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Giardia spp. and Cryptosporidium spp. removal efficiency of a combined fixed-film system treating domestic wastewater receiving hospital effluent

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Abstract

Giardia and Cryptosporidium have caused numerous outbreaks of diarrhea as a result of the ingestion of water contaminated with sewage. In Brazil, the efficiency of Giardia and Cryptosporidium removal by combined fixed-film systems has rarely been studied. The aims of the present study were therefore to verify the removal efficiency of Giardia and Cryptosporidium by a combined system (anaerobic/anoxic filter and aerated submerged biofilter) and to perform the genetic characterization of these parasites. The (oo)cysts were detected by centrifuge concentration and membrane filtration from raw sewage, effluents, adhered biomass, and sludge samples. Immunofluorescence assay and differential interference contrast microscopy were used for the visualization of the (oo)cysts. Nested PCR was applied to confirm Giardia and Cryptosporidium. Giardia and Cryptosporidium were detected in 27% and 5.5% of the 144 analyzed samples of raw sewage and effluents, respectively. A total of 33,000 cysts/L were recovered in the adhered biomass samples (n = 25) from different points of the aerated submerged biofilter, while 6000 oocysts/L were registered in a single point. An average of 11,800 cysts/L were found in the sludge samples (n = 5). The combined system exhibited a removal efficiency of Giardia cysts of 1.8 ± 1.0 log removal. The C and BIV assemblages of Giardia were identified in the raw sewage while AII was found in the treated effluent sample. It was not possible to calculate the removal efficiency of Cryptosporidium oocysts by the combined system. The combined system exhibited some potential as a suitable treatment for the removal of parasites from sewage.

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References

  • Abdelgadir A, Chen X, Liu J, Xie X, Zhang J, Zhang K, Wang H, Liu N (2014) Characteristics, process parameters, e inner components of anaerobic bioreactors. Biomed Res Int 2014:1–10. https://doi.org/10.1155/2014/841573

    Article  CAS  Google Scholar 

  • Ameen ESM, Muyibi SA, Abdulkarim MI (2011) Microfiltration of pretreated sanitary landfill leachate. Environmentalist 31:208–215

    Article  Google Scholar 

  • Amorós I, Moreno Y, Reyes M, Moreno-Mesonero L, Alonso JL (2016) Prevalence of Cryptosporidium oocysts and Giardia cysts in raw and treated sewage sludges. Environ Technol 37(22):2898–2904

    Article  Google Scholar 

  • APHA, AWWA, WEF (2012) Standard methods for the examination of water and wastewater, 21st edn. APHA, AWWA, WEF, Washington DC, USA

    Google Scholar 

  • Appelbee AJ, Frederick LM, Heitman TL, Olson ME (2003) Prevalence and genotyping of Giardia duodenalis from beef calves in Alberta, Canada. Vet Parasitol 112:289–294

    Article  CAS  Google Scholar 

  • Ayed BL, Yang W, Widmer G, Cama V, Ortega Y, Xiao L (2012) Survey and genetic characterization of wastewater in Tunisia for Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi, Cyclospora cayetanensis and Eimeria spp. J Water Health 10:431–444

    Article  Google Scholar 

  • Berglund B, Dienus O, Sokolova E, Berglind E, Matussek A, Pettersson T, Lindgren P-E (2017) Occurrence and removal efficiency of parasitic protozoa in Swedish wastewater treatment plants. Sci Total Environ 598:821–827

    Article  CAS  Google Scholar 

  • Boarato-David E, Guimarães S, and Cacciò S (2016) Giardia duodenalis. http://www.waterpathogens.org/sites/default/files/Giardia%20duodenalis.pdf. Accessed 25 May 2018

  • Brunetti F (2008) Mecânica dos fluidos. Pearson Prentice Hall, 2° ed. rev., São Paulo

  • Bueno Franco RM, Branco N, Trainotti Amaro BC, Neto RC, da Silva Fiuza VR (2016) Cryptosporidium species and Giardia genotypes detected in surface water supply of Campinas, Southeast Brazil, by molecular methods. J Vet Med Res 3(3):1053

