Occurrence and Control of Legionella in Recycled Water Systems

Legionella pneumophila is on the United States Environmental Protection Agency (USEPA) Candidate Contaminant list (CCL) as an important pathogen. It is commonly encountered in recycled water and is typically associated with amoeba, notably Naegleria fowleri (also on the CCL) and Acanthamoeba sp. No legionellosis outbreak has been linked to recycled water and it is important for the industry to proactively keep things that way. A review was conducted examine the occurrence of Legionella and its protozoa symbionts in recycled water with the aim of developing a risk management strategy. The review considered the intricate ecological relationships between Legionella and protozoa, methods for detecting both symbionts, and the efficacy of various disinfectants.

[1]  P. Pernin,et al.  Comparative Recoveries of Naegleria fowleri Amoebae from Seeded River Water by Filtration and Centrifugation , 1998, Applied and Environmental Microbiology.

[2]  Nicholas J Ashbolt,et al.  The Efficacy of Heat and Chlorine Treatment against Thermotolerant Acanthamoebae and Legionellae , 2004, Scandinavian journal of infectious diseases.

[3]  Donald E. Thompson,et al.  Validation of hollow fiber ultrafiltration and real-time PCR using bacteriophage PP7 as surrogate for the quantification of viruses from water samples. , 2007, Water research.

[4]  K. Goh,et al.  Epidemiology and Control of Legionellosis, Singapore , 2011, Emerging infectious diseases.

[5]  P. Wutzler,et al.  Virucidal efficacy of a combination of 0.2% peracetic acid and 80% (v/v) ethanol (PAA-ethanol) as a potential hand disinfectant. , 2000, The Journal of hospital infection.

[6]  A. P. Frasson,et al.  Potentially pathogenic Acanthamoeba in swimming pools: a survey in the southern Brazilian city of Porto Alegre , 2009, Annals of tropical medicine and parasitology.

[7]  C. Hadjichristodoulou,et al.  Legionella species colonization in cooling towers: risk factors and assessment of control measures. , 2010, American journal of infection control.

[8]  R. L. Sauer,et al.  Effects of culture conditions and biofilm formation on the iodine susceptibility of legionella pneumophila , 1992 .

[9]  Donald E. Low,et al.  Biofilms: The Stronghold of Legionella pneumophila , 2013, International Journal of Molecular Sciences.

[10]  V L Yu,et al.  Intermittent use of copper-silver ionization for Legionella control in water distribution systems: a potential option in buildings housing individuals at low risk of infection. , 1998, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[11]  Mark W. LeChevallier,et al.  Review of the leading challenges in maintaining reclaimed water quality during storage and distribution , 2014 .

[12]  R. Sommer,et al.  Effect of UV irradiation (253.7 nm) on free Legionella and Legionella associated with its amoebae hosts. , 2014, Water research.

[13]  F. Ollevier,et al.  A duplex real-time PCR assay for the quantitative detection of Naegleria fowleri in water samples. , 2007, Water research.

[14]  V L Yu,et al.  Comparative assessment of chlorine, heat, ozone, and UV light for killing Legionella pneumophila within a model plumbing system , 1987, Applied and environmental microbiology.

[15]  M. Exner,et al.  Hospital-acquired legionellosis originating from a cooling tower during a period of thermal inversion. , 2008, International journal of hygiene and environmental health.

[16]  Gilbert Greub,et al.  Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. , 2008, Environmental microbiology.

[17]  Y. Yamaguchi,et al.  Disinfectant effects of hot water, ultraviolet light, silver ions and chlorine on strains of Legionella and nontuberculous mycobacteria. , 2000, Microbios.

[18]  R. Colwell,et al.  Long-term survival of Legionella pneumophila serogroup 1 under low-nutrient conditions and associated morphological changes , 1992 .

[19]  M. Baker,et al.  Epidemiological investigation of a Legionnaires' disease outbreak in Christchurch, New Zealand: the value of spatial methods for practical public health , 2012, Epidemiology and Infection.

[20]  T. Schwartz,et al.  Formation of natural biofilms during chlorine dioxide and u.v. disinfection in a public drinking water distribution system , 2003, Journal of applied microbiology.

[21]  V. Yu,et al.  Individual and combined effects of copper and silver ions on inactivation of Legionella pneumophila , 1996 .

[22]  T. Hindré,et al.  Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation. , 2008, Microbiology.

