The Impact of Human Activities on the Ecology of
Nontuberculous Mycobacteria
Joseph O. Falkinham, III
Department of Biological Sciences
Virginia Tech
Blacksburg, Virginia, USA
Correspondence:
J.O. Falkinham, III
Department of Biological Sciences
Virginia Tech
Blacksburg, VA 24061-0406
USA
Phone 1-540-231-5931
FAX 1-540-231-9307
E-mail [email protected]
Summary
Nontuberculous mycobacteria (NTM) are environmental opportunistic pathogens of
humans and animals. They are found in a wide variety of habitats that are also occupied by humans;
including drinking water distribution systems and household water and plumbing. In that regard,
they are distinct from their obligate pathogenic relatives, the members of the Mycobacterium tuberculosis
complex. Because of the presence of NTM in the human environment, human activities have had
direct impacts on their ecology and hence their epidemiology.
NTM are oligotrophic, able to grow at low organic matter concentrations and over a wide
range of temperatures and even at low oxygen concentrations. Thus, NTM are normal inhabitants of
natural waters and drinking waters. Discovery of the presence of NTM polluted soils is not
surprising in light of the ability of NTM to degrade a variety of hydrocarbon pollutants.
A major human activity selecting for the growth and predominance of mycobacteria is
habitats is disinfection. Compared to other bacteria, NTM are relatively disinfectant-, heavy metal-,
and antibiotic-resistant. Thus, the use of any anti-microbial agent selects for mycobacteria.
Employment of disinfectants for drinking water treatment, leads to selection for mycobacteria that
can grow and come to dominate in drinking water distribution systems in the absence of
disinfectant-sensitive competing microorganisms. NTM selection may also occur as consequence of
the presence of antibiotics in drinking water and drinking water sources.
Keywords: Mycobacteria, Drinking Water Distribution Systems, Disinfectant, Antibiotic,
Selection, Oligotrophic, Household Plumbing
Introduction
It is the objective of this review to cite instances illustrating how human activities may have
impacts on the ecology of the nontuberculous mycobacteria (NTM). NTM are soil- and water-
borne human and animal opportunistic pathogens whose environmental distribution includes
habitats to which humans are regularly and routinely exposed (e.g., drinking water). Consequently,
human activities such as water disinfection, water transmission, and pollution have direct and
positive effects on NTM populations.
The Nontuberculous Mycobacteria (NTM)
The nontuberculous mycobacteria (NTM) are environmental opportunistic pathogenic
members of the genus Mycobacterium. There are over 120 species, most of which have described in
the past 20 years [1]. Some NTM species, namely the Mycobacterium avium complex (MAC, which
includes Mycobacterium intracellulare), Mycobacterium kansasii, Mycobacterium malmoense, Mycobacterium
xenopi, Mycobacterium ulcerans, Mycobacterium fortuitum, Mycobacterium abscessus, and Mycobacterium chelonae
(Table 1) are responsible for a disproportionate number of infections [2, 3, 4, 5]. NTM cause
diseases in humans [5] and wild and domesticated animals (e.g., cattle, deer, sheep, and goats), wild
and domesticated birds, fish, reptiles, and amphibians [6].
NTM are opportunistic pathogens. In humans, an individual with one or more of a particular
set of genetic or physiologic conditions is at risk for NTM disease. Historically, the risk factors for
pulmonary NTM disease include prior Mycobacterium tuberculosis infection, alcoholism, occupational
exposure to dusts (e.g., farmers, coal miners), and silicosis [5, 7]. Surgery is also a risk factor for
NTM disease, particularly for members of rapidly growing species [4]. M. avium is associated with
cervical lymphadenitis in young children [8]. NTM bacteremia is found in immunosuppressed
individuals as a consequence of HIV-infection, chemotherapy, cancer, or transplant-associated
immunosuppression [5]. In addition to those two groups, there is a population of individuals at
increased risk for NTM pulmonary disease, yet who lack the classic risk factors and are not
immunosuppressed [9, 10, 11]. The patients share the characteristic of being slender and elderly.
Most are women (50 % more women than men). Amongst that group of NTM patients are found
those with cystic fibrosis or those heterozygous for one of the mutations in the cystic fibrosis
transport regulator (CFTR) gene or with α-1-antitrypsin deficiencies [12]. Gastroesophageal reflux
disease (GERD) has also been suggested to place individuals at increased risk for NTM pulmonary
disease [13, 14].
