Semin Respir Crit Care Med 2018; 39(03): 325-335
DOI: 10.1055/s-0038-1651491
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Epidemiology of Nontuberculous Mycobacteriosis

Jennifer Adjemian
1   Epidemiology Unit, Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
2   Commissioned Corps, United States Public Health Service, Rockville, Maryland
,
Shelby Daniel-Wayman
1   Epidemiology Unit, Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
,
Emily Ricotta
1   Epidemiology Unit, Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
,
D. Rebecca Prevots
1   Epidemiology Unit, Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland
› Author Affiliations
Further Information

Publication History

Publication Date:
02 August 2018 (online)

Abstract

Annual prevalence estimates for pulmonary nontuberculous mycobacterial (PNTM) disease in the contiguous United States range from 1.4 to 13.9 per 100,000 persons, while one study found an annual prevalence of up to 44 per 100,000 persons in Hawaii. PNTM prevalence varies by region, sex, and race/ethnicity, with higher prevalence among women and persons of Asian ancestry, as well as in the Southern United States and Hawaii. Studies consistently indicate that PNTM prevalence is increasing, with estimates ranging from 2.5 to 8% per year. Most PNTM disease is associated with Mycobacterium avium complex (MAC), although the proportion of disease attributed to MAC varies by region. Host factors identified as influencing disease risk include structural lung disease, immunomodulatory medication, as well as variants in connective tissue, mucociliary clearance, and immune genes. Environmental variables including measures of atmospheric moisture and concentrations of certain soil factors have also been shown to correlate with higher PNTM prevalence. Prevalence of extrapulmonary NTM disease is lower, stable, and associated with different risk factors, including primary immune deficiencies or HIV infection.