    Google Scholar 

  • Cacciò SM, Ryan U (2008) Molecular epidemiology of giardiasis. Mol Biochem Parasitol 160(2):75–80

    Article  Google Scholar 

  • Cantusio Neto R, Santos LU, Franco RMB (2006) Evaluation of activated sludge treatment and the efficiency of the disinfection of Giardia species cysts e Cryptosporidium oocysts by UV at an sludge treatment plant in Campinas, south-east Brazil. Wat Sci Technol 54(3):89–94

    Article  CAS  Google Scholar 

  • Carraro E, Bonetta S, Bertino C, Lorenzi E, Gilli G (2016) Hospital effluents management: chemical, physical, microbiological risks and legislation in different countries. J Environ Manag 168:185–199

    Article  CAS  Google Scholar 

  • Chan YJ, Chong MF, Law CL, Hassell DG (2009) A review on anaerobic-aerobic treatment of industrial and municipal wastewater. Chem Eng J 155:1–18

    Article  CAS  Google Scholar 

  • Chang R, Goldsby KA (2012) Chemistry, 11th edn. McGrawHill Education, New York

    Google Scholar 

  • Chernicharo CAL, van Lier JB, Noyola A, Bressani Ribeiro T (2015) Anaerobic sewage treatment: state of the art, constraints and challenges. Rev Environ Sci Biotechnol 14(4):649–679

    Article  CAS  Google Scholar 

  • Coelho CH, Durigan M, Leal DAG, Schneider AB, Franco RMB, Singer SM (2017) Giardiasis as a neglected disease in Brazil: systematic review of 20 years of publications. PLoS Negl Trop Dis 11(10):e0006005. https://doi.org/10.1371/journal.pntd.0006005

    Article  Google Scholar 

  • Colli CM, Bezagio RC, Nishi L, Bignotto TS, Ferreira ÉC, Falavigna-Guilherme AL et al (2015) Identical assemblage of Giardia duodenalis in humans, animals and vegetables in an urban area in southern Brazil indicates a relationship among them. PLoS ONE 10(3):e0118065

    Article  Google Scholar 

  • De Sanctis M, Del Moro G, Chimienti S, Ritelli P, Levantesi C, Di Iaconi C (2017) Removal of pollutants and pathogens by a simplified treatment scheme for municipal wastewater reuse in agriculture. Sci Total Environ 580:17–25

    Article  Google Scholar 

  • Dezzoti M, Sant'anna JR GL, Bassin JP (2011) Advanced biological processes for effluent treatment and molecular biology techniques for the study of microbial diversity. Interciência, First edition, Rio de Janeiro, Brazil

  • Dilallo R, Albertson OE (1961) Volatile acids by direct titration. J Water Pollut Control Fed 33(4):357–365

    Google Scholar 

  • Durigan M, Abreu AG, Zucchi MI, Franco RMB, De Souza AP (2014) Genetic diversity of Giardia duodenalis: multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLoS One 9(12):e115489. https://doi.org/10.1371/journal.pone.0115489

    Article  CAS  Google Scholar 

  • Efstratiou A, Ongerth J, Karanis P (2017) Evolution of monitoring for Giardia and Cryptosporidium in water. Water Res 123:96–112

    Article  CAS  Google Scholar 

  • Feng Y, Ryan UM, Xiao L (2018) Genetic diversity and population structure of Cryptosporidium. Trends Parasitol 34(11):997–1011

    Article  CAS  Google Scholar 

  • Fernandes LN, de Souza PP, de Araújo RS, Razzolini MTP, Soares RM, Sato MIZ, Hachich EM, Cutolo SA, Matté GR, Matté MH (2011) Detection of assemblages A and B of Giardia duodenalis in water and sewage from São Paulo state, Brazil. J Water Health 9(2):361–367

    Article  CAS  Google Scholar 

  • Foco MLR (2014) Effluent recirculation aiming denitrification in anaerobic-aerobic combined systems for sewage treatment, Thesis, University of Campinas

  • Foco MLR, Greinert-Goulart JA, Leal DAG, Franco RMB, Nour EAA (2011) Treatment of sanitary sewage from hospital complex by anaerobic filter and aerated submerged biofilter: removal of Giardia spp. cysts and Cryptosporidium spp. oocysts. 26o Brazilian Congress of Sanitary and Environmental Engineer, Porto Alegre, State of Rio Grande do Sul, 2011