Habitats Populated by Nontuberculous Mycobacteria
NTM populate a variety of natural and human-engineered habitats (Table 2). Populate was
chosen deliberately as NTM are normal inhabitants of both natural and engineered environments;
not contaminants. In all the habitats where NTM have been recovered, the mycobacteria are part of
the normal flora, existing as stable, resident, and growing populations. An exception may be M.
avium subsp. paratuberculosis whose growth and persistence in the environment has not been reported.
Natural habitats for NTM include soils and rivers, ponds, lakes, and bays [15, 16, 17]. As NTM are
in soils and natural waters, dusts and aerosols (respectively) carry NTM [18, 19]. NTM have also
been isolated from polluted waste dumps [20, 21]. NTM also populate drinking water distribution
systems [22, 23], buildings [24, 25], and household plumbing [26, 27]. Numbers of NTM are highest
in biofilms [23, 28]. In both natural and human-engineered habitats, NTM coexist with phagocytic
protozoa and amoebae [29, 30]. Simply because humans are exposed to drinking water routinely and
regularly, it is likely that the most important source of NTM exposure for humans is drinking water,
compared to natural waters and soils.
Physiologic Traits as Determinants of NTM Distribution
NTM Hydrophobicity and Impermeability
As NTM are slow growing (i.e., generation times of 24 hr and 4 hr for slowly and rapidly
growing NTM at 37° C, respectively), they would not be expected to be successful competitors in
natural and human-engineered environments. However, they are quite good competitors and as
documented above, found in a wide variety of natural and human-engineered habitats. At least two
factors contribute to the relatively slow growth of NTM. First, NTM are surrounded by a lipid-rich
outer membrane that is quite impermeable to hydrophilic compounds [31, 32]. Second, NTM have
either one (slowly growing) or two (rapidly growing) copies of the rRNA operons [33]. Thus, NTM
growth is limited by its reduced protein-synthetic capacity. Although NTM grow slowly, their rate
of metabolism, measured by oxygen consumption, is equal to that of bacteria that grow substantially
faster [34].
The high lipid content of NTM cells (i.e., 60-70 % of cell weight principally in the outer
membrane), results in membrane impermeability [35] and the highest cell surface hydrophobicity
amongst bacteria [36]. NTM hydrophobicity and impermeability are major determinants of their
ecology (Table 3); but act as a two-edged sword. Advantages of NTM hydrophobicity and
impermeability include: resistance to disinfectants [37, 38] and heavy metals [39, 40], preferential
attachment to surfaces and air-water interfaces [18], concentration in bubbles rising in a water
column and concentration in water droplets ejected from waters [41], and ability to degrade
hydrocarbons (see below). Disadvantages of NTM hydrophobicity and impermeability include: slow
growth and reduced rates of transport of hydrophilic compounds [35].
NTM Disinfectant Resistance
NTM, for example Mycobacterium avium and Mycobacterium intracellulare, are resistant to
disinfectants commonly used in the treatment of drinking water (i.e., chlorine, chloramines, chlorine
dioxide, and ozone) [37]. NTM-disinfectant resistance is increased by growth of NTM cells in
biofilms [42]. In addition to resistance provided by layers of cells and extracellular material of NTM
cells in biofilms, biofilm growth induces adaptive resistance. M. avium cells grown in biofilms, yet
isolated from biofilms and washed and exposed to disinfectant in suspension are more disinfectant-
resistant compared to cells grown in suspension [42]. The survival of such cells is intermediate
between that of cells grown in suspension (sensitive) and of cells grown and exposed to disinfectant
in biofilms [42]. The biofilm-growth-induced resistance is adaptive based on the fact that it is lost
by growth of cells in suspension [42]. Other than determine that the adaptive resistance requires 18-
14 hours of cultivation at 37° C in suspension, no further experiments have been undertaken to
date. The slow growth rate of NTM also directly contributes to the relative resistance of NTM to
disinfectants [44]. In slowly growing cells it is more difficult to provoke lethal events by unbalancing
macromolecular synthetic events [45].
