Shower water contributes viable nontuberculous mycobacteria to indoor air

Abstract Nontuberculous mycobacteria (NTM) are frequently present in municipal drinking water and building plumbing, and some are believed to cause respiratory tract infections through inhalation of NTM-containing aerosols generated during showering. However, the present understanding of NTM transfer from water to air is insufficient to develop NTM risk mitigation strategies. This study aimed to characterize the contribution of shower water to the abundance of viable NTM in indoor air. Shower water and indoor air samples were collected, and 16S rRNA and rpoB genes were sequenced. The sequencing results showed that running the shower impacted the bacterial community structure and NTM species composition in indoor air by transferring certain bacteria from water to air. A mass balance model combined with NTM quantification results revealed that on average 1/132 and 1/254 of NTM cells in water were transferred to air during 1 hour of showering using a rain and massage showerhead, respectively. A large fraction of the bacteria transferred from water to air were membrane-damaged, i.e. they had compromised membranes based on analysis by live/dead staining and flow cytometry. However, the damaged NTM in air were recoverable as shown by growth in a culture medium mimicking the respiratory secretions of people with cystic fibrosis, implying a potential infection risk by NTM introduced to indoor air during shower running. Among the recovered NTM, Mycobacterium mucogenicum was the dominant species as determined by rpoB gene sequencing. Overall, this study lays the groundwork for future pathogen risk management and public health protection in the built environment.

[1]  Hong Wang,et al.  Opportunistic pathogens exhibit distinct growth dynamics in rainwater and tap water storage systems. , 2021, Water research.

[2]  Liping Wang,et al.  Assessment of the UV/Chlorine Process in the Disinfection of Pseudomonas aeruginosa: Efficiency and Mechanism. , 2021, Environmental science & technology.

[3]  M. Veillette,et al.  Condensation sampler efficiency for the recovery and infectivity preservation of viral bioaerosols , 2021, Aerosol Science and Technology.

[4]  S. Guikema,et al.  Emerging investigator series: bacterial opportunistic pathogen gene markers in municipal drinking water are associated with distribution system and household plumbing characteristics , 2020, Environmental Science: Water Research & Technology.

[5]  R. Smith,et al.  Effect of disinfectant residuals on infection risks from Legionella pneumophila released by biofilms grown under simulated premise plumbing conditions. , 2020, Environment international.

[6]  Kaisen Lin,et al.  Humidity-Dependent Decay of Viruses, But Not Bacteria, in Aerosols and Droplets Follows Disinfection Kinetics. , 2019, Environmental science & technology.

[7]  A. Okayama,et al.  Pseudo-outbreak of Mycobacterium paragordonae in a hospital: possible relation to the aerator/rectifier connected to the faucet of the water supply system. , 2019, The Journal of hospital infection.

[8]  L. Raskin,et al.  Nontuberculous mycobacteria in drinking water systems - the challenges of characterization and risk mitigation. , 2019, Current opinion in biotechnology.

[9]  C. McGoverin,et al.  Optimisation of the Protocol for the LIVE/DEAD® BacLightTM Bacterial Viability Kit for Rapid Determination of Bacterial Load , 2019, Front. Microbiol..

[10]  Mark Hernandez,et al.  High fidelity recovery of airborne microbial genetic materials by direct condensation capture into genomic preservatives. , 2019, Journal of microbiological methods.

[11]  K. Mui,et al.  Aerosol generation rates for showerheads , 2019, Building Services Engineering Research and Technology.

[12]  C. Haas,et al.  Risk-Based Critical Concentrations of Legionella pneumophila for Indoor Residential Water Uses. , 2019, Environmental science & technology.

[13]  B. Rosati,et al.  Effect of Aerosolization and Drying on the Viability of Pseudomonas syringae Cells , 2018, Front. Microbiol..

[14]  Matthew J. Gebert,et al.  Ecological Analyses of Mycobacteria in Showerhead Biofilms and Their Relevance to Human Health , 2018, mBio.

[15]  Hiroyuki Yamada,et al.  Prevention of aerosol isolation of nontuberculous mycobacterium from the patient's bathroom , 2018, ERJ Open Research.

[16]  S. Hering,et al.  Collection of airborne bacteria and yeast through water-based condensational growth , 2018, Aerobiologia.

[17]  M. Donohue Increasing nontuberculous mycobacteria reporting rates and species diversity identified in clinical laboratory reports , 2018, BMC Infectious Diseases.

[18]  Y. Hassan,et al.  Droplet distribution and airborne bacteria in an experimental shower unit. , 2018, Water research.

[19]  L. Raskin,et al.  A High-Throughput Approach for Identification of Nontuberculous Mycobacteria in Drinking Water Reveals Relationship between Water Age and Mycobacterium avium , 2018, mBio.

[20]  L. Marr,et al.  Physico-chemical characteristics of evaporating respiratory fluid droplets , 2018, Journal of The Royal Society Interface.

[21]  L. Raskin,et al.  Biofilms in Full-Scale Drinking Water Ozone Contactors Contribute Viable Bacteria to Ozonated Water. , 2018, Environmental science & technology.

