in the studies included in this review is probably due to the molecular techniques used in each study, geographic region, types of clinical specimens, trained TB laboratory personnel, sanitation, and living conditions. We showed that the combined prevalence of NTMs isolated from clinical samples in Iran during 2000 - 2022 was 4.5 %. Because the manifestations of NTM and tuberculosis are similar and all non - tuberculosis mycobacteria are acid - fast and cannot be segregated by phenotypic methods, NTM may be mistaken for tuberculosis, also diseases resulted from NTM, typically does not respond to anti - tuberculosis drugs.^25-28In addition, in some cases, it found that patients considered having Multi - Drug Resistance (MDR) - TB had NTMs. Of course, studies and reports should be interpreted with caution, because it is frequently challenging to differentiate if the NTMs are a real source of infection or a contaminant in clinical samples.^29-36Reports from Saudi Arabia reported the same prevalence of NTMs 1.4 %. In agreement with our study, Pokka both from Nigeria reported NTM prevalence of 16.5 %, and 15 %, respectively. Similarly, studies from Canada and the Netherlands reported a higher NTM prevalence of 33 %, and 25 %, respectively. A systematic review and Meta - analysis conducted from Iran showed that the pooled prevalence of NTMs about 10.2 % that is higher than our current study, where the combined prevalence of NTMs was reported 11.2 %.^37-42 This difference in prevalence of NTMs from the identical place (Iran), probably referred to sources of NTMs, because we reported them from clinical samples, but they reported from Suspected TB patients. In recent years, there are increased reports of NTM, the reasons for this are, active searching for NTM, improvements in culture methods, and most importantly, the use of molecular sensitive techniques. Here, we presented the combined prevalence of 4.5 % in clinical specimens that it agreement with previous study conducted in Iran in 2016. Subgroup analysis in our review showed that the combined prevalence of "M. simiae (35.8 % [95 % CI 16.4 - 44.4]), M intracellular (19 % [95 % CI 8.7 - 28.3]), and "M. kansasii (13.4 % [95 % CI 7.3 - 24.3]) were the most common NTM species among SGM, while "M. fortuitum (24.6 % [95 % CI 12.9 - 46.7]), "M. terrae (18.5 % [95 % CI 11.5 - 29.2), and "M. gastri (15.9 % [95 % CI 6.0 - 41.2]) were the most prevalent NTM species among rapidly growing mycobacteria (RGM). RGM species are among the most predominant NTM associated with nosocomial infections.^43-49As described by previous reports, tap water, dialysis water provided from tap water, drinking water, and shower water, piped water systems in clinical settings such as hospitals are the common sources of NTM nosocomial infections. Another point is that RGMs are somewhat resistant to standard disinfectants such as chlorine, alkaline glutaraldehydes, and antimicrobial agents compared to TB, thus, their eradication is difficult. Therefore, they will make major problems for programs of hospital control strategies. In line with our study, a previous review that has studied the distribution of NTM species from environmental and clinical samples in the Middle East, from NTM isolated from clinical specimens in the Middle East, 58.7 % were SGM and 41.2 % were RGM, also, they reported the similar prevalence of SGM / RGM (56.4 % / 44.6 %) in Iran. Besides, comparable with our findings, they reported M fortuitum (60.1 %) as the most prevalent RGM retrieved from the clinical specimens in Middle East. As well, they reported M fortuitum in 71.9 %, 54.4 %, 46.6 %, and 48.9 % of RGM isolates recovered from Iran, Saudi Arabia, Turkey, and Pakistan, respectively. Other reports from neighboring countries (Saudi Arabia and Kuwait) found M fortuitum as the prevalent isolate, too The proportions of RGM in pulmonary diseases from Iran and other Asian countries are much higher than in other European and American countries for example, studies from Netherlands and the United States, this rate was about 3 % and 5 %, respectively simian was the most predominant SGM from studied NTM isolates in this meta - analysis. This finding is in accordant with previous reviews from Iran. On contrary, in developed countries, avium complex has been described as the most common NTM species.^50-59 It is worth to mention that "M. simiae is an endemic SGM in Iran. It often is not distinguishable from TB complex due to its similar clinical and radiologic manifestations also with no response to ant - TB drugs. Therefore, it should be strongly sought for simian in cases where anti - TB treatment does not respond.

