Tuberculosis and Respiratory Diseases

The Korean Academy of Tuberculosis and Respiratory Diseases (대한결핵및호흡기학회)
권호 표지
DOI QR코드

DOI QR Code

Infection Source and Epidemiology of Nontuberculous Mycobacterial Lung Disease

  • Jeon, Doosoo (Department of Internal Medicine, Pusan National University Yangsan Hospital, Pusan National University School of Medicine)
  • Received : 2018.03.25
  • Accepted : 2018.05.11
  • Published : 2019.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Nontuberculous mycobacteria (NTM) are ubiquitous organisms that are generally found not only in the natural environment but also in the human engineered environment, including water, soil, and dust. These organisms can form biofilms and can be readily aerosolized because they are hydrophobic owing to the presence of the lipid-rich outer membrane. Aerosolization and subsequent inhalation were the major route of NTM lung disease. Water distribution systems and household plumbing are ideal habit for NTM and the main transmission route from natural water to household. NTM have been isolated from drinking water, faucets, pipelines, and water tanks. Studies that used genotyping have shown that NTM isolates from patients are identical to those in the environment, that is, from shower water, showerheads, tap water, and gardening soil. Humans are likely to be exposed to NTM in their homes through simple and daily activities, such as drinking, showering, or gardening. In addition to environmental factors, host factors play an important role in the development of NTM lung disease. The incidence and prevalence of NTM lung disease are increasing worldwide, and this disease is rapidly becoming a major public health problem. NTM lung disease is associated with substantially impaired quality of life, increased morbidity and mortality, and high medical costs. A more comprehensive understanding of the infection source and epidemiology of NTM is essential for the development of new strategies that can prevent and control NTM infection.

Keywords

References

  1. Griffith DE, Aksamit T, Brown-Elliott BA, Catanzaro A, Daley C, Gordin F, et al. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med 2007;175:367-416. https://doi.org/10.1164/rccm.200604-571ST
  2. Haworth CS, Banks J, Capstick T, Fisher AJ, Gorsuch T, Laurenson IF, et al. British Thoracic Society guidelines for the management of non-tuberculous mycobacterial pulmonary disease (NTM-PD). Thorax 2017;72(Suppl 2):ii1-64.
  3. Runyon EH. Anonymous mycobacteria in pulmonary disease. Med Clin North Am 1959;43:273-90. https://doi.org/10.1016/S0025-7125(16)34193-1
  4. Griffith DE, Aksamit TR. Understanding nontuberculous mycobacterial lung disease: it's been a long time coming. F1000Res 2016;5:2797. https://doi.org/10.12688/f1000research.9272.1
  5. Koh WJ. Nontuberculous mycobacteria: overview. Microbiol Spectr 2017 Jan [Epub]. https://doi.org/10.1128/microbiolspec.TNMI7-0024-2016.
  6. Ryu YJ, Koh WJ, Daley CL. Diagnosis and treatment of nontuberculous mycobacterial lung disease: clinicians' perspectives. Tuberc Respir Dis 2016;79:74-84. https://doi.org/10.4046/trd.2016.79.2.74
  7. Stout JE, Koh WJ, Yew WW. Update on pulmonary disease due to non-tuberculous mycobacteria. Int J Infect Dis 2016;45:123-34. https://doi.org/10.1016/j.ijid.2016.03.006
