Tuberculosis and Respiratory Diseases

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

DOI QR Code

Epidemiological Characteristics of Nontuberculous Mycobacterial Pulmonary Disease in South Korea: A Meta-analysis of Individual Participant Data

  • Geunin Lee (Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine) ;
  • Sol Kim (Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine) ;
  • Shihwan Chang (Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine) ;
  • Hojoon Sohn (Department of Preventive Medicine, Seoul National University College of Medicine) ;
  • Young Ae Kang (Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine) ;
  • Youngmok Park (Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Severance Hospital, Yonsei University College of Medicine)
  • Received : 2023.12.13
  • Accepted : 2024.04.07
  • Published : 2024.07.31
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Despite the global increase in nontuberculous mycobacterial pulmonary disease (NTM-PD), clinical characteristics show geographical variations. We investigated the clinical characteristics of patients with NTM-PD in South Korea. Methods: We systematically reviewed articles concerning patients with NTM-PD in South Korea until February 2022. Individual participant data, regardless of treatment, were collected using a standard case report form. Results: Data of 6,489 patients from 11 hospitals between 2002 and 2019 were analyzed. The mean age was 61.5±11.7 years, of whom 57.7% were women. Mycobacterium avium (41.4%) and Mycobacterium intracellulare (38.4%) comprised most of the causative species, followed by Mycobacterium abscessus subspecies abscessus (8.6%) and M. abscessus subspecies massiliense (7.8%). Bronchiectasis (59.4%) was the most common pulmonary comorbidity. Although reported cases of NTM-PD increased over the years, the proportions of causative species and radiologic forms remained similar. Distinct clinical characteristics were observed according to age and sex. Men were older at the time of diagnosis (median 63.8 years vs. 59.9 years, p<0.001), and had more cavitary lesions than women (38.8% vs. 21.0%, p<0.001). The older group (≥65 years) had higher proportions of patients with body mass index <18.5 kg/m2 (27.4% vs. 18.6%, p<0.001) and cavitary lesions (29.9% vs. 27.6%, p=0.009) than the younger group. Conclusion: We conducted a meta-analysis of the clinical characteristics of patients with NTM-PD in South Korea, and found age- and sex-related differences in disease-specific severity. Further investigation would enhance our comprehension of the nature of the disease, and inherited and acquired host factors.

Keywords

Acknowledgement

This research was supported by the Korea Disease Control and Prevention Agency research project (No.20211111777-00). The funding body had no role in the design of the study, or in the analysis or interpretation of data.

