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Semin Respir Crit Care Med 2013; 34(01): 095-102
DOI: 10.1055/s-0033-1333568
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Ecology of Nontuberculous Mycobacteria—Where Do Human Infections Come from?

Joseph O. Falkinham III
1   Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia
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Publication History

Publication Date:
04 March 2013 (online)

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Abstract

Nontuberculous mycobacteria (NTM) are environmental, opportunistic human pathogens whose reservoirs include peat-rich potting soil and drinking water in buildings and households. In fact, humans are likely surrounded by NTM. NTM are ideally adapted for residence in drinking water distribution systems and household and building plumbing as they are disinfectant-resistant, surface adherent, and able to grow on low concentrations of organic matter. For individuals at risk for NTM infection, measures can be taken to reduce NTM exposure. These include avoiding inhalation of dusts from peat-rich potting soil and aerosols from showers, hot tubs, and humidifiers. A riskanalysis of the presence of NTM in drinking water has not been initiated because the virulence of independent isolates of even single NTM species (e.g., Mycobacterium avium) is quite broad, and virulence determinants have not been identified.

Keywords

nontuberculous mycobacteria - mycobacteria - Mycobacterium avium - environmental niches - aerosols
 

  • References

  • 1 Tortoli E. Impact of genotypic studies on mycobacterial taxonomy: the new mycobacteria of the 1990s. Clin Microbiol Rev 2003; 16 (2) 319-354
    CrossrefPubMedGoogle Scholar
  • 2 Stahl DA, Urbance JW. The division between fast- and slow-growing species corresponds to natural relationships among the mycobacteria. J Bacteriol 1990; 172 (1) 116-124
    PubMedGoogle Scholar
  • 3 Bang D, Herlin T, Stegger M , et al. Mycobacterium arosiense sp. nov., a slowly growing, scotochromogenic species causing osteomyelitis in an immunocompromised child. Int J Syst Evo Microbiol 2008; 58 (Pt 10) 2398-2402
    PubMedGoogle Scholar
  • 4 Tortoli E, Rindi L, Garcia MJ , et al. Proposal to elevate the genetic variant MAC-A, included in the Mycobacterium avium complex, to species rank as Mycobacterium chimaera sp. nov. Int J Syst Evol Microbiol 2004; 54 (Pt 4) 1277-1285
    CrossrefPubMedGoogle Scholar
  • 5 Murcia MI, Tortoli E, Menendez MC, Palenque E, Garcia MJ. Mycobacterium colombiense sp. nov., a novel member of the Mycobacterium avium complex and description of MAC-X as a new ITS genetic variant. Int J Syst Evol Microbiol 2006; 56 (Pt 9) 2049-2054
    CrossrefPubMedGoogle Scholar
  • 6 Ben Salah I, Cayrou C, Raoult D, Drancourt M. Mycobacterium marseillense sp. nov., Mycobacterium timonense sp. nov.and Mycobacterium bouchedurhonense sp. nov., members of the Mycobacterium avium complex. Int J Syst Evol Microbiol 2009; 59 (Pt 11) 2803-2808
    CrossrefPubMedGoogle Scholar
  • 7 Wasem CF, McCarthy CM, Murray LW. Multilocus enzyme electrophoresis analysis of the Mycobacterium avium complex and other mycobacteria. J Clin Microbiol 1991; 29 (2) 264-271
    PubMedGoogle Scholar
  • 8 Frothingham R, Wilson KH. Sequence-based differentiation of strains in the Mycobacterium avium complex. J Bacteriol 1993; 175 (10) 2818-2825
    PubMedGoogle Scholar
  • 9 Brennan PJ, Nikaido H. The envelope of mycobacteria. Annu Rev Biochem 1995; 64: 29-63
    CrossrefPubMedGoogle Scholar
  • 10 Daffé M, Draper P. The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 1998; 39: 131-203
    PubMedGoogle Scholar
  • 11 Jarlier V, Nikaido H. Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol Lett 1994; 123 (1-2) 11-18
    CrossrefPubMedGoogle Scholar
  • 12 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 (5) 666-677
    CrossrefPubMedGoogle Scholar