NTM Antibiotic-Resistance
NTM are resistant to a wide variety of commonly employed antibiotics; for example, the
penicillins [31, 46, 47]. That has necessitated the search for anti-mycobacterial antibiotics, many of
which have utility only against the mycobacteria; for example isoniazid (isonicotinic acid hydrazide,
INH) and ethambutol. However, most NTM are resistant to isoniazid unlike Mycobacterium
tuberculosis, which is sensitive (M. kansasii is one exception). It is likely that, as is the case for
disinfectant-resistance, that the architecture of the NTM envelope contributes to antibiotic-
resistance as well [46]. Hydrophobicity reduces the ability of antibiotics, many of which are polar, to
interact with the mycobacterial surface and envelope. The reduced permeability of antibiotics
through the outer membrane [35] also contributes to antibiotic resistance of mycobacteria. As was
the case for increased disinfectant-resistance of M. avium grown in biofilms, M. avium grown in
catheter biofilms is more resistant to antibiotics compared to suspension-grown cells [48]. It has
been suggested that as the majority of NTM cells in drinking water distribution systems [23] and
infected patients [49] are on surfaces, in vitro antibiotic susceptibility measurements ought to be
performed on biofilm-grown cells.
NTM Heavy Metal Resistance
NTM, including M. avium, M. intracellulare, and M. scrofulaceum can tolerate heavy metals such
as mercury (Hg+2), cadmium (Cd+2), and copper (Cu+2) at concentrations that are approximately 10-
fold higher than those tolerated by other bacteria [39, 40]. It is likely that one factor leading to
relative heavy metal resistant is the impermeability of the NTM envelope [46]. In addition, the
heavy metals Cu+2 and Cd+2 were found to be precipitated as sulfides and sequestered in the
envelope by a strain of M. scrofulaceum [34, 50, resp.]. Mercury (Hg+2) resistance of an M. avium strain
isolated from a mercury-polluted sediment collected from the Chester River near the Chesapeake
Bay was shown to be due to the plasmid-encoded production of mercuric reductase [51]. As the
cells containing the mercuric reductase would volatize mercury (Hg0), their presence in a habitat
would lead to reduction in Hg+2 concentrations [51]. Thus, not only would the M. avium cells survive,
but other members of the microbial community would survive.
NTM Temperature-Resistance
Nontuberculous mycobacteria are relatively resistant to temperatures that can be attained in
hot water heaters [i.e., 50° C (122° F) and 55° C (131° F)] (Table 4) [from 52]. Temperature-
resistance of M. avium, M. intracellulare, M. scrofulaceum, and M. xenopi is considerably higher than that
of Legionella pneumophila. M. xenopi, whose infections are epidemiologically linked to hot water
distribution systems [3], is the most heat-resistant among the mycobacteria. If water in a water heater
at was 50° C (122° F) had 1,000 M. avium cells/mL, it would take 50 hours to reduce the number to
1 M. avium cell/mL. At 55° C (131° F) it would take 2.7 hr and at 60° C (140° F) it would take 12
min. In contrast, if water in a water heater was at 50° C (122° F) had 1,000 L. pneumophila cells/mL,
it would take 8.25 hours to reduce the number to 1 L. pneumophila cell/mL. At 55° C (131° F) it
would take 1 hour and at 60° C (140° F) it would take approximately 5 min. Therefore, raising the
temperature of a water heater to temperatures able to inhibit the growth or kill L. pneumophila would
be insufficient to kill M. avium, M. intracellulare and M. xenopi.
Growth of NTM at Low Nutrient Concentrations
Available evidence suggests that NTM are oligotrophic; capable of growth at low nutrient
concentrations [53, 54, 55]. There are several experimental studies supporting this observation.
First, a variety of NTM species, most notably M. avium, M. intracellulare, M. chelonae, M. abscessus and
M. fortuitum have been shown to grow in drinking water [53, 54, 55]. In one study, a pilot drinking
water distribution system, it was shown that a strain of M. avium was able to grow at assimilable
organic carbon (AOC) levels as low as 50 µg/L [55]. In that study the carbon source was ozonated
humic acid. Consistent with that growth pattern is the fact that numbers of NTM correlate with
humic and fulvic acid concentrations [17] and humic and fulvic acids stimulate the growth of M.
