Environmental (Saprozoic) Pathogens of Engineered Water Systems: Understanding Their Ecology for Risk Assessment and Management

Major waterborne (enteric) pathogens are relatively well understood and treatment controls are effective when well managed. However, water-based, saprozoic pathogens that grow within engineered water systems (primarily within biofilms/sediments) cannot be controlled by water treatment alone prior to entry into water distribution and other engineered water systems. Growth within biofilms or as in the case of Legionella pneumophila, primarily within free-living protozoa feeding on biofilms, results from competitive advantage. Meaning, to understand how to manage water-based pathogen diseases (a sub-set of saprozoses) we need to understand the microbial ecology of biofilms; with key factors including biofilm bacterial diversity that influence amoebae hosts and members antagonistic to water-based pathogens, along with impacts from biofilm substratum, water temperature, flow conditions and disinfectant residual—all control variables. Major saprozoic pathogens covering viruses, bacteria, fungi and free-living protozoa are listed, yet today most of the recognized health burden from drinking waters is driven by legionellae, non-tuberculous mycobacteria (NTM) and, to a lesser extent, Pseudomonas aeruginosa. In developing best management practices for engineered water systems based on hazard analysis critical control point (HACCP) or water safety plan (WSP) approaches, multi-factor control strategies, based on quantitative microbial risk assessments need to be developed, to reduce disease from largely opportunistic, water-based pathogens.

[1]  Palak G. Patel,et al.  Regulatory control of temporally expressed integration host factor (IHF) in Legionella pneumophila. , 2013, Microbiology.

[2]  M. Behr,et al.  Molecular epidemiology of nontuberculous mycobacteria. , 2009, Future microbiology.

[3]  C. Desnues,et al.  Evidence of the megavirome in humans. , 2013, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[4]  Rosalyn Murphy-Jenkins Department of Agriculture Food Safety and Inspection Service 9 CFR Parts 317 and 381 Descriptive Designation for Raw Meat and Poultry Products Containing Added Solutions , 2022 .

[5]  R. Muthusamy,et al.  Prevalence of Simkania negevensis in chlorinated water from spa swimming pools and domestic supplies , 2015, Journal of applied microbiology.

[6]  V. Gomez-Alvarez,et al.  Bacterial composition in a metropolitan drinking water distribution system utilizing different source waters. , 2015, Journal of water and health.

[7]  N. Pace,et al.  Molecular analysis of point-of-use municipal drinking water microbiology. , 2014, Water research.

[8]  L. Raskin,et al.  Differential resistance of drinking water bacterial populations to monochloramine disinfection. , 2014, Environmental science & technology.

[9]  J. Gilbert,et al.  Diverse protist grazers select for virulence-related traits in Legionella , 2015, The ISME Journal.

[10]  A. Nocker,et al.  Quantification of viable Legionella pneumophila cells using propidium monoazide combined with quantitative PCR. , 2011, Journal of microbiological methods.

[11]  O. Landt,et al.  Detection of non-tuberculous mycobacteria in hospital water by culture and molecular methods. , 2009, International journal of medical microbiology : IJMM.

[12]  B. Parker,et al.  Epidemiology of infection by nontuberculous mycobacteria. IV. Preferential aerosolization of Mycobacterium intracellulare from natural waters. , 1983, The American review of respiratory disease.

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

[14]  J. Morató,et al.  Well Water as a Possible Source of Waddlia chondrophila Infections , 2012, Microbes and environments.

[15]  Gilbert GREUB,et al.  Free-living amoebae: Biological by-passes in water treatment. , 2010, International journal of hygiene and environmental health.

[16]  K. Winthrop,et al.  Update on the Epidemiology of Pulmonary Nontuberculous Mycobacterial Infections , 2013, Seminars in Respiratory and Critical Care Medicine.

[17]  Amy Pruden,et al.  Environmental Health Perspectives Epidemiology and Ecology of Opportunistic Premise Plumbing Pathogens: Legionella Pneumophila, Mycobacterium Avium, and Pseudomonas Aeruginosa Epidemiology and Ecology of Opportunistic Premise Plumbing Pathogens: Legionella Pneumophila, Mycobacterium Avium, and Pseud , 2022 .