  8. Wallace RJ Jr, Zhang Y, Brown-Elliott BA, Yakrus MA, Wilson RW, Mann L, et al. Repeat positive cultures in Mycobacterium intracellulare lung disease after macrolide therapy represent new infections in patients with nodular bronchiectasis. J Infect Dis 2002;186:266-73. https://doi.org/10.1086/341207
  9. Wallace RJ Jr, Brown-Elliott BA, McNulty S, Philley JV, Killingley J, Wilson RW, et al. Macrolide/Azalide therapy for nodular/bronchiectatic mycobacterium avium complex lung disease. Chest 2014;146:276-82. https://doi.org/10.1378/chest.13-2538
  10. Koh WJ, Moon SM, Kim SY, Woo MA, Kim S, Jhun BW, et al. Outcomes of Mycobacterium avium complex lung disease based on clinical phenotype. Eur Respir J 2017;50:1602503. https://doi.org/10.1183/13993003.02503-2016
  11. Falkinham JO 3rd. Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol 2009;107:356-67. https://doi.org/10.1111/j.1365-2672.2009.04161.x
  12. Falkinham JO 3rd. Environmental sources of nontuberculous mycobacteria. Clin Chest Med 2015;36:35-41. https://doi.org/10.1016/j.ccm.2014.10.003
  13. Brennan PJ, Nikaido H. The envelope of mycobacteria. Annu Rev Biochem 1995;64:29-63. https://doi.org/10.1146/annurev.bi.64.070195.000333
  14. Bodmer T, Miltner E, Bermudez LE. Mycobacterium avium resists exposure to the acidic conditions of the stomach. FEMS Microbiol Lett 2000;182:45-9. https://doi.org/10.1111/j.1574-6968.2000.tb08871.x
  15. Rastogi N, Frehel C, Ryter A, Ohayon H, Lesourd M, David HL. Multiple drug resistance in Mycobacterium avium: is the wall architecture responsible for exclusion of antimicrobial agents? Antimicrob Agents Chemother 1981;20:666-77. https://doi.org/10.1128/AAC.20.5.666
  16. Taylor RH, Falkinham JO 3rd, Norton CD, LeChevallier MW. Chlorine, chloramine, chlorine dioxide, and ozone susceptibility of Mycobacterium avium. Appl Environ Microbiol 2000;66:1702-5. https://doi.org/10.1128/AEM.66.4.1702-1705.2000
  17. Schulze-Robbecke R, Buchholtz K. Heat susceptibility of aquatic mycobacteria. Appl Environ Microbiol 1992;58:1869-73. https://doi.org/10.1128/AEM.58.6.1869-1873.1992
  18. Cirillo JD, Falkow S, Tompkins LS, Bermudez LE. Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 1997;65:3759-67. https://doi.org/10.1128/IAI.65.9.3759-3767.1997
  19. Faria S, Joao I, Jordao L. General overview on nontuberculous mycobacteria, biofilms, and human infection. J Pathog 2015;2015:809014. https://doi.org/10.1155/2015/809014
  20. Parker BC, Ford MA, Gruft H, Falkinham JO 3rd. Epidemiology of infection by nontuberculous mycobacteria. IV. Preferential aerosolization of Mycobacterium intracellulare from natural waters. Am Rev Respir Dis 1983;128:652-6.
  21. Adjemian J, Olivier KN, Seitz AE, Falkinham JO 3rd, Holland SM, Prevots DR. Spatial clusters of nontuberculous mycobacterial lung disease in the United States. Am J Respir Crit Care Med 2012;186:553-8. https://doi.org/10.1164/rccm.201205-0913OC
  22. Adjemian J, Olivier KN, Prevots DR. Nontuberculous mycobacteria among patients with cystic fibrosis in the United States: screening practices and environmental risk. Am J Respir Crit Care Med 2014;190:581-6. https://doi.org/10.1164/rccm.201405-0884OC
  23. Nishiuchi Y, Iwamoto T, Maruyama F. Infection sources of a common non-tuberculous mycobacterial pathogen, Mycobacterium avium complex. Front Med (Lausanne) 2017;4:27.
