Abstract
The use of lagooning as a complementary natural method of treating secondary effluents of wastewater treatment plants has been employed as an affordable and easy means of producing reclaimed water. However, using reclaimed water for some purposes, for example, for food irrigation, presents some risks if the effluents contain microbial pathogens. Classical bacterial indicators that are used to assess faecal contamination in water do not always properly indicate the presence of bacterial or viral pathogens. In the current study, the presence of faecal indicator bacteria (FIB), heterotrophic bacterial counts (HBC), pathogens and opportunistic pathogens, such as Legionella spp., Aeromonas spp., Arcobacter spp., free-living amoeba (FLA), several viral indicators (human adenovirus and polyomavirus JC) and viral pathogens (noroviruses and hepatitis E virus) were analysed for 1 year in inlet and outlet water to assess the removal efficiency of a lagooning system. We observed 2.58 (1.17–4.59) and 1.65 (0.15–3.14) log reductions in Escherichia coli (EC) and intestinal enterococci (IE), respectively, between the inlet and outlet samples. Genomic copies of the viruses were log reduced by 1.18 (0.24–2.93), 0.64 (0.12–1.97), 0.45 (0.04–2.54) and 0.72 (0.22–2.50) for human adenovirus (HAdV), JC polyomavirus (JCPyV) and human noroviruses (NoV GI and GII), respectively. No regrowth of opportunistic pathogens was observed within the system. FLA, detected in all samples, did not show a clear trend. The reduction of faecal pathogens was irregular with 6 out of 12 samples and 4 out of 12 samples exceeding the EC and IE values, specified in the Spanish legislation for reclaimed water (RD 1620/2007). This data evidences that there is a need for more studies to evaluate the removal mechanisms of lagooning systems in order to optimize pathogen reduction. Moreover, surveillance of water used to irrigate raw edible vegetables should be conducted to ensure the fulfilment of the microbial requirements for the production of safe reclaimed water.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allard A, Albinsson B, Wadell G (2001) Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. J Clin Microbiol 39(2):498–505, Available from: http://jcm.asm.org/content/39/2/498
Baggi F, Demarta A, Peduzzi R (2001) Persistence of viral pathogens and bacteriophages during sewage treatment: lack of correlation with indicator bacteria. Res Microbiol 152(8):743–51, Available from: http://www.ncbi.nlm.nih.gov/pubmed/11686388
Battistini R, Marcucci E, Verani M, Di Giuseppe G, Dini F, Carducci A (2013) Ciliate-adenovirus interactions in experimental co-cultures of Euplotes octocarinatus and in wastewater environment. Eur J Protistol 49(3):381–8, Available from: http://www.sciencedirect.com/science/article/pii/S0932473912000946
Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29(4):1165–88
Berg G (1973) Removal of viruses from sewage, effluents, and waters. I. A review. Bull World Health Organ 49(5):451–60, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2480995&tool=pmcentrez&rendertype=abstract
Bernard H, Faber M, Wilking H, Haller S, Höhle M, Schielke A et al (2014) Large multistate outbreak of norovirus gastroenteritis associated with frozen strawberries, Germany, 2012. Euro Surveil 19(8):20719, Available from: http://www.ncbi.nlm.nih.gov/pubmed/24602278
Blanky M, Rodríguez-Martínez S, Halpern M, Friedler E (2015) Legionella pneumophila: from potable water to treated greywater; quantification and removal during treatment. Sci Total Environ 533:557–65, Available from: http://www.ncbi.nlm.nih.gov/pubmed/26188406