[18]  Jon H. Standridge,et al.  Aeromonas Isolates from Human Diarrheic Stool and Groundwater Compared by Pulsed-Field Gel Electrophoresis , 2003, Emerging infectious diseases.

[19]  Jean-Marie Decuypere The last taboo. , 1999, New scientist.

[20]  S. Berk,et al.  The tetrahymena and acanthamoeba model systems. , 2013, Methods in molecular biology.

[21]  D. Keim,et al.  Comparison of strand-specific transcriptomes of enterohemorrhagic Escherichia coli O157:H7 EDL933 (EHEC) under eleven different environmental conditions including radish sprouts and cattle feces , 2014, BMC Genomics.

[22]  O. Köster,et al.  Abundance and composition of indigenous bacterial communities in a multi-step biofiltration-based drinking water treatment plant. , 2014, Water research.

[23]  I. Miettinen,et al.  Drinking water quality and formation of biofilms in an office building during its first year of operation, a full scale study. , 2014, Water research.

[24]  N. Ashbolt,et al.  Legionella pneumophila Transcriptional Response following Exposure to CuO Nanoparticles , 2013, Applied and Environmental Microbiology.

[25]  M. T. Crespo,et al.  Free chlorine inactivation of fungi in drinking water sources. , 2013, Water research.

[26]  J. Morató,et al.  Amoeba-related health risk in drinking water systems: could monitoring of amoebae be a complementary approach to current quality control strategies? , 2012, Future microbiology.

[27]  R. Baquero,et al.  Presence of potentially pathogenic free-living amoebae strains from well water samples in Guinea-Bissau , 2014, Pathogens and global health.

[28]  J B Boxall,et al.  Bacterial water quality and network hydraulic characteristics: a field study of a small, looped water distribution system using culture‐independent molecular methods , 2012, Journal of applied microbiology.

[29]  D. Raoult,et al.  Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. , 2010, FEMS microbiology reviews.

[30]  L. Moulin,et al.  First evidence of amoebae-mycobacteria association in drinking water network. , 2014, Environmental science & technology.

[31]  Ord,et al.  Microbial Risk Assessment Guideline: Pathogenic Microorganisms with Focus on Food and Water , 2013 .

[32]  P. Martikainen,et al.  Formation of biofilms in drinking water distribution networks, a case study in two cities in Finland and Latvia , 2004, Journal of Industrial Microbiology and Biotechnology.

[33]  M. Vieira,et al.  Interaction of legionella pneumophila and helicobacter pylori with bacterial species isolated from drinking water biofilms , 2011, BMC Microbiology.

[34]  J.Y. Hu,et al.  Interaction between phosphorus and biodegradable organic carbon on drinking water biofilm subject to chlorination , 2009, Journal of applied microbiology.

[35]  J. Lawrence,et al.  Advanced techniques for in situ analysis of the biofilm matrix (structure, composition, dynamics) by means of laser scanning microscopy. , 2014, Methods in molecular biology.

[36]  A. Camper,et al.  Viable Real-Time PCR in Environmental Samples: Can All Data Be Interpreted Directly? , 2010, Microbial Ecology.

[37]  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.

[38]  D. Kooij,et al.  Invertebrates and Protozoa (Free‐Living) in Drinking Water Distribution Systems , 2003 .

[39]  Xiao-jian Zhang,et al.  Biofilm bacterial communities in urban drinking water distribution systems transporting waters with different purification strategies , 2014, Applied Microbiology and Biotechnology.

[40]  M. Deloge-Abarkan,et al.  Pontiac fever: an operational definition for epidemiological studies , 2006, BMC public health.

[41]  J. Morató,et al.  Searching Simkania negevensis in environmental waters , 2011, Folia Microbiologica.

[42]  Nicholas J Ashbolt,et al.  Do free-living amoebae in treated drinking water systems present an emerging health risk? , 2011, Environmental science & technology.

[43]  A. Basson,et al.  Evaluation of Adherence, Hydrophobicity, Aggregation, and Biofilm Development of Flavobacterium johnsoniae-Like Isolates , 2007, Microbial Ecology.