[23]  F. Breidt,et al.  Enumeration of Viable Listeria monocytogenes Cells by Real-Time PCR with Propidium Monoazide and Ethidium Monoazide in the Presence of Dead Cells , 2007, Applied and Environmental Microbiology.

[24]  T. Ezaki,et al.  Factors Stimulating Propagation of Legionellae in Cooling Tower Water , 1992, Applied and environmental microbiology.

[25]  N. Caroff,et al.  Real-time PCR assay for the detection and quantification of Legionella pneumophila in environmental water samples: utility for daily practice. , 2008, International journal of hygiene and environmental health.

[26]  C. Gerba,et al.  Naegleria fowleri in Well Water , 2008, Emerging infectious diseases.

[27]  P. Jjemba Environmental Microbiology: Principles And Applications , 2004 .

[28]  P. Pernin,et al.  An Enzyme-Linked ImmunoSorbent Assay (ELISA) for the Identification of Naegleria fowleri in Environmental Water Samples , 2003, The Journal of eukaryotic microbiology.

[29]  Joseph C. Carpenter,et al.  Effect of monochloramine disinfection of municipal drinking water on risk of nosocomial Legionnaires'disease , 1999, The Lancet.

[30]  P. Pernin,et al.  Use of Multiplex PCR and PCR Restriction Enzyme Analysis for Detection and Exploration of the Variability in the Free-Living Amoeba Naegleria in the Environment , 2002, Applied and Environmental Microbiology.

[31]  B. Olson,et al.  Development of a quantitative PCR method to differentiate between viable and nonviable bacteria in environmental water samples , 2009, Applied Microbiology and Biotechnology.

[32]  S. Clarke,et al.  Ultraviolet Light Disinfection in the Use of Individual Water Purification Devices , 2006 .

[33]  J. D. de Jonckheere,et al.  Differences in destruction of cysts of pathogenic and nonpathogenic Naegleria and Acanthamoeba by chlorine , 1976, Applied and environmental microbiology.

[34]  R. Fujioka,et al.  Detection of Legionella species in reclaimed water and air with the EnviroAmp Legionella PCR kit and direct fluorescent antibody staining , 1995, Applied and environmental microbiology.

[35]  O. Pancorbo,et al.  Effects of three oxidizing biocides on Legionella pneumophila serogroup 1 , 1988, Applied and environmental microbiology.

[36]  N. Ashbolt,et al.  Exposure to Synthetic Gray Water Inhibits Amoeba Encystation and Alters Expression of Legionella pneumophila Virulence Genes , 2014, Applied and Environmental Microbiology.

[37]  S. Berk,et al.  Production of Respirable Vesicles Containing LiveLegionella pneumophila Cells by TwoAcanthamoeba spp , 1998, Applied and Environmental Microbiology.

[38]  P. Valenti,et al.  Metal complexes of lactoferrin and their effect on the intracellular multiplication of Legionella pneumophila , 2000, Biometals.

[39]  D. Slater,et al.  The Activity of Peracetic Acid on Sewage Indicator Bacteria and Viruses , 1991 .

[40]  S A Mueller,et al.  Literature review--efficacy of various disinfectants against Legionella in water systems. , 2002, Water research.

[41]  S. Sattar,et al.  Investigation of opportunistic pathogens in municipal drinking water under different supply and treatment regimes. , 2004, Water science and technology : a journal of the International Association on Water Pollution Research.

[42]  S Hills,et al.  Microbiological water quality in a large in-building, water recycling facility. , 2004, Water science and technology : a journal of the International Association on Water Pollution Research.

[43]  S. Kilvington,et al.  Survival of Legionella pneumophila within cysts of Acanthamoeba polyphaga following chlorine exposure. , 1990, The Journal of applied bacteriology.

[44]  E. Varughese,et al.  Cryptosporidium Propidium Monoazide-PCR, a Molecular Biology-Based Technique for Genotyping of Viable Cryptosporidium Oocysts , 2009, Applied and Environmental Microbiology.

[45]  M. Vieira,et al.  Comparison between standard culture and peptide nucleic acid 16S rRNA hybridization quantification to study the influence of physico-chemical parameters on Legionella pneumophila survival in drinking water biofilms , 2009, Biofouling.

[46]  W. Johnson,et al.  Virulence conversion of Legionella pneumophila serogroup 1 by passage in guinea pigs and embryonated eggs , 1982, Infection and immunity.