 
  • References

  • 1 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 (08) 881-886
  • 2 Adjemian J, Frankland TB, Daida YG. , et al. Epidemiology of nontuberculous mycobacterial lung disease and tuberculosis, Hawaii, USA. Emerg Infect Dis 2017; 23 (03) 439-447
  • 3 Marras TK, Chedore P, Ying AM, Jamieson F. Isolation prevalence of pulmonary non-tuberculous mycobacteria in Ontario, 1997 2003. Thorax 2007; 62 (08) 661-666
  • 4 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 (10) 1576-1583
  • 5 Ko RE, Moon SM, Ahn S. , 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 (08) e65
  • 6 Shah NM, Davidson JA, Anderson LF. , et al. Pulmonary Mycobacterium avium-intracellulare is the main driver of the rise in non-tuberculous mycobacteria incidence in England, Wales and Northern Ireland, 2007-2012. BMC Infect Dis 2016; 16: 195
  • 7 Adjemian J, Olivier KN, Seitz AE, Falkinham III JO, Holland SM, Prevots DR. Spatial clusters of nontuberculous mycobacterial lung disease in the United States. Am J Respir Crit Care Med 2012; 186 (06) 553-558
  • 8 Falkinham III JO. Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol 2009; 107 (02) 356-367
  • 9 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 (05) 581-586
  • 10 Griffith DE, Aksamit T, Brown-Elliott BA. , et al; ATS Mycobacterial Diseases Subcommittee; American Thoracic Society; Infectious Disease Society of America. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med 2007; 175 (04) 367-416
  • 11 Okoro CA, Zhao G, Fox JB, Eke PI, Greenlund KJ, Town M. Surveillance for health care access and health services use, adults aged 18–64 years - Behavioral Risk Factor Surveillance System, United States, 2014. MMWR Surveill Summ 2017; 66 (07) 1-42
  • 12 Winthrop KL, Baxter R, Liu L. , et al. The reliability of diagnostic coding and laboratory data to identify tuberculosis and nontuberculous mycobacterial disease among rheumatoid arthritis patients using anti-tumor necrosis factor therapy. Pharmacoepidemiol Drug Saf 2011; 20 (03) 229-235
  • 13 Prevots DR, Shaw PA, Strickland D. , et al. Nontuberculous mycobacterial lung disease prevalence at four integrated health care delivery systems. Am J Respir Crit Care Med 2010; 182 (07) 970-976
  • 14 Smith GS, Ghio AJ, Stout JE. , et al. Epidemiology of nontuberculous mycobacteria isolations among central North Carolina residents, 2006-2010. J Infect 2016; 72 (06) 678-686
  • 15 Winthrop KL, McNelley E, Kendall B. , et al. Pulmonary nontuberculous mycobacterial disease prevalence and clinical features: an emerging public health disease. Am J Respir Crit Care Med 2010; 182 (07) 977-982
  • 16 Henkle E, Hedberg K, Schafer S, Novosad S, Winthrop KL. Population-based incidence of pulmonary nontuberculous mycobacterial disease in Oregon 2007 to 2012. Ann Am Thorac Soc 2015; 12 (05) 642-647
  • 17 Donohue MJ, Wymer L. Increasing prevalence rate of nontuberculous mycobacteria infections in five states, 2008–2013. Ann Am Thorac Soc 2016; 13 (12) 2143-2150
  • 18 Strollo SE, Adjemian J, Adjemian MK, Prevots DR. The burden of pulmonary nontuberculous mycobacterial disease in the United States. Ann Am Thorac Soc 2015; 12 (10) 1458-1464
  • 19 Adjemian J, Olivier KN, Prevots DR. Epidemiology of pulmonary nontuberculous mycobacterial sputum positivity in patients with cystic fibrosis in the United States, 2010–2014. Ann Am Thorac Soc 2018; 15 (07) 817-826
  • 20 Smith MJ, Efthimiou J, Hodson ME, Batten JC. Mycobacterial isolations in young adults with cystic fibrosis. Thorax 1984; 39 (05) 369-375
  • 21 Knapp EA, Fink AK, Goss CH. , et al. The Cystic Fibrosis Foundation Patient Registry. Design and methods of a national observational disease registry. Ann Am Thorac Soc 2016; 13 (07) 1173-1179
  • 22 McKone EF, Goss CH, Aitken ML. CFTR genotype as a predictor of prognosis in cystic fibrosis. Chest 2006; 130 (05) 1441-1447
  • 23 Spaulding AB, Lai YL, Zelazny AM. , et al. Geographic distribution of nontuberculous mycobacterial species identified among clinical isolates in the United States, 2009–2013. Ann Am Thorac Soc 2017; 14 (11) 1655-1661
  • 24 Brode SK, Jamieson FB, Ng R. , et al. Increased risk of mycobacterial infections associated with anti-rheumatic medications. Thorax 2015; 70 (07) 677-682
  • 25 Noone PG, Leigh MW, Sannuti A. , et al. Primary ciliary dyskinesia: diagnostic and phenotypic features. Am J Respir Crit Care Med 2004; 169 (04) 459-467
  • 26 Chao WC, Lin CH, Liao TL. , et al. The risk of nontuberculous mycobacterial infection in patients with Sjögren's syndrome: a nationwide, population-based cohort study. BMC Infect Dis 2017; 17 (01) 796
  • 27 du Moulin GC, Sherman IH, Hoaglin DC, Stottmeier KD. Mycobacterium avium complex, an emerging pathogen in Massachusetts. J Clin Microbiol 1985; 22 (01) 9-12
  • 28 Seitz AE, Olivier KN, Adjemian J, Holland SM, Prevots DR. Trends in bronchiectasis among Medicare beneficiaries in the United States, 2000 to 2007. Chest 2012; 142 (02) 432-439
