Trends in the Antibiotic Resistance of Non-Tuberculous Mycobacteria in Iran: A Systematic Review and Meta-Analysis
-
Hamid Heidari
,
Parisa Kalantari
,
Mohammad Sholeh
,
Sahel Hamze Pour
,
Atieh Darbandi
,
Abbas Maleki
,
Abbas Ghaysouri
,
Hossein Kazemian
Abstract
Background: Non-tuberculous mycobacteria (NTM) infections have been continuously increasing as major concerns of public health in Iran. Because innate resistance of NTM species, the treatment of these infections is difficult task, but until now resistance pattern of NTM and suitable regimens are not determined.
Methods: We systematically searched the relevant studies in PubMed, Scopus, and Embase (Until Dec 2022). All statistical analyses were carried out using the statistical package R.
Results: Eleven studies included in the analysis were performed in 6 provinces and investigated 1223 NTM clinical species. The majority of the studies originated in Tehran. Among the first-line anti-TB drugs, almost all NTM species were highly resistant to first-line anti-TB drugs. No significant difference in the isoniazid resistance rate was found in the slow or rapid-growing species and Runyon's classification of NTM isolates. A decreased in the prevalence of ciprofloxacin, clarithromycin, and moxifloxacin resistance were showed in during 2013-2022 years.
Conclusion: Most investigated antibiotics have a minor effect on NTM species and a steady increase of resistance has been seen in last few years then, need more-effective alternative regimens is clear.
1. Katoch VM (2004). Infections due to non-tuberculous mycobacteria (NTM). Indian J Med Res, 120(4):290-304.
2. Stout JE, Koh WJ, Yew WW (2016). Update on pulmonary disease due to non-tuberculous mycobacteria. Int J Infect Dis, 45:123-134.
3. Wassilew N, Hoffmann H, Andrejak C, Lange CJR (2016). Pulmonary disease caused by non-tuberculous mycobacteria. Respiration, 91(5):386-402.
4. Daley CL, Iaccarino JM, Lange C, et al (2020). Treatment of nontuberculous mycobacterial pulmonary disease: an official ATS/ERS/ESCMID/IDSA clinical practice guideline. 71:e1-e36.
5. Nasiri MJ, Dabiri H, Darban-Sarokhalil D, Hashemi Shahraki AJPo (2015). Prevalence of non-tuberculosis mycobacterial infections among tuberculosis suspects in Iran: systematic review and meta-analysis. PLoS One, 10(6):e0129073.
6. Schwarzer GJRn (2007). meta: An R package for meta-analysis. 7:40-45. https://www.researchgate.net/publication/285729385_meta_An_R_Package_for_Meta-Analysis
7. Team RCJhwR-po (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
8. Karami-Zarandi M, Bahador A, Feyisa SG, et al (2019). Identification of non-tuberculosis mycobacteria by line probe assay and determination of drug resistance patterns of isolates in Iranian patients. Arch Razi Inst, 74(4):375-384.
9. Heidarieh P, Mirsaeidi M, Hashemzadeh M, et al (2016). In Vitro Antimicrobial Susceptibility of Nontuberculous Mycobacteria in Iran. Microb Drug Resist, 22(2):172-8.
10. Saifi M, Jabbarzadeh E, Bahrmand AR, et al (2013). HSP65-PRA identification of non-tuberculosis mycobacteria from 4892 samples suspicious for mycobacterial infections. Clin Microbiol Infect, 19(8):723-8.
11. Khosravi AD, Mirsaeidi M, Farahani A, et al (2018). Prevalence of nontuberculous mycobacteria and high efficacy of D-cycloserine and its synergistic effect with clarithromycin against mycobacterium fortuitum and mycobacterium abscessus. Infect Drug Resist , 7:11:2521-2532.
12. Feysia SG, Hasan-Nejad M, Amini S, et al (2020). Incidence, Clinical Manifestation, Treatment Outcome, and Drug Susceptibility Pattern of Nontuberculous Mycobacteria in HIV Patients in Tehran, Iran. Ethiop J Health Sci, 30(1):75-84.
13. Daneshfar S, Khosravi AD, Hashemzadeh M (2022). Drug susceptibility profiling and genetic determinants of drug resistance in Mycobacterium simiae isolates obtained from regional tuberculosis reference laboratories of Iran. PLoS One, 17(8):e0267320.
14. Shafipour M, Shirzad-Aski H, Ghaemi EA, et al (2021). Occurrence and risk factors of nontuberculous mycobacteria in tuberculosis-suspected patients in the north of Iran. Iran J Microbiol, 13(2):190-198.
