The International Journal of Mycobacteriology

: 2020  |  Volume : 9  |  Issue : 4  |  Page : 347--362

Hospital ice, ice machines, and water as sources of nontuberculous mycobacteria: Description of qualitative risk assessment models to determine host–Nontuberculous mycobacteria interplay

Beverley Cherie Millar, John Edmund Moore 
 Laboratory for Disinfection and Pathogen Elimination Studies, Northern Ireland Public Health Laboratory, Nightingale (Belfast City) Hospital, Belfast, Northern Ireland, UK

Correspondence Address:
John Edmund Moore
Laboratory for Disinfection and Pathogen Elimination Studies, Northern Ireland Public Health Laboratory, Nightingale (Belfast City) Hospital, Lisburn Road, Belfast, BT9 7AD, Northern Ireland


Over the last 30 years, there have been at least 17 published reports of nontuberculous mycobacteria (NTMs) being isolated from hospital ice or ice-making machines. Of these, 12 were reports of pseudo-outbreaks, i.e., the nosocomial transmission of organism from hospital ice/ice machines to patients, resulting in patient colonization, but with no disease manifestations. In addition, there were five outbreaks that resulted in clinical disease/pathology associated with NTM organism. Eleven different species of NTMs have been associated with these reports, where over half (59%) of the species identified were Mycobacterium fortuitum (18%), Mycobacterium gordonae (14%), Mycobacterium mucogenicum (14%), and Mycobacterium porcinum (14%). Several of these reports clearly documented that ice machines had been properly maintained, cleaned, and serviced in accordance with the CDC guidelines yet became contaminated with NTM organisms. These reports frequently detail that after extensive cleaning/disinfection following the discovery of NTM organisms, ice machines remained contaminated with NTM organisms, highlighting the difficulty in eradicating these from ice machines, once contaminated. Several reports identified that the only remedy to the contamination problem was to replace the ice machine with a new machine. Two qualitative risk assessment models are presented for (i) patients exposed to contaminated ice machine but before NTM colonization/infection and (ii) patients already colonized with NTMs from ice machines. Therefore, to protect immunocompromised/immunosuppressed patients' safety, especially during surgical or respiratory procedures, ice should not be sourced from the ice machine but should be made from sterile water and stored safely and separately away from the ice machine.

How to cite this article:
Millar BC, Moore JE. Hospital ice, ice machines, and water as sources of nontuberculous mycobacteria: Description of qualitative risk assessment models to determine host–Nontuberculous mycobacteria interplay.Int J Mycobacteriol 2020;9:347-362

How to cite this URL:
Millar BC, Moore JE. Hospital ice, ice machines, and water as sources of nontuberculous mycobacteria: Description of qualitative risk assessment models to determine host–Nontuberculous mycobacteria interplay. Int J Mycobacteriol [serial online] 2020 [cited 2021 Jan 23 ];9:347-362
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Full Text


Nontuberculous mycobacteria (NTMs) have now emerged as important opportunistic bacterial pathogens, particularly among immunocompromised hosts.[1],[2] Current estimates indicate that NTM-related infections now supersede disease associated with Mycobacterium tuberculosis (MTB),[3] which is estimated to cause 10 million new cases of tuberculosis every year.[4] NTM organisms are found primarily in the natural environment, particularly in soil and water sources. However, changing social demographic patterns of housing, use of water, movement of people, travel, and employment are the factors that maybe increase the association between humans and the risk of them acquiring an environmental NTM, which may progress to disease.[5] Clinically, these NTM organisms present several challenges including clinical and laboratory diagnosis, as well as a treatment dilemma, due to high levels of antimicrobial resistance.

