Environmental Science and Pollution Research

, Volume 22, Issue 9, pp 6610–6618 | Cite as

Effect of chlorine and temperature on free-living protozoa in operational man-made water systems (cooling towers and hot sanitary water systems) in Catalonia

  • Oriol Canals
  • Alejandra Serrano-Suárez
  • Humbert Salvadó
  • Javier Méndez
  • Sílvia Cervero-Aragó
  • Vicenç Ruiz de Porras
  • Jordi Dellundé
  • Rosa Araujo
Research Article
First Online:
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Accepted:

Abstract

In recent decades, free-living protozoa (FLP) have gained prominence as the focus of research studies due to their pathogenicity to humans and their close relationship with the survival and growth of pathogenic amoeba-resisting bacteria. In the present work, we studied the presence of FLP in operational man-made water systems, i.e. cooling towers (CT) and hot sanitary water systems (HSWS), related to a high risk of Legionella spp. outbreaks, as well as the effect of the biocides used, i.e. chlorine in CT and high temperature in HSWS, on FLP. In CT samples, high-chlorine concentrations (7.5 ± 1.5 mg chlorine L−1) reduced the presence of FLP by 63.8 % compared to samples with low-chlorine concentrations (0.04 ± 0.08 mg chlorine L−1). Flagellates and amoebae were observed in samples collected with a level of 8 mg chlorine L−1, which would indicate that some FLP, including the free-living amoeba (FLA) Acanthamoeba spp., are resistant to the discontinuous chlorine disinfection method used in the CT studied. Regarding HSWS samples, the amount of FLP detected in high-temperatures samples (53.1 ± 5.7 °C) was 38 % lower than in low-temperature samples (27.8 ± 5.8 °C). The effect of high temperature on FLP was chiefly observed in the results obtained by the culture method, in which there was a clear reduction in the presence of FLP at temperatures higher than 50 °C, but not in those obtained by PCR. The findings presented here show that the presence of FLP in operational man-made water systems should be taken into account in future regulations.

Keywords

Free-living amoebae Ciliates Chlorine Temperature Disinfection Free-living protozoa 
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Notes

Acknowledgments

This work was supported by the Spanish Ministry of Education and Science (MEC-CGL 2005–01465).