  • 13 Steed KA, Falkinham III JO. Effect of growth in biofilms on chlorine susceptibility of Mycobacterium avium and Mycobacterium intracellulare. Appl Environ Microbiol 2006; 72 (6) 4007-4011
    CrossrefPubMedGoogle Scholar
  • 14 Falkinham III JO. Growth in catheter biofilms and antibiotic resistance of Mycobacterium avium. J Med Microbiol 2007; 56 (Pt 2) 250-254
    CrossrefPubMedGoogle Scholar
  • 15 Parker BC, Ford MA, Gruft H, Falkinham III JO. Epidemiology of infection by nontuberculous mycobacteria. IV. Preferential aerosolization of Mycobacterium intracellulare from natural waters. Am Rev Respir Dis 1983; 128 (4) 652-656
    PubMedGoogle Scholar
  • 16 Bercovier H, Kafri O, Sela S. Mycobacteria possess a surprisingly small number of ribosomal RNA genes in relation to the size of their genome. Biochem Biophys Res Commun 1986; 136 (3) 1136-1141
    PubMedGoogle Scholar
  • 17 Schulze-Röbbecke R, Buchholtz K. Heat susceptibility of aquatic mycobacteria. Appl Environ Microbiol 1992; 58 (6) 1869-1873
    PubMedGoogle Scholar
  • 18 Falkinham III JO. Nontuberculous mycobacteria from household plumbing of patients with nontuberculous mycobacteria disease. Emerg Infect Dis 2011; 17 (3) 419-424
    CrossrefPubMedGoogle Scholar
  • 19 Slosárek M, Kubín M, Jaresová M. Water-borne household infections due to Mycobacterium xenopi. Cent Eur J Public Health 1993; 1 (2) 78-80
    PubMedGoogle Scholar
  • 20 Bodmer T, Miltner E, Bermudez LE. Mycobacterium avium resists exposure to the acidic conditions of the stomach. FEMS Microbiol Lett 2000; 182 (1) 45-49
    CrossrefPubMedGoogle Scholar
  • 21 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
    CrossrefPubMedGoogle Scholar
  • 22 Thomas V, Herrera-Rimann K, Blanc DS, Greub G. Biodiversity of amoebae and amoeba-resisting bacteria in a hospital water network. Appl Environ Microbiol 2006; 72 (4) 2428-2438
    CrossrefPubMedGoogle Scholar
  • 23 Cirillo JD, Falkow S, Tompkins LS, Bermudez LE. Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 1997; 65 (9) 3759-3767
    PubMedGoogle Scholar
  • 24 Strahl ED, Gillaspy GE, Falkinham III JO. Fluorescent acid-fast microscopy for measuring phagocytosis of Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum by Tetrahymena pyriformis and their intracellular growth. Appl Environ Microbiol 2001; 67 (10) 4432-4439
    CrossrefPubMedGoogle Scholar
  • 25 Norton CD, Le Chevallier MW, Falkinham III JO. Survival of Mycobacterium avium in a model distribution system. Water Res 2004; 38 (6) 1457-1466
    CrossrefPubMedGoogle Scholar
  • 26 Falkinham III JO, Parker BC, Gruft H. Epidemiology of infection by nontuberculous mycobacteria. I. Geographic distribution in the eastern United States. Am Rev Respir Dis 1980; 121 (6) 931-937
    PubMedGoogle Scholar
  • 27 George KL, Parker BC, Gruft H, Falkinham III JO. Epidemiology of infection by nontuberculous mycobacteria, II: Growth and survival in natural waters. Am Rev Respir Dis 1980; 122 (1) 89-94
    PubMedGoogle Scholar
  • 28 Schousboe P, Rasmussen L. Survival of Tetrahymena thermophila at low initial cell densities. Effects of lipids and long-chain alcohols. J Eukaryot Microbiol 1994; 41 (3) 195-199
    CrossrefPubMedGoogle Scholar
  • 29 Pryor M, Springthorpe S, Riffard S , et al. Investigation of opportunistic pathogens in municipal drinking water under different supply and treatment regimes. Water Sci Technol 2004; 50 (1) 83-90
    PubMedGoogle Scholar
  • 30 Archuleta RJ, Yvonne Hoppes P, Primm TP. Mycobacterium avium enters a state of metabolic dormancy in response to starvation. Tuberculosis (Edinb) 2005; 85 (3) 147-158
    CrossrefPubMedGoogle Scholar
  • 31 von Reyn CF, Maslow JN, Barber TW, Falkinham III JO, Arbeit RD. Persistent colonisation of potable water as a source of Mycobacterium avium infection in AIDS. Lancet 1994; 343 (8906) 1137-1141
    CrossrefPubMedGoogle Scholar
  • 32 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
    CrossrefPubMedGoogle Scholar