  • França RB (2007) Cryptosporidium spp., Giardia spp. and helminthes eggs in raw hospital sewage: destruction and structural damage of protozoa after photoelectrochemical process, Dissertation, University of Campinas

  • Franco RMB, Rocha-Eberhardt R, Cantusio Neto R (2001) Occurrence of Cryptosporidium oocysts and Giardia cysts in raw water from the Atibaia River, Campinas, Brazil. Rev Inst Med Trop São Paulo 43:109–111

    Article  CAS  Google Scholar 

  • Gallas-Lindemann C, Sotiriadou I, Plutzer J, Noack MJ, Mahmoudi MR, Karanis P (2016) Giardia and Cryptosporidium spp. dissemination during wastewater treatment and comparative detection via immunofluorescence assay (IFA), nested polymerase chain reaction (nested PCR) and loop mediated isothermal amplification (LAMP). Acta Trop 158:43–51

    Article  CAS  Google Scholar 

  • Garvey M, Coughlan G, Murphy N, Rowan N (2016) The pulsed light inactivation of veterinary relevant microbial biofilms and the use of a RTPCR assay to detect parasite species within biofilm structures. Open Veterinary Journal 6(1):15–22

    Article  CAS  Google Scholar 

  • Greinert-Goulart JA (2013) Removal study of Giardia spp. and Cryptosporidium spp. and characterization of microfauna in wastewater treatment plants: assessment instruments and process control, Thesis, University of Campinas.

  • Gullicks H, Hasan H, Das D, Moretti C, Hung Y-T (2011) Biofilm fixed film systems. Water 3(3):843–868

    Article  CAS  Google Scholar 

  • Hachich EM, Sato MIZ, Galvani AT, Menegon JRN, Mucci JLN (2004) Giardia and Cryptosporidium in source waters of São Paulo state, Brazil. Wat Sci Technol 50(1):239–245

    Article  CAS  Google Scholar 

  • Hachich EM, Galvani AT, Padula JA, Stoppe NC, Garcia SC, Bonanno VMS, Barbosa MRF, Sato MIZ (2013) Pathogenic parasites and enteroviruses in wastewater: support for a regulation on water reuse. Water Sci Technol 67(7):1512–1518

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hatam-Nahavandi K, Mohebali M, Mahvi AH, Keshavarz H, Mirjalali H, Rezaei S, Meamar AR, Rezaeian M (2017) Subtype analysis of Giardia duodenalis isolates from municipal and domestic raw wastewaters in Iran. Environ Sci Pollut Res 24:12740–12747

    Article  CAS  Google Scholar 

  • Jagai JS, Castronovo DA, Monchak J, Naumova EM (2009) Seasonality of cryptosporidiosis: a meta-analysis approach. Environ Res 109(4):465–478

    Article  CAS  Google Scholar 

  • Jiang J, Alderisio KA, Singh A, Xiao L (2005) Development of procedures for direct extraction of Cryptosporidium DNA from water concentrates and for relief of PCR inhibitors. Appl Environment Microbiol 71:1135–1141

    Article  CAS  Google Scholar 

  • Kassab G, Halalsheh M, Klapwijk A, Fayyad M, van Lier JB (2010) Sequential anaerobic-aerobic treatment for domestic wastewater—a review. Bioresour Technol 101:3299–3310

    Article  CAS  Google Scholar 

  • Kitajima M, Haramoto E, Iker BC, Gerba CP (2014) Occurrence of Cryptosporidium, Giardia, and Cyclospora in influent and effluent water at wastewater treatment plants in Arizona. Sci Total Environ 484:129–136

    Article  CAS  Google Scholar 

  • Kohli A, Bushen OY, Pinkerton RC, Houpt E, Newman RD, Sears CL, Lima AAM, Guerrant RL (2008) Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg 102:718–725

    Article  Google Scholar 

  • Kothavade RJ (2012) Potential molecular tools for assessing the public health risk associated with waterborne Cryptosporidium oocysts. J Med Microbiol 61:1039–1051