Conflict of interest

There is no conflict of interest.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2 CrossRefGoogle Scholar
  2. Barbeau J, Buhler T (2001) Biofilms augment the number of free-living amoebae in dental unit waterlines. Res Microbiol 152(8):753–760. doi: 10.1016/S0923-2508(01)01256-6 CrossRefGoogle Scholar
  3. Behets J, Declerck P, Delaedt Y, Verelst L, Ollevier F (2007) Survey for the presence of specific free-living amoebae in cooling waters from Belgian power plants. Parasitol Res 100(6):1249–1256. doi: 10.1007/s00436-006-0399-1 CrossRefGoogle Scholar
  4. Boletín Oficial del Estado (2003) Real Decreto 140/2003 por el que se establecen los criterios sanitarios de la calidad del agua de consumo humano. BOE 45:7228–7245Google Scholar
  5. Cateau E, Delafont V, Hechard Y, Rodier MH (2014) Free-living amoebae: what part do they play in healthcare-associated infections? J Hosp Infect 87:131–140. doi: 10.1016/j.jhin.2014.05.001 CrossRefGoogle Scholar
  6. Cervero-Aragó S, Rodríguez-Martínez S, Canals O, Salvadó H, Araujo R (2013) Effect of thermal treatment on free-living amoeba inactivation. J Appl Microbiol 116(3):728–736. doi: 10.1111/jam.12379 CrossRefGoogle Scholar
  7. Coloun C, Collignon A, McDonnell G, Thomas V (2010) Resistance of Acanthamoeba cysts to disinfection treatments used in health care settings. J Clin Microbiol 48(8):2689–2697. doi: 10.1128/JCM. 00309-10 CrossRefGoogle Scholar
  8. Delafont V, Brouke A, Bouchon D, Moulin L, Héchard Y (2013) Microbiome of free-living amoebae isolated from drinking water. Water Res 47(19):6958–6965. doi: 10.1016/j.watres.2013.07.047 CrossRefGoogle Scholar
  9. Fernández-Galiano D (1994) The ammoniacal silver carbonate method as a general procedure in the study of protozoa from sewage (and other) waters. Water Res 28(2):495–496. doi: 10.1016/0043-1354(94)90288-7 CrossRefGoogle Scholar
  10. Fields BS, Shotts EB Jr, Feeley JC, Gorman GW, Martin WT (1984) Proliferation of Legionella pneumophila as an intracellular parasite of the ciliated protozoan Tetrahymena pyriformis. Appl Environ Microbiol 47(3):467–471Google Scholar
  11. Foissner W (1993) Colpodea. Gustav Fischer Verlag, StuttgartGoogle Scholar
  12. Greub G, Raoult D (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17(2):413–433. doi: 10.1128/CMR. 17.2.413-433.2004 CrossRefGoogle Scholar
  13. International Organization for Standardization. 2005. Water quality - General guidance on the enumeration of micro-organisms by culture. ISO 8199:2005Google Scholar
  14. Kim BR, Anderson JE, Mueller SA, Gaines WA, Kendall AM (2002) Literature review—efficacy of various disinfectants against Legionella in water systems. Water Res 36(18):4433–4444. doi: 10.1016/S0043-1354(02)00188-4 CrossRefGoogle Scholar
  15. Kuchta JM, Navratil JS, Shepherd ME, Wadowsky RM, Dowling JN, States SJ, Yee RB (1993) Impact of chlorine and heat on the survival of Hartmannella vermiformis and subsequent growth of Legionella pneumophila. Appl Environ Microbiol 59(12):4096–4100Google Scholar
  16. Lasheras A, Boulestreau H, Rogues AM, Ohayon-Courtes C, Labadie JC, Gachie JP (2006) Influence of amoebae and physical and chemical characteristics of water on presence and proliferation of Legionella species in hospital water systems. Am J Infect Control 34(8):520–525. doi: 10.1016/j.ajic.2006.03.007 CrossRefGoogle Scholar
  17. Lee JJ, Soldo AT (Eds.) (1992) Protocols in protozoology. AllenPress, Inc. Lawrence, KansasGoogle Scholar
  18. Lee S, Leedale GF, Bradbury P (Eds.) (2000) The illustrated guide to the protozoa. In: Society of Protozoologists, second ed., vol. I and II. Allen Press, Inc, Lawrence, KansasGoogle Scholar
  19. Loret JF, Greub G (2010) Free-living amoebae: biological by-passes in water treatment. Int J Hyg Environ Health 213(3):167–175. doi: 10.1016/j.ijheh.2010.03.004 CrossRefGoogle Scholar
  20. Ménard-Szczebara F, Berthelot N, Cavereau D, Oberti S, Héchard Y, Sarroca V, Rivière D, Mazoua S (2008) Ecology of free-amoebae in real in-house water networks. Eur J Water Qual 39:65–76 (in French)CrossRefGoogle Scholar
  21. Mogoa E, Bodet C, Legube B, Héchard Y (2010) Acanthamoeba castellanii: cellular changes induced by chlorination. Exp Parasitol 126(1):97–102. doi: 10.1016/j.exppara.2009.12.005 CrossRefGoogle Scholar
  22. Page FC (1988) A New Key to Freshwater and Soil Gymnamoebae with Instructions for Culture. Freshwater Biological Association, AmblesideGoogle Scholar