15. Aghajani J, Farnia P, Farnia P, et al (2022). Effect of COVID-19 pandemic on incidence of mycobacterial diseases among suspected tuberculosis pulmonary patients in Tehran, Iran. Int J Mycobacteriol, 11(4):415-422.
16. Khosravi AD, Hashemzadeh M, Rokhfirooz P (2022). Molecular identification of nontuberculous mycobacteria using the rpoB, argH and cya genes analysis. AMB Express, 12(1):121.
17. Akrami S, Dokht Khosravi A, Hashemzadeh M (2023). Drug resistance profiles and related gene mutations in slow-growing non-tuberculous mycobacteria isolated in regional tuberculosis reference laboratories of Iran: a three year cross-sectional study. Pathog Glob Health, 117(1):52-62.
18. Dezhkhi H, Farnia P, Haddadi A, Farnia P, Velayati AA (2021). Characterization of Clinical Isolates of Mycobacterium simiae Using Drug Susceptibility Tests and Molecular Analyses. Curr Microbiol, 78(6):2324-2331.
19. Saxena S, Spaink HP, Forn-Cuní G (2021). Drug resistance in nontuberculous mycobacteria: mechanisms and models. Biology(Basel), 10(2):96.
20. Rajendran P, Padmapriyadarsini C, Mondal R (2021). Nontuberculous mycobacterium: An emerging pathogen: Indian perspective. Int J Mycobacteriol, 10(3):217-227.
21. Johansen MD, Herrmann JL, Kremer L (2020). Non-tuberculous mycobacteria and the rise of Mycobacterium abscessus. Nat Rev Microbiol, 18(7):392-407.
22. Araj GF, Baba OZ, Itani LY, Avedissian AZ, Sobh GM (2019). Non-tuberculous mycobacteria profiles and their anti-mycobacterial resistance at a major medical center in Lebanon. J Infect Dev Ctries, 13(7):612-618.
23. Quang NT, Jang J (2021). Current Molecular Therapeutic Agents and Drug Candidates for Mycobacterium abscessus. Front Pharmacol, 12: 724725.
24. Rajendran P, Padmapriyadarsini C, Vijayaraghavan V,et al (2021). Drug susceptibility profiling of pulmonary Mycobacterium kansasii and its correlation with treatment outcome. Ann Thorac Med, 16(4):323-328.
25. Rindi L (2020). Efflux pump inhibitors against nontuberculous mycobacteria. Int J Mol Sci, 21(12):4191.
26. Ye M, Yuan W, Molaeipour L, Azizian K, Ahmadi A, Kouhsari E (2021). Antibiotic heteroresistance in Mycobacterium tuberculosis isolates: a systematic review and meta-analysis. Ann Clin Microbiol Antimicrob, 20(1):73.
27. Timmins GS, Deretic V (2006). Mechanisms of action of isoniazid. Mol Microbiol, 62(5):1220-1227.
28. Nessar R, Cambau E, Reyrat JM, Murray A, Gicquel B (2012). Mycobacterium abscessus: a new antibiotic nightmare. J Antimicrob Chemother, 67(4):810-818.
29. Brown-Elliott BA, Vasireddy S, Vasireddy R, et al (2015). Utility of sequencing the erm (41) gene in isolates of Mycobacterium abscessus subsp. abscessus with low and intermediate clarithromycin MICs. J Clin Microbiol, 53(4):1211-1215.
30. Wu TS, Leu HS, Chiu CH, et al (2009). Clinical manifestations, antibiotic susceptibility and molecular analysis of Mycobacterium kansasii isolates from a university hospital in Taiwan. J Antimicrob Chemother, 64(3):511-514.
31. Luthra S, Rominski A, Sander P (2018). The role of antibiotic-target-modifying and antibiotic-modifying enzymes in Mycobacterium abscessus drug resistance. Front Microbiol, 9:2179.
32. Sharma M, Malhotra B, Khandelwal S (2021). Drug susceptibiity testing of nontuberculous mycobacteria by broth microdilution method. Indian J Med Microbiol, 39(3):306-310.
33. Huh HJ, Kim SY, Jhun BW, Shin SJ, Koh WJ (2019). Recent advances in molecular diagnostics and understanding mechanisms of drug resistance in nontuberculous mycobacterial diseases. Infect Genet Evol, 72:169-182.