[22]  C. Haas,et al.  Human health risks for Legionella and Mycobacterium avium complex (MAC) from potable and non-potable uses of roof-harvested rainwater. , 2017, Water research.

[23]  J S Vrouwenvelder,et al.  Flow cytometric bacterial cell counts challenge conventional heterotrophic plate counts for routine microbiological drinking water monitoring. , 2017, Water research.

[24]  F. Maruyama,et al.  Infection Sources of a Common Non-tuberculous Mycobacterial Pathogen, Mycobacterium avium Complex , 2017, Front. Med..

[25]  W. Koh Nontuberculous Mycobacteria-Overview. , 2017, Microbiology spectrum.

[26]  J. Philley,et al.  Rapidly Growing Mycobacteria. , 2017, Microbiology spectrum.

[27]  B. Kreiswirth,et al.  Deaths Related to Nontuberculous Mycobacterial Infections in the United States, 1999-2014. , 2016, Annals of the American Thoracic Society.

[28]  S. Riffard,et al.  Characterization of aerosols containing Legionella generated upon nebulization , 2016, Scientific Reports.

[29]  S. Hering,et al.  Highly efficient collection of infectious pandemic influenza H1N1 virus (2009) through laminar-flow water based condensation , 2016 .

[30]  L. Raskin,et al.  Anaerobic microbial community response to methanogenic inhibitors 2‐bromoethanesulfonate and propynoic acid , 2016, MicrobiologyOpen.

[31]  W. Nazaroff Indoor bioaerosol dynamics , 2014, Indoor air.

[32]  Linsey C. Marr,et al.  Sources of airborne microorganisms in the built environment , 2015, Microbiome.

[33]  Steven E. Lindow,et al.  Relative and contextual contribution of different sources to the composition and abundance of indoor air bacteria in residences , 2015, Microbiome.

[34]  Michael K Adjemian,et al.  The Burden of Pulmonary Nontuberculous Mycobacterial Disease in the United States. , 2015, Annals of the American Thoracic Society.

[35]  P. Lukeš,et al.  Membrane damage and active but nonculturable state in liquid cultures of Escherichia coli treated with an atmospheric pressure plasma jet. , 2015, Bioelectrochemistry.

[36]  P. Price,et al.  Review: Environmental mycobacteria as a cause of human infection. , 2015, International journal of mycobacteriology.

[37]  T. Covert,et al.  Increased Frequency of Nontuberculous Mycobacteria Detection at Potable Water Taps within the United States. , 2015, Environmental science & technology.

[38]  M. Whiteley,et al.  Essential genome of Pseudomonas aeruginosa in cystic fibrosis sputum , 2015, Proceedings of the National Academy of Sciences.

[39]  J. Falkinham Environmental sources of nontuberculous mycobacteria. , 2015, Clinics in chest medicine.

[40]  Amy Pruden,et al.  Anticipating Challenges with In‐Building Disinfection for Control of Opportunistic Pathogens , 2014, Water environment research : a research publication of the Water Environment Federation.

[41]  R. Lordo,et al.  Assessment of relative potential for Legionella species or surrogates inhalation exposure from common water uses. , 2014, Water research.

[42]  Y. Kook,et al.  Mycobacterium paragordonae sp. nov., a slowly growing, scotochromogenic species closely related to Mycobacterium gordonae. , 2014, International journal of systematic and evolutionary microbiology.

[43]  R. Moilleron,et al.  atpE gene as a new useful specific molecular target to quantify Mycobacterium in environmental samples , 2013, BMC Microbiology.

[44]  D. Fennell,et al.  Release of Free DNA by Membrane-Impaired Bacterial Aerosols Due to Aerosolization and Air Sampling , 2013, Applied and Environmental Microbiology.

[45]  J. Bartram,et al.  Pathogenic Mycobacteria in Water: A Guide to Public Health Consequences, Monitoring and Management , 2013 .

[46]  Nico Boon,et al.  Routine bacterial analysis with automated flow cytometry. , 2013, Journal of microbiological methods.

[47]  M. Hargreaves,et al.  Isolation of Nontuberculous Mycobacteria (NTM) from Household Water and Shower Aerosols in Patients with Pulmonary Disease Caused by NTM , 2013, Journal of Clinical Microbiology.

[48]  Sarah L. Westcott,et al.  Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform , 2013, Applied and Environmental Microbiology.

[49]  I. Miettinen,et al.  Comparison of culture and qPCR methods in detection of mycobacteria from drinking waters. , 2013, Canadian journal of microbiology.

[50]  A. Nocker,et al.  Effect of air drying on bacterial viability: A multiparameter viability assessment. , 2012, Journal of microbiological methods.

[51]  A. Pruden,et al.  Molecular Survey of the Occurrence of Legionella spp., Mycobacterium spp., Pseudomonas aeruginosa, and Amoeba Hosts in Two Chloraminated Drinking Water Distribution Systems , 2012, Applied and Environmental Microbiology.