The increasing incidence of NTM-related disease has now become well established globally. Several factors have been associated with the etiology of the disease, including (i) an aging population, (ii) an increase in levels of immunosuppression due to increased employment of biologics, immunosuppressive therapies, and steroids, (iii) an increase in populations of immunocompromised individuals, including those with HIV and AIDS, (iv) macrolide antibiotic usage, and (v) medical tourism. For a seminal review on the factors responsible for driving this increase in NTM clinical cases, please see Rivero-Lezcano et al.[6]

The genus, Mycobacterium, currently consists of 205 species, with a validly published name, including synonyms, constituting (i) the MTB complex consisting of MTB, Mycobacterium africanum, Mycobacterium bovis, Mycobacterium microti, and Mycobacterium canetti; (ii) Mycobacterium leprae and Mycobacterium lepromatosis; and (iii) the NTM. Sometimes, the NTMs are referred to as “environmental mycobacteria,” “atypical mycobacteria,” and “mycobacteria other than tuberculosis.” Historically, the genus Mycobacterium was a sole genus within the family Mycobacteriaceae, but recently in 2018, there were radical changes to the taxonomical organization within this family to now include an additional seven genera,[7] now including Bactoderma, Mycobacterium, Mycobacteroides, Mycolicibacillus, Mycolicibacter, Mycolicibacterium, and Stibiobacter. The development of improved molecular technologies and bioinformatics and the adoption of whole-genome sequencing to more isolates have allowed for a re-analysis of the existing taxa within the genus Mycobacterium. In 2018, Gupta et al.[7] proposed an amended genus encompassing the “Tuberculosis-Simiae” clade, which includes all of the major human pathogens, and four novel genera, viz., Mycolicibacterium gen. nov., Mycolicibacter gen. nov., Mycolicibacillus gen. nov., and Mycobacteroides gen. nov., corresponding to the “Fortuitum-Vaccae,” “Terrae,” “Triviale,” and “Abscessus-Chelonae” clades, respectively.[7]

 Hospital Ice, Hospital Ice Machines, and Water as a Source of Nontuberculous Mycobacteria

Hospital ice machines are a source of bacteria and yeasts.[8] NTMs are commonly isolated from a wide variety of water sources. [Table 1] lists recently documented reports of NTM in a variety of waters, including potable water, as well as in water systems. [Table 2] details recent healthcare-associated infections, outbreaks, and pseudo-outbreaks associated with NTMs and water. [Table 3] gives the details of NTM organisms isolated from water in the community and [Table 4] details hospital ice and hospital ice machines as the etiological sources of outbreaks and pseudo-outbreaks in patients with NTM organisms. There have been at least 17 published reports of NTM organisms being isolated from hospital ice, hospital ice water, or hospital ice machines. Of these, 12 were reports of pseudo-outbreaks, i.e., the nosocomial transmission of organism from hospital ice/ice machine to patients, resulting in colonization, but with no pathology or disease manifestations. In addition, there were five outbreaks that resulted in true clinical disease/pathology associated with an NTM organism. Eleven different species of NTMs have been associated with these reports [Figure 1], where over half (59%) of the species identified were Mycobacterium fortuitum (18%), Mycobacterium gordonae (14%), Mycobacterium mucogenicum (14%), and Mycobacterium porcinum (14%). Therefore, approximately 2.4% of the described species within the genus Mycobacterium have now been associated with documented contamination of hospital ice and ice machines.{Table 1}{Table 2}{Table 3}{Table 4}

Ice is commonly used in the hospital setting for a wide variety of applications, and it is estimated that daily ice requirement is approximately 5 kg per patient per day ( [Table 5] lists 20 indications where ice may be employed in procedures or as therapies, indicating the range of patient types that may be exposed to ice and water from ice.{Figure 1}{Table 5}

The isolation of NTM organisms from hospital ice and the related ice machine creates a dilemma for clinicians, healthcare professionals, and infection-prevention specialists. Events relating to the ice machine becoming culturally positive for NTM organisms may manifest as three possible scenarios:

Ice machine becomes chronically colonized with NTM organisms with no associated increase in positivity in clinical specimens over extended periods of timeEpidemiological surveillance highlights an increase in the positivity of NTM organisms, similar to the strain found in the ice machine in patients' specimens, without any associated pathology/disease in these patients (pseudo-outbreak)NTM organisms are found in clinical specimens from patients with NTM clinical disease, with similar genotypic characteristics to the ice machine strain (true outbreak).