  23. Paszko-Kolva C, Yamamoto H, Shahamat M, Sawyer TK, Morris G, Colwell RR (1991) Isolation of amoebae and Pseudomonas and Legionella spp. from eyewash stations. Appl Environ Microbiol 57(1):163–167Google Scholar
  24. Patterson WJ, Hay J, Seal DV, McLuckie JC (1997) Colonization of transplant unit water supplies with Legionella and protozoa: precautions required to reduce the risk of legionellosis. J Hosp Infect 37(1):7–17. doi: 10.1016/S0195-6701(97)90068-2 CrossRefGoogle Scholar
  25. Rohr U, Weber S, Michel R, Selenka F, Wilhelm M (1998) Comparison of free-living amoebae in hot water systems of hospitals with isolates from moist sanitary areas by identifying genera and determining temperature tolerance. Appl Environ Microbiol 64(5):1822–1824Google Scholar
  26. Rowbotham TJ (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33(12):1179–1183. doi: 10.1136/jcp.33.12.1179 CrossRefGoogle Scholar
  27. Serrano-Suárez A (2009) Relación de Legionella spp. con parámetros microbiológicos y fisicoquímicos en aguas. Dissertation, Universitat de BarcelonaGoogle Scholar
  28. Serrano-Suárez A, Dellundé J, Salvadó H, Cerveró-Aragó S, Méndez J, Canals O, Blanco S, Arcas A, Araujo R (2013) Microbial and physicochemical parameters associated with Legionella contamination in hot water recirculation systems. Environ Sci Pollut Res Int 20(8):5534–5544. doi: 10.1007/s11356-013-1557-5 CrossRefGoogle Scholar
  29. Shoff ME, Rogerson A, Kessler K, Schatz S, Seal DV (2008) Prevalence of Acanthamoeba and other naked amoebae in South Florida domestic water. J Water Health 6(1):99–104. doi: 10.2166/wh.2007.014 CrossRefGoogle Scholar
  30. Storey MV, Winiecka-Krusnell J, Ashbolt NJ, Stenström TA (2004) The efficacy of heat and chlorine treatment against thermotolerant Acanthamoebae and Legionellae. Scand J Infect Dis 36(9):656–662. doi: 10.1080/00365540410020785 CrossRefGoogle Scholar
  31. Sutherland EE, Berk SG (1996) Survival of protozoa in cooling tower biocides. J Ind Microbiol 16(1):73–78. doi: 10.1007/BF01569925 CrossRefGoogle Scholar
  32. Thomas V, Bouchez T, Nicolas V, Robert S, Loret JF, Levi Y (2004) Amoebae in domestic water systems: resistance to disinfection treatments and implication in Legionella persistence. J Appl Microbiol 97(5):950–963. doi: 10.1111/j.1365-2672.2004.02391.x CrossRefGoogle Scholar
  33. Thomas V, Herrera-Rimann K, Blanc DS, Greub G (2006) Biodiversity of amoebae and amoeba-resisting bacteria in a hospital water network. Appl Environ Microbiol 72(4):2428–2438. doi: 10.1128/AEM. 72.4.2428-2438.2006 CrossRefGoogle Scholar
  34. Thomas V, Loret JF, Jousset M, Greub G (2008) Biodiversity of amoebae-resisting bacteria in a drinking water treatment plant. Environ Microbiol 10(10):2728–2745. doi: 10.1111/j.1462-2920.2008.01693.x CrossRefGoogle Scholar
  35. Trabelsi H, Dendana F, Sellami A, Sellami H, Cheikhrouhou F, Neji S, Makni F, Ayadi A (2012) Pathogenic free-living amoebae: epidemiology and clinical review. Pathol Biol 60(6):399–405. doi: 10.1016/j.patbio.2012.03.002 CrossRefGoogle Scholar
  36. Valster RM, Wullings BA, Bakker G, Smidt H, van der Kooij D (2009) Free-living protozoa in two unchlorinated drinking water supplies, identified by phylogenic analysis of 18S rRNA gene sequences. Appl Environ Microbiol 75(14):4736–4746. doi: 10.1128/AEM. 02629-08 CrossRefGoogle Scholar
  37. Visvesvara GS, Moura H, Schuster FL (2007) Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri and Sappinia diploidea. FEMS Immunol Med Microbiol 50(1):1–26. doi: 10.1111/j.1574-695X.2007.00232.x CrossRefGoogle Scholar
  38. Yamamoto H, Sugiura M, Kusunoki S, Yukiezaki T, Ikedo M, Yabuuchi E (1992) Factors stimulating propagation of Legionellae in cooling tower water. Appl Environ Microbiol 58(4):1394–1397Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Oriol Canals
    • 1
  • Alejandra Serrano-Suárez
    • 2
  • Humbert Salvadó
    • 1
  • Javier Méndez
    • 2
  • Sílvia Cervero-Aragó
    • 2
  • Vicenç Ruiz de Porras
    • 2
  • Jordi Dellundé
    • 3
  • Rosa Araujo
    • 2
  1. 1.Laboratory of Protistology, Departament de Biologia Animal, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  2. 2.Departament de Microbiologia, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain
  3. 3.J.D. AssessorsBarcelonaSpain

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