Do free-living amoebae in treated drinking water systems present an emerging health risk?

There is an expanding body of evidence that free-living amoebae (FLA) increase both the numbers and virulence of water-based, human-pathogenic, amoeba-resisting microorganisms (ARM). Legionella spp., Mycobacterium spp., and other opportunistic human pathogens are known to be both ARM and also the etiologic agents of potentially fatal human lung infections. However, comparatively little is known about the FLA that may facilitate ARM growth in drinking water. This review examines the available literature on FLA in treated drinking water systems; in total 26 studies from 18 different countries. FLA were reported to breakthrough the water treatment barrier and enter distribution systems, in addition to the expected post-treatment system ingress. Once in the distribution system there is evidence of FLA colonization and regrowth especially in reservoirs and in-premise plumbing storage tanks. At the point of use the average FLA detection rate was 45% but highly variable (n = 16, σ = 31) due to both differences in both assay methods and the type of water systems examined. This review reveals that FLA are consistently detected in treated drinking water systems around the world and present a yet unquantified emerging health risk. However, more research is urgently required before accurate risks assessments can be undertaken to assess the impacts on human health, in households and institutions, due to exposure to FLA facilitated pathogenic ARM.

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

[2]  K. Birkness,et al.  Mycobacterium avium Bacilli Grow Saprozoically in Coculture with Acanthamoeba polyphaga and Survive within Cyst Walls , 1998, Applied and Environmental Microbiology.

[3]  C. Amblard,et al.  Seasonal evolution of microbial community structure in a drinking water reservoir , 1996 .

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

[5]  R. Hoffmann,et al.  Distribution of free-living amoebae (FLA) during preparation and supply of drinking water. , 2001, International journal of hygiene and environmental health.

[6]  G. Visvesvara Classification of Acanthamoeba. , 1991, Reviews of infectious diseases.

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

[8]  R. Baker,et al.  Interactions between Naegleria fowleri and Legionella pneumophila , 1985, Infection and immunity.

[9]  H Alizadeh,et al.  Resistance of Acanthamoeba castellanii Cysts to Physical, Chemical, and Radiological Conditions , 2002, The Journal of parasitology.

[10]  Rowbotham Tj,et al.  Current views on the relationships between amoebae, legionellae and man. , 1986 .

[11]  F. Schuster,et al.  Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. , 2004, International journal for parasitology.

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

[13]  Michael Wagner,et al.  Amoebae as Training Grounds for Intracellular Bacterial Pathogens , 2005, Applied and Environmental Microbiology.

[14]  A. Maciejewska,et al.  The Occurrence Acanthamoeba (Free Living Amoeba) in Environmental and Respiratory Samples in Poland , 2009 .

[15]  T. Fritsche,et al.  Occurrence of bacterial endosymbionts in Acanthamoeba spp. isolated from corneal and environmental specimens and contact lenses , 1993, Journal of clinical microbiology.

[16]  T. Fenchel,et al.  Ecology of Protozoa: The Biology of Free-living Phagotrophic Protists , 1987 .

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

[18]  M. Jamerson,et al.  Free-living amoebae, Legionella and Mycobacterium in tap water supplied by a municipal drinking water utility in the USA. , 2010, Journal of water and health.

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

[20]  R. Breiman,et al.  Incubation of water samples containing amoebae improves detection of legionellae by the culture method , 1992, Applied and environmental microbiology.

[21]  S. Falkow,et al.  Growth of Legionella pneumophila in Acanthamoeba castellanii enhances invasion , 1994, Infection and immunity.

[22]  D. Lecky,et al.  Bacterial-protozoa interactions; an update on the role these phenomena play towards human illness. , 2006, Microbes and infection.

[23]  F. Rivera,et al.  Pathogenic and free-living protozoa cultured from the nasopharyngeal and oral regions of dental patients: II. , 1986, Environmental research.

[24]  I. V. van Driel,et al.  Molecular Pathogenesis of Infections Caused by Legionella pneumophila , 2010, Clinical Microbiology Reviews.

[25]  M. Heidtman,et al.  The Legionella pneumophila replication vacuole: making a cosy niche inside host cells , 2009, Nature Reviews Microbiology.