  24. Thomson R, Tolson C, Sidjabat H, Huygens F, Hargreaves M. Mycobacterium abscessus isolated from municipal water: a potential source of human infection. BMC Infect Dis 2013;13:241. https://doi.org/10.1186/1471-2334-13-241
  25. Torvinen E, Suomalainen S, Lehtola MJ, Miettinen IT, Zacheus O, Paulin L, et al. Mycobacteria in water and loose deposits of drinking water distribution systems in Finland. Appl Environ Microbiol 2004;70:1973-81. https://doi.org/10.1128/AEM.70.4.1973-1981.2004
  26. Tuffley RE, Holbeche JD. Isolation of the Mycobacterium avium-M. intracellulare-M. scrofulaceum complex from tank water in Queensland, Australia. Appl Environ Microbiol 1980;39:48-53. https://doi.org/10.1128/AEM.39.1.48-53.1980
  27. Falkinham JO 3rd, Norton CD, LeChevallier MW. Factors influencing numbers of Mycobacterium avium , Mycobacterium intracellulare , and other mycobacteria in drinking water distribution systems. Appl Environ Microbiol 2001;67:1225-31. https://doi.org/10.1128/AEM.67.3.1225-1231.2001
  28. Falkinham JO 3rd. Nontuberculous mycobacteria from household plumbing of patients with nontuberculous mycobacteria disease. Emerg Infect Dis 2011;17:419-24. https://doi.org/10.3201/eid1703.101510
  29. Thomson R, Tolson C, Carter R, Coulter C, Huygens F, Hargreaves M. Isolation of nontuberculous mycobacteria (NTM) from household water and shower aerosols in patients with pulmonary disease caused by NTM. J Clin Microbiol 2013;51:3006-11. https://doi.org/10.1128/JCM.00899-13
  30. Falkinham JO 3rd, Iseman MD, de Haas P, van Soolingen D. Mycobacterium avium in a shower linked to pulmonary disease. J Water Health 2008;6:209-13. https://doi.org/10.2166/wh.2008.232
  31. Feazel LM, Baumgartner LK, Peterson KL, Frank DN, Harris JK, Pace NR. Opportunistic pathogens enriched in showerhead biofilms. Proc Natl Acad Sci U S A 2009;106:16393-9. https://doi.org/10.1073/pnas.0908446106
  32. von Reyn CF, Maslow JN, Barber TW, Falkinham JO 3rd, Arbeit RD. Persistent colonisation of potable water as a source of Mycobacterium avium infection in AIDS. Lancet 1994;343:1137-41. https://doi.org/10.1016/S0140-6736(94)90239-9
  33. Reznikov M, Dawson DJ. Serological investigation of strains of Mycobacterium intracellulare ("battey" bacillus) isolated from house-dusts. Med J Aust 1971;1:682-3. https://doi.org/10.5694/j.1326-5377.1971.tb87788.x
  34. De Groote MA, Pace NR, Fulton K, Falkinham JO 3rd. Relationships between Mycobacterium isolates from patients with pulmonary mycobacterial infection and potting soils. Appl Environ Microbiol 2006;72:7602-6. https://doi.org/10.1128/AEM.00930-06
  35. Sood G, Parrish N. Outbreaks of nontuberculous mycobacteria. Curr Opin Infect Dis 2017;30:404-9. https://doi.org/10.1097/QCO.0000000000000386
  36. Allen KB, Yuh DD, Schwartz SB, Lange RA, Hopkins R, Bauer K, et al. Nontuberculous Mycobacterium infections associated with heater-cooler devices. Ann Thorac Surg 2017;104:1237-42. https://doi.org/10.1016/j.athoracsur.2017.04.067
  37. Williamson D, Howden B, Stinear T. Mycobacterium chimaera spread from heating and cooling units in heart surgery. N Engl J Med 2017;376:600-2. https://doi.org/10.1056/NEJMc1612023
  38. Prevots DR, Adjemian J, Fernandez AG, Knowles MR, Olivier KN. Environmental risks for nontuberculous mycobacteria: individual exposures and climatic factors in the cystic fibrosis population. Ann Am Thorac Soc 2014;11:1032-8. https://doi.org/10.1513/AnnalsATS.201404-184OC
  39. Halstrom S, Price P, Thomson R. Review: environmental mycobacteria as a cause of human infection. Int J Mycobacteriol 2015;4:81-91. https://doi.org/10.1016/j.ijmyco.2015.03.002
  40. O'Brien DP, Currie BJ, Krause VL. Nontuberculous mycobacterial disease in northern Australia: a case series and review of the literature. Clin Infect Dis 2000;31:958-67. https://doi.org/10.1086/318136
  41. Bryant JM, Grogono DM, Greaves D, Foweraker J, Roddick I, Inns T, et al. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 2013;381:1551-60. https://doi.org/10.1016/S0140-6736(13)60632-7
  42. Bryant JM, Grogono DM, Rodriguez-Rincon D, Everall I, Brown KP, Moreno P, et al. Emergence and spread of a human-transmissible multidrug-resistant nontuberculous mycobacterium. Science 2016;354:751-7. https://doi.org/10.1126/science.aaf8156
  43. Prevots DR, Loddenkemper R, Sotgiu G, Migliori GB. Nontuberculous mycobacterial pulmonary disease: an increasing burden with substantial costs. Eur Respir J 2017;49:1700374. https://doi.org/10.1183/13993003.00374-2017
  44. Prevots DR, Marras TK. Epidemiology of human pulmonary infection with nontuberculous mycobacteria: a review. Clin Chest Med 2015;36:13-34. https://doi.org/10.1016/j.ccm.2014.10.002
  45. Adjemian J, Olivier KN, Seitz AE, Holland SM, Prevots DR. Prevalence of nontuberculous mycobacterial lung disease in U.S. Medicare beneficiaries. Am J Respir Crit Care Med 2012;185:881-6. https://doi.org/10.1164/rccm.201111-2016OC
  46. Marras TK, Mendelson D, Marchand-Austin A, May K, Jamieson FB. Pulmonary nontuberculous mycobacterial disease, Ontario, Canada, 1998-2010. Emerg Infect Dis 2013;19:1889-91.