[52]  Brandi L Dorsey,et al.  Recovery efficiencies for Burkholderia thailandensis from various aerosol sampling media , 2012, Front. Cell. Inf. Microbio..

[53]  Nicholas J Ashbolt,et al.  Legionellae in engineered systems and use of quantitative microbial risk assessment to predict exposure. , 2012, Water research.

[54]  Nicholas J Ashbolt,et al.  An in-premise model for Legionella exposure during showering events. , 2011, Water research.

[55]  Rob Knight,et al.  Bayesian community-wide culture-independent microbial source tracking , 2011, Nature Methods.

[56]  C. Chang,et al.  Methodologies for quantifying culturable, viable, and total Legionella pneumophila in indoor air. , 2011, Indoor air.

[57]  D. Wagner,et al.  [Tuberculosis and nontuberculous mycobacterial infections]. , 2011, Deutsche medizinische Wochenschrift.

[58]  Frederik Hammes,et al.  Kinetics of membrane damage to high (HNA) and low (LNA) nucleic acid bacterial clusters in drinking water by ozone, chlorine, chlorine dioxide, monochloramine, ferrate(VI), and permanganate. , 2011, Water research.

[59]  T. Laws,et al.  The Cell Membrane as a Major Site of Damage during Aerosolization of Escherichia coli , 2010, Applied and Environmental Microbiology.

[60]  T. Adékambi Mycobacterium mucogenicum group infections: a review. , 2009, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[61]  Shih-cheng Hu,et al.  Influence of bathroom ventilation rates and toilet location on odor removal , 2009 .

[62]  L. T. Angenent,et al.  Potentially Pathogenic Bacteria in Shower Water and Air of a Stem Cell Transplant Unit , 2009, Applied and Environmental Microbiology.

[63]  Mark Johnson,et al.  NCBI BLAST: a better web interface , 2008, Nucleic Acids Res..

[64]  D. van Soolingen,et al.  Mycobacterium avium in a shower linked to pulmonary disease , 2008 .

[65]  Bradley J. Hernlem,et al.  Application of flow cytometry and cell sorting to the bacterial analysis of environmental aerosol samples. , 2007, Journal of environmental monitoring : JEM.

[66]  T W Armstrong,et al.  A Quantitative Microbial Risk Assessment Model for Legionnaires' Disease: Animal Model Selection and Dose‐Response Modeling , 2007, Risk analysis : an official publication of the Society for Risk Analysis.

[67]  L. Newman,et al.  Nontuberculous Mycobacteria in Aerosol Droplets and Bulk Water Samples from Therapy Pools and Hot Tubs , 2007, Journal of occupational and environmental hygiene.

[68]  Frederik Hammes,et al.  Assessment and Interpretation of Bacterial Viability by Using the LIVE/DEAD BacLight Kit in Combination with Flow Cytometry , 2007, Applied and Environmental Microbiology.

[69]  Robert Horsburgh,et al.  An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. , 2007, American journal of respiratory and critical care medicine.

[70]  Yung-Sung Cheng,et al.  Particle Size Distribution and Inhalation Dose of Shower Water Under Selected Operating Conditions , 2007, Inhalation toxicology.

[71]  L. T. Angenent,et al.  Molecular identification of potential pathogens in water and air of a hospital therapy pool. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[72]  H. Alpas,et al.  Injury recovery of foodborne pathogens in high hydrostatic pressure treated milk during storage. , 2004, FEMS immunology and medical microbiology.

[73]  A. Fraire,et al.  A case of "hot tub lung" due to Mycobacterium avium complex in an immunocompetent host. , 2003, Archives of internal medicine.

[74]  Roulet Claude-Alain,et al.  Simple and Cheap Air Change Rate Measurement Using CO2 Concentration Decays , 2002 .

[75]  Alessandra Ghiani,et al.  Resolution of Viable and Membrane-Compromised Bacteria in Freshwater and Marine Waters Based on Analytical Flow Cytometry and Nucleic Acid Double Staining , 2001, Applied and Environmental Microbiology.

[76]  W. H. Engelmann,et al.  The National Human Activity Pattern Survey (NHAPS): a resource for assessing exposure to environmental pollutants , 2001, Journal of Exposure Analysis and Environmental Epidemiology.

[77]  M. Labra,et al.  Two and three-color fluorescence flow cytometric analysis of immunoidentified viable bacteria. , 2000, Cytometry.

[78]  Robert H. Taylor,et al.  Chlorine, Chloramine, Chlorine Dioxide, and Ozone Susceptibility of Mycobacterium avium , 2000, Applied and Environmental Microbiology.

[79]  R. Colwell,et al.  Effect of aerosolization on culturability and viability of gram-negative bacteria , 1997, Applied and environmental microbiology.

[80]  M. Para,et al.  Aerosols containing Legionella pneumophila generated by shower heads and hot-water faucets , 1985, Applied and environmental microbiology.

[81]  J. M. Wood Perspectives on : The response to osmotic challenges Bacterial responses to osmotic challenges , 2022 .