Bofill-Mas S, Albinana-Gimenez N, Clemente-Casares P, Hundesa A, Rodriguez-Manzano J, Allard A et al (2006) Quantification and stability of human adenoviruses and polyomavirus JCPyV in wastewater matrices. Appl Environ Microbiol 72(12):7894–6, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1694247&tool=pmcentrez&rendertype=abstract
Bofill-Mas S, Rusiñol M, Fernandez-Cassi X, Carratalà A, Hundesa A, Girones R (2013) Quantification of human and animal viruses to differentiate the origin of the fecal contamination present in environmental samples. Biomed Res Int 2013:192089, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3671278&tool=pmcentrez&rendertype=abstract
Calgua B, Mengewein A, Grunert A, Bofill-Mas S, Clemente-Casares P, Hundesa A et al (2008) Development and application of a one-step low cost procedure to concentrate viruses from seawater samples. J Virol Methods 153(2):79–83, Available from: http://www.ncbi.nlm.nih.gov/pubmed/18765255
Calgua B, Rodriguez-Manzano J, Hundesa A, Suñen E, Calvo M, Bofill-Mas S et al (2013) New methods for the concentration of viruses from urban sewage using quantitative PCR. J Virol Methods 187(2):215–21, Available from: http://www.sciencedirect.com/science/article/pii/S0166093412003710
Callejón RM, Rodríguez-Naranjo MI, Ubeda C, Hornedo-Ortega R, Garcia-Parrilla MC, Troncoso AM (2015) Reported foodborne outbreaks due to fresh produce in the United States and European Union: trends and causes. Foodborne Pathog Dis 12(1):32–8, Available from: http://www.ncbi.nlm.nih.gov/pubmed/25587926
Campos C, Guerrero A, Cárdenas M (2002) Removal of bacterial and viral faecal indicator organisms in a waste stabilization pond system in Choconta, Cundinamarca (Colombia). Water Sci Technol 45(1):61–6, Available from: http://www.ncbi.nlm.nih.gov/pubmed/11833732
Carter MJ (2005) Enterically infecting viruses: pathogenicity, transmission and significance for food and waterborne infection. J Appl Microbiol 98(6):1354–80, Available from: http://www.ncbi.nlm.nih.gov/pubmed/15916649
Cervero-Aragó S, Rodríguez-Martínez S, Canals O, Salvadó H, Araujo RM (2013) Effect of thermal treatment on free-living amoeba inactivation. J Appl Microbiol. Oct 30 [cited 2014 Dec 28]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/24251398
Cervero-Aragó S, Rodríguez-Martínez S, Puertas-Bennasar A, Araujo RM (2015) Effect of common drinking water disinfectants, chlorine and heat, on free legionella and Amoebae-associated Legionella. PLoS One 10(8):e0134726, Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0134726
Chacón MR, Castro-Escarpulli G, Soler L, Guarro J, Figueras MJ (2002) A DNA probe specific for Aeromonas colonies. Diagn Microbiol Infect Dis 44(3):221–5, Available from: http://www.ncbi.nlm.nih.gov/pubmed/12493167
Collado L, Figueras MJ (2011) Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter. Clin Microbiol Rev 24(1):174–92, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3021208&tool=pmcentrez&rendertype=abstract
Collado L, Inza I, Guarro J, Figueras MJ (2008) Presence of Arcobacter spp. in environmental waters correlates with high levels of fecal pollution. Environ Microbiol 10(6):1635–40, Available from: http://www.ncbi.nlm.nih.gov/pubmed/18215159
Collado L, Kasimir G, Perez U, Bosch A, Pinto R, Saucedo G et al (2010) Occurrence and diversity of Arcobacter spp. along the Llobregat River catchment, at sewage effluents and in a drinking water treatment plant. Water Res 44(12):3696–702, Available from: http://www.ncbi.nlm.nih.gov/pubmed/20427071
R Core Team (2013) R: A language and environment for statistical computing. [Internet]. Available from: http://www.r-project.org/