avium in a minimal defined medium [56]. Second, numerical taxonomic studies of the NTM that
identified the carbon and nitrogen sources utilized by different NTM species grew the strains in
minimal, defined media that lacked organic carbon and nitrogen sources [57]. Notably, the strains
grew in the absence of oleic acid; a constituent of Middlebrook 7H9 broth and 7H10 agar, originally
developed for the cultivation of Mycobacterium tuberculosis [58]. However, I am aware of one exception
to the rule that NTM are not auxotrophs. Strains of M. avium and M. intracellulare form
interconvertible colonial variants, transparent and opaque [59] and only the transparent variants
require oleic acid for growth (Falkinham, unpublished observation). That oleic acid auxotrophy may
be of significance, as the transparent variants are more virulent and drug-resistant and the form most
commonly recovered from patients [60].
Metabolism of Hydrocarbons by NTM
One under-appreciated area of NTM metabolism is that NTM are capable of degrading
hydrocarbons, including chlorinated hydrocarbons. Recent reports document the presence of
hydrocarbon pollutants and other chemical contaminants in rivers used as drinking water sources
[61, 62]. A number of Mycobacterium species, including Mycobacterium tuberculosis, have been shown
capable of dehalogenation of holoalkanes [63]. This is critical as it has been shown that NTM can be
isolated from polluted dumps [20, 21]. It is likely that the participation of NTM in consortia
involved in the mineralization of pollutants has been missed in many studies because of the necessity
of incubating cultures for periods as long as 4-6 weeks. The list of hydrocarbons, chlorinated
hydrocarbons, and pollutants subject to degradation and metabolism by NTM is quite long (Table
5). Further, a number of mycobacterial strains are used to prepare cholesterol metabolites [64, 65].
As human activities lead to pollution and a number of pollutants are substrates for NTM growth
(Table 5), it follows that pollution would be expected to both stimulate the growth and select for
NTM.
Summary: Habitats Where Human Activities Influence NTM
Based on the background on the habitats and physiology of the nontuberculous
mycobacteria, I propose the hypothesis that human activities have a direct effect on NTM
populations. To support that hypothesis I provide a number of scenarios, namely habitats
influenced by humans and occupied by both humans and NTM. They are listed in Table 6. Note
that one common feature of many of these habitats is that anti-microbial agents are routinely
employed.
Scenario 1. Does Disinfection Select for NTM in Drinking Water?
Passage of the Clean Water Acts, starting in 1970 and continuing, there has been a marked
improvement in water quality across the United States [66]. Those Acts provided funds for water
treatment, including disinfection (e.g., chlorination) and have substantially contributed to reducing
numbers of water-borne diseases. Disinfection reduces the number of microorganisms and viruses
causing gastro-intestinal disease, but has little effect on mycobacterial numbers [37]. In fact,
disinfection leads to selection for mycobacteria in drinking water distribution systems [55]. In the
absence of competitors, mycobacteria have all the available carbon. Additional support for the
hypothesis that disinfection leads to NTM selection comes from a study of individuals with NTM
disease [67]. Patients whose source water was from bore holes were less likely to be infected with
NTM than individuals whose water was from piped systems [67]. A direct test for the hypothesis
could be performed by measuring NTM numbers in systems with and without disinfection. The
systems would not use groundwater: NTM are infrequently detected in groundwater [68] and NTM
are less likely to be found in household plumbing whose source of water is from wells (Falkinham,
in preparation). Quite possibly, a correlation between levels of disinfectant (e.g., chlorine) and
numbers of NTM or NTM disease in various locations might yield useful information.
Scenario 2. Do Antibiotics Select for NTM in Drinking Water?
It is well established that streams and rivers in the United States contain antibiotics [61, 62].
Further, the presence of antibiotics has been correlated with the presence of antibiotic-resistant
microorganisms [68, 69] and antibiotic-resistance genes [68, 70, 71]. The more antibiotics in the
stream water or drinking water, the more likely antibiotic-resistant bacteria and antibiotic-resistance
genes are detected [68, 69, 70, 71, 72]. As exposure of bacteria to vanadium-induced multidrug
resistance [73], it is possible that the presence of metals, particularly heavy metals, in drinking water
may induce antibiotic resistance.