[26]  Gilbert GREUB,et al.  Amoeba/Amoebal Symbiont Genetic Transfers: Lessons from Giant Virus Neighbours , 2010, Intervirology.

[27]  I. Bolívar,et al.  Molecular phylogeny and classification of the lobose amoebae. , 2005, Protist.

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

[29]  E. Linder,et al.  Free-living Acanthamoeba and Naegleria spp. amebae in water sources of León, Nicaragua. , 2007, Revista de biologia tropical.

[30]  S. Hrudey,et al.  Published Case Studies of Waterborne Disease Outbreaks—Evidence of a Recurrent Threat , 2007, Water environment research : a research publication of the Water Environment Federation.

[31]  D. Caron,et al.  Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. , 2009, Trends in microbiology.

[32]  B. Barbeau,et al.  Protection of waterborne pathogens by higher organisms in drinking water: a review. , 2008, Canadian journal of microbiology.

[33]  C. Buchrieser,et al.  Molecular mimicry: an important virulence strategy employed by Legionella pneumophila to subvert host functions. , 2009, Future microbiology.

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

[35]  Y. Lévi,et al.  Amoebae in domestic water systems: resistance to disinfection treatments and implication in Legionella persistence , 2004, Journal of applied microbiology.

[36]  J. Chun,et al.  Phylogenetic characterization of Legionella-like endosymbiotic X-bacteria in Amoeba proteus: a proposal for 'Candidatus Legionella jeonii' sp. nov. , 2004, Environmental microbiology.

[37]  Gilbert GREUB,et al.  Saccamoeba lacustris, sp. nov. (Amoebozoa: Lobosea: Hartmannellidae), a new lobose amoeba, parasitized by the novel chlamydia 'Candidatus Metachlamydia lacustris' (Chlamydiae: Parachlamydiaceae). , 2010, European journal of protistology.

[38]  L. Engstrand,et al.  Uptake and Replication of Salmonella enterica in Acanthamoeba rhysodes , 2004, Applied and Environmental Microbiology.

[39]  J. Långmark,et al.  The effects of UV disinfection on distribution pipe biofilm growth and pathogen incidence within the greater Stockholm area, Sweden. , 2007, Water research.

[40]  M. Wagner,et al.  The Genome of the Amoeba Symbiont “Candidatus Amoebophilus asiaticus” Reveals Common Mechanisms for Host Cell Interaction among Amoeba-Associated Bacteria , 2009, Journal of bacteriology.

[41]  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.

[42]  M. Šuša,et al.  Heterogeneity in intracellular replication and cytopathogenicity of Legionella pneumophila and Legionella micdadei in mammalian and protozoan cells. , 1999, Microbial pathogenesis.

[43]  Gunther F. Craun,et al.  Causes of Outbreaks Associated with Drinking Water in the United States from 1971 to 2006 , 2010, Clinical Microbiology Reviews.

[44]  S. Kahane,et al.  Evidence for the Presence of Simkania negevensis in Drinking Water and in Reclaimed Wastewater in Israel , 2004, Applied and Environmental Microbiology.

[45]  O. Harb,et al.  Invasion of Protozoa by Legionella pneumophila and Its Role in Bacterial Ecology and Pathogenesis , 1998, Applied and Environmental Microbiology.

[46]  K. Caumo,et al.  Potentially Pathogenic Acanthamoeba Isolated from a Hospital in Brazil , 2010, Current Microbiology.

[47]  Fabien Burki,et al.  Untangling the Phylogeny of Amoeboid Protists 1 , 2009, The Journal of eukaryotic microbiology.

[48]  C. Gerba,et al.  Health effects of Acanthamoeba spp. and its potential for waterborne transmission. , 2004, Reviews of environmental contamination and toxicology.

[49]  D. Raoult,et al.  Parachlamydia acanthamoeba Is Endosymbiotic or Lytic for Acanthamoeba polyphaga Depending on the Incubation Temperature , 2003, Annals of the New York Academy of Sciences.

[50]  H. Jeong,et al.  The role of domestic tap water in Acanthamoeba contamination in contact lens storage cases in Korea. , 2005, The Korean journal of parasitology.