  47. Moore JE, Kruijshaar ME, Ormerod LP, Drobniewski F, Abubakar I. Increasing reports of non-tuberculous mycobacteria in England, Wales and Northern Ireland, 1995-2006. BMC Public Health 2010;10:612. https://doi.org/10.1186/1471-2458-10-612
  48. Thomson RM; NTM working group at Queensland TB Control Centre and Queensland Mycobacterial Reference Laboratory. Changing epidemiology of pulmonary nontuberculous mycobacteria infections. Emerg Infect Dis 2010;16:1576-83. https://doi.org/10.3201/eid1610.091201
  49. Ide S, Nakamura S, Yamamoto Y, Kohno Y, Fukuda Y, Ikeda H, et al. Epidemiology and clinical features of pulmonary nontuberculous mycobacteriosis in Nagasaki, Japan. PLoS One 2015;10:e0128304. https://doi.org/10.1371/journal.pone.0128304
  50. Lai CC, Tan CK, Chou CH, Hsu HL, Liao CH, Huang YT, et al. Increasing incidence of nontuberculous mycobacteria, Taiwan, 2000-2008. Emerg Infect Dis 2010;16:294-6. https://doi.org/10.3201/eid1602.090675
  51. Kwon YS, Koh WJ. Diagnosis and treatment of nontuberculous mycobacterial lung disease. J Korean Med Sci 2016;31:649-59. https://doi.org/10.3346/jkms.2016.31.5.649
  52. Ko RE, Moon SM, Ahn S, Jhun BW, Jeon K, Kwon OJ, et al. Changing epidemiology of nontuberculous mycobacterial lung diseases in a tertiary referral hospital in Korea between 2001 and 2015. J Korean Med Sci 2018;33:e65. https://doi.org/10.3346/jkms.2018.33.e65
  53. Park YS, Lee CH, Lee SM, Yang SC, Yoo CG, Kim YW, et al. Rapid increase of non-tuberculous mycobacterial lung diseases at a tertiary referral hospital in South Korea. Int J Tuberc Lung Dis 2010;14:1069-71.
  54. Lee SK, Lee EJ, Kim SK, Chang J, Jeong SH, Kang YA. Changing epidemiology of nontuberculous mycobacterial lung disease in South Korea. Scand J Infect Dis 2012;44:733-8. https://doi.org/10.3109/00365548.2012.681695
  55. Yoo JW, Jo KW, Kim MN, Lee SD, Kim WS, Kim DS, et al. Increasing trend of isolation of non-tuberculous mycobacteria in a tertiary university hospital in South Korea. Tuberc Respir Dis 2012;72:409-15. https://doi.org/10.4046/trd.2012.72.5.409
  56. Koh WJ, Chang B, Jeong BH, Jeon K, Kim SY, Lee NY, et al. Increasing recovery of nontuberculous mycobacteria from respiratory specimens over a 10-year period in a tertiary referral hospital in South Korea. Tuberc Respir Dis 2013;75:199-204. https://doi.org/10.4046/trd.2013.75.5.199
  57. Kim JK, Rheem I. Identification and distribution of nontuberculous mycobacteria from 2005 to 2011 in cheonan, Korea. Tuberc Respir Dis 2013;74:215-21. https://doi.org/10.4046/trd.2013.74.5.215
  58. Lee MY, Lee T, Kim MH, Byun SS, Ko MK, Hong JM, et al. Regional differences of nontuberculous mycobacteria species in Ulsan, Korea. J Thorac Dis 2014;6:965-70.