Although the concentrations of antibiotics in drinking water and their sources are low and
below the minimal inhibitory concentrations necessary to inhibit growth or kill microorganisms [61,
62], evidence of the increase in frequency of antibiotic-resistance genes [68, 70, 71, 72] and
antibiotic-resistant microorganisms [68, 69] is consistent with that the low concentrations are
sufficient to selective for antibiotic-resistance [74]. Further, it is possible that selection occurs not
within the streams and rivers, but within the source of the contaminating antibiotics.
It follows that antibiotics in river and drinking waters would serve as selective agents,
promoting an increase in proportion of the antibiotic-resistant NTM at the expense of antibiotic-
sensitive members of the microbial flora. In drinking water, chlorination during water treatment has
been shown to result in an increase in the proportion of antibiotic-resistant bacteria [75]. Although
that would be a factor in selecting for antibiotic-resistant bacteria during water treatment, it would
not influence the increase in the proportion of antibiotic-resistant bacteria in drinking water sources.
Thus, antibiotics in source waters might increase the proportion of the antibiotic-resistant NTM in
drinking water sources.
Scenario 3. Are Humans Exposed to NTM in Showers, Hot Tubs, and Therapy Baths?
As a consequence of the very high cell surface hydrophobicity, particularly documented for
M. avium and M. intracellulare, NTM are readily aerosolized from water [41]. The concentration of
NTM cells in droplets ejected from waters can be as high at 10,000-fold higher than the
concentration of cells in the bulk suspension [41]. There are a number of sites where aerosolization
of NTM cells can occur. In particular, showers and hot tubs (spas) are sites where humans can be
exposed to aerosolized NTM cells. M. avium pulmonary disease was linked to M. avium exposure in a
shower [27]. There are a variety of reports linking hot tub (spa) aerosol NTM exposure to either
NTM pulmonary disease [75] or hypersensitivity penumonitis [77, 78].
In the instances cited above, a common thread is exposure to aerosols generated in closed
spaces from water-borne NTM. In addition, many of the instances of hot tub (spa) NTM aerosol
exposure have followed routine disinfection [76]. Disinfection would be expected to kill off
disinfectant-susceptible microorganisms, but leave the disinfectant-resistant NTM unaffected,
leading to their proliferation in the absence of competition.
Scenario 4. Are Workers Exposed to NTM Aerosols from Metal Recovery Fluids?
Outbreaks of hypersensitivity pneumonitis (HP) among automobile workers have been
associated with exposures to metal recovery fluids [79]. Metal recovery fluids (MRF) are often oil:
water emulsions used to cool metal-cutting or grinding tools and carry off metal particles during the
cutting and grinding of metal castings. Mycobacteria, in particular the newly described species
Mycobacterium immunogenum, have been recovered from metal recovery fluids [80]. NTM are capable
of utilizing the non-aqueous constituents of MRF, including tall oils [81]. It is likely that the MRF
concentrates that are added to water are free of NTM; the NTM sources include the water used for
mixing, as well as due to the recycling of MRF in flowing system with NTM in biofilms. In mostly
all of the outbreaks, HP has appeared after disinfectant (biocide) was added to the MRF to reduce
the growth of Gram-negative bacteria [79]. As M. immunogenum was shown to be relatively resistant
to most biocides used in disinfection of MRFs [38], it follows that biocide use may have led to the
proliferation of M. immunogenum (or other NTM) in the absence of competition.
Scenario 5. Are NTM Agents of Pollutant Degradation and Nutrient Cycling?
A number of NTM, including the rapidly growing species Mycobacterium austroafricanum,
Mycobacterium frederiksbergense, and Mycobacterium tusciae, have been detected in Belgian soils
contaminated with polycyclic aromatic hydrocarbons (PAHs) by amplification of the 16S rRNA
gene for rapidly growing mycobacteria [20]. Polluted sites in Japan yielded isolates of Mycobacterium
austroafricanum, Mycobacterium chubuense, Mycobacterium chlorophenicolicum, Mycobacterium frederiksbergense,
Mycobacterium mageritense, and Mycobacterium vanbaalenii [21]. It is likely that the ubiquitous water-borne
slowly growing Mycobacterium species such as M. avium were also present, but either undetected [20]
or not isolated due to insufficient time for colony development [21].