References

  1. Jeon D. Infection source and epidemiology of nontuberculous mycobacterial lung disease. Tuberc Respir Dis (Seoul) 2019;82:94-101.
  2. Ahn K, Kim YK, Hwang GY, Cho H, Uh Y. Continued upward trend in non-tuberculous mycobacteria isolation over 13 years in a tertiary care hospital in Korea. Yonsei Med J 2021;62:903-10.
  3. Kim JY, Kwak N, Yim JJ. The rise in prevalence and related costs of nontuberculous mycobacterial diseases in South Korea, 2010-2021. Open Forum Infect Dis 2022;9:ofac649.
  4. Kwon YS, Koh WJ, Daley CL. Treatment of Mycobacterium avium complex pulmonary disease. Tuberc Respir Dis (Seoul) 2019;82:15-26.
  5. Ryu YJ, Koh WJ, Daley CL. Diagnosis and treatment of nontuberculous mycobacterial lung disease: clinicians' perspectives. Tuberc Respir Dis (Seoul) 2016;79:74-84.
  6. Griffith DE, Eagle G, Thomson R, Aksamit TR, Hasegawa N, Morimoto K, et al. Amikacin liposome inhalation suspension for treatment-refractory lung disease caused by Mycobacterium avium complex (CONVERT): a prospective, open-label, randomized study. Am J Respir Crit Care Med 2018;198:1559-69.
  7. Kwak N, Park J, Kim E, Lee CH, Han SK, Yim JJ. Treatment outcomes of Mycobacterium avium complex lung disease: a systematic review and meta-analysis. Clin Infect Dis 2017;65:1077-84.
  8. Kwak N, Dalcolmo MP, Daley CL, Eather G, Gayoso R, Hasegawa N, et al. Mycobacterium abscessus pulmonary disease: individual patient data meta-analysis. Eur Respir J 2019;54:1801991.
  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.
  10. Lee BY, Kim S, Hong Y, Lee SD, Kim WS, Kim DS, et al. Risk factors for recurrence after successful treatment of Mycobacterium avium complex lung disease. Antimicrob Agents Chemother 2015;59:2972-7.
  11. Zo S, Kim H, Kwon OJ, Jhun BW. Antibiotic maintenance and redevelopment of nontuberculous mycobacteria pulmonary disease after treatment of Mycobacterium avium complex pulmonary disease. Microbiol Spectr 2022;10:e0108822.
  12. 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 NTM-NET collaborative study. Eur Respir J 2013;42:1604-13.
  13. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71.
  14. 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.
  15. Kim HJ, Kwak N, Hong H, Kang N, Im Y, Jhun BW, et al. BACES score for predicting mortality in nontuberculous mycobacterial pulmonary disease. Am J Respir Crit Care Med 2021;203:230-6.
  16. Park Y, Kim CY, Park MS, Kim YS, Chang J, Kang YA. Age-and sex-related characteristics of the increasing trend of nontuberculous mycobacteria pulmonary disease in a tertiary hospital in South Korea from 2006 to 2016. Korean J Intern Med 2020;35:1424-31.
  17. Kim CH, Im KH, Yoo SS, Lee SY, Cha SI, Jung HY, et al. Comparison of the incidence between tuberculosis and nontuberculous mycobacterial disease after gastrectomy. Infection 2014;42:697-704.
  18. Jeong JH, Heo M, Ju S, Lee SJ, Cho YJ, Jeong YY, et al. Pulmonary mycobacterial infection is associated with increased mortality in patients with acute respiratory distress syndrome. Medicine (Baltimore) 2021;100:e26969.
  19. Park SW, Song JW, Shim TS, Park MS, Lee HL, Uh ST, et al. Mycobacterial pulmonary infections in patients with idiopathic pulmonary fibrosis. J Korean Med Sci 2012;27:896-900.
  20. Hong KS, Ahn JH, Choi EY, Jin HJ, Shin KC, Chung JH, et al. Microbiologic distribution and clinical features of nontuberculous mycobacteria in the tertiary hospital in Daegu. Yeungnam Univ J Med 2015;32:71-9.
  21. Kim YK, Hahn S, Uh Y, Im DJ, Lim YL, Choi HK, et al. Comparable characteristics of tuberculous and non-tuberculous mycobacterial cavitary lung diseases. Int J Tuberc Lung Dis 2014;18:725-9.
  22. Lee SH, Lee JH, Chang JH, Kim SJ, Yoon HY, Shim SS, et al. Hemoptysis requiring bronchial artery embolization in patients with nontuberculous mycobacterial lung disease. BMC Pulm Med 2019;19:117.
  23. Kim EY, Chi SY, Oh IJ, Kim KS, Kim YI, Lim SC, et al. Treatment outcome of combination therapy including clarithromycin for Mycobacterium avium complex pulmonary disease. Korean J Intern Med 2011;26:54-9.