  59. Kim N, Yi J, Chang CL. Recovery rates of non-tuberculous mycobacteria from clinical specimens are increasing in Korean tertiary-care hospitals. J Korean Med Sci 2017;32:1263-7. https://doi.org/10.3346/jkms.2017.32.8.1263
  60. Yoon HJ, Choi HY, Ki M. Nontuberculosis mycobacterial infections at a specialized tuberculosis treatment centre in the Republic of Korea. BMC Infect Dis 2017;17:432. https://doi.org/10.1186/s12879-017-2532-4
  61. Brode SK, Daley CL, Marras TK. The epidemiologic relationship between tuberculosis and non-tuberculous mycobacterial disease: a systematic review. Int J Tuberc Lung Dis 2014;18:1370-7. https://doi.org/10.5588/ijtld.14.0120
  62. Hoefsloot W, van Ingen J, Andrejak C, Angeby K, Bauriaud R, Bemer P, et al. The geographic diversity of nontuberculous mycobacteria isolated from pulmonary samples: an NTMNET collaborative study. Eur Respir J 2013;42:1604-13. https://doi.org/10.1183/09031936.00149212
  63. Koh WJ, Kwon OJ, Jeon K, Kim TS, Lee KS, Park YK, et al. Clinical significance of nontuberculous mycobacteria isolated from respiratory specimens in Korea. Chest 2006;129:341-8. https://doi.org/10.1378/chest.129.2.341
  64. Jang MA, Koh WJ, Huh HJ, Kim SY, Jeon K, Ki CS, et al. Distribution of nontuberculous mycobacteria by multigene sequence-based typing and clinical significance of isolated strains. J Clin Microbiol 2014;52:1207-12. https://doi.org/10.1128/JCM.03053-13
  65. Kim HS, Lee Y, Lee S, Kim YA, Sun YK. Recent trends in clinically significant nontuberculous mycobacteria isolates at a Korean general hospital. Ann Lab Med 2014;34:56-9. https://doi.org/10.3343/alm.2014.34.1.56
  66. Honda JR, Knight V, Chan ED. Pathogenesis and risk factors for nontuberculous mycobacterial lung disease. Clin Chest Med 2015;36:1-11. https://doi.org/10.1016/j.ccm.2014.10.001
  67. Kartalija M, Ovrutsky AR, Bryan CL, Pott GB, Fantuzzi G, Thomas J, et al. Patients with nontuberculous mycobacterial lung disease exhibit unique body and immune phenotypes. Am J Respir Crit Care Med 2013;187:197-205. https://doi.org/10.1164/rccm.201206-1035OC
  68. Kim RD, Greenberg DE, Ehrmantraut ME, Guide SV, Ding L, Shea Y, et al. Pulmonary nontuberculous mycobacterial disease: prospective study of a distinct preexisting syndrome. Am J Respir Crit Care Med 2008;178:1066-74. https://doi.org/10.1164/rccm.200805-686OC
  69. Szymanski EP, Leung JM, Fowler CJ, Haney C, Hsu AP, Chen F, et al. Pulmonary nontuberculous mycobacterial infection: a multisystem, multigenic disease. Am J Respir Crit Care Med 2015;192:618-28. https://doi.org/10.1164/rccm.201502-0387OC
  70. Yeung MW, Khoo E, Brode SK, Jamieson FB, Kamiya H, Kwong JC, et al. Health-related quality of life, comorbidities and mortality in pulmonary nontuberculous mycobacterial infections: a systematic review. Respirology 2016;21:1015-25. https://doi.org/10.1111/resp.12767
  71. Novosad SA, Henkle E, Schafer S, Hedberg K, Ku J, Siegel SA, et al. Mortality after respiratory isolation of nontuberculous mycobacteria: a comparison of patients who did and did not meet disease criteria. Ann Am Thorac Soc 2017;14:1112-9. https://doi.org/10.1513/AnnalsATS.201610-800OC
  72. Huang CT, Tsai YJ, Wu HD, Wang JY, Yu CJ, Lee LN, et al. Impact of non-tuberculous mycobacteria on pulmonary function decline in chronic obstructive pulmonary disease. Int J Tuberc Lung Dis 2012;16:539-45. https://doi.org/10.5588/ijtld.11.0412
  73. Park HY, Jeong BH, Chon HR, Jeon K, Daley CL, Koh WJ. Lung function decline according to clinical course in nontuberculous mycobacterial lung disease. Chest 2016;150:1222-32. https://doi.org/10.1016/j.chest.2016.06.005