The main point of this comprehensive review is that missing NTM infection particularly pulmonary diseases lead to unsuitable treatment, imposing health costs on patients and health systems, increasing mortality, and economic consequences. Nevertheless, most of the laboratories do not yet have a diagnosis of non - tuberculosis in their program owing to the lack of appropriate equipment and qualified experts. In most recent studies, improved molecular methods led to more and better diagnosis of NTM. National TB Reference Laboratories necessitate to standardizing existing protocols for the identification of NTM in Middle Eastern countries. Thus, owing to the rising importance of NTM, quick and trustworthy identification is significant as an active management strategy against NTM Infections. The main limitation of the current study is that studies published other English and Persian languages have been missed of our review.^60-66

Conclusion

In summary, our study reported a relatively high combined prevalence of NTMs in clinical samples, which some of them such as "M. simiae can have clinical and radiologic manifestations similar to TB and because they do not respond to anti - TB drugs, they are considered Multi - Drug Resistance (MDR) - TB. Therefore, standardizing laboratories and the use of molecular methods for the detection of NTM is necessary.

Conflicts of Interest

None declared.

Acknowledgement

None, we declare that we do not have any competing interests.

References

1. Raju RM, Raju SM, Zhao Y, et al. Leveraging advances in tuberculosis diagnosis and treatment to address nontuberculous mycobacterial disease. Emerg Infect Dis 2016;22(3):365.

   [Crossref][Google Scholar][Indexed]

2. Khaledi A, Bahador A, Esmaeili D, et al. Prevalence of Nontuberculous Mycobacteria (NTM) in Iranian clinical specimens: systematic review and meta-analysis. J Med Microbiol 2016;5(3-4):29-40.

   [Google Scholar]22222

3. Falkinham J. Epidemiology of infection by nontuberculous mycobacteria. Clin Microbiol Rev 1996;9(2):177-215.

   [Crossref][Google Scholar][Indexed]

4. Khaledi A, Bahador A, Esmaeili D, et al. Prevalence of nontuberculous mycobacteria isolated from environmental samples in Iran: A meta - analysis. J Res Med Sci 2016;21.

   [Crossref][Google Scholar][Indexed At]

5. Hagiwara E, Komatsu S, Nishihira R, et al. Clinical characteristics and prevalence of pneumothorax in patients with pulmonary Mycobacterium avium complex disease. J Infect Chemother 2013;19(4):588-592.

   [Crossref][Google Scholar][Indexed]

6. Hett EC, Rubin EJ. Bacterial growth and cell division: a mycobacterial perspective. Microbiol Mol Biol Rev 2008;72(1):126-56.

   [Crossref][Google Scholar][Indexed]

7. van Ingen J, Boeree MJ, van Soolingen D, et al. Resistance mechanisms and drug susceptibility testing of nontuberculous mycobacteria. Drug Resist Updat 2012;15(3):149-161.

   [Crossref][Google Scholar][Indexed]

8. Faria S, Joao I, Jordao L. General overview on nontuberculous mycobacteria, biofilms, and human infection. J Pathog 2015.

   [Crossref][Google Scholar][Indexed]

9. Griffith DE, Aksamit T, Brown-Elliott BA, et al. An official ATS / IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med 2007;175(4):367-416.

   [Crossref][Google Scholar][Indexed]

10. Gopinath K, Singh S. Non - "tuberculous mycobacteria in TB-endemic countries: are we neglecting the danger? PLoS Negl Trop Dis 2010;4(4):615.

    [Crossref][Google Scholar][Indexed]

11. Muyoyeta M, Schaap J, De Haas P, et al. Comparison of four culture systems for "Mycobacterium tuberculosis in the Zambian National Reference Laboratory. Int J Tuberc Lung Dis 2009;13(4):460-465.

    [Google Scholar][Indexed]

12. Aliyu G, El - Kamary SS, Abimiku Al, et al. Prevalence of non-tuberculous mycobacterial infections among tuberculosis suspects in Nigeria. PloS one 2013;8(5):63170.

    [Crossref][Google Scholar][Indexed]

13. Pokam BT, Asuquo AE. Acid-fast bacilli other than mycobacteria in tuberculosis patients receiving directly observed therapy short course in cross river state, Nigeria. Tuberc Res Treat 2012;2012:30105.

    [Crossref][Google Scholar][Indexed]

14. Ernst P, Fitzgerald JM, Spier S. Canadian asthma consensus conference summary of recommendations. Can Respir J 1996;3(2):89-101.

