Nontuberculous mycobacteria in drinking water systems – the challenges of characterization and risk mitigation

doi:10.1016/j.copbio.2019.03.010

Current Opinion in Biotechnology

Volume 57, June 2019, Pages 127-136

https://doi.org/10.1016/j.copbio.2019.03.010 Get rights and content

Highlights

•
Nontuberculous mycobacteria (NTM) are pervasive in drinking water systems.
•
NTM are resistant to disinfection and are found in pipe and showerhead biofilms.
•
Inhalation and/or aspiration of drinking water might cause NTM pulmonary infections.
•
Improved infection reporting is needed to better characterize NTM health burden.
•
Linking NTM infections to water sources is difficult and requires further study.

Nontuberculous mycobacteria (NTM) pulmonary infections are a growing concern worldwide, with a disproportionate incidence in persons with pre-existing health conditions. NTM have frequently been found in municipally-treated drinking water and building plumbing, leading to the hypothesis that an important source of NTM exposure is drinking water. The identification and quantification of NTM in environmental samples are complicated by genetic variability among NTM species, making it challenging to determine if clinically relevant NTM are present. Additionally, their unique cellular features and lifestyles make NTM and their nucleic acids difficult to recover. This review highlights a recent work focused on quantification and characterization of NTM and on understanding the influence of source water, treatment plants, distribution systems, and building plumbing on the abundance of NTM in drinking water.

Graphical abstract

Introduction

Infections due to opportunistic pathogens (OPs) are a growing public health concern. OPs generally only infect susceptible persons, including those with pre-existing health conditions and the immunocompromised. Like other water-associated OPs such as Legionella pneumophila and Pseudomonas aeruginosa, nontuberculous mycobacteria (NTM) are present in the environment and can proliferate in drinking water systems. NTM possess waxy, ‘acid-fast’ cell walls, which render them more hydrophobic and might allow them to be more readily aerosolized than other bacteria [1]. Sometimes called ‘biofilm pioneers’, NTM can attach to a variety of surfaces and establish biofilms, and are among select bacteria with the ability to enter and survive within amoebae [1,2]. This combination of properties confers the resistance needed to survive conventional water treatment and proliferate in drinking water systems despite the presence of disinfectant residuals [1].

NTM predominately cause pulmonary infections but also cause skin, soft tissue, and post-operative infections [3, 4, 5, 6]. A 2012 study estimated the annual cost of hospitalizations in the U.S. due to pulmonary NTM infections to be $194 million [7]. NTM infection prevalence has increased over the last two decades. Specifically, positive specimen reporting rates in four U.S. states increased from 8.2 to 16 per 100 000 persons from 1994 to 2014, and rates in England, Wales, and Northern Ireland rose from 0.9 to 7.6 per 100 000 persons from 1995 to 2012 [8^•,9,10^•]. However, the true prevalence of NTM infection is unknown and challenging to determine due to the lack of reporting requirements and difficulties with NTM identification from clinical specimens.

Despite the health and economic importance of NTM infections, little is known about specific sources of human exposure to NTM. Recent work has found NTM in drinking water and water system biofilms, suggesting that contact with drinking water might be one source of pulmonary infections [11,12^•]. However, substantial knowledge gaps, including the lack of risk assessment models, difficulty in evaluating mechanisms of exposure, and host-specific factors that influence susceptibility, have made it difficult to link NTM infections to drinking water and develop mitigation strategies. Given the recent increases in NTM infections, it is paramount that we:

a)
understand the sources and routes of NTM exposure;
b)
identify the risk factors associated with NTM infections; and
c)
develop risk mitigation strategies to reduce NTM infection.

This review focuses on recent efforts to characterize NTM transfer from natural environments to human hosts through drinking water.

Section snippets

Identification of NTM and their characteristics

The genus Mycobacterium consists of more than 170 species [13, 14, 15]. The vast majority of these species comprise the so-called ‘nontuberculous mycobacteria’, of which only a few account for most human NTM infections [8^•,16]. Examples of NTM often associated with infection are the Mycobacterium avium complex (MAC, which includes M. avium, Mycobacterium intracellulare, and Mycobacterium chimaera), the Mycobacterium abscessus complex (MAB, which includes M. abscessus subsp. massiliense, M.

NTM in source waters used for drinking water production

Regional clustering of pulmonary NTM infections has led to investigations of links between NTM infection and geographic and environmental factors, including characteristics of source waters used for drinking water production. An analysis of NTM infections in Medicare patients in the U.S. found 55 counties in eight states with clusters of infection, and the two counties with the highest risk were located in Louisiana and Hawaii [24]. Geographic factors that correlate with elevated NTM infection

NTM survival through drinking water treatment processes

M. avium has been a potential concern in drinking water for decades and has been included on all U.S. Environmental Protection Agency Contaminant Candidate Lists. Nevertheless, NTM monitoring and reporting for drinking water is not required in the U.S. or other countries. This lack of surveillance has limited the evaluation of NTM removal through treatment systems. Much of the NTM-related drinking water research thus far has focused on NTM inactivation through disinfection. Pure cultures of M.