[51]  R. Breiman,et al.  Association of shower use with Legionnaires' disease. Possible role of amoebae. , 1990, JAMA.

[52]  D. Seal,et al.  Microbial keratitis in Hong Kong: relationship to climate, environment and contact-lens disinfection. , 2001, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[53]  H. Mergeryan The prevalence of Acanthamoeba in the human environment. , 1991, Reviews of infectious diseases.

[54]  R. Qualls,et al.  UV inactivation of pathogenic and indicator microorganisms , 1985, Applied and environmental microbiology.

[55]  C. Buchrieser,et al.  Legionella pneumophila — a human pathogen that co-evolved with fresh water protozoa , 2007, Cellular and Molecular Life Sciences.

[56]  Stefan Panaiotov,et al.  The identification of free-living environmental isolates of amoebae from Bulgaria , 2004, Parasitology Research.

[57]  J. Barbeau,et al.  Biofilms augment the number of free-living amoebae in dental unit waterlines. , 2001, Research in microbiology.

[58]  R. Bentham,et al.  The efficacy of biocides and other chemical additives in cooling water systems in the control of amoebae , 2009, Journal of applied microbiology.

[59]  S. Field,et al.  Lung disease due to the more common nontuberculous mycobacteria. , 2006, Chest.

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

[61]  P. Cho,et al.  Detection of Acanthamoeba in Tap Water and Contact Lens Cases Using Polymerase Chain Reaction , 2008, Optometry and vision science : official publication of the American Academy of Optometry.

[62]  M. Coletta,et al.  Standardized Method of MeasuringAcanthamoeba Antibodies in Sera from Healthy Human Subjects , 2001, Clinical Diagnostic Laboratory Immunology.

[63]  K. Heuner,et al.  Dictyostelium as host model for pathogenesis , 2005, Cellular microbiology.

[64]  M. R. Brown,et al.  Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. , 1994, Microbiology.

[65]  T. Rowbotham,et al.  Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. , 1980, Journal of clinical pathology.

[66]  S. Kahane,et al.  Infection of Acanthamoeba polyphagawith Simkania negevensis and S. negevensis Survival within Amoebal Cysts , 2001, Applied and Environmental Microbiology.

[67]  Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution , 2010 .

[68]  S. Hrudey,et al.  Drinking-water safety: challenges for community-managed systems. , 2008, Journal of water and health.

[69]  S. Berk,et al.  Stimulatory effect of cooling tower biocides on amoebae , 1993, Applied and environmental microbiology.

[70]  L. Zöller,et al.  An extraordinary endocytobiont in Acanthamoeba sp. isolated from a patient with keratitis , 2008, Parasitology Research.

[71]  Susan J. Brown,et al.  Guide to the methods of study and identification of soil gymnamoebae , 2004 .

[72]  Gilbert GREUB,et al.  Amoebal pathogens as emerging causal agents of pneumonia. , 2010, FEMS microbiology reviews.

[73]  Gilbert Greub,et al.  Biodiversity of amoebae and amoeba-associated bacteria in water treatment plants. , 2010, International journal of hygiene and environmental health.

[74]  H. Smidt,et al.  Free-Living Protozoa in Two Unchlorinated Drinking Water Supplies, Identified by Phylogenic Analysis of 18S rRNA Gene Sequences , 2009, Applied and Environmental Microbiology.

[75]  H. Tanowitz,et al.  Diagnosis of Infections Caused by Pathogenic Free-Living Amoebae , 2009, Interdisciplinary perspectives on infectious diseases.

[76]  O. Harb,et al.  From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. , 2000, Environmental microbiology.

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

[78]  D V Seal,et al.  Prevalence of Acanthamoeba and other naked amoebae in South Florida domestic water. , 2008, Journal of water and health.

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

[80]  M V Storey,et al.  Biofilms, thermophilic amoebae and Legionella pneumophila--a quantitative risk assessment for distributed water. , 2004, Water science and technology : a journal of the International Association on Water Pollution Research.

[81]  H. Voorde,et al.  Differences in destruction of cysts of pathogenic and nonpathogenic Naegleria and Acanthamoeba by chlorine. , 1976 .