    [Crossref][Google Scholar]

15. Runyon EH. Anonymous mycobacteria in pulmonary disease. Med Clin North Am 1959;43(1):273-290.

    [Crossref][Google Scholar][Indexed]

16. Jarzembowski JA, Young MB. Nontuberculous mycobacterial infections. Infection 2008;132(8):1333-1341.

    [Crossref][Google Scholar][Indexed]

17. Porvaznik I, Solovic I, Mokry J. Non-tuberculous mycobacteria: classification, diagnostics, and therapy. Adv Exp Med Biol 2016:19-25.

    [Crossref][Google Scholar][Indexed]

18. Hanak V, Kalra S, Aksamit TR, et al. Hot tub lung: presenting features and clinical course of 21 patients. Respir Med 2006;100(4):610-615.

    [CrossRef][Google Scholar][Indexed]

19. Nasiri MJ, Dabiri H, Darban-Sarokhalil D, et al. Prevalence of non-tuberculosis mycobacterial infections among tuberculosis suspects in Iran: systematic review and meta-analysis. PloS one 2015;10(6):0129073.

    [Crossref][Google Scholar][Indexed]

20. Programme CAS (2006) 10 questions to help you make sense of qualitative research.
21. Hosseini M, Shakerimoghaddam A, Ghazalibina M, et al. Aspergillus coinfection among patients with pulmonary tuberculosis in Asia and Africa countries; a systematic review and meta-analysis of cross-sectional studies. Microb Pathog 2020;141:104018.

    [Crossref][Google Scholar][Indexed]

22. Velayati AA, Rahideh S, Nezhad ZD, et al. Nontuberculous mycobacteria in Middle East: Current situation and future challenges. Int J Mycobacteriol 2015;4(1):7-17.

    [Crossref][Google Scholar][Indexed]

23. Velayati AA, Farnia P, Mozafari M, et al. Nontuberculous mycobacteria isolation from clinical and environmental samples in Iran: twenty years of surveillance. Biomed Res Int 2015;254285.

    [Crossref][Google Scholar][Indexed]

24. Varghese B, Memish Z, Abuljadayel N, et al. Emergence of clinically relevant non-tuberculous mycobacterial infections in Saudi Arabia. PLoS Negl Trop Dis 2013;7(5):2234.

    [Crossref][Google Scholar][Indexed]

25. Maiga M, Siddiqui S, Diallo S, et al. Failure to recognize nontuberculous mycobacteria leads to misdiagnosis of chronic pulmonary tuberculosis. PloS one 2012;7(5):36902.

    [Crossref][Google Scholar][Indexed]

26. Shahraki AH, Heidarieh P, Bostanabad SZ, et al. "Multidrug-resistant tuberculosis� may be nontuberculous mycobacteria. Eur J Intern Med 2015;26(4):279-284.

    [Crossref][Google Scholar][Indexed]

27. Van Ingen J, Bendien SA, De Lange WC, et al. Clinical relevance of non-tuberculous mycobacteria isolated in the Nijmegen-Arnhem region, The Netherlands. Thorax 2009;64(6):502-506.

    [Crossref][Google Scholar][Indexed]

28. Marras TK, Daley CL. Epidemiology of human pulmonary infection with nontuberculous mycobacteria. Clin Chest Med 2002;23(3):553-568.

    [Crossref][Google Scholar][Indexed]

29. Chu H, Zhao L, Xiao H, et al. Prevalence of nontuberculous mycobacteria in patients with bronchiectasis: a meta-analysis. Arch Med Sci 2014;10(4):661.

    [Crossref][Google Scholar][Indexed]

30. Hernandez - Garduno E. Nontuberculous Mycobacteria Isolation from Clinical and Environmental Samples in Iran: Twenty Years of Surveillance. BioMed research international 2015.

    [CrossRef][GoogleScholar][Indexed]

31. De Groote M, Huitt G. Infections due to rapidly growing mycobacteria. Clin Infect Dis 2006;42:1756â??1763.

    [Crossref][Google Scholar][Indexed]

32. Carson LA, Petersen NJ, Favero MS, et al. Growth characteristics of atypical mycobacteria in water and their comparative resistance to disinfectants. Appl Environ Microbiol 1978;36(6):839-46.

    [Crossref][Google Scholar][Indexed]

33. Mokaddas E, Ahmad S. Species spectrum of nontuberculous mycobacteria isolated from clinical specimens in Kuwait. Current microbiology 2008;56(5):413-417.

