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Microbial Indicators, Opportunistic Bacteria, and Pathogenic Protozoa for Monitoring Urban Wastewater Reused for Irrigation in the Proximity of a Megacity

EcoHealth volume 13, pages 672–686 (2016)Cite this article

Abstract

In Latin America and the Caribbean, with a population of approximately 580 million inhabitants, less than 20 % of wastewater is treated. Megacities in this region face common challenges and problems related with water quality and sanitation, which require urgent actions, such as changes in the sustainable use of water resources. The Mexico City Metropolitan Area is one of the most populous urban agglomerations in the world, with over 20 million inhabitants, and is no exception to the challenges of sustainable water management. For more than 100 years, wastewater from Mexico City has been transported north to the Mezquital Valley, which is ranked as the largest wastewater-irrigated area in the world. In this study, bacteria and pathogenic protozoa were analyzed to determine the association between the presence of such microorganisms and water types (WTs) across sampling sites and seasons in Mexico City and the Mezquital Valley. Our results show a difference in microbiological water quality between sampling sites and WTs. There is no significant interaction between sampling sites and seasons in terms of bacterial concentration, demonstrating that water quality remains constant at each site regardless of whether it is the dry or the rainy season. The results illustrate the quantity of these microorganisms in wastewater, provide a current diagnosis of water quality across the area which could affect the health of residents in both Mexico City and the Mezquital Valley, and demonstrate the need to transition in the short term to treat wastewater from a local to a regional scale.

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References

  • American Public Health Association (APHA), American Water Works Association, Water Environmental Federation (2005) Standard Methods for Examination of Water and Wastewater, Washington, DC: United Book Press

    Google Scholar 

  • Asano T, Burton FL, Leverenz H, Tsuchihashi R, Tchobanoglous G (2007) Water Reuse: Issues, Technologies and Applications, New York: McGraw-Hill

    Google Scholar 

  • Ashbolt NJ, Grabow OK, Snozzi M (2001) Indicators of microbial water quality. In: Water Quality: Guidelines, Standards and Health, Fewtrell L, Bartram J (editors), London, UK: IWA Publishing, pp 259–315

    Google Scholar 

  • Betancourt W, Querales L (2008) Parásitos protozoarios entéricos en ambientes acuáticos: métodos de concentración y detección. Interciencia 33:418–423

    Google Scholar 

  • Bodley-Tickell AT, Kitchen SE, Sturdee AP (2002) Occurrence of Cryptosporidium in agricultural surface waters during an annual farming cycle in lowland UK. Water Research 36:1880–1886

    CAS  Article  PubMed  Google Scholar 

  • Burns E (2009) Tratar y reusar las aguas residuales. In: Repensar la cuenca: La Gestión de Ciclos del Agua en el Valle de México, México: UAM-Centro Sustentabilidad Incalli Ixcahuicopa (CENTLI) (Editores), pp 37–49

    Google Scholar 

  • Castro-Hermida JA, García-Presedo I, Almeida A, González-Warleta M, Correia JM, Mezo M (2009) Detection of Cryptosporidium spp. and Giardia duodenalis in surface water: a health risk for humans and animals. Water Research 43:4133–4142

    CAS  Article  PubMed  Google Scholar 

  • Cedillo-Rivera R (1989) Es la giardiasis un problema real? Boletín Mensual de Epidemiología 4:1–6

    Google Scholar 

  • Chávez A, Maya C, Gibson R, Jiménez B (2011) The removal of microorganisms and organic micropollutants from wastewater during infiltration to aquifers after irrigation of farmland in the Tula Valley, Mexico. Environmental Pollution 159:1354–1362

    Article  PubMed  Google Scholar 

  • Cifuentes E, Blumenthal U, Ruíz-Palacios G, Bennett S, Peasey A (1994) Escenario epidemiológico del uso agrícola del agua residual: El Valle del Mezquital, México. Salud Pública de México 36:5–9