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

[83]  R Amann,et al.  Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii , 1997, Applied and environmental microbiology.

[84]  H. Northoff,et al.  Influence of Acanthamoeba castellanii on Intracellular Growth of Different Legionella Species in Human Monocytes , 2000, Applied and Environmental Microbiology.

[85]  Barry S. Fields,et al.  Legionella and Legionnaires' Disease: 25 Years of Investigation , 2002, Clinical Microbiology Reviews.

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

[87]  L. Bermudez,et al.  Mycobacterium avium Grown inAcanthamoeba castellanii Is Protected from the Effects of Antimicrobials , 2000, Antimicrobial Agents and Chemotherapy.

[88]  G. Puzon,et al.  Rapid detection of Naegleria fowleri in water distribution pipeline biofilms and drinking water samples. , 2009, Environmental science & technology.

[89]  P. Bonilla-Lemus,et al.  Acanthamoeba spp. in domestic tap water in houses of contact lens wearers in the metropolitan area of Mexico City. , 2010, Experimental parasitology.

[90]  R. Hoffmann,et al.  Natural infection with microsporidian organisms (KW19) in Vannella spp. (Gymnamoebia) isolated from a domestic tap-water supply , 1997, Parasitology Research.

[91]  A. Bomo,et al.  Bacterial removal and protozoan grazing in biological sand filters. , 2004, Journal of environmental quality.

[92]  T. Broman,et al.  Protozoan Acanthamoeba polyphaga as a Potential Reservoir for Campylobacter jejuni , 2005, Applied and Environmental Microbiology.

[93]  J. Costerton A Short History of the Development of the Biofilm Concept , 2004 .

[94]  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.

[95]  W. Johnson,et al.  Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion , 1996, Infection and immunity.

[96]  Gilbert Greub,et al.  Microorganisms Resistant to Free-Living Amoebae , 2004, Clinical Microbiology Reviews.

[97]  S. Rodríguez-Zaragoza Ecology of free-living amoebae. , 1994, Critical reviews in microbiology.

[98]  Christian Amblard,et al.  Evolution saisonniere de la structure des communautes microbiennes dans un reservoir d'eau potable , 1996 .

[99]  B. Drasar,et al.  Association of Vibrio cholerae with fresh water amoebae. , 1992, Journal of medical microbiology.

[100]  M. Woodhead Community-acquired pneumonia in Europe: causative pathogens and resistance patterns , 2002, European Respiratory Journal.

[101]  E. Linder,et al.  Free-living amoebae protecting Legionella in water: the tip of an iceberg? , 1999, Scandinavian journal of infectious diseases.

[102]  S Falkow,et al.  Interaction of Mycobacterium avium with environmental amoebae enhances virulence , 1997, Infection and immunity.

[103]  R. Tyndall,et al.  Cocultivation of Legionella pneumophila and free-living amoebae , 1982, Applied and environmental microbiology.

[104]  M. Valvano,et al.  Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. , 1999, Microbiology.

[105]  P. Servais,et al.  Efficacy of disinfectant residualon microbial intrusion: A review of experiments , 2008 .

[106]  D. Seal,et al.  Possible environmental sources of Acanthamoeba spp in contact lens wearers. , 1992, British Journal of Ophthalmology.

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

[108]  Z Lewandowski,et al.  Biofilms, the customized microniche , 1994, Journal of bacteriology.

[109]  K. Schleifer,et al.  Microbiological safety of drinking water. , 2000, Annual review of microbiology.

[110]  B. Fields,et al.  Legionella pneumophila associated with the protozoan Hartmannella vermiformis in a model multi-species biofilm has reduced susceptibility to disinfectants , 2005, Biofouling.

[111]  E. Linder,et al.  Bacterial infections of free-living amoebae. , 2001, Research in microbiology.

[112]  M. R. Brown,et al.  Relationship between Legionella pneumophila and Acanthamoeba polyphaga: Physiological Status and Susceptibility to Chemical Inactivation , 1992, Applied and environmental microbiology.

[113]  J. Feeley,et al.  Intracellular multiplication ofLegionella pneumophila in amoebae isolated from hospital hot water tanks , 1989, Current Microbiology.