    [Crossref][Google Scholar][Indexed]

34. Simons S, Van Ingen J, Hsueh PR, et al. Nontuberculous mycobacteria in respiratory tract infections, eastern Asia. Emerg Infect Dis 2011;17(3):343.

    [Crossref][Google Scholar][Indexed]

35. O'Brien RJ, Geiter LJ, Snider Jr DE. The epidemiology of nontuberculous mycobacterial diseases in the United States: results from a national survey. Am Rev Respir Dis 1987;135(5):1007-14.

    [Crossref][Google Scholar][Indexed]

36. Cowman S, Burns K, Benson S, et al. The antimicrobial susceptibility of non-tuberculous mycobacteria. J Infect 2016;72(3):324-31.

    [Crossref][Google Scholar][Indexed]

37. Baghaei P, Tabarsi P, Farnia P, et al. Pulmonary disease caused by Mycobacterium simiae in Iranâ??s national referral center for tuberculosis. J Infect Dev Ctries 2012;6(01):23-28.

    [Crossref][Google Scholar][Indexed]

38. Tabarsi P, Baghaei P, Farnia P, et al. Nontuberculous mycobacteria among patients who are suspected for multidrug-resistant tuberculosis–need for earlier identification of nontuberculosis mycobacteria. Am J Med Sci 2009;337(3):182-184.

    [Crossref][Google Scholar][Indexed]

39. Dvorska L, Bartos M, Martin G, et al. Strategies for differentiation, identification and typing of medically important species of mycobacteria by molecular methods. Vet Med 2001;46(11/12):309-328.

    [Google Scholar]

40. Bahador A, Esmaeili D, Khaledi A, et al. An "in vitro assessment of the antibacterial properties of nanosilver Iranian MTA against Porphyromonas gingivalis. J Chem Pharm Res 2013;5(10):65-71.

    [Google Scholar]

41. Derakhshani Z FP, Eslami F, Afrai M, et al. The epidemiology of nontuberculosis mycobacteria in patients referred to TB Reference Laboratory. Kurdestan Med J 2014;19:31-39.
42. Heidari F FP NJ, Majd A, et al. Rapid detection atepic mycobacteria in patients with signs of pulmonary tuberculosis: assessment of QUB 3232 (590 bp) lucose by VNTR method. Zanjan Univ Med Sci 2009;17:33-44.
43. Nasiri MJ, Dabiri H, Darban-Sarokhalil D, et al. Prevalence of drug-resistant tuberculosis in Iran: systematic review and meta-analysis. Am J Infect Control 2014;42(11):1212-1218.

    [Crossref][Google Scholar][Indexed]

44. Javid NGE MA, Rafihi S, et al. Resistance to rifampin and isoniazid from isolated Mycobacterium tuberculosis from tuberculosis patients of Golestan province. J Lab Sci 2007;3(1):8.

    [Google Scholar]

45. Shafipour M, Ghane M, Alang SR, et al. Non tuberculosis Mycobacteria isolated from tuberculosis patients in Golestan province, North of Iran. Ann Biol Res 2013;4:133-137.
46. Moghtaderi P MR RNea. Drug resistance of nontuberculous mycobacteria causative pulmonary infections to first and second line anti TB drugs Irn J Infect Dis 2000-2010;17(58):59-66.
47. Heidarnejad H, Nagili B. Primary resistance of Mycobacterium tuberculosis to isoniazid, streptomycin, rifampin, and ethambutol in pulmonary tuberculosis. Arch Iran Med 2001;4:1-4.

    [Google Scholar]

48. Farivar TN. Prevalence of Non Tuberculosis Mycobacteria. J Med Sci 2006;6(2):292-295.
49. Naderi M, Alavi-Naini R, Sharifi-Mood B, et al. Prevalence of tuberculosis and non-tuberculosis Mycobacterium in Zahedan, Southeast of Iran. Indian J Med Res 2010;5(10):1067-1069.

    [Google Scholar][Indexed]

50. Namaei MH NNMea. Drug resistance in isolated Mycobacterium tuberculosis from tuberculosis patients in Mashhad. J Ardabil Uni Med Sci 2003;2(7). [Google Scholar]
51. Hashemi-Shahraki A, Bostanabad SZ, Heidarieh P, et al. Species spectrum of nontuberculous mycobacteria isolated from suspected tuberculosis patients, identification by multi locus sequence analysis. Infect Genet Evol 2013;20:312-24.