34. Kwon Y-S, Daley CL, Koh W-J (2019). Managing antibiotic resistance in nontuberculous mycobacterial pulmonary disease: challenges and new approaches. Expert Rev Respir Med, 13(9):851-861.
35. Wu M-L, Aziz DB, Dartois V, Dick T (2018). NTM drug discovery: status, gaps and the way forward. Drug Discov Today, 23(8):1502-1519.
36. Dubée V, Bernut A, Cortes M, et al (2015). β-Lactamase inhibition by avibactam in Mycobacterium abscessus. J Antimicrob Chemother, 70(4):1051-1058.
37. Lavollay M, Dubee V, Heym B, et al (2014). In vitro activity of cefoxitin and imipenem against Mycobacterium abscessus complex. Clin Microbiol Infect, 20(5):O297-O300.
38. Hobbie SN, Pfister P, Brüll C, Westhof E, Böttger EC (2005). Analysis of the contribution of individual substituents in 4, 6-aminoglycoside-ribosome interaction. Antimicrob Agents Chemother, 49(12):5112-5118.
39. Prammananan T, Sander P, Brown BA, et al (1998). A single 16S ribosomal RNA substitution is responsible for resistance to amikacin and other 2-deoxystreptamine aminoglycosides in Mycobacterium abscessus and Mycobacterium chelonae. J Infect Dis, 177(6):1573-1581.
40. Haworth CS, Banks J, Capstick T, et al (2017). British Thoracic Society guidelines for the management of non-tuberculous mycobacterial pulmonary disease (NTM-PD). Thorax, 72(Suppl 2):ii1-ii64.
41. Miotto P, Tessema B, Tagliani E,et al (2017). A standardised method for interpreting the association between mutations and phenotypic drug resistance in Mycobacterium tuberculosis. Eur Respir J, 50(6):1701354.
42. Coll F, Phelan J, Hill-Cawthorne GA,et al (2018). Genome-wide analysis of multi-and extensively drug-resistant Mycobacterium tuberculosis. Nat Genet, 50:307-316.
43. Aldred KJ, Kerns RJ, Osheroff N (2014). Mechanism of quinolone action and resistance. Biochemistry, 53(10):1565-1574.
44. Maurer FP, Bruderer VL, Ritter C, Castelberg C, Bloemberg GV, Böttger EC (2014). Lack of antimicrobial bactericidal activity in Mycobacterium abscessus. Antimicrob Agents Chemother, 58(7):3828-3836.
45. Pfister P, Jenni S, Poehlsgaard J, Thomas A, Douthwaite S, Ban N, Böttger EC (2004). The structural basis of macrolide–ribosome binding assessed using mutagenesis of 23 S rRNA positions 2058 and 2059. J Mol Biol, 342(5):1569-1581.
2. Stout JE, Koh WJ, Yew WW (2016). Update on pulmonary disease due to non-tuberculous mycobacteria. Int J Infect Dis, 45:123-134.
3. Wassilew N, Hoffmann H, Andrejak C, Lange CJR (2016). Pulmonary disease caused by non-tuberculous mycobacteria. Respiration, 91(5):386-402.
4. Daley CL, Iaccarino JM, Lange C, et al (2020). Treatment of nontuberculous mycobacterial pulmonary disease: an official ATS/ERS/ESCMID/IDSA clinical practice guideline. 71:e1-e36.
5. Nasiri MJ, Dabiri H, Darban-Sarokhalil D, Hashemi Shahraki AJPo (2015). Prevalence of non-tuberculosis mycobacterial infections among tuberculosis suspects in Iran: systematic review and meta-analysis. PLoS One, 10(6):e0129073.
6. Schwarzer GJRn (2007). meta: An R package for meta-analysis. 7:40-45. https://www.researchgate.net/publication/285729385_meta_An_R_Package_for_Meta-Analysis
7. Team RCJhwR-po (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
8. Karami-Zarandi M, Bahador A, Feyisa SG, et al (2019). Identification of non-tuberculosis mycobacteria by line probe assay and determination of drug resistance patterns of isolates in Iranian patients. Arch Razi Inst, 74(4):375-384.
9. Heidarieh P, Mirsaeidi M, Hashemzadeh M, et al (2016). In Vitro Antimicrobial Susceptibility of Nontuberculous Mycobacteria in Iran. Microb Drug Resist, 22(2):172-8.
10. Saifi M, Jabbarzadeh E, Bahrmand AR, et al (2013). HSP65-PRA identification of non-tuberculosis mycobacteria from 4892 samples suspicious for mycobacterial infections. Clin Microbiol Infect, 19(8):723-8.