Da Silva AK, Le Saux JC, Parnaudeau S, Pommepuy M, Elimelech M, Le Guyader FS (2007) Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Appl Environ Microbiol 73(24):7891–7
Danes L, Cerva L (1981) Survival of polioviruses and echoviruses in Acanthamoeba castellanii cultivated in vitro. J Hyg Epidemiol Microbiol Immunol 25(2):169–74, Available from: http://www.ncbi.nlm.nih.gov/pubmed/6265550
Danes L, Cerva L (1984) Poliovirus and echovirus survival in Tetrahymena pyriformis culture in vivo. J Hyg Epidemiol Microbiol Immunol 28(2):193–200, Available from: http://www.ncbi.nlm.nih.gov/pubmed/6088623
Dare A (2015) Irrigation with treated municipal wastewater in Indiana, United States. J Soil Water Conserv 70(4):89A–94A, Available from: http://www.jswconline.org/content/70/4/89A.extract
Declerck P (2010) Biofilms: the environmental playground of Legionella pneumophila. Environ Microbiol 12(3):557–66, Available from: http://www.ncbi.nlm.nih.gov/pubmed/19678829
Declerck P, Behets J, van Hoef V, Ollevier F (2007) Detection of Legionella spp. and some of their amoeba hosts in floating biofilms from anthropogenic and natural aquatic environments. Water Res 41(14):3159–67, Available from: http://www.ncbi.nlm.nih.gov/pubmed/17544473
Derry C, Attwater R (2014) Regrowth of enterococci indicator in an open recycled-water impoundment. Sci Total Environ 468-469:63–7, Available from: http://www.ncbi.nlm.nih.gov/pubmed/24008073
Diederen BMW, de Jong CMA, Marmouk F, Kluytmans JAJW, Peeters MF, Van der Zee A (2007) Evaluation of real-time PCR for the early detection of Legionella pneumophila DNA in serum samples. J Med Microbiol 56(Pt 1):94–101, Available from: http://www.ncbi.nlm.nih.gov/pubmed/17172523
Donnison AM, Ross CM (1995) Somatic and F-specific coliphages in New Zealand waste treatment lagoons. Water Res 29(4):1105–10, Available from: http://www.sciencedirect.com/science/article/pii/004313549400227X
Erker JC, Desai SM, Schlauder GG, Dawson GJ, Mushahwar IK (1999) A hepatitis E virus variant from the United States: molecular characterization and transmission in cynomolgus macaques. J Gen Virol 80(3):681–90, Available from: http://www.ncbi.nlm.nih.gov/pubmed/10092008
Figueras MJ, Borrego JJ (2010) New perspectives in monitoring drinking water microbial quality. Int J Environ Res Public Health 7(12):4179–202, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3037048&tool=pmcentrez&rendertype=abstract
Figueras MJ, Levican A, Collado L (2012) Updated 16S rRNA-RFLP method for the identification of all currently characterised Arcobacter spp. BMC Microbiol 12:292, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3548738&tool=pmcentrez&rendertype=abstract
Figueras MJ, Levican A, Pujol I, Ballester F, Rabada Quilez MJ, Gomez-Bertomeu F (2014) A severe case of persistent diarrhoea associated with Arcobacter cryaerophilus but attributed to Campylobacter sp. and a review of the clinical incidence of Arcobacter spp. New Microbes New Infect 2(2):31–7, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4184587&tool=pmcentrez&rendertype=abstract
Fisher JC, Levican A, Figueras MJ, McLellan SL (2014) Population dynamics and ecology of Arcobacter in sewage. Front Microbiol 5:525, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4224126&tool=pmcentrez&rendertype=abstract
Fleischer J, Schlafmann K, Otchwemah R, Botzenhart K (2000) Elimination of enteroviruses, other enteric viruses, F-specific coliphages, somatic coliphages and E. coli in four sewage treatment plants of southern Germany. J Water Supply Res Technol AQUA 49(3):127–38, Available from: http://aqua.iwaponline.com/content/49/3/127.abstract