[44]  M. Slaný,et al.  The water environment as a source of potentially pathogenic mycobacteria. , 2014, Journal of water and health.

[45]  A. Keegan,et al.  Detection of Legionella, L. pneumophila and Mycobacterium Avium Complex (MAC) along Potable Water Distribution Pipelines , 2014, International journal of environmental research and public health.

[46]  N. Ashbolt,et al.  The role of biofilms and protozoa in Legionella pathogenesis: implications for drinking water , 2009, Journal of applied microbiology.

[47]  Michael J. Taylor,et al.  Legionella detection by culture and qPCR: Comparing apples and oranges , 2014, Critical reviews in microbiology.

[48]  C. W. Keevil,et al.  Persistence of Helicobacter pylori in Heterotrophic Drinking-Water Biofilms , 2008, Applied and Environmental Microbiology.

[49]  Gilbert Greub,et al.  Novel Chlamydiales strains isolated from a water treatment plant. , 2009, Environmental microbiology.

[50]  M. Exner,et al.  Prevention and control of health care-associated waterborne infections in health care facilities. , 2005, American journal of infection control.

[51]  Z. Hubálek,et al.  Emerging Human Infectious Diseases: Anthroponoses, Zoonoses, and Sapronoses , 2003, Emerging infectious diseases.

[52]  J. Mckinney,et al.  A single-cell perspective on non-growing but metabolically active (NGMA) bacteria. , 2013, Current topics in microbiology and immunology.

[53]  M. Beach,et al.  Direct healthcare costs of selected diseases primarily or partially transmitted by water , 2012, Epidemiology and Infection.

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

[55]  Amy Pruden,et al.  Probiotic approach to pathogen control in premise plumbing systems? A review. , 2013, Environmental science & technology.

[56]  M. Vargha,et al.  Infection control by point-of-use water filtration in an intensive care unit - a Hungarian case study. , 2014, Journal of water and health.

[57]  J. Turton,et al.  Outbreak of Stenotrophomonas maltophilia on an intensive care unit. , 2013, The Journal of hospital infection.

[58]  G. Medema,et al.  Screening-level microbial risk assessment of urban water locations: a tool for prioritization. , 2014, Environmental science & technology.

[59]  Analysis of Black Fungal Biofilms Occurring at Domestic Water Taps (I): Compositional Analysis Using Tag-Encoded FLX Amplicon Pyrosequencing , 2013, Mycopathologia.

[60]  R. Koch An Address on Cholera and its Bacillus , 1884, British medical journal.

[61]  C. Biggs,et al.  A new coupon design for simultaneous analysis of in situ microbial biofilm formation and community structure in drinking water distribution systems , 2010, Applied Microbiology and Biotechnology.

[62]  N. Ashbolt,et al.  Molecular survey of occurrence and quantity of Legionella spp., Mycobacterium spp., Pseudomonas aeruginosa and amoeba hosts in municipal drinking water storage tank sediments , 2015, Journal of applied microbiology.

[63]  Tae-ho Yoon,et al.  Inactivation of environmental mycobacteria by free chlorine and UV. , 2010, Water research.

[64]  Nicholas J. Ashbolt,et al.  Comparative human health risk analysis of coastal community water and waste service options. , 2014, Environmental science & technology.

[65]  V. Yu,et al.  Controlling Legionella in Hospital Drinking Water: An Evidence-Based Review of Disinfection Methods , 2011, Infection Control & Hospital Epidemiology.

[66]  J. Vreeburg,et al.  Pyrosequencing reveals bacterial communities in unchlorinated drinking water distribution system: an integral study of bulk water, suspended solids, loose deposits, and pipe wall biofilm. , 2014, Environmental science & technology.

[67]  N. Ashbolt,et al.  Establishment and early succession of bacterial communities in monochloramine-treated drinking water biofilms. , 2013, FEMS microbiology ecology.

[68]  Shandra R. Day,et al.  Caenorhabditis is a metazoan host for Legionella , 2010, Cellular microbiology.