While scenario iii will ultimately emerge as patients present with NTM-related disease, informative surveillance systems will intercept scenarios i and ii at an early stage, thereby giving early insight to potential clinical problems downstream. However, how do you decide how clinically significant finding NTMs in the ice machine is and the risks this poses to your patient cohort?

Risk assessment model A (before patient colonization/infection)

We present a color-coded qualitative risk assessment model [Figure 2] to help estimate the various variables between host and NTM that may influence the potential of NTM organisms from ice machine manifesting in clinical disease.{Figure 2}

The model is composed of four intersecting variables as illustrated in this Venn diagram [Figure 2]. These variables consist of:

Host factors: What is the immune status of the patient? Contributing factors here include level of immunosuppression (steroid usage, chemotherapy resulting in profound neutropenia in the case of hematological malignancy, posttransplant status, use of biologics, etc.), if immunocompromised (age, HIV/AIDS, CD4 count, hypogammaglobulinemia, asplenic, etc.), genetic susceptibility, and HLA typeNTM virulence factors: Not all NTMs have equal potential for causing disease in hosts. This is demonstrated by only a narrow range of those NTMs found in ice machines actually manifesting in true pathology. Future studies should target the power of whole-genome sequencing techniques to identify the virulence determinants in environmental NTM organisms, thereby allowing a prediction of potential NTM disease pathophysiology in the host. Accumulation and identification of several genetic virulence markers may predict the presence of a virulent strain of NTM with an unfavorable disease pathNTM environmental persistence factors: NTM organisms may become persistent in the environment, such as in an ice machine, due to their production of biofilm and other physiological adaptations to promote environmental survival, including resistance to biocides and disinfectantsNTM antibiotic resistance factors: NTM organisms are considered resistant to several classes of antibiotics. An NTM organism with high level of in vitro antibiotic resistance may therefore be difficult to treat successfully with antibiotics, which may influence the clinician's clinical approach and the threshold and staging of therapeutic intervention.

The greatest risk (Level 4 Red) is where all four risk variables interplay and where the potential risk of the NTM manifesting in related disease in the patient is highest. Clinicians should carefully risk assess these scenarios with a view to therapeutic intervention. In the descending order of risk, Level 3 Orange is where three risk factors intersect, Level 2 Yellow is where two risk factors combine, and Level 1 Green is where there is a single or isolated risk factor. The model has purposefully not attributed quantitative risk of NTM exposure to a patient, nor any weighting to any of the four risk variables, but simply wishes to help clinicians in qualitatively identifying the variables that are likely to lead to potential NTM infection, which may be mitigated by early intervention with anti-NTM antibiotic regimens.

Risk assessment model B (on-patient colonization with nontuberculous mycobacteria)

[Table 6] highlights eight criteria that may help in deciding how clinically significant finding NTM from the ice machine (or other environmental source) in patients' respiratory secretions and helping to decide whether to treat or not to treat, or to alternatively adopt a “wait-and-see” policy, before initiating any antibiotic intervention.{Table 6}