  • 33 Falkinham III JO, Iseman MD, de Haas P, van Soolingen D. Mycobacterium avium in a shower linked to pulmonary disease. J Water Health 2008; 6 (2) 209-213
    PubMedGoogle Scholar
  • 34 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 (38) 16393-16399
    CrossrefPubMedGoogle Scholar
  • 35 Falkinham III JO, Norton CD, Le Chevallier MW. Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellulare, and other Mycobacteria in drinking water distribution systems. Appl Environ Microbiol 2001; 67 (3) 1225-1231
    CrossrefPubMedGoogle Scholar
  • 36 Portaels F, Pattyn SR. Growth of mycobacteria in relation to the pH of the medium. Ann Microbiol (Paris) 1982; 133 (2) 213-221
    PubMedGoogle Scholar
  • 37 Wolinsky E. Mycobacterial lymphadenitis in children: a prospective study of 105 nontuberculous cases with long-term follow-up. Clin Infect Dis 1995; 20 (4) 954-963
    CrossrefPubMedGoogle Scholar
  • 38 van Oss CJ, Gillman CF, Neumann AW. Phagocytic Engulfment and Cell Adhesiveness as Cellular Phenomena. New York, NY: Marcel Dekker; 1975
    Google Scholar
  • 39 Thomson RM, Armstrong JG, Looke DF. Gastroesophageal reflux disease, acid suppression, and Mycobacterium avium complex pulmonary disease. Chest 2007; 131 (4) 1166-1172
    CrossrefPubMedGoogle Scholar
  • 40 Koh W-J, Lee JH, Kwon YS , et al. Prevalence of gastroesophageal reflux disease in patients with nontuberculous mycobacterial lung disease. Chest 2007; 131 (6) 1825-1830
    CrossrefPubMedGoogle Scholar
  • 41 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 (4) 367-416
    CrossrefPubMedGoogle Scholar
  • 42 Prince DS, Peterson DD, Steiner RM , et al. Infection with Mycobacterium avium complex in patients without predisposing conditions. N Engl J Med 1989; 321 (13) 863-868
    CrossrefPubMedGoogle Scholar
  • 43 Rodgers MR, Blackstone BJ, Reyes AL, Covert TC. Colonisation of point of use water filters by silver resistant non-tuberculous mycobacteria. J Clin Pathol 1999; 52 (8) 629
    PubMedGoogle Scholar
  • 44 Taylor RH, Falkinham III JO, Norton CD, LeChevallier MW. Chlorine, chloramine, chlorine dioxide, and ozone susceptibility of Mycobacterium avium. Appl Environ Microbiol 2000; 66 (4) 1702-1705
    CrossrefPubMedGoogle Scholar
  • 45 David HL. Response of Mycobacteria to ultraviolet light radiation. Am Rev Respir Dis 1973; 108 (5) 1175-1185
    PubMedGoogle Scholar
  • 46 Reddy VM, Parikh K, Luna-Herrera J, Falkinham III JO, Brown S, Gangadharam PRJ. Comparison of virulence of Mycobacterium avium complex (MAC) strains isolated from AIDS and non-AIDS patients. Microb Pathog 1994; 16 (2) 121-130
    CrossrefPubMedGoogle Scholar
  • 47 Meissner G. The value of animal models for study of infection due to atypical mycobacteria. Rev Infect Dis 1981; 3 (5) 953-959
    CrossrefPubMedGoogle Scholar
  • 48 Falkinham III JO. Factors influencing the chlorine susceptibility of Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum. Appl Environ Microbiol 2003; 69 (9) 5685-5689
    CrossrefPubMedGoogle Scholar
  • 49 Collins FM. Relative susceptibility of acid-fast and non-acid-fast bacteria to ultraviolet light. Appl Microbiol 1971; 21 (3) 411-413
    PubMedGoogle Scholar
  • 50 Lee E-S, Yoon T-H, Lee M-Y, Han S-H, Ka J-O. Inactivation of environmental mycobacteria by free chlorine and UV. Water Res 2010; 44 (5) 1329-1334
    CrossrefPubMedGoogle Scholar
  • 51 David HL, Jones Jr WD, Newman CM. Ultraviolet light inactivation and photoreactivation in the mycobacteria. Infect Immun 1971; 4 (3) 318-319
    PubMedGoogle Scholar
  • 52 McCarthy CM, Schaefer JO. Response of Mycobacterium avium to ultraviolet irradiation. Appl Microbiol 1974; 28 (1) 151-153
    PubMedGoogle Scholar
  • 53 Hayes SL, Sivaganesan M, White KM, Pfaller SL. Assessing the effectiveness of low-pressure ultraviolet light for inactivating Mycobacterium avium complex (MAC) micro-organisms. Lett Appl Microbiol 2008; 47 (5) 386-392
    CrossrefPubMedGoogle Scholar