Francy DS, Stelzer EA, Bushon RN, Brady AMG, Williston AG, Riddell KR et al (2012) Comparative effectiveness of membrane bioreactors, conventional secondary treatment, and chlorine and UV disinfection to remove microorganisms from municipal wastewaters. Water Res 46(13):4164–78, Available from: http://www.ncbi.nlm.nih.gov/pubmed/22682268
FSA (2006) Review of the analytical terminology for codex use in the procedural manual. FOOD Stand AGENCY Inf Bull METHODS Anal Sampl Foodst 68(March 2006):1–15
Garcia A, Goñi P, Cieloszyk J, Fernandez MT, Calvo-Beguería L, Rubio E et al (2013) Identification of free-living amoebae and amoeba-associated bacteria from reservoirs and water treatment plants by molecular techniques. Environ Sci Technol 47(7):3132–40
Gerba CP, Goyal SM, LaBelle RL, Cech I, Bodgan GF (1979) Failure of indicator bacteria to reflect the occurrence of enteroviruses in marine waters. Am J Public Health 69(11):1116–9, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1619291&tool=pmcentrez&rendertype=abstract
Goyal B (2013) Case study on evaluation of the performance of waste stabilization pond system of Jodhpur, Rajasthan, India. Water Pract Technol 8(1):95–104, Available from: http://wpt.iwaponline.com/content/8/1/wpt.2013011.abstract
Greub G, Raoult D (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17(2):413–33
Gurría A (2012) OECD environmental outlook to 2050: the consequences of inaction - key facts and figures [Internet]. Eur. World. [cited 2015 Nov 20]. Available from: http://www.oecd.org/env/indicators-modelling-outlooks/oecdenvironmentaloutlookto2050theconsequencesofinaction-keyfactsandfigures.htm
Haramoto E, Katayama H, Oguma K, Yamashita H, Tajima A, Nakajima H et al (2006) Seasonal profiles of human noroviruses and indicator bacteria in a wastewater treatment plant in Tokyo, Japan. Water Sci Technol 54(11-12):301–8, Available from: http://www.ncbi.nlm.nih.gov/pubmed/17302333
Harwood VJ, Levine AD, Scott TM, Chivukula V, Lukasik J, Farrah SR et al (2005) Validity of the indicator organism paradigm for pathogen reduction in reclaimed water and public health protection. Appl Environ Microbiol 71(6):3163–70, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1151840&tool=pmcentrez&rendertype=abstract
Hassani L, Imziln B, Boussaid A, Gauthier MJ (1992) Seasonal incidence of and antibiotic resistance among Aeromonas species isolated from domestic wastewater before and after treatment in stabilization ponds. Microb Ecol 23(3):227–37, Available from: http://www.ncbi.nlm.nih.gov/pubmed/24192933
Hernroth BE, Conden-Hansson A-C, Rehnstam-Holm A-S, et al (2002) Environmental factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilus edulis: the first Scandinavian report. Appl Environ Microbiol 68:4523–4533
Herpers BL, de Jongh BM, van der Zwaluw K, van Hannen EJ (2003) Real-time PCR assay targets the 23S-5S spacer for direct detection and differentiation of Legionella spp. and Legionella pneumophila. J Clin Microbiol 41(10):4815–6, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=254366&tool=pmcentrez&rendertype=abstract
Hoekstra AY, Mekonnen MM, Chapagain AK, Mathews RE, Richter BD (2012) Global monthly water scarcity: blue water footprints versus blue water availability. Añel JA, editor. PLoS One 7(2):e32688, Available from: http://dx.plos.org/10.1371/journal.pone.0032688
Hot D, Legeay O, Jacques J, Gantzer C, Caudrelier Y, Guyard K et al (2003) Detection of somatic phages, infectious enteroviruses and enterovirus genomes as indicators of human enteric viral pollution in surface water. Water Res 37(19):4703–10, Available from: http://www.ncbi.nlm.nih.gov/pubmed/14568057