 Maintenance of Hospital Ice Machines

Several of these reports clearly documented that ice machines had been properly maintained, cleaned, and serviced in accordance with the CDC guidelines [Table 7][112] yet became contaminated with NTM organisms [Table 4]. Hence, how do hospital ice machines become and stay contaminated with NTM organisms? [Table 1] details how NTM organisms may contaminate potable water distribution systems that supply hospital ice machines. NTM organisms are ubiquitous in nature and may easily enter ice machines from other exogenous sources. Previous reports demonstrated that dust and air conditioners were contaminated by NTM organisms,[119] which may enter when the chest door is open, when collecting ice. In addition, the nonhygienic collection of ice by the handler may allow for the contamination of ice due to NTM organisms being deposited from poorly sanitized hands. M. gordonae, Mycobacterium avium, and M. avium complex organisms were recently isolated from stools in clinically significant cases,[120] as well as being described as a component of the gut in certain chronic intestinal inflammatory disease states, including Crohn's disease.[121] Thus, NTMs may enter the ice machine via water, via plumbing systems, or via exogenous contamination through dust or from human handling of ice scoops. Once NTM organisms have entered the ice machine, they may persist due to the microbiological reasons detailed below.{Table 7}

Once established, subsequent removal of surviving NTMs may be difficult to achieve. The control interventions detailed in the CDC guidelines may not be of sufficient lethality to eradicate contaminating NTM organisms, which have now become endemic in the ice machine. Routine maintenance of the ice machine as described [Table 7] may be able to eradicate nonmycobacterial organisms on account of these Gram-positive and Gram-negative organisms, having a biology making them susceptible to the control measures detailed, but previous reports highlight that such interventions are not effective for NTM organisms [Table 4]. This is not surprising as NTM organisms are noted for their resistance to several biocides. In a recent study,[122] the effect of several hospital biocides on pulmonary Mycobacterium abscessus isolates was examined. Seven commonly employed hospital biocides with generic ingredients as follows: acetone, propan-2-ol, diethylene glycol, 5-chloro-2-methyl-4-isothiazolin-3-one and 2-methyl-4-isothiazolin-3-one, chlorine dioxide, 4% chlorhexidine, alcohol, and disodium carbonate, compound with hydrogen peroxide, 10% sodium hypochlorite were assayed for their biocidal activity against M. abscessus. Fresh cultures of M. abscessus were exposed to biocide in liquid medium as per the manufacturers' instruction and were immediately plated following the completion of the contact period. All M. abscessus isolates survived in alkyl dimethyl benzyl ammonium chloride, 5-chloro-2-methyl-2H-isothiazol-3-one (EC No. 247-500-7) and 2-methyl-2H-isothiazol-3-one, 4% chlorhexidine™, O-phenylphenol and sodium lauryl sulfate™ and disodium carbonate, compound with hydrogen peroxide. One strain of M. abscessus was killed by chlorine dioxide™ and one by sodium dichloroisocyanurate™, representing a 5-log kill. Two isolates were killed by Alcohol™ again representing a 5-log kill. Following enrichment, O-phenylphenol and sodium lauryl sulfate™ showed the greatest biocidal activity with 11/13 isolates, whereas 2/13 cultures were killed by sodium dichloroisocyanurate™. All other biocide/culture combinations yielded growth, indicating that M. abscessus may persist after exposure to several common hospital biocides.[122]

Commercial ice-making machines are relatively simple in design consisting of a cooling/refrigerant unit, a mains water supply, and a collection chamber for the ice, all which is enclosed in a stainless steel casing with an open/close lid. Mains water flows into the unit and is slowly deposited over a metal evaporator unit, in the shape of multiple cuboid cells, hence the shape of the resulting ice cubes. The metal cells are fused to copper coils that form part of the recirculating cooling/refrigerant unit, which draws heat from the water and allows the water to slowly freeze over time in a continuous process, within the cuboid cell. Heat from the water is dissipated through the recirculating cooling/refrigerant unit utilizing fans to exhaust excess heat to the environment. The engineering design problem with such systems is that all components of the ice-making machine in contact with water, namely, the intake tubing/pipework, the evaporator unit, or the ice collection bin, are detachable that would allow access for remote cleaning and disinfection. Thus, all cleaning and disinfection procedures are required to be carried out in situ. Where inaccessible areas remain, these areas evade these interventions, resulting in residual survival of NTM organisms for the reasons described below.