    Google Scholar 

  • Cifuentes E, Gómez M, Blumenthal U, Téllez-Rojo MM, Romieu I, Ruiz-Palacios G, Ruíz-Velazco S (2000) Risk factors for Giardia intestinalis infection in agricultural villages practicing wastewater irrigation in Mexico. American Journal of Tropical Medicine and Hygiene 62:388–392

    CAS  PubMed  Google Scholar 

  • Comisión Nacional del Agua (CONAGUA, 2007) Equilibrio Hidrológico en la Cuenca del Valle de México: XXIV Congreso Nacional de Ingeniería Civil. Available at: http://agua.org.mx/h2o/index.php?option=com_content&view=article&id=21162:equilibrio-hidrologico-en-la-cuenca-del-valle-de-mexico&catid=1220:cuenca-del-valle-demexico&Itemid=110 (accessed May 28, 2014)

  • Comisión Nacional del Agua (CONAGUA, 2008) Documentos de Licitación para “La Prestación de Servicios de Tratamiento de Aguas Residuales del Valle de México por 25 Años, que incluye la elaboración del proyecto ejecutivo, construcción, equipamiento electromecánico, pruebas, operación, conservación y mantenimiento de la planta de tratamiento de aguas residuales denominada PTAR Atotonilco”

  • Comisión Nacional del Agua (CONAGUA, 2011) Agenda del agua 2030. Available at: (http://agendadelagua2030.conagua.gob.mx/Doc_Foroagendadelagua2030/Respuesta/ZMVMCUENCASEQUILIBRIO.pdf (accessed October 20, 2014)

  • Comisión Nacional del Agua (CONAGUA, 2013) Estadísticas del Agua en México. Available at: http://www.conagua.gob.mx/CONAGUA07/Noticias/SGP-2-14Web.pdf (accessed December 13, 2014)

  • Contreras-Montiel JE (2011) Implicaciones territoriales de la producción industrial en la microrregión Tula-Tepeji del Río. Tesis (PhD), Facultad de Arquitectura, Universidad Nacional Autónoma de México, México

  • Cox SE, William F, Doremus L, Huffman RL, Defawe RM (2005) Ground Water/Surface Water Interactions and Quality of Discharging Ground Water in Streams of the Lower Nooksack River Basin, Whatcom County, Washington, Washington, DC: USGS report 2005-5255

  • Dalkmann P, Broszat M, Siebe C, Willaschek E, Sakinc T, Huebner J, Amelung W, Grohmann E, Siemens J (2012) Accumulation of pharmaceuticals, Enterococcus, and resistance genes in soils irrigated with wastewater for zero to 100 years in Central Mexico. PLoS One 7:e45397

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Domínguez R (2001) El sistema principal de drenaje del área Metropolitana del Valle de México. Instituto de Ingeniería, Universidad Nacional Autónoma de México. Series del Instituto de Ingeniería 22:33

  • Downs TJ, Cifuentes-García E, Suffet IM (1999) Risk screening for exposure to groundwater pollution in a wastewater irrigation district of the Mexico City Region. Environmental Health Perspectives 107:553–561

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Draper NR, Smith H (1998) Applied regression analysis, New York: Wiley

    Book  Google Scholar 

  • DuPont HL, Chappell C, Sterling C, Okhuysen P, Rose JB, Jakubowski W (1995) The infectivity of Cryptosporidium parvum in healthy volunteers. The New England Journal of Medicine 332:855–859

    CAS  Article  PubMed  Google Scholar 

  • Escolero OA, Martínez S, Kralish S, Perevochikova M (2009) Vulnerabilidad de las fuentes de abastecimiento de agua de la Ciudad de México en el contexto de cambio climático. Informe Final. Available at: http://www.cvcccm-atmosfera.unam.mx/sis_admin/archivos/agua_escolero__inffinal_org.pdf (accessed May 9, 2014)

  • Espinosa-García AC, Arias CF, Sánchez-Colón S, Mazari-Hiriart M (2009) Comparative study of enteric viruses, coliphages and indicator bacteria for evaluating water quality in a tropical high altitude system. Environmental Health 8:1–34