International Organization for Standardization (1998a) ISO 7899-1:1998 water quality—detection and enumeration of intestinal enterococci—part 1: miniaturized method (Most Probable Number) for surface and waste water
International Organization for Standardization (1998b) ISO 11731:1998. Water quality -- detection and enumeration of Legionella
International Organization for Standardization (1999) ISO 6222:1999 water quality -- enumeration of culturable micro-organisms -- colony count by inoculation in a nutrient agar culture medium
International Organization for Standardization (2005) ISO 8199:2005. Water quality—general guidance on the enumeration of micro-organisms by culture
International Organization for Standardization (2012) ISO 9308-2:2012 water quality—enumeration of Escherichia coli and coliform bacteria—part 2: most probable number method
Jiang SC (2006) Human adenoviruses in water: occurrence and health implications: a critical review †. Environ Sci Technol 40(23):7132–40, Available from: http://dx.doi.org/10.1021/es060892o
Jjemba PK, Weinrich LA, Cheng W, Giraldo E, Lechevallier MW (2010) Regrowth of potential opportunistic pathogens and algae in reclaimed-water distribution systems. Appl Environ Microbiol 76(13):4169–78, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2897422&tool=pmcentrez&rendertype=abstract
Joly P, Falconnet P-A, André J, Weill N, Reyrolle M, Vandenesch F et al (2006) Quantitative real-time Legionella PCR for environmental water samples: data interpretation. Appl Environ Microbiol 72(4):2801–8, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1449029&tool=pmcentrez&rendertype=abstract
Jurzik L, Hamza IA, Wilhelm M (2015) Investigating the reduction of human adenovirus (HAdV) and human polyomavirus (HPyV) in a sewage treatment plant with a polishing pond as a tertiary treatment. Water Air Soil Pollut 226(9):284, Available from: http://link.springer.com/10.1007/s11270-015-2545-9
Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S, Hoshino FB et al (2003) Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 41(4):1548–57, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=153860&tool=pmcentrez&rendertype=abstract
Katayama H, Haramoto E, Oguma K, Yamashita H, Tajima A, Nakajima H et al (2008) One-year monthly quantitative survey of noroviruses, enteroviruses, and adenoviruses in wastewater collected from six plants in Japan. Water Res 42(6-7):1441–8, Available from: http://www.ncbi.nlm.nih.gov/pubmed/17996920
Koo HL, Ajami N, Atmar RL, DuPont HL (2010) Noroviruses: the leading cause of gastroenteritis worldwide. Discov Med 10(50):61–70, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3150746&tool=pmcentrez&rendertype=abstract
Kozak GK, MacDonald D, Landry L, Farber JM (2013) Foodborne outbreaks in Canada linked to produce: 2001 through 2009. J Food Prot 76(1):173–83, Available from: http://www.ncbi.nlm.nih.gov/pubmed/23317873
Kroneman A, Verhoef L, Harris J, Vennema H, Duizer E, van Duynhoven Y et al (2008) Analysis of integrated virological and epidemiological reports of norovirus outbreaks collected within the Foodborne Viruses in Europe network from 1 July 2001 to 30 June 2006. J Clin Microbiol 46(9):2959–65, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2546741&tool=pmcentrez&rendertype=abstract
Legrand-Abravanel F, Mansuy J-M, Dubois M, Kamar N, Peron J-M, Rostaing L et al (2009) Hepatitis E virus genotype 3 diversity, France. Emerg Infect Dis 15(1):110–4, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2660688&tool=pmcentrez&rendertype=abstract