[47]  Rosa Araujo,et al.  Microbial and physicochemical parameters associated with Legionella contamination in hot water recirculation systems , 2013, Environmental Science and Pollution Research.

[48]  Rahman S Hariri,et al.  Evaluation of a New Monochloramine Generation System for Controlling Legionella in Building Hot Water Systems , 2014, Infection Control & Hospital Epidemiology.

[49]  B. Langlais,et al.  Action of Ozone on Trophozoites and Free Amoeba cysts, Whether Pathogenic or Not , 1986 .

[50]  Gilbert GREUB,et al.  Amoebae-resisting bacteria in drinking water: risk assessment and management. , 2008, Water science and technology : a journal of the International Association on Water Pollution Research.

[51]  LEGIONNAIRES' DISEASE: REDUCTION IN RISKS ASSOCIATED WITH FOAMING IN EVAPORATIVE COOLING TOWERS , 1987, The Lancet.

[52]  P. Yiallouros,et al.  First outbreak of nosocomial Legionella infection in term neonates caused by a cold mist ultrasonic humidifier. , 2013, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[53]  S. Yoshida,et al.  Development of a new seminested PCR method for detection of Legionella species and its application to surveillance of legionellae in hospital cooling tower water , 1997, Applied and environmental microbiology.

[54]  Y. Kwaik Invasion of mammalian and protozoan cells by Legionella pneumophila. , 2000, Sub-cellular biochemistry.

[55]  J. Froines,et al.  UNITED STATES ENVIRONMENTAL PROTECTION AGENCY , 1995 .

[56]  J. Lindo,et al.  Pathogenic Acanthamoeba strains from water sources in Jamaica, West Indies , 2005, Annals of tropical medicine and parasitology.

[57]  N. Garrec,et al.  Efficiency of water disinfectants against Legionella pneumophila and Acanthamoeba. , 2011, Water research.

[58]  S. Yoshida,et al.  Temperature-Regulated Formation of Mycelial Mat-Like Biofilms by Legionella pneumophila , 2006, Applied and Environmental Microbiology.

[59]  J. D. de Jonckheere Occurrence of Naegleria and Acanthamoeba in aquaria , 1979, Applied and environmental microbiology.

[60]  K. Botzenhart,et al.  Inactivation of Bacteria and Coliphages by Ozone and Chlorine Dioxide in a Continuous Flow Reactor , 1993 .

[61]  C. Anselme,et al.  Élimination des amibes libres par les procédés de traitement de l’eau potable , 2008 .

[62]  C. Haas,et al.  Legionnaires' disease: evaluation of a quantitative microbial risk assessment model. , 2008, Journal of water and health.

[63]  A. Calderón,et al.  Pathogenic and free-living amoebae isolated from swimming pools and physiotherapy tubs in Mexico. , 1993, Environmental Research.

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

[65]  R. L. Sauer,et al.  Effects of culture conditions and biofilm formation on the iodine susceptibility of Legionella pneumophila. , 1992, Canadian journal of microbiology.

[66]  Gilbert Greub,et al.  Biodiversity of Amoebae and Amoeba-Resisting Bacteria in a Hospital Water Network , 2006, Applied and Environmental Microbiology.

[67]  P. Karanis,et al.  Isolation and genotyping of potentially pathogenic Acanthamoeba and Naegleria species from tap-water sources in Osaka, Japan , 2009, Parasitology Research.

[68]  J. Loret,et al.  Disinfection of domestic water systems for Legionella pneumophila , 2003 .

[69]  Lisa B. Gelling,et al.  Reducing Legionella Colonization of Water Systems with Monochloramine , 2006, Emerging infectious diseases.

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

[71]  R. Field,et al.  Quantitative real-time PCR analysis of total and propidium monoazide-resistant fecal indicator bacteria in wastewater. , 2009, Water research.

[72]  M. Lechevallier,et al.  Regrowth of Potential Opportunistic Pathogens and Algae in Reclaimed-Water Distribution Systems , 2010, Applied and Environmental Microbiology.

[73]  Y. Kwaik,et al.  Cell biology of the intracellular infection by Legionella pneumophila. , 2004, Microbes and infection.

[74]  L. LaPat-Polasko,et al.  Identification of Naegleria fowleri in Domestic Water Sources by Nested PCR , 2003, Applied and Environmental Microbiology.

[75]  F. Ollevier,et al.  Replication of Legionella pneumophila in biofilms of water distribution pipes. , 2009, Microbiological research.