NTM in distribution systems and building plumbing

Approximately 90% of the U.S. population receives drinking water treated in centralized treatment plants (U.S. Environmental Protection Agency; www.epa.gov/ground-water-and-drinking-water/safe-drinking-water-information-system-sdwis-federal-reporting). Treated water is transported through underground distribution systems and storage tanks, reaching consumers through building plumbing. Although utilities in the U.S. and many other countries provide a disinfectant residual to control microbial

Routes of exposure and infection

Studies have repeatedly shown that rates of NTM pulmonary infection around the world are increasing. While the reasons for this rise are unclear, increased exposure to NTM might be a contributing factor [59]. Linking NTM infections to a particular source is challenging and is complicated by often long periods of time between NTM exposure and diagnosis, lack of standardized methods for strain genotyping, and the pervasiveness of NTM in the environment. The most probable routes of NTM pulmonary

Future work

Although our ability to detect and identify NTM has greatly improved over the last two decades, little is known about how the observed concentrations of various NTM in drinking water correlate to the disease burden. As shown in Figure 3, considerable work is needed to assess how various exposure mechanisms, concentrations of NTM, and host-specific factors contribute to risk of pulmonary infection. Aerosolization of NTM is in particular need of additional investigation given the hypothesis that

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

The authors would like to thank Terese Olson, Amy Pruden, Dongjuan Dai, and Linda Kalikin for helpful discussions. This research was supported with funding from the Water Research Foundation (Project #4721) and the Cystic Fibrosis Foundation (LIPUMA15G0). Katherine Dowdell was supported by a National Science Foundation Graduate Research Fellowship under Grant No. DGE 1256260 and a NWRI-BioLargo Fellowship for Water Science Research. Sarah-Jane Haig was supported by an Alfred P. Sloan Foundation

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Nontuberculous mycobacteria in drinking water systems – the challenges of characterization and risk mitigation

Highlights

Graphical abstract

Introduction

Section snippets

Identification of NTM and their characteristics

NTM in source waters used for drinking water production

NTM survival through drinking water treatment processes

NTM in distribution systems and building plumbing

Routes of exposure and infection

Future work

Conflict of interest statement

References and recommended reading

Acknowledgements

Ann Thorac Surg

Diagn Microbiol Infect Dis

mBio

Pediatr Pulmonol

Appl Environ Microbiol

Environ Sci Technol

Front Med

BMC Res Notes

J Clin Microbiol

J Clin Microbiol

J Clin Microbiol

Mycobacterium avium complex: adherence as a way of life

AIMS Microbiol

Microorganisms resistant to free-living amoebae

Clin Microbiol Rev

Current epidemiologic trends of the nontuberculous mycobacteria (NTM)

Curr Environ Health Rep

Skin and soft tissue infections due to nontuberculous mycobacteria

Curr Infect Dis Rep

Multistate US outbreak of rapidly growing mycobacterial infections associated with medical tourism to the Dominican Republic, 2013-2014

Emerg Infect Dis

Direct healthcare costs of selected diseases primarily or partially transmitted by water

Epidemiol Infect

Increasing nontuberculous mycobacteria reporting rates and species diversity identified in clinical laboratory reports

BMC Infect Dis

Increasing reports of non-tuberculous mycobacteria in England, Wales and Northern Ireland, 1995-2006

BMC Public Health

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

Increased frequency of nontuberculous mycobacteria detection at potable water taps within the United States

Environ Sci Technol

Ecological analyses of mycobacteria in showerhead biofilms and their relevance to human health

mBio

Microbiological features and clinical relevance of new species of the genus Mycobacterium

Clin Microbiol Rev

Environmental sources of nontuberculous mycobacteria

Clin Chest Med

Genomic characterization of nontuberculous mycobacteria

Sci Rep

An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases

Am J Respir Crit Care Med

Mycobacterium abscessus: “Pleased to meet you, hope you guess my name…”

Ann Am Thorac Soc

Culture-independent identification of nontuberculous mycobacteria in cystic fibrosis respiratory samples

PLoS One

Differences in drug susceptibility pattern between Mycobacterium avium and Mycobacterium intracellulare isolated in respiratory specimens

J Infect Chemother

Environmental nontuberculous mycobacteria in the Hawaiian Islands

PLoS Negl Trop Dis

Mycobacterium avium in community and household water, suburban Philadelphia, Pennsylvania, USA, 2010–2012

Emerg Infect Dis

Spatial clusters of nontuberculous mycobacterial lung disease in the United States

Am J Respir Crit Care Med

Geographic distribution of nontuberculous mycobacterial species identified among clinical isolates in the United States, 2009-2013

Ann Am Thorac Soc

Distribution comparison and risk assessment of free-floating and particle-attached bacterial pathogens in urban recreational water: implications for water quality management

Sci Total Environ

Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellulare, and other mycobacteria in drinking water distribution systems

Appl Environ Microbiol

A retrospective analysis of nontuberculous mycobacterial infection and monochloramine disinfection of municipal drinking water in Michigan

mSphere

Pace NR: longitudinal and source-to-tap New Orleans, LA, U.S.A. drinking water microbiology

Environ Sci Technol

The abundance of opportunistic bacterial pathogens in municipal drinking water is impacted by dissolved iron concentration and distribution system and household plumbing characteristics

Environ Sci Technol

Inactivation of two mycobacteria by free chlorine: Effectiveness, influencing factors, and mechanisms