Lipp EK, Farrah SA, Rose JB (2001) Assessment and impact of microbial fecal pollution and human enteric pathogens in a coastal community. Mar Pollut Bull 42(4):286–93, Available from: http://www.ncbi.nlm.nih.gov/pubmed/11381749
Lodder WJ, de Roda Husman AM (2005) Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Appl Environ Microbiol 71(3):1453–61, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1065170&tool=pmcentrez&rendertype=abstract
Loisy F, Atmar RL, Guillon P, Le Cann P, Pommepuy M, Le Guyader FS (2005) Real-time RT-PCR for norovirus screening in shellfish. J Virol Methods 123(1):1–7, Available from: http://www.ncbi.nlm.nih.gov/pubmed/15582692
Lopman B, Vennema H, Kohli E, Pothier P, Sanchez A, Negredo A et al (2004) Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet (Lond Engl) 363(9410):682–8, Available from: http://www.ncbi.nlm.nih.gov/pubmed/15001325
Lorenzo-Morales J, Coronado-Alvarez N, Martínez-Carretero E, Maciver SK, Valladares B (2007) Detection of four adenovirus serotypes within water-isolated strains of Acanthamoeba in the Canary Islands, Spain. Am J Trop Med Hyg 77(4):753–6, Available from: http://www.ajtmh.org/content/77/4/753.abstract
Magnet a, Fenoy S, Galván a L, Izquierdo F, Rueda C, Fernandez Vadillo C et al (2013) A year long study of the presence of free living amoeba in Spain. Water Res 47(19):6966–72
Mara DD, Pearson HW (1987) Waste stabilization ponds: design manual for mediterranean Europe [Internet]. [cited 2015 Jul 19]. Available from: https://books.google.es/books/about/Waste_Stabilization_Ponds.html?id=D_8nAQAAMAAJ&pgis=1
MARA DD, MILLS SW, PEARSON HW, ALABASTER GP (1992) Waste stabilization ponds: a viable alternative for small community treatment systems. Water Environ J 6(3):72–8, Available from: http://doi.wiley.com/10.1111/j.1747-6593.1992.tb00740.x
Marzouk Y (1980) Relationship of viruses and indicator bacteria in water and wastewater of Israel. Water Res 14(11):1585–90, Available from: http://www.sciencedirect.com/science/article/pii/0043135480900627
Masclaux FG, Hotz P, Friedli D, Savova-Bianchi D, Oppliger A (2013) High occurrence of hepatitis E virus in samples from wastewater treatment plants in Switzerland and comparison with other enteric viruses. Water Res 47(14):5101–9, Available from: http://www.sciencedirect.com/science/article/pii/S0043135413004806
Maunula L, Kaupke A, Vasickova P, Söderberg K, Kozyra I, Lazic S et al (2013) Tracing enteric viruses in the European berry fruit supply chain. Int J Food Microbiol 167(2):177–85, Available from: http://www.ncbi.nlm.nih.gov/pubmed/24135674
Maynard HE, Ouki SK, Williams SC (1999) Tertiary lagoons: a review of removal mecnisms and performance. Water Res 33(1):1–13, Available from: http://www.ingentaconnect.com/content/els/00431354/1999/00000033/00000001/art00198
Medema G, Wullings B, Roeleveld P, van der Kooij D (2004) Risk assessment of Legionella and enteric pathogens in sewage treatment works. Water Sci Technol Water Supply [Internet]. [cited 2015 Nov 18];125–32. Available from: http://bvsalud.org/portal/resource/esSiqueira/rep-18894
Merga JY, Royden A, Pandey AK, Williams NJ (2014) Arcobacter spp. isolated from untreated domestic effluent. Lett Appl Microbiol 59(1):122–6, Available from: http://www.ncbi.nlm.nih.gov/pubmed/24666283
Monfort P, Baleux B (1990) Dynamics of Aeromonas hydrophila, Aeromonas sobria, and Aeromonas caviae in a sewage treatment pond. Appl Environ Microbiol 56(7):1999–2006, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=184551&tool=pmcentrez&rendertype=abstract
Niquette P, Servais P, Savoir R (2001) Bacterial Dynamics in the drinking water distribution system of Brussels. Water Res 35(3):675–82, Available from: http://www.sciencedirect.com/science/article/pii/S0043135400003031