11. Khosravi AD, Mirsaeidi M, Farahani A, et al (2018). Prevalence of nontuberculous mycobacteria and high efficacy of D-cycloserine and its synergistic effect with clarithromycin against mycobacterium fortuitum and mycobacterium abscessus. Infect Drug Resist , 7:11:2521-2532.
12. Feysia SG, Hasan-Nejad M, Amini S, et al (2020). Incidence, Clinical Manifestation, Treatment Outcome, and Drug Susceptibility Pattern of Nontuberculous Mycobacteria in HIV Patients in Tehran, Iran. Ethiop J Health Sci, 30(1):75-84.
13. Daneshfar S, Khosravi AD, Hashemzadeh M (2022). Drug susceptibility profiling and genetic determinants of drug resistance in Mycobacterium simiae isolates obtained from regional tuberculosis reference laboratories of Iran. PLoS One, 17(8):e0267320.
14. Shafipour M, Shirzad-Aski H, Ghaemi EA, et al (2021). Occurrence and risk factors of nontuberculous mycobacteria in tuberculosis-suspected patients in the north of Iran. Iran J Microbiol, 13(2):190-198.
15. Aghajani J, Farnia P, Farnia P, et al (2022). Effect of COVID-19 pandemic on incidence of mycobacterial diseases among suspected tuberculosis pulmonary patients in Tehran, Iran. Int J Mycobacteriol, 11(4):415-422.
16. Khosravi AD, Hashemzadeh M, Rokhfirooz P (2022). Molecular identification of nontuberculous mycobacteria using the rpoB, argH and cya genes analysis. AMB Express, 12(1):121.
17. Akrami S, Dokht Khosravi A, Hashemzadeh M (2023). Drug resistance profiles and related gene mutations in slow-growing non-tuberculous mycobacteria isolated in regional tuberculosis reference laboratories of Iran: a three year cross-sectional study. Pathog Glob Health, 117(1):52-62.
18. Dezhkhi H, Farnia P, Haddadi A, Farnia P, Velayati AA (2021). Characterization of Clinical Isolates of Mycobacterium simiae Using Drug Susceptibility Tests and Molecular Analyses. Curr Microbiol, 78(6):2324-2331.
19. Saxena S, Spaink HP, Forn-Cuní G (2021). Drug resistance in nontuberculous mycobacteria: mechanisms and models. Biology(Basel), 10(2):96.
20. Rajendran P, Padmapriyadarsini C, Mondal R (2021). Nontuberculous mycobacterium: An emerging pathogen: Indian perspective. Int J Mycobacteriol, 10(3):217-227.
21. Johansen MD, Herrmann JL, Kremer L (2020). Non-tuberculous mycobacteria and the rise of Mycobacterium abscessus. Nat Rev Microbiol, 18(7):392-407.
22. Araj GF, Baba OZ, Itani LY, Avedissian AZ, Sobh GM (2019). Non-tuberculous mycobacteria profiles and their anti-mycobacterial resistance at a major medical center in Lebanon. J Infect Dev Ctries, 13(7):612-618.
23. Quang NT, Jang J (2021). Current Molecular Therapeutic Agents and Drug Candidates for Mycobacterium abscessus. Front Pharmacol, 12: 724725.
24. Rajendran P, Padmapriyadarsini C, Vijayaraghavan V,et al (2021). Drug susceptibility profiling of pulmonary Mycobacterium kansasii and its correlation with treatment outcome. Ann Thorac Med, 16(4):323-328.
25. Rindi L (2020). Efflux pump inhibitors against nontuberculous mycobacteria. Int J Mol Sci, 21(12):4191.
26. Ye M, Yuan W, Molaeipour L, Azizian K, Ahmadi A, Kouhsari E (2021). Antibiotic heteroresistance in Mycobacterium tuberculosis isolates: a systematic review and meta-analysis. Ann Clin Microbiol Antimicrob, 20(1):73.
27. Timmins GS, Deretic V (2006). Mechanisms of action of isoniazid. Mol Microbiol, 62(5):1220-1227.
28. Nessar R, Cambau E, Reyrat JM, Murray A, Gicquel B (2012). Mycobacterium abscessus: a new antibiotic nightmare. J Antimicrob Chemother, 67(4):810-818.