    [Crossref][Google Scholar][Indexed]

52. Hashemi-Shahraki A, Darban-Sarokhalil D, Heidarieh P, et al. Mycobacterium simiae: a possible emerging pathogen in Iran. Jpn J Infect Dis diseases 2013;66(6):475-479.

    [Crossref][Google Scholar][Indexed]

53. Khosravi A, Seghatoleslami S, Hashemzadeh M. Application of PCR-based fingerprinting for detection of nontuberculous mycobacteria among patients referred to tuberculosis reference center of Khuzestan Province, Iran. Res J Microbiol 2009;4(4):143-149.

    [Google Scholar]

54. MK SY, Jabbari H. Primary drug resistance patterns in newly diagnosed tuberculosis patients in Yazd, Southern Province of Iran. Afr J Biotechnol 2012;11(3):702-706.

    [Crossref][Google Scholar]

55. Zilaee MR, Firozeh F, Moniri R, et al. Prevalence of non-tuberculous mycobactera isolated from patients referring to tuberculosis center of Kashan University of Medical Sciences. Sci J Kurd Univ Med Sci 2016;21(5):50-59.

    [Crossref][Google Scholar]

56. Nour - Neamatollahie A, Ebrahimzadeh N, Siadat SD, et al. Distribution of non-tuberculosis mycobacteria strains from suspected tuberculosis patients by heat shock protein 65 PCRâ??RFLP. S Saudi J Biol Sci 2017;24(6):1380-1386.

    [Crossref][Google Scholar][Indexed]

57. Nasiri MJ, Dabiri H, Fooladi AAI, et al. High rates of nontuberculous mycobacteria isolation from patients with presumptive tuberculosis in Iran. New Microbes New Infect 2018;21:12-17.

    [Crossref][Google Scholar][Indexed]

58. Nasiri MJ, Feizabadi MM, Dabiri H, et al. Prevalence of nontuberculous Mycobacteria: A single center study in Tehran, Iran. Arch Clin Infect 2018;13(3):1-4.

    [Crossref][Google Scholar]

59. Irandoost M, Ghanbari MZ, Sakhaee F, et al. High rates of Mycobacterium fortuitum isolation in respiratory samples from Iranian patients with suspected tuberculosis: is it clinically important? J Med Microbiol 2018;67(9):1243-1248.

    [Crossref][Google Scholar][Indexed]

60. Aghajani J, Saif S, Farnia P, et al. An 8-year study on the prevalence and drug resistance of mycobacteria in clinical specimens (2011â??2018). Clinical Epidemiology and Global Health 2020;8(2):557-561.

    [Crossref][Google Scholar]

61. Mortazavi Z, Bahrmand A, Sakhaee F, et al. Evaluating the clinical significance of nontuberculous mycobacteria isolated from respiratory samples in Iran: an often overlooked disease. Infect Drug Resist 2019;12:1917.

    [Crossref][Google Scholar][Indexed]

62. Davari M, Irandoost M, Sakhaee F, et al. Genetic diversity and prevalence of nontuberculous mycobacteria isolated from clinical samples in Tehran, Iran. Microb Drug Resist 2019;25(2):264-270.

    [Crossref][Google Scholar][Indexed]

63. Karami-Zarandi M, Bahador A, Gizaw Feysia S, et al. Identification of non-tuberculosis mycobacteria by line probe assay and determination of drug resistance patterns of isolates in Iranian patients. Archiv Arch Razi Inst 2019;74(4):375-384.

    [Crossref][Google Scholar][Indexed]

64. Khosravi AD, Mirsaeidi M, Farahani A, et al. Prevalence of nontuberculous mycobacteria and high efficacy of D-cycloserine and its synergistic effect with clarithromycin against Mycobacterium fortuitum and Mycobacterium abscessus. Infection and drug resistance 2018;11:2521.

    [Crossref][Google Scholar][Indexed]

65. Ayoubi S, Farnia P, Farnia P, et al. Prevalence of non-tuberculosis mycobacteria among samples deposited from the National Tuberculous Reference Laboratory of Iran (2011-2018). Asian Pac J Trop Med 2021;14(10):451.

    [Crossref][Google Scholar]

66. Shafipour M, Shirzad-Aski H, Ghaemi EA, et al. Occurrence and risk factors of nontuberculous mycobacteria in tuberculosis-suspected patients in the north of Iran. Iran J Microbiol 2021;13(2):190-198.

    [Crossref][Google Scholar][Indexed]