Although underappreciated, NTM are capable of degrading a wide range of pollutants,
including a number of organic wastewater contaminants found in U.S. streams, including:
anthracene, benzo[a]pyrene, fluoranthene, naphthalene, phenanthrene, phenol, pyrene, and
tetrachloroethylene [61, 62]. A list of organic pollutants degraded by NTM are listed in Table 5. In
addition to the degradation of pollutants, a substantial proportion of Mycobacterium species, including
Mycobacterium tuberculosis and the major water-borne pathogens Mycobacterium avium, Mycobacterium
chelonae, Mycobacterium kansasii possess haloalkane dehalogenase activity [63]. Cholesterol, another
organic wastewater contaminant found in U.S. streams [61, 62] is subject to NTM metabolism and
transformation. In fact, NTM are used in industrial production of some cholesterol derivatives [64,
65].
It is likely that NTM hydrophobicity contributes to their ability to metabolize organic
wastewater contaminants; the majority of which are non-polar and partition in the organic phase.
One reason for the lack of appreciation for the role of NTM in nutrient cycling and degradation of
organic wastewater contaminants is their slow growth. Most surveys of microorganisms responsible
or involved in pollutant degradation fail to incubate media for enough time for the appearance of
NTM colonies. Thus, NTM haven’t been detected as members of pollutant-degrading microbial
consortia.
Scenario 6. Have Humans Activities Resulted in the Disappearance of Mycobacterium
scrofulaceum?
Before approximately 1985, M. scrofulaceum was the predominant mycobacterium isolated
from cervical lymph nodes in children suffering from cervical lymphadenitis [8]. However, since
1985, Mycobacterium avium has been isolated almost exclusively from children with cervical
lymphadenitis [8]. M. scrofulaceum has disappeared; it is seldom recovered from pulmonary patients
and not isolated it from drinking water. In surveys of natural waters (e.g., streams, ponds, rivers,
and lakes) performed from 1975-1983, we recovered M. scrofulaceum [15]….but no more [22, 23, 25].
We have only isolated M. avium and Mycobacterium intracellulare, but never M. scrofulaceum and have not
altered the isolation regimen. The only published M. scrofulaceum isolations are from untreated water
and patients exposed to untreated water [67].
Why has M. scrofulaceum disappeared? M. scrofulaceum grows significantly faster than either M.
avium or M. intracellulare. Therefore, in untreated water, M. scrofulaceum is the predominant
mycobacterium. However, M. scrofulaceum is significantly more susceptible to chlorine and other
disinfectants used in water treatment [37]. As M. avium, M. intracellulare, and M. scrofulaceum occupy
many of the same environments, chlorination (brought about by the Clean Water Acts) killed off M.
scrofulaceum , such that its habitats are now occupied solely by M. avium and M. intracellulare.
Future Perspective
The overlap between the habitats shared by nontuberculous mycobacteria (NTM) and
humans, demonstrates that human behaviors (e.g., disinfection and transmission of water, and
generation of aerosols), select for the proliferation and transmission of NTM. Current examples of
human influences on NTM ecology and epidemiology suggest that the incidence of NTM disease
will continue to increase. Although the review focuses on NTM, it is anticipated that human
behaviors may be selecting for proliferation and transmission of other microorganisms.
Executive Summary
Nontuberculous mycobacteria (NTM) are opportunistic pathogens of humans and animals
whose source is the environment. In addition to the natural environment (e.g., soils and waters),
NTM are normal inhabitants of environments where they can come in contact with humans and
animals; namely their habitats overlap. Importantly, a number of human behaviors, such as
disinfection and transmission of drinking water lead to increased numbers of NTM. Others, such as
the generation of aerosols in either households or industry, lead to increased transmission of NTM
to humans. These increases are due to the fact that NTM cells grow at low carbon concentrations
and are hydrophobic. Hydrophobicity leads to disinfectant-resistance and preferential aerosolization
and attachment to pipe surfaces. Attachment leads to formation of biofilms leading to further
increases in disinfectant-resistance. Discovery that human behaviors lead to selection and
proliferation of NTM in habitats occupied by both humans and NTM, creates the dilemma that
human actions taken to reduce pathogen exposure (i.e., water disinfection), lead to possible
increased NTM disease; an unforeseen consequence.
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Financial Disclosure
The author has no conflict of interest.