    Article  CAS  Google Scholar 

  • Lalle M, Pozio E, Capelli G, Bruschi F, Crotti D, Caccio SM (2005) Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol 35:207–213

    Article  CAS  Google Scholar 

  • Leetz AS, Sotiriadou I, Ongerth J, Karanis P (2007) An evaluation of primers amplifying DNA targets for the detection of Cryptosporidium spp. using C. parvum HNJ-1 Japanese isolate in water samples. Parasitol Res 101(4):951–962

    Article  Google Scholar 

  • Leonel LP, Tonetti AL, Silva JCPD, Nunes EA, Anaruma Filho F (2016) Reuse of sewage treated effluent in agricultural practices: an alarming presence of Giardia spp. cysts. Ecol Eng 94:682–687

    Article  Google Scholar 

  • Ligon G, Bartram J (2016) Literature review of associations among attributes of reported drinking water disease outbreaks. Int J Environ Res Public Health 13(6):527

    Article  Google Scholar 

  • Liu A, Yang F, Shen Y, Zhang W, Wang R, Zhao W, Zhang L, Ling H, Cao J (2014) Genetic analysis of the Gdh and Bg genes of animal-derived Giardia duodenalis isolates in northeastern China and evaluation of zoonotic transmission potential. PLoS One 9(4):e95291

    Article  Google Scholar 

  • Ma J, Feng Y, Hu Y, Villegas EN, Xiao L (2016) Human infective potential of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in urban wastewater treatment plant effluents. J Water Health 14(3):411–423

    Article  Google Scholar 

  • Manore AJW, Harper SL, Aguilar B, Weese JS, Shapiro K (2019) Comparison of freeze-thaw cycles for nucleic acid extraction and molecular detection of Cryptosporidium parvum and Toxoplasma gondii oocysts in environmental matrices. J Microbiol Methods 156:1–4

    Article  CAS  Google Scholar 

  • Marín I, Goñi P, Lasheras AM, Ormad MP (2014) Efficiency of a Spanish wastewater treatment plant for removal potentially pathogens: characterization of bacteria and protozoa along water and sludge treatment lines. Ecol Eng 74:28–32

    Article  Google Scholar 

  • Medema GJ, Schets FM, Teunis PFM, Havelaar AH (1998) Sedimentation of free and attached Cryptosporidium oocysts and Giardia cysts in water. Appl Environ Microbiol 64(11):4460–4466

    CAS  Google Scholar 

  • Mekala GD, Davidson B (2016) A review of literature on the factors affecting wastewater treatment and recycling across a broad spectrum of economic stages of development. Water Policy 18(1):217–234

    Google Scholar 

  • Mishra AK (2014) Application of nanotechnology in water research. John Wiley & Sons, Inc., Hoboken, NJ, USA

    Book  Google Scholar 

  • Moreira NA, Bondelind M (2017) Safe drinking water and waterborne outbreaks. J Water Health 15(1):83–96

    Article  CAS  Google Scholar 

  • National Environmental Council (2006) Resolução CONAMA n° 375, Brasília, Brazil. Defines criteria and procedures for the agricultural use of sewage sludge generated in sewage treatment plants and their by-products, and provides other measures. http://www.mma.gov.br/port/conama/res/res06/res37506.pdf. Accessed 25 May 2018

  • National Environmental Council (2011) Resolução CONAMA n° 430, Brasília, Brazil. Provides for the conditions and effluent discharge standards, and modifying resolution n°. 357. http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi=646. Accessed 25 May 2018

  • Ongerth JE (2013) The concentration of Cryptosporidium and Giardia in water—the role and importance of recovery efficiency. Wat Res 47:2479–2488

    Article  CAS  Google Scholar 

  • Painter JE, Hlavsa MC, Collier SA, Xiao L, Yoder JS (2015) Cryptosporidiosis surveillance—United States, 2011–2012. MMWR Surveillance Summaries. / May 1/ Vol. 64 / No. 3, 2015

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2014. http://www.R-project.org/. Accessed 13 Dec 2016