29. Brown-Elliott BA, Vasireddy S, Vasireddy R, et al (2015). Utility of sequencing the erm (41) gene in isolates of Mycobacterium abscessus subsp. abscessus with low and intermediate clarithromycin MICs. J Clin Microbiol, 53(4):1211-1215.
30. Wu TS, Leu HS, Chiu CH, et al (2009). Clinical manifestations, antibiotic susceptibility and molecular analysis of Mycobacterium kansasii isolates from a university hospital in Taiwan. J Antimicrob Chemother, 64(3):511-514.
31. Luthra S, Rominski A, Sander P (2018). The role of antibiotic-target-modifying and antibiotic-modifying enzymes in Mycobacterium abscessus drug resistance. Front Microbiol, 9:2179.
32. Sharma M, Malhotra B, Khandelwal S (2021). Drug susceptibiity testing of nontuberculous mycobacteria by broth microdilution method. Indian J Med Microbiol, 39(3):306-310.
33. Huh HJ, Kim SY, Jhun BW, Shin SJ, Koh WJ (2019). Recent advances in molecular diagnostics and understanding mechanisms of drug resistance in nontuberculous mycobacterial diseases. Infect Genet Evol, 72:169-182.
34. Kwon Y-S, Daley CL, Koh W-J (2019). Managing antibiotic resistance in nontuberculous mycobacterial pulmonary disease: challenges and new approaches. Expert Rev Respir Med, 13(9):851-861.
35. Wu M-L, Aziz DB, Dartois V, Dick T (2018). NTM drug discovery: status, gaps and the way forward. Drug Discov Today, 23(8):1502-1519.
36. Dubée V, Bernut A, Cortes M, et al (2015). β-Lactamase inhibition by avibactam in Mycobacterium abscessus. J Antimicrob Chemother, 70(4):1051-1058.
37. Lavollay M, Dubee V, Heym B, et al (2014). In vitro activity of cefoxitin and imipenem against Mycobacterium abscessus complex. Clin Microbiol Infect, 20(5):O297-O300.
38. Hobbie SN, Pfister P, Brüll C, Westhof E, Böttger EC (2005). Analysis of the contribution of individual substituents in 4, 6-aminoglycoside-ribosome interaction. Antimicrob Agents Chemother, 49(12):5112-5118.
39. Prammananan T, Sander P, Brown BA, et al (1998). A single 16S ribosomal RNA substitution is responsible for resistance to amikacin and other 2-deoxystreptamine aminoglycosides in Mycobacterium abscessus and Mycobacterium chelonae. J Infect Dis, 177(6):1573-1581.
40. Haworth CS, Banks J, Capstick T, et al (2017). British Thoracic Society guidelines for the management of non-tuberculous mycobacterial pulmonary disease (NTM-PD). Thorax, 72(Suppl 2):ii1-ii64.
41. Miotto P, Tessema B, Tagliani E,et al (2017). A standardised method for interpreting the association between mutations and phenotypic drug resistance in Mycobacterium tuberculosis. Eur Respir J, 50(6):1701354.
42. Coll F, Phelan J, Hill-Cawthorne GA,et al (2018). Genome-wide analysis of multi-and extensively drug-resistant Mycobacterium tuberculosis. Nat Genet, 50:307-316.
43. Aldred KJ, Kerns RJ, Osheroff N (2014). Mechanism of quinolone action and resistance. Biochemistry, 53(10):1565-1574.
44. Maurer FP, Bruderer VL, Ritter C, Castelberg C, Bloemberg GV, Böttger EC (2014). Lack of antimicrobial bactericidal activity in Mycobacterium abscessus. Antimicrob Agents Chemother, 58(7):3828-3836.
45. Pfister P, Jenni S, Poehlsgaard J, Thomas A, Douthwaite S, Ban N, Böttger EC (2004). The structural basis of macrolide–ribosome binding assessed using mutagenesis of 23 S rRNA positions 2058 and 2059. J Mol Biol, 342(5):1569-1581.
| Files | ||
| Issue | Vol 52 No 11 (2023) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v52i11.14028 | |
| Keywords | ||
| Non-tuberculous mycobacteria (NTM) Antibiotic Resistance Systematic review Meta-analysis | ||
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How to Cite
1.
Heidari H, Kalantari P, Sholeh M, Hamze Pour S, Darbandi A, Maleki A, Ghaysouri A, Kazemian H. Trends in the Antibiotic Resistance of Non-Tuberculous Mycobacteria in Iran: A Systematic Review and Meta-Analysis. Iran J Public Health. 2023;52(11):2286-2298.