Nordgren J, Matussek A, Mattsson A, Svensson L, Lindgren P-E (2009) Prevalence of norovirus and factors influencing virus concentrations during one year in a full-scale wastewater treatment plant. Water Res 43(4):1117–25, Available from: http://www.sciencedirect.com/science/article/pii/S0043135408005940
Ogorzaly L, Cauchie H-M, Penny C, Perrin A, Gantzer C, Bertrand I (2013) Two-day detection of infectious enteric and non-enteric adenoviruses by improved ICC-qPCR. Appl Microbiol Biotechnol 97(9):4159–66, Available from: http://www.ncbi.nlm.nih.gov/pubmed/23558583
Oki T, Kanae S (2006) Global hydrological cycles and world water resources. Science 313(5790):1068–72, Available from: http://www.sciencemag.org/content/313/5790/1068
Oragui JI, Curtis TP, Silva SA, Mara DD (2011) The removal of excreted bacteria and viruses in deep waste stabilization ponds in Northeast Brazil. IWA Publishing. Feb 16 [cited 2014 Dec 30]; Available from: http://www.iwaponline.com/wst/01810/wst018100031.htm
Ottoson J, Hansen A, Björlenius B, Norder H, Stenström TA (2006a) Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. Water Res 40(7):1449–57, Available from: http://www.sciencedirect.com/science/article/pii/S0043135406000789
Ottoson J, Hansen A, Björlenius B, Norder H, Stenström TA (2006b) Removal of viruses, parasitic protozoa and microbial indicators in conventional and membrane processes in a wastewater pilot plant. Water Res 40(7):1449–57, Available from: http://www.ncbi.nlm.nih.gov/pubmed/16533517
Pal A, Sirota L, Maudru T, et al (2006) Real-time, quantitative PCR assays for the detection of virus-specific DNA in samples with mixed populations of polyomaviruses. J Virol Methods 135:32–42. doi:10.1016/j.jviromet.2006.01.018
Palmer CJ, Tsai YL, Paszko-Kolva C, Mayer C, Sangermano LR (1993) Detection of Legionella species in sewage and ocean water by polymerase chain reaction, direct fluorescent-antibody, and plate culture methods. Appl Environ Microbiol 59(11):3618–24, Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=182507&tool=pmcentrez&rendertype=abstract
Pay Drechsel CAS, Liqa Raschid-Sally MR, Bahri A, Wastewater Irrigation and Health (2010) Assessing and mitigating risk in low-income countries. Dunstan house, London
Peña M, Rodriguéz J, Mara DD, Sepulveda M (2000) UASBs or anaerobic ponds in warm climates? a preliminary answer from Colombia. Water Sci Technol [Internet]. [cited 2015 Nov 18];59–65. Available from: http://www.bvsde.paho.org/bvsacd/leeds/uasb.pdf
Pusch D, Oh D-Y, Wolf S, Dumke R, Schröter-Bobsin U, Höhne M et al (2005) Detection of enteric viruses and bacterial indicators in German environmental waters. Arch Virol 150(5):929–47, Available from: http://www.ncbi.nlm.nih.gov/pubmed/15645371
Richards AM, Von Dwingelo JE, Price CT, Abu Kwaik Y (2013) Cellular microbiology and molecular ecology of Legionella-amoeba interaction. Virulence 4(4):307–14, Available from: http://www.tandfonline.com/doi/full/10.4161/viru.24290
Riera-Montes M, Brus Sjölander K, Allestam G, Hallin E, Hedlund K-O, Löfdahl M (2011) Waterborne norovirus outbreak in a municipal drinking-water supply in Sweden. Epidemiol Infect 139(12):1928–35, Available from: http://www.ncbi.nlm.nih.gov/pubmed/21251349
Rodríguez-Martínez S, Blanky M, Friedler E, Halpern M (2015) Legionella spp. isolation and quantification from greywater. MethodsX [Internet]. Nov [cited 2015 Nov 21]; Available from: http://www.sciencedirect.com/science/article/pii/S221501611500059X