[69]  C. Daley,et al.  The epidemiologic relationship between tuberculosis and non-tuberculous mycobacterial disease: a systematic review. , 2014, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[70]  Min Yang,et al.  Molecular analysis of long-term biofilm formation on PVC and cast iron surfaces in drinking water distribution system. , 2014, Journal of environmental sciences.

[71]  S. Yandow,et al.  Perspective: One Health: a compelling convergence. , 2013, Academic medicine : journal of the Association of American Medical Colleges.

[72]  C. Keevil,et al.  Influence of copper surfaces on biofilm formation by Legionella pneumophila in potable water , 2015, BioMetals.

[73]  C. Valcke,et al.  Molecular Viability Testing of Bacterial Pathogens from a Complex Human Sample Matrix , 2013, PloS one.

[74]  D. Raoult,et al.  Shan Virus: A New Mimivirus Isolated from the Stool of a Tunisian Patient with Pneumonia , 2013, Intervirology.

[75]  D. Pinto,et al.  Thirty years of viable but nonculturable state research: Unsolved molecular mechanisms , 2015, Critical reviews in microbiology.

[76]  M. Prevost,et al.  Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. , 2010, Environmental microbiology.

[77]  Guangxue Wu,et al.  Effect of bacterial communities on the formation of cast iron corrosion tubercles in reclaimed water. , 2015, Water research.

[78]  Thomas Backhaus,et al.  Human Health Risk Assessment (HHRA) for Environmental Development and Transfer of Antibiotic Resistance , 2013, Environmental health perspectives.

[79]  Vincent Thomas,et al.  Free-living amoebae and their intracellular pathogenic microorganisms: risks for water quality. , 2010, FEMS microbiology reviews.

[80]  Michael O. Ryan,et al.  Evaluating the Potential for a Helicobacter pylori Drinking Water Guideline , 2014, Risk analysis : an official publication of the Society for Risk Analysis.

[81]  N. Ashbolt Microbial Contamination of Drinking Water and Human Health from Community Water Systems , 2015, Current Environmental Health Reports.

[82]  S. Fenoy,et al.  A year long study of the presence of free living amoeba in Spain. , 2013, Water research.

[83]  P. W. van der Wielen,et al.  Nontuberculous Mycobacteria, Fungi, and Opportunistic Pathogens in Unchlorinated Drinking Water in the Netherlands , 2012, Applied and Environmental Microbiology.

[84]  C. Biggs,et al.  Methodological approaches for studying the microbial ecology of drinking water distribution systems. , 2014, Water research.

[85]  L. Bakaletz,et al.  Biofilm-derived Legionella pneumophila evades the innate immune response in macrophages , 2013, Front. Cell. Infect. Microbiol..

[86]  J. Falkinham Hospital water filters as a source of Mycobacterium avium complex. , 2010, Journal of medical microbiology.

[87]  N. Ashbolt,et al.  Microbial diversities (16S and 18S rRNA gene pyrosequencing) and environmental pathogens within drinking water biofilms grown on the common premise plumbing materials unplasticized polyvinylchloride and copper. , 2014, FEMS microbiology ecology.

[88]  Lutgarde Raskin,et al.  Spatial-Temporal Survey and Occupancy-Abundance Modeling To Predict Bacterial Community Dynamics in the Drinking Water Microbiome , 2014, mBio.

[89]  Guillermo L. Monroy,et al.  Role of biofilm roughness and hydrodynamic conditions in Legionella pneumophila adhesion to and detachment from simulated drinking water biofilms. , 2015, Environmental science & technology.

[90]  Irene Krämer,et al.  Lesser-known or hidden reservoirs of infection and implications for adequate prevention strategies: Where to look and what to look for , 2015, GMS hygiene and infection control.

[91]  D. Low,et al.  The Legionella pneumophila Collagen-Like Protein Mediates Sedimentation, Autoaggregation, and Pathogen-Phagocyte Interactions , 2013, Applied and Environmental Microbiology.

[92]  Seoktae Kang,et al.  The role of conditioning film formation in Pseudomonas aeruginosa PAO1 adhesion to inert surfaces in aquatic environments , 2013 .

[93]  P. Stewart,et al.  Biophysics of biofilm infection. , 2014, Pathogens and disease.