  • Ramo A, Del Cacho E, Sánchez-Acedo C, Quílez J (2017) Occurrence and genetic diversity of Cryptosporidium and Giardia in urban wastewater treatment plants in north-eastern Spain. Sci Total Environ 598:628–638

    Article  CAS  Google Scholar 

  • Read CM, Monis PT, Thompson RCA (2004) Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infect Genet Evol 4:125–130

    Article  CAS  Google Scholar 

  • Ripley LE, Boyle WC, Converse JC (1986) Improved alkalimetric monitoring for anaerobic digestion of high-strength wastes. J Water Pollut Control Fed 58(5):406–411

    CAS  Google Scholar 

  • Robertson LJ (2018) Chapter four—parasites in food: from a neglected position to an emerging issue. Adv Food Nutr Res 86:71–113

    Article  Google Scholar 

  • Rosado-García FM, Guerrero-Flórez M, Karanis G, Hinojosa MDC, Karanis P (2017) Water-borne protozoa parasites: the Latin American perspective. Int J Hyg Environ Health 220:783–798

    Article  Google Scholar 

  • Ryan U, Càccio SM (2013) Zoonotic potential of Giardia. Int J Parasitol 43:943–956

    Article  CAS  Google Scholar 

  • Ryan U, Paparini A, Monis P, Hijjawi N (2016) It’s official—Cryptosporidium is a gregarine: what are the implications for the water industry? Water Res 105:305–313

    Article  Google Scholar 

  • Ryan U, Hijjawi N, Xiao L (2018) Foodborne cryptosporidiosis. Int J Parasitol 48(1):1–12

    Article  Google Scholar 

  • Ryan U, Hijjawi N, Xiao L (2019) Giardia: an under-reported foodborne parasite. Int J Parasitol 49(1):1–11

    Article  Google Scholar 

  • Samie A, Ntekele P (2014) Genotypic detection and evaluation of the removal efficiency of Giardia duodenalis at municipal wastewater treatment plants in northern South Africa. Trop Biomed 31:122–133

    CAS  Google Scholar 

  • Santín M, Trout JM, Xiao L, Zhou L, Greiner E, Fayer R (2004) Prevalence and age-related variation of Cryptosporidium species and genotypes in dairy calves. Vet Parasitol 122(2):103–117

    Article  Google Scholar 

  • Santos PRD, Daniel LA (2017) Occurrence and removal of Giardia spp. cysts and Cryptosporidium spp. oocysts from a municipal wastewater treatment plant in Brazil. Environ Technol 38(10):1245–1254

    Article  CAS  Google Scholar 

  • Santos LU, Bonatti TR, Cantusio Neto R, Franco RMB (2004) Occurrence of Giardia cysts and Cryptosporidium oocysts in activated sludge samples in Campinas, SP, Brazil. Rev Inst Med Trop São Paulo 46(6):309–313

    Article  Google Scholar 

  • Sato MIZ, Galvani AT, Padula JA, Nardocci AC, Lauretto MS, Razzolini MTP, Hachich EM (2013) Assessing the infection risk of Giardia and Cryptosporidium in public drinking water delivered by surface water systems in Sao Paulo state, Brazil. Sci Total Environ 442:389–396

    Article  CAS  Google Scholar 

  • Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17(1):7–15

    Article  Google Scholar 

  • Shi Y, Huang J, Zeng G, Gu Y, Chen Y, Hu Y, Tang B, Zhou J, Yang Y, Shi L (2017) Exploiting extracellular polymeric substances (EPS) controlling strategies for performance enhancement of biological wastewater treatments: an overview. Chemosphere 180:396–411

    Article  CAS  Google Scholar 

  • Silva GP (2014a) Tendências e debates I-Tecnologias de Tratamento de esgoto. Um breve comparativo. Trends and debates I—treatment technologies of sewage. A brief comparison. Ministério das Cidades. https://slideplayer.com.br/slide/2338277/. Acessed 07 February 2019

  • Silva GP (2014b) Tendências e debates I-Tecnologias de Tratamento de esgoto. Um breve comparativo. Ministério das Cidades. https://slideplayer.com.br/slide/2338277/. Accessed 07 February 2019