  24. Hwang JA, Kim S, Jo KW, Shim TS. Natural history of Mycobacterium avium complex lung disease in untreated patients with stable course. Eur Respir J 2017;49:1600537.
  25. Kwon BS, Lee JH, Koh Y, Kim WS, Song JW, Oh YM, et al. The natural history of non-cavitary nodular bronchiectatic Mycobacterium avium complex lung disease. Respir Med 2019;150:45-50.
  26. Jo KW, Park YE, Chong YP, Shim TS. Spontaneous sputum conversion and reversion in Mycobacterium abscessus complex lung disease. PLoS One 2020;15:e0232161.
  27. Kwon YS, Kwon BS, Kim OH, Park YE, Shim TS, Chong YP, et al. Treatment outcomes after discontinuation of ethambutol due to adverse events in Mycobacterium avium complex lung disease. J Korean Med Sci 2020;35:e59.
  28. Han DW, Jo KW, Kim OH, Shim TS. Cavity formation and its predictors in noncavitary nodular bronchiectatic Mycobacterium avium complex pulmonary disease. Respir Med 2021;179:106340.
  29. Moon SM, Jhun BW, Baek SY, Kim S, Jeon K, Ko RE, et al. Long-term natural history of non-cavitary nodular bronchiectatic nontuberculous mycobacterial pulmonary disease. Respir Med 2019;151:1-7.
  30. Jhun BW, Moon SM, Jeon K, Kwon OJ, Yoo H, Carriere KC, et al. Prognostic factors associated with long-term mortality in 1445 patients with nontuberculous mycobacterial pulmonary disease: a 15-year follow-up study. Eur Respir J 2020;55:1900798.
  31. Kim HJ, Lee JH, Yoon SH, Kim SA, Kim MS, Choi SM, et al. Nontuberculous mycobacterial pulmonary disease diagnosed by two methods: a prospective cohort study. BMC Infect Dis 2019;19:468.
  32. Kwak N, Lee JH, Kim HJ, Kim SA, Yim JJ. New-onset nontuberculous mycobacterial pulmonary disease in bronchiectasis: tracking the clinical and radiographic changes. BMC Pulm Med 2020;20:293.
  33. Gu KM, Kang HR, Park J, Kwak N, Yim JJ. Usefulness of post-bronchoscopy sputum culture for diagnosis of nontuberculous mycobacterial pulmonary disease. J Korean Med Sci 2021;36:e202.
  34. Izumi K, Morimoto K, Hasegawa N, Uchimura K, Kawatsu L, Ato M, et al. Epidemiology of adults and children treated for nontuberculous mycobacterial pulmonary disease in Japan. Ann Am Thorac Soc 2019;16:341-7.
  35. Daley CL, Iaccarino JM, Lange C, Cambau E, Wallace RJ Jr, Andrejak C, et al. Treatment of nontuberculous mycobacterial pulmonary disease: an official ATS/ERS/ESCMID/IDSA clinical practice guideline. Clin Infect Dis 2020;71:e1-36.
  36. Hwang H, Lee JK, Heo EY, Kim DK, Lee HW. The factors associated with mortality and progressive disease of nontuberculous mycobacterial lung disease: a systematic review and meta-analysis. Sci Rep 2023;13:7348.
  37. Olivier KN, Griffith DE, Eagle G, McGinnis JP 2nd, Micioni L, Liu K, et al. Randomized trial of liposomal amikacin for inhalation in nontuberculous mycobacterial lung disease. Am J Respir Crit Care Med 2017;195:814-23.
  38. Cadelis G, Ducrot R, Bourdin A, Rastogi N. Predictive factors for a one-year improvement in nontuberculous mycobacterial pulmonary disease: an 11-year retrospective and multicenter study. PLoS Negl Trop Dis 2017;11:e0005841.
  39. Holt MR, Kasperbauer SH, Koelsch TL, Daley CL. Similar characteristics of nontuberculous mycobacterial pulmonary disease in men and women. Eur Respir J 2019;54:1900252.
  40. Chan ED, Iseman MD. Slender, older women appear to be more susceptible to nontuberculous mycobacterial lung disease. Gend Med 2010;7:5-18.
  41. Choi H, Han K, Yang B, Shin DW, Sohn JW, Lee H. Female reproductive factors and incidence of nontuberculous mycobacterial pulmonary disease among postmenopausal women in Korea. Clin Infect Dis 2022;75:1397-404.
  42. Loebinger MR, Quint JK, van der Laan R, Obradovic M, Chawla R, Kishore A, et al. Risk factors for nontuberculous mycobacterial pulmonary disease: a systematic literature review and meta-analysis. Chest 2023;164:1115-24.
  43. Honda JR, Virdi R, Chan ED. Global environmental nontuberculous mycobacteria and their contemporaneous man-made and natural niches. Front Microbiol 2018;9:2029.