Hyperchlorination is not an effective long-term control measure for mycobacteria residing in healthcare premise plumbing.[123] In their study, which also examined point-of-use membrane filters in the waterline with a new ice machine, over a 24-week study period, Mycobacterium chelonae and two unknown species of NTM were identified and enumerative counts of rapidly growing mycobacteria increased from nondetection (<7 colony forming units [cfu]/L) at 12 weeks to 1.52, 1.84, and 2.54 log10 cfu/L at 16, 20, and 24 weeks, respectively, indicating that membrane filtration cannot be considered an absolute control intervention for NTM in ice machines. Successful methods for the elimination of NTM organisms from hospital ice machines are a shared problem in the decontamination of hospital equipment from NTM organisms involving water. Heater/cooler units employed in cardiopulmonary bypass also suffer from inadequate eradication of Mycobacterium chimaera. Extensive cleaning and disinfection regimens of these units have included a monthly disinfection with 2% tosylchloramide sodium and water changes biweekly, supplemented with a weekly treatment with 2% chloramine-T for the entire water volume of the device, as well as treatment of the system with 5% chloramine-T solution for 24 h, if NTMs are found, with the inclusion of a 0.2 μm terminal water filter. A recent Italian study demonstrated that NTMs were detected in both predisinfection (50.1%) and postdisinfection (55.7%) samples and concluded that manufacturer's procedures for disinfection were ineffective and/or inadequate.[124]

Therefore, technological innovations are urgently required to eliminate NTMs from hospital ice machines. This is a priority so that absolute controls may be designed into the fabrication of units, thus ensuring elimination of all residual NTM organisms.

Given the refractive nature of NTM organisms to extensive and enhanced disinfection procedures, there is no absolute certainty that the current disinfection protocols for NTMs in hospital ice machines will eliminate all NTM organisms, thereby creating the hazard of NTM contamination of ice, with the sustained risk of its occurrence/recurrence, even after ice machine disinfection. Therefore, to protect immunocompromised/immunosuppressed patients' safety, especially during surgical or respiratory procedures, ice should not be sourced from standard ice machines but should be made from sterile water and stored safely and separately away from the ice machine. For provision of sterile ice for such purposes, clinicians and other healthcare professionals should therefore discuss their requirements for sterile ice with their hospital pharmacy department.

 Factors That Contribute to Nontuberculous Mycobacteria Persistence in Hospital Ice Machines

Cell wall structure and related architecture

Mycobacterium spp. are unique in nature that they have a highly unusual cell wall structure, which differ from conventional Gram-positive and Gram-negative bacteria and represent one of the most complicated architectural structures within the prokaryotes. In addition, this hydrophobic cell wall structure aids their resistance to several antibiotics. Mycobacterial cell walls are dominated by lipids and carbohydrates that provide a permeability barrier against hydrophilic drugs and are crucial for its survival and virulence. The cell wall consists of (i) a cell membrane, (ii) periplasm, (iii) peptidoglycan layer, (iv) arabinogalactan layer, (v) mycobacterial outer membrane consisting of mycolic acids, glycolipids, and free lipids, and (vi) a capsule consisting of α-glucans and arabinans, as well as capsular proteins and lipids. The richness of lipids in its cell wall architecture may provide NTM with a mechanism to maintain cell wall fluidity under ice storage conditions, thereby aiding its tolerance to freezing.