  • Siqueira-Castro ICV, Greinert-Goulart JA, Bonatti TR, Yamashiro S, Franco RMB (2016) First report of predation of Giardia sp. cysts by ciliated protozoa and confirmation of predation of Cryptosporidium spp. oocysts by ciliate species. Environ Sci Pollut Res:1–6. https://doi.org/10.1007/s11356-016-6689-y

  • SNIS – Sistema Nacional de Informações sobre Saneamento, Brasil. Diagnóstico dos Serviços de Água e Esgoto (2016) Ministério das Cidades – Secretaria Nacional de Saneamento Ambiental, Brasília: DF. [National System of Information about Sanitation. Diagnosis of services of water and sewage [Internet]. Ministry of Cities – National Secretaria of Environmental Sanitation, Brasília: DF. 2016. http://www.snis.gov.br/diagnostico-agua-e-esgotos/diagnostico-ae-2016. Accessed 25 May 2018

  • Soliman RH, Fuentes I, Rubio JM (2011) Identification of a novel assemblage B subgenotype and a zoonotic assemblage C in human isolates of Giardia intestinalis in Egypt. Parasitol Int 60:507–511

    Article  CAS  Google Scholar 

  • Strien J, Sanft J, Mall G (2013) Enhancement of PCR amplification of moderate GC-containing and highly GC-rich DNA sequences. Mol Biotechnol 54(3):1048–1054

    Article  CAS  Google Scholar 

  • Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, Schantz PM, Daz P, Lal AA, Xiao L (2003) Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis 9:1444–1452

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  Google Scholar 

  • Tawfik A, El-Zamel T, Herrawy A, El-Taweel G (2015) Fate of parasites and pathogenic bacteria in an anaerobic hybrid reactor followed by downflow hanging sponge system treating domestic wastewater. Environ Sci Pollut Res 22:12235–12245

    Article  CAS  Google Scholar 

  • Thompson RCA (2004) The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol 126(1–2):15–35

    Article  Google Scholar 

  • Thompson RCA, Ash A (2016) Molecular epidemiology of Giardia and Cryptosporidium infections. Infect Genet Evol 40:315–323

    Article  CAS  Google Scholar 

  • Xiao L, Fayer R (2008) Molecular characterization of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol 38(11):1239–1255

    Article  CAS  Google Scholar 

  • Xiao L, Escalante L, Yang C, Sulaiman I, Escalante AA, Montali RJ, Fayer R, Lal AA (1999) Phylogenetic analysis of Cryptosporidium parasites based on the small-subunit rRNA gene locus. Appl Environ Microbiol 65:1578–1583

    CAS  Google Scholar 

  • Xiao L, Alderisio K, Limor J, Royer M, Lal AA (2000) Identification of species and sources of Cryptosporidium oocysts in storm waters with a small-subunit rRNA-based diagnostic and genotyping tool. Appl Environ Microbiol 66:5492–5498

    Article  CAS  Google Scholar 

  • Yamashiro S, Fiuza VRS, Teixeira ATLS, Branco N, Levy CE, Siqueira-Castro ICV, Franco RMB (2017) Enterocytozoon bieneusi detected by molecular methods in raw sewage and treated effluent from a combined system in Brazil. Mem Inst Oswaldo Cruz:1–7. https://doi.org/10.1590/0074-02760160435

  • Yoder JS, Harral C, Beach MJ (2012) Giardiasis surveillance—United States, 2009–2010. MMWR CDC Surveill Summ 59:15–25

    Google Scholar 

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Acknowledgments

The authors would like to thank CAPES (Coordination for the Improvement of Higher Education Personnel) for the scholarships granted, and FAPESP (São Paulo Research Foundation, PROCESSO: n° 2011/21878-9) and FAEPEX (Fundo de Apoio ao Ensino, à Pesquisa e Extensão/UNICAMP) for financing this study.

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Yamashiro, S., Foco, M.L.R., Pineda, C.O. et al. Giardia spp. and Cryptosporidium spp. removal efficiency of a combined fixed-film system treating domestic wastewater receiving hospital effluent. Environ Sci Pollut Res 26, 22756–22771 (2019). https://doi.org/10.1007/s11356-019-05500-8

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