[76]  J. Lorenzo-Morales,et al.  Isolation and identification of pathogenic Acanthamoeba strains in Tenerife, Canary Islands, Spain from water sources , 2005, Parasitology Research.

[77]  C. Buchrieser,et al.  Specific Real-Time PCR for Simultaneous Detection and Identification of Legionella pneumophila Serogroup 1 in Water and Clinical Samples , 2010, Applied and Environmental Microbiology.

[78]  E. Shotts,et al.  Survival of coliforms and bacterial pathogens within protozoa during chlorination , 1988, Applied and environmental microbiology.

[79]  P. Lambert,et al.  Influence of intra-amoebic and other growth conditions on the surface properties of Legionella pneumophila , 1993, Infection and immunity.

[80]  Anne K Camper,et al.  Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. , 2006, Journal of microbiological methods.

[81]  Changyu Zhang,et al.  A Study on Urban Water Reuse Management Modeling , 2006 .

[82]  Tara D. Raftery,et al.  Altered Host Cell–Bacteria Interaction due to Nanoparticle Interaction with a Bacterial Biofilm , 2012, Microbial Ecology.

[83]  R. Berkelman,et al.  Increasing incidence of legionellosis in the United States, 1990-2005: changing epidemiologic trends. , 2008, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[84]  R. Armon,et al.  Legionella pneumophila serogroup 3 prevalence in drinking water survey in Israel (2003–2007) , 2010 .

[85]  W. Hijnen,et al.  Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. , 2006, Water research.

[86]  Mahesh G. Nagarkatti,et al.  Ozone in Water Treatment: Application and Engineering , 1991 .

[87]  C. W. Keevil,et al.  Control ofLegionella pneumophila in a hospital water system by chlorine dioxide , 1995, Journal of Industrial Microbiology.

[88]  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.

[89]  A. Rubin,et al.  Inactivation of Naegleria and Giardia cysts in water by ozonation , 1984 .

[90]  C. Gerba,et al.  Influence of residence time of reclaimed water within distribution systems on water quality , 2013 .

[91]  P. Pernin,et al.  Application of isoenzymatic typing to the identification of nonaxenic strains ofNaegleria (Protozoa, Rhizopoda) , 2004, Parasitology Research.

[92]  F. M. da Silva,et al.  Genotyping, physiological features and proteolytic activities of a potentially pathogenic Acanthamoeba sp. isolated from tap water in Brazil. , 2009, Experimental parasitology.

[93]  Y. Tsai,et al.  Detection of Legionella species in sewage and ocean water by polymerase chain reaction, direct fluorescent-antibody, and plate culture methods , 1993, Applied and environmental microbiology.

[94]  C. Gaylarde,et al.  Comparison of sodium hypochlorite and peracetic acid as sanitising agents for stainless steel food processing surfaces using epifluorescence microscopy. , 2000, International journal of food microbiology.

[95]  John N. Dowling,et al.  Impact of Chlorine and Heat on the Survival of Hartmannella vermiformis and Subsequent Growth of Legionella pneumophila , 1993, Applied and environmental microbiology.

[96]  D. Frazer,et al.  Acanthamoeba keratitis: the role of domestic tap water contamination in the United Kingdom. , 2004, Investigative ophthalmology & visual science.

[97]  B. Fields,et al.  Type IV pili and type II secretion play a limited role in Legionella pneumophila biofilm colonization and retention. , 2006, Microbiology.

[98]  S. Kilvington Activity of water biocide chemicals and contact lens disinfectants on pathogenic free-living amoebae , 1990 .

[99]  J. Clancy,et al.  Naegleria fowleri: An emerging drinking water pathogen , 2014 .

[100]  L. Tay,et al.  Comparison of polymerase chain reaction and conventional culture for the detection of legionellae in cooling tower waters in Singapore , 1997, Letters in applied microbiology.

[101]  P. Cabanes,et al.  Development of a nested PCR assay to detect the pathogenic free-living amoeba Naegleria fowleri , 2002, Parasitology Research.

[102]  J. Gleason,et al.  Community outbreak of legionellosis and an environmental investigation into a community water system , 2014, Epidemiology and Infection.

[103]  D. T. John,et al.  Seasonal distribution of pathogenic free-living amebae in Oklahoma waters , 1995, Parasitology Research.

[104]  B. J. Hayes,et al.  Occurrence of infected amoebae in cooling towers compared with natural aquatic environments: implications for emerging pathogens. , 2006, Environmental science & technology.