  74. Diel R, Jacob J, Lampenius N, Loebinger M, Nienhaus A, Rabe KF, et al. Burden of non-tuberculous mycobacterial pulmonary disease in Germany. Eur Respir J 2017;49:1602109. https://doi.org/10.1183/13993003.02109-2016

Cited by

  1. Recent advances in nontuberculous mycobacterial lung infections vol.8, 2019, https://doi.org/10.12688/f1000research.20096.1
  2. Treatment of Mycobacterium abscessus Pulmonary Disease vol.94, pp.4, 2019, https://doi.org/10.3904/kjm.2019.94.4.343
  3. Characterization of non-tuberculous mycobacterial pulmonary disease in Nanjing district of China vol.19, pp.1, 2019, https://doi.org/10.1186/s12879-019-4412-6
  4. Prevalence, incidence, and mortality of nontuberculous mycobacterial infection in Korea: a nationwide population-based study vol.19, pp.1, 2019, https://doi.org/10.1186/s12890-019-0901-z
  5. Epidemiology, diagnosis & treatment of non-tuberculous mycobacterial diseases vol.152, pp.3, 2019, https://doi.org/10.4103/ijmr.ijmr_902_20
  6. Molecular Identification, and Characterization of Mycobacterium kansasii Strains Isolated from Four Tuberculosis Regional Reference Laboratories in Iran During 2016–2018 vol.13, 2019, https://doi.org/10.2147/idr.s245295
  7. 5-Alkylamino- N -phenylpyrazine-2-carboxamides: Design, Preparation, and Antimycobacterial Evaluation vol.25, pp.7, 2019, https://doi.org/10.3390/molecules25071561
  8. Non-Tuberculous Mycobacteria: Molecular and Physiological Bases of Virulence and Adaptation to Ecological Niches vol.8, pp.9, 2019, https://doi.org/10.3390/microorganisms8091380
  9. European Respiratory Society International Congress, Madrid, 2019: nontuberculous mycobacterial pulmonary disease highlights vol.6, pp.4, 2019, https://doi.org/10.1183/23120541.00317-2020
  10. Evaluation of plasma anti-GPL-core IgA and IgG for diagnosis of disseminated non-tuberculous mycobacteria infection vol.15, pp.11, 2019, https://doi.org/10.1371/journal.pone.0242598
  11. Biofilms of the non-tuberculous Mycobacterium chelonae form an extracellular matrix and display distinct expression patterns vol.6, 2019, https://doi.org/10.1016/j.tcsw.2020.100043
  12. Identification of Nontuberculous Mycobacteria in Patients with Pulmonary Diseases in Gyeongnam, Korea, Using Multiplex PCR and Multigene Sequence-Based Analysis vol.2021, 2021, https://doi.org/10.1155/2021/8844306
  13. Lower Recovery of Nontuberculous Mycobacteria from Outdoor Hawai’i Environmental Water Biofilms Compared to Indoor Samples vol.9, pp.2, 2019, https://doi.org/10.3390/microorganisms9020224
  14. Mortality and Prognostic Factors of Nontuberculous Mycobacterial Infection in Korea: A Population-based Comparative Study vol.72, pp.10, 2019, https://doi.org/10.1093/cid/ciaa1381
  15. Non‐tuberculous mycobacteria immunopathogenesis: Closer than they appear. a prime of innate immunity trade‐off and NTM ways into virulence vol.94, pp.2, 2019, https://doi.org/10.1111/sji.13035
  16. Evaluating the Prevalence and Incidence of Bronchiectasis and Nontuberculous Mycobacteria in South Korea Using the Nationwide Population Data vol.18, pp.17, 2019, https://doi.org/10.3390/ijerph18179029
  17. Nontuberculous mycobacterial lung disease caused by Mycobacterium avium complex - disease burden, unmet needs, and advances in treatment developments vol.15, pp.11, 2019, https://doi.org/10.1080/17476348.2021.1987891
  18. Species diversity and molecular analysis of opportunistic Mycobacterium, Nocardia and Rhodococcus isolated from the hospital environment in a developing country, a potential resources for nosocomial i vol.43, pp.1, 2019, https://doi.org/10.1186/s41021-021-00173-7