Rusiñol M, Fernandez-Cassi X, Timoneda N, Carratalà A, Abril JF, Silvera C et al (2015) Evidence of viral dissemination and seasonality in a Mediterranean river catchment: implications for water pollution management. J Environ Manage 159:58–67, Available from: http://www.ncbi.nlm.nih.gov/pubmed/26046988
Sales-Ortells H, Fernandez-Cassi X, Timoneda N, Dürig W, Girones R, Medema G (2015) Health risks derived from consumption of lettuces irrigated with tertiary effluent containing norovirus. Food Res Int 68:70–7, Available from: http://www.sciencedirect.com/science/article/pii/S0963996914005560
Scheid P, Schwarzenberger R (2012) Acanthamoeba spp. as vehicle and reservoir of adenoviruses. Parasitol Res 111(1):479–85, Available from: http://www.ncbi.nlm.nih.gov/pubmed/22290448
Serrano-Suárez A, Araujo R (2013) Evaluation of Legionella presence in the water system of a public building by semi-nested polymerase chain reaction as a rapid screening method complementary to plate count. Water Sci Technol Water Supply 13(6):1560, Available from: http://www.iwaponline.com/ws/01306/ws013061560.htm
Serrano-Suárez A, Dellundé J, Salvadó H, Cervero-Aragó S, Méndez J, Canals O et al (2013) Microbial and physicochemical parameters associated with Legionella contamination in hot water recirculation systems. Environ Sci Pollut Res Int 20(8):5534–44, Available from: http://www.ncbi.nlm.nih.gov/pubmed/23436060
Shuval HI (1990) Summary—wastewater irrigation in developing countries—health effects and technical solutions. UNDP World Bank Water Sanit Progr 51:74
Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV (2004) Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot 67(10):2342–53, Available from: http://www.ncbi.nlm.nih.gov/pubmed/15508656
Steinert M, Emödy L, Amann R, Hacker J (1997) Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl Environ Microbiol 63(5):2047–53
Teunis PFM, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS et al (2008) Norwalk virus: how infectious is it? J Med Virol 80(8):1468–76, Available from: http://www.ncbi.nlm.nih.gov/pubmed/18551613
Tyagi VK, Kazmi AA, Chopra AK (2008) Removal of fecal indicators and pathogens in a waste stabilization pond system treating municipal wastewater in India. Water Environ Res 80(11):2111–7, Available from: http://www.ingentaconnect.com/content/wef/wer/2008/00000080/00000011/art00004
Wheaton TA, Castle WS (2001) High application rates of reclaimed water benefit citrus tree growth and fruit production. HortSci 36:1273–7, Available from: http://www.mendeley.com/catalog/high-application-rates-reclaimed-water-benefit-citrus-tree-growth-fruit-production/
Acknowledgments
The study reported here was partially founded by programa Recercaixa 2012 ACUP-00300 and AGL2011-30461-C02-01/ALI of the Spanish Ministry of Science and Innovation and Consolidated Research Groups Program of the Catalan Government (2014SGR529 and VirBaP 2014SRG914). Xavier Fernandez-Cassi and Fadua Latif-Eugenín acknowledge the AGAUR Agency of the Catalan Government and the Universitat Rovira i Virgili, respectively, which supported their PhD grants. The authors would like to thank the lagooning system manager, Conrad Martorell, for his collaboration during this project.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Robert Duran
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 6 kb)
Rights and permissions
About this article
Cite this article
Fernandez-Cassi, X., Silvera, C., Cervero-Aragó, S. et al. Evaluation of the microbiological quality of reclaimed water produced from a lagooning system. Environ Sci Pollut Res 23, 16816–16833 (2016). https://doi.org/10.1007/s11356-016-6812-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-6812-0