Acknowledgements
Investigations in the author’s laboratory have been supported by the NonTuberculous Mycobacteria
Information and Research Foundation (NTMir, Inc.), the American Water Works Association
Research Foundation (AWWARF, now the Water Research Foundation, WRF), the National
Institutes of Allergy and Infectious Diseases, and the United States Council for Automotive
Research (USCAR).
Table1. NTM of Medical Importance.
Mycobacterium species
Mycobacterium avium and Mycobacterium intracellulare (M. avium complex, MAC)
Mycobacterium kansasii
Mycobacterium malmoense
Mycobacterium xenopi
Mycobacterium ulcerans
Mycobacterium fortuitum
Mycobacterium abscessus
Mycobacterium chelonae
(Marras and Daley, 2002) [5].
Table 2. Habitats Occupied by NTM
Habitats Reference(s)
Natural Waters [15]
Natural Aerosols [18]
Drinking Water Distribution Systems [22, 23]
Household Plumbing [26, 27]
Spas and Hot Tubs [75]
Aerosols in Showers [27]
Metal-Recovery Fluid [77]
Soils [16, 19]
Potting Soils [19, 81]
Waste Dumps [20, 21]
Table 3. Advantages and disadvantages of NTM Hydrophobicity
Advantages Disadvantages
Disinfactant- Antibiotic- and Low Permeability to Hydrophilic Nutrients
Heavy Metal-Resistance Low Transport Rates of hydrophilic Nutrients
Surface Attachment = Reduced Washout Slow Growth
Slow Growth = Anti-microbial Resistance
Aerosolization
Hydrocarbon Degradation
Table 4. Time (in minutes) necessary to kill 90 % of different species of Mycobacterium and Legionella
pneumophila at temperatures relevant to those attained in hot water heaters in households or boilers in
buildings [52].
Mycobacterium spp. or 50° C (122° F) 55° C (131° F) 60° C (140° F)
Legionella pneumophila
M. avium 1,000 min 54 min 4 min
M. intracellulare 550 min 24 min 1.5 min
M. scrofulaceum 934 min 61 min 5.3 min
M. kansasii 77 min 6.6 min 0.7 min
M. marinum 75 min 13 min 1 min
M. xenopi No Killing in 48 hr 346 min 33 min
M. chelonae 169 min 23 min 4.3 min
M. fortuitum 100 min 25 min 3.7 min
Legionella pneumophila 165 min 17 min 1.8 min
Table 5. Organic Wastewater Contaminants Degraded by NTM
Contaminant a Mycobacterium Strain(s) Reference
Anthracene Mycobacterium sp. strain PYR-1 [82]
Benzo[a]pyrene Mycobacterium sp. strain PYR-1 [82]
Cholesterol Mycobacterium sp. strains DP and
ATCC 29472 [64]
Fluoranthene Mycobacterium sp. strain PYR-1 [82]
Mycobacterium sp. strain CH-1 [83]
Naphthalene Mycobacterium convolutum ATCC 29673 and
Mycobacterium vaccae JOB5 [84]
Phenanthrene Mycobacterium sp. strain PYR-1 [82]
Mycobacterium sp. strain CH-1 [83]
Phenol Mycobacterium vaccae strain JOB5 [85]
Pyrene Mycobacterium sp. strain PYR-1 [82]
Mycobacterium sp. strain CH-1 [83]
Tetrachloroethylene Mycobacterium vaccae strain JOB5 84]
a [61, 62]
Table 6. Habitats where Human Activities Influence NTM
Habitat Human Influence
Drinking Water Distribution Systems (1) Disinfection kills competitors
(2) Nutrient removal favors oligotrophs
(3) Biofilm formation supports growth and persistence
Household Plumbing (1) Heated water favors NTM growth
(2) Hot Water Temperatures favor NTM
(3) Biofilm formation in hot water heater
Household Showers (1) Showerhead collects particulates
(2) Showerhead biofilm formation
(3) Efficient generation of NTM-enriched aerosols
Hot tubs and Spas (1) Organic contamination reduces disinfectant concentration
(2) Efficient generation of NTM-enriched aerosols
Food Baths (1) Organic contamination reduces disinfectant concentration
Metal Removal Fluid (1) MRF constituents support NTM growth
(2) Biocides kill NTM competitors
(3) MRF organics reduce biocide concentration
(4) High velocity spray generates NTM-enriched aerosol