  • 29 Sakatani M. [The epidemiology of pulmonary disease caused by Mycobacterium avium complex in Japan]. Kekkaku 1993; 68 (01) 43-46
  • 30 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 (04) 958-967
  • 31 Pang SC. Mycobacterium kansasii infections in Western Australia (1962-1987). Respir Med 1991; 85 (03) 213-218
  • 32 Wang HX, Yue J, Han M. , et al. Nontuberculous mycobacteria: susceptibility pattern and prevalence rate in Shanghai from 2005 to 2008. Chin Med J (Engl) 2010; 123 (02) 184-187
  • 33 Ding LW, Lai CC, Lee LN, Hsueh PR. Disease caused by non-tuberculous mycobacteria in a university hospital in Taiwan, 1997-2003. Epidemiol Infect 2006; 134 (05) 1060-1067
  • 34 Park YS, Lee CH, Lee SM. , 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 (08) 1069-1071
  • 35 Falkinham JO. Impact of human activities on the ecology of nontuberculous mycobacteria. Future Microbiol 2010; 5 (06) 951-960
  • 36 Winthrop KL, Chang E, Yamashita S, Iademarco MF, LoBue PA. Nontuberculous mycobacteria infections and anti-tumor necrosis factor-alpha therapy. Emerg Infect Dis 2009; 15 (10) 1556-1561
  • 37 Colello K. Where Do Older Americans Live? Geographic Distribution of the Older Population. Washington, DC: Division of Digital Signal Processing; 2007
  • 38 Griffith DE, Winthrop KL. Mycobacterium avium complex lung disease therapy. Am J Respir Crit Care Med 2012; 186 (06) 477-479
  • 39 Adjemian J, Prevots DR, Gallagher J, Heap K, Gupta R, Griffith D. Lack of adherence to evidence-based treatment guidelines for nontuberculous mycobacterial lung disease. Ann Am Thorac Soc 2014; 11 (01) 9-16
  • 40 van Ingen J, Wagner D, Gallagher J. , et al; NTM-NET. Poor adherence to management guidelines in nontuberculous mycobacterial pulmonary diseases. Eur Respir J 2017; 49 (02) 49
  • 41 van Ingen J, Egelund EF, Levin A. , et al. The pharmacokinetics and pharmacodynamics of pulmonary Mycobacterium avium complex disease treatment. Am J Respir Crit Care Med 2012; 186 (06) 559-565
  • 42 Field SK, Fisher D, Cowie RL. Mycobacterium avium complex pulmonary disease in patients without HIV infection. Chest 2004; 126 (02) 566-581
  • 43 Huang JH, Kao PN, Adi V, Ruoss SJ. Mycobacterium avium-intracellulare pulmonary infection in HIV-negative patients without preexisting lung disease: diagnostic and management limitations. Chest 1999; 115 (04) 1033-1040
  • 44 Vinnard C, Longworth S, Mezochow A, Patrawalla A, Kreiswirth BN, Hamilton K. Deaths related to nontuberculous mycobacterial infections in the United States, 1999–2014. Ann Am Thorac Soc 2016; 13 (11) 1951-1955
  • 45 Novosad SA, Henkle E, Schafer S. , 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 (07) 1112-1119
  • 46 Dirac MA, Horan KL, Doody DR. , et al. Environment or host?: A case-control study of risk factors for Mycobacterium avium complex lung disease. Am J Respir Crit Care Med 2012; 186 (07) 684-691
  • 47 Lande L, Peterson DD, Gogoi R. , et al. Association between pulmonary Mycobacterium avium complex infection and lung cancer. J Thorac Oncol 2012; 7 (09) 1345-1351
  • 48 Olivier KN, Weber DJ, Wallace Jr RJ. , et al; Nontuberculous Mycobacteria in Cystic Fibrosis Study Group. Nontuberculous mycobacteria. I: multicenter prevalence study in cystic fibrosis. Am J Respir Crit Care Med 2003; 167 (06) 828-834
  • 49 Fowler CJ, Olivier KN, Leung JM. , et al. Abnormal nasal nitric oxide production, ciliary beat frequency, and Toll-like receptor response in pulmonary nontuberculous mycobacterial disease epithelium. Am J Respir Crit Care Med 2013; 187 (12) 1374-1381
  • 50 Winthrop KL, Baxter R, Liu L. , et al. Mycobacterial diseases and antitumour necrosis factor therapy in USA. Ann Rheum Dis 2013; 72 (01) 37-42
  • 51 Brode SK, Jamieson FB, Ng R. , et al. Risk of mycobacterial infections associated with rheumatoid arthritis in Ontario, Canada. Chest 2014; 146 (03) 563-572
  • 52 Binder AM, Adjemian J, Olivier KN, Prevots DR. Epidemiology of nontuberculous mycobacterial infections and associated chronic macrolide use among persons with cystic fibrosis. Am J Respir Crit Care Med 2013; 188 (07) 807-812
  • 53 Kim RD, Greenberg DE, Ehrmantraut ME. , et al. Pulmonary nontuberculous mycobacterial disease: prospective study of a distinct preexisting syndrome. Am J Respir Crit Care Med 2008; 178 (10) 1066-1074
  • 54 Leung JM, Fowler C, Smith C. , et al. A familial syndrome of pulmonary nontuberculous mycobacteria infections. Am J Respir Crit Care Med 2013; 188 (11) 1373-1376
  • 55 Colombo RE, Hill SC, Claypool RJ, Holland SM, Olivier KN. Familial clustering of pulmonary nontuberculous mycobacterial disease. Chest 2010; 137 (03) 629-634
  • 56 Szymanski EP, Leung JM, Fowler CJ. , et al. Pulmonary nontuberculous mycobacterial infection. A multisystem, multigenic disease. Am J Respir Crit Care Med 2015; 192 (05) 618-628