Slow growth and dormancy

Characteristic slow growth associated with the NTM organisms allows them to adapt to unfavorable and stressful conditions, thus making them less susceptible to antibiotics and disinfectants. Investment of energy by the NTM organisms away from cell replication/multiplication into long-chain lipid outer membrane synthesis confers environmental survival advantages that allow the persistence of the organism in harsh conditions, which many other Gram-positive and Gram-negative organisms would be unable to tolerate.[1] Dormancy is well described for MTB but not so for the NTMs.[125] The ability of NTM to enter a phase of metabolic dormancy is important to aid their survival, during times of environmental stress, particularly nutrient depletion and starvation. While mycobacterial organisms do not have the ability to be fully protected against such extreme environmental stresses through the production of endospores, they have been shown to have protective mechanisms that they may utilize, including formation of the viable but nonculturable (VBNC) state. The VBNC phase has been described with Mycobacterium smegmatis when grown under suboptimal conditions, resulting in a reduced growth rate or maximal cell concentration; the organism entered the VBNC phase after 3–4 days incubation in stationary phase.[126] It remains unclear if any of the other NTM organisms can utilize this VBNC phase as a means to survive in harsh environmental conditions, such as in ice machines.

Biofilm formation and quorum sensing

NTM organisms are noted for their ability to form biofilm-like structures, on account of their high surface hydrophobicity.[1] Hydrophobic interactions between fatty acid tails of the glycopeptidolipids of NTM and the hydrophobic solid surface enable attachment to surfaces and biofilm formation.[127]

Intracellular survival in ameba

NTM organisms have the ability to survive phagocytosis with protozoa in a similar manner to how MTB and other pathogenic mycobacteria can evade lytic activity of lysosomes and macrophages. Within protozoa, NTM organisms may grow as endosymbionts and such relationships with protozoa confer important protective properties against environmental stresses, including dehydration and the ability to stay protected intracellularly within the protozoa, thus evading surface disinfectants and biocides.[1]

Overall, this review has shown that NTM organisms are bacterial experts at adaptation at the environment/anthropogenic interface, namely in an ice machine. The NTM organisms possess several characteristics which make them the ideal environmental persister. This review has shown that NTM organisms may be a bacterial contaminant of hospital ice machines, with potential for downstream nosocomial patient colonization, resulting in either pseudo-outbreaks, or less commonly, in true clinical outbreaks. Given the emergence of the hospital-at-home service, the role of domestic freezers and ice-making facilities in the home merits further scrutiny as there is a paucity of data detailing the occurrence of microbial contaminants of domestic ice and domestic freezers, including data on the occurrence of NTM in these domestic environments. There are however limited data showing that fresh and frozen foods may be heavily contaminated with NTM organisms,[128] which may be frozen as part of their preservation, with the potential risk of cross-contaminating the freezer environment which such foodstuffs share with domestic ice-making facilities. Therefore, future research should address the risks to patients who require ice as part of their hospital-at-home clinical care.


Over the last 30 years, there have been at least 17 published reports of NTMs being isolated from hospital ice or ice-making machines. Of these, 12 were reports of pseudo-outbreaks, i.e., the nosocomial transmission of organism from hospital ice/ice machines to patients, resulting in patient colonization, but with no disease manifestations. In addition, there were five outbreaks which resulted in clinical disease/pathology associated with the NTM organism. Eleven different species of NTMs have been associated with these reports, where over half (59%) of the species identified were M. fortuitum (18%), M. gordonae (14%), M. mucogenicum (14%), and M. porcinum (14%). Several of these reports clearly documented that ice machines had been properly maintained, cleaned, and serviced in accordance with the CDC guidelines yet became contaminated with NTM organisms. These reports frequently detail that after extensive cleaning/disinfection following discovery of NTM organisms, ice machines remained contaminated with NTM organisms, highlighting the difficulty in eradicating these from ice machines, once contaminated. Several reports identified that the only remedy to the contamination problem was to replace the ice machine with a new machine. Two qualitative risk assessment models are presented for (i) patients exposed to contaminated ice machine but before NTM colonization/infection and (ii) patients already colonized with NTMs from ice machines. Therefore, to protect immunocompromised/immunosuppressed patients' safety, especially during surgical or respiratory procedures, ice should not be sourced from the ice machine but should be made from sterile water and stored safely and separately away from the ice machine.

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