[94]  J. Falkinham,et al.  Epidemiology of infection by nontuberculous mycobacteria , 1996, Clinical microbiology reviews.

[95]  K. Bibby,et al.  Shift in the Microbial Ecology of a Hospital Hot Water System following the Introduction of an On-Site Monochloramine Disinfection System , 2014, PloS one.

[96]  T. Stenström,et al.  Diversity, persistence, and virulence of Aeromonas strains isolated from drinking water distribution systems in Sweden , 1997, Applied and environmental microbiology.

[97]  Laam Li,et al.  The importance of the viable but non-culturable state in human bacterial pathogens , 2014, Front. Microbiol..

[98]  Bernard La Scola,et al.  Amoebas as mimivirus bunkers: increased resistance to UV light, heat and chemical biocides when viruses are carried by amoeba hosts , 2013, Archives of Virology.

[99]  A. Reid,et al.  Microbes in Pipes: The Microbiology of the Water Distribution System , 2013 .

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

[101]  F. Hammes,et al.  Drinking water microbiology--from measurement to management. , 2015, Current opinion in biotechnology.

[102]  A. Keegan,et al.  The presence of opportunistic pathogens, Legionella spp., L. pneumophila and Mycobacterium avium complex, in South Australian reuse water distribution pipelines. , 2015, Journal of water and health.

[103]  I B Gomes,et al.  An overview on the reactors to study drinking water biofilms. , 2014, Water research.

[104]  Nicholas J Ashbolt,et al.  Preferential colonization and release of Legionella pneumophila from mature drinking water biofilms grown on copper versus unplasticized polyvinylchloride coupons. , 2014, International journal of hygiene and environmental health.

[105]  M. Wagener,et al.  Efficacy of new point-of-use water filter for preventing exposure to Legionella and waterborne bacteria. , 2004, American journal of infection control.

[106]  H. Flemming,et al.  Biofilms in drinking water and their role as reservoir for pathogens. , 2011, International journal of hygiene and environmental health.

[107]  C. Biggs,et al.  Aggregation and biofilm formation of bacteria isolated from domestic drinking water , 2013 .

[108]  N J Ashbolt,et al.  Impact of drinking water conditions and copper materials on downstream biofilm microbial communities and Legionella pneumophila colonization , 2014, Journal of applied microbiology.

[109]  K. Sabbe,et al.  Interactions of Foodborne Pathogens with Free‐living Protozoa: Potential Consequences for Food Safety , 2014 .

[110]  A. Shane The Last Taboo: Opening the Door on the Global Sanitation Crisis , 2009, Emerging Infectious Diseases.

[111]  Chaofeng Shen,et al.  Exploring the potential environmental functions of viable but non-culturable bacteria , 2013, World journal of microbiology & biotechnology.

[112]  Mark W. LeChevallier,et al.  Enteric virus infection risk from intrusion of sewage into a drinking water distribution network. , 2010, Environmental science & technology.

[113]  Michèle Prévost,et al.  Temperature diagnostic to identify high risk areas and optimize Legionella pneumophila surveillance in hot water distribution systems. , 2015, Water research.

[114]  Jothikumar Narayanan,et al.  The first association of a primary amebic meningoencephalitis death with culturable Naegleria fowleri in tap water from a US treated public drinking water system. , 2015, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[115]  N. Ashbolt,et al.  Dose–response algorithms for water-borne Pseudomonas aeruginosa folliculitis , 2014, Epidemiology and Infection.

[116]  Leah M. Feazel,et al.  Opportunistic pathogens enriched in showerhead biofilms , 2009, Proceedings of the National Academy of Sciences.

[117]  J. Snow On the Mode of Communication of Cholera , 1856, Edinburgh medical journal.

[118]  J. Banfield,et al.  Community transcriptomics reveals unexpected high microbial diversity in acidophilic biofilm communities , 2014, The ISME Journal.

[119]  O. Garraud,et al.  Viable but Not Culturable Forms of Legionella pneumophila Generated After Heat Shock Treatment Are Infectious for Macrophage-Like and Alveolar Epithelial Cells After Resuscitation on Acanthamoeba polyphaga , 2014, Microbial Ecology.