  • 57 Jang MA, Kim SY, Jeong BH. , et al. Association of CFTR gene variants with nontuberculous mycobacterial lung disease in a Korean population with a low prevalence of cystic fibrosis. J Hum Genet 2013; 58 (05) 298-303
  • 58 Ziedalski TM, Kao PN, Henig NR, Jacobs SS, Ruoss SJ. Prospective analysis of cystic fibrosis transmembrane regulator mutations in adults with bronchiectasis or pulmonary nontuberculous mycobacterial infection. Chest 2006; 130 (04) 995-1002
  • 59 Edwards LB, Acquaviva FA, Livesay VT, Cross FW, Palmer CE. Clinical and laboratory studies of tuberculosis and respiratory disease: the navy recruit program. Am Rev Respir Dis 1969; 99: 1-132
  • 60 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 (07) 1032-1038
  • 61 Mirsaeidi M, Machado RF, Garcia JG, Schraufnagel DE. Nontuberculous mycobacterial disease mortality in the United States, 1999-2010: a population-based comparative study. PLoS One 2014; 9 (03) e91879
  • 62 Adjemian J, Prevots DR, Ricotta E. , et al. Epidemiology of nontuberculous mycobacterial lung disease among cystic fibrosis patients residing in Hawaii, USA. IDWeek; San Diego, CA; 2017
  • 63 Hennessee CT, Seo JS, Alvarez AM, Li QX. Polycyclic aromatic hydrocarbon-degrading species isolated from Hawaiian soils: Mycobacterium crocinum sp. nov., Mycobacterium pallens sp. nov., Mycobacterium rutilum sp. nov., Mycobacterium rufum sp. nov. and Mycobacterium aromaticivorans sp. nov. Int J Syst Evol Microbiol 2009; 59 (Pt 2): 378-387
  • 64 United States Department of Agriculture. Soil survey of the territory of Hawaii: Islands of Hawaii, Kauaii, Lanai, Maui, Molokai, and Oahu. Soil Survey Series 1955; 1939: 1-64
  • 65 Kirschner Jr RA, Parker BC, Falkinham III JO. Epidemiology of infection by nontuberculous mycobacteria. Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum in acid, brown-water swamps of the southeastern United States and their association with environmental variables. Am Rev Respir Dis 1992; 145 (2 Pt 1): 271-275
  • 66 Falkinham III JO. Nontuberculous mycobacteria from household plumbing of patients with nontuberculous mycobacteria disease. Emerg Infect Dis 2011; 17 (03) 419-424
  • 67 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 (09) 3006-3011
  • 68 Schulze-Röbbecke R, Buchholtz K. Heat susceptibility of aquatic mycobacteria. Appl Environ Microbiol 1992; 58 (06) 1869-1873
  • 69 Lipner EM, Knox D, French J, Rudman J, Strong M, Crooks JL. A geospatial epidemiologic analysis of nontuberculous mycobacterial infection: an ecological study in Colorado. Ann Am Thorac Soc 2017; 14 (10) 1523-1532
  • 70 De Groote MA, Pace NR, Fulton K, Falkinham III JO. Relationships between Mycobacterium isolates from patients with pulmonary mycobacterial infection and potting soils. Appl Environ Microbiol 2006; 72 (12) 7602-7606
  • 71 Fujita K, Ito Y, Hirai T. , et al. Genetic relatedness of Mycobacterium avium-intracellulare complex isolates from patients with pulmonary MAC disease and their residential soils. Clin Microbiol Infect 2013; 19 (06) 537-541
  • 72 Reed C, von Reyn CF, Chamblee S. , et al. Environmental risk factors for infection with Mycobacterium avium complex. Am J Epidemiol 2006; 164 (01) 32-40
  • 73 Maekawa K, Ito Y, Hirai T. , et al. Environmental risk factors for pulmonary Mycobacterium avium-intracellulare complex disease. Chest 2011; 140 (03) 723-729
  • 74 Aitken ML, Limaye A, Pottinger P. , et al. Respiratory outbreak of Mycobacterium abscessus subspecies massiliense in a lung transplant and cystic fibrosis center. Am J Respir Crit Care Med 2012; 185 (02) 231-232
  • 75 Bryant JM, Grogono DM, Greaves D. , et al. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 2013; 381 (9877): 1551-1560
  • 76 Bryant JM, Grogono DM, Rodriguez-Rincon D. , et al. Emergence and spread of a human-transmissible multidrug-resistant nontuberculous mycobacterium. Science 2016; 354 (6313): 751-757
  • 77 Tettelin H, Davidson RM, Agrawal S. , et al. High-level relatedness among Mycobacterium abscessus subsp. massiliense strains from widely separated outbreaks. Emerg Infect Dis 2014; 20 (03) 364-371
  • 78 Strong M, Davidson RM. Microbiology: bacterial transmission tactics. Nature 2017; 543 (7646): 495-496
  • 79 Malcolm KC, Caceres SM, Honda JR. , et al. Mycobacterium abscessus displays fitness for fomite transmission. Appl Environ Microbiol 2017; 83 (19) 83
  • 80 Henkle E, Hedberg K, Schafer SD, Winthrop KL. Surveillance of extrapulmonary nontuberculous mycobacteria infections, Oregon, USA, 2007-2012. Emerg Infect Dis 2017; 23 (10) 1627-1630
  • 81 Adjemian J, Lai Y, Ricotta E. . DR P. Epidemiology of extrapulmonary nontuberculous mycobacterial infections among hospitalized patients in the United States American Thoracic Society Annual Conference; 2018; San Diego, CA
  • 82 Piersimoni C, Scarparo C. Extrapulmonary infections associated with nontuberculous mycobacteria in immunocompetent persons. Emerg Infect Dis 2009; 15 (09) 1351-1358 , quiz 1544