    Article  Google Scholar 

  • Fondo Nacional de Fomento al Turismo (FONATUR). Secretaria de Turismo del Gobierno del Estado de Hidalgo (2007) Programa Estratégico para el Aprovechamiento Turístico de los Balnearios en el Estado de Hidalgo: Resumen Ejecutivo. Available at: http://intranet.ehidalgo.gob.mx/NormatecaE/Archivos/Programa_Balnearios07.pdf (accessed January 12, 2014)

  • Gállego J (2007) Manual de Parasitología: Morfología y Bióloga de los Parásitos de Interés Sanitario, Barcelona: Universidad de Barcelona, España

    Google Scholar 

  • Garza-Almanza V (2000) Reúso Agrícola de las Aguas Residuales de Ciudad Juárez, Chihuahua, México. Revista Salud Pública y Nutrición. Available at: http://www.Bvsde.paho.org/bvsair/e/repindex/repi84/vleh/fulltext/acrobat/garza.pdf (accessed May 27, 2014)

  • Gibson R, Becerril-Bravo E, Silva-Castro V, Jiménez B (2007) Determination of acidic pharmaceuticals and potential endocrine disrupting compounds in wastewaters and spring waters by selective elution and analysis by gas chromatography and mass spectrometry. Journal of Chromatography 1169:31–39

    CAS  Article  PubMed  Google Scholar 

  • Hermanowicz SW (2008) Sustainability in water resources management—changes in meaning and perception. Sustainability Science 3:181–188

    Article  Google Scholar 

  • Hill VR, Polaczyk AL, Hahn D, Narayanan J, Cromeans TL, et al. (2005) Development of a rapid method for simultaneous recovery in diverse microbes in drinking water by ultrafiltration with sodium polyphosphate and surfactants. Applied and Environmental Microbiology 71(11):6878–6884

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hogg RV, Craig AT (1995) Introduction to mathematical statistics, New York: Prentice Hall

    Google Scholar 

  • Ikehata K (2013) Hazardous agents in wastewater: public health impacts and treatment options for safe disposal and reuse. In: Wastewater Reuse and Management, Sharma SK, Sanghi R (editors), New York: Springer, pp 165–191

    Chapter  Google Scholar 

  • International Water Management Institute (IWMI, 2010) Wastewater Use in Agriculture: Not Only an Issue Where Water is Scarce! Colombo, Sri Lanka: International Water Management Institute (DOI: 10.5337/2010.217 (online 14 June 2013)

  • Jiménez B (2003) El agua en el Valle de México. Revista Páramo del Campo y de la Ciudad 1:26–33

    Google Scholar 

  • Jiménez B, Chávez A (2004) Quality assessment a potential use of an aquifer recharged with wastewater: “El Mezquital case”. Water Science and Technology 50:269–276

    PubMed  Google Scholar 

  • Jiménez B, Siebe C, Cifuentes E (2005) El reúso intencional y no intencional del agua en el Valle de Tula. In: El Agua en México Vista Desde la Academia, Jiménez B, Marín L (Editores), México: Academia Mexicana de Ciencias, México pp 33–56

  • Jordan R, Rehner J, Samariego J (editors, 2010) Regional Panorama Latin America. Megacities and Sustainability Project Document, Santiago de Chile: United Nations (UN). Available at: http://www.cepal.org/en/publications/3856-regional-panorama-latin-america-megacities-andsustainability (accessed June 15, 2015)

  • Kates RW, Clark WC, Corell R, Hall JM, Jaeger CC, et al. (2001) Sustainability science. Science 292(5517): 641–642

    CAS  Article  PubMed  Google Scholar 

  • Kutner MH, Neter J, Nachsheim C, Wasserman W (2005) Applied Linear Regression Models, 5th ed., New York: McGraw-Hill

    Google Scholar 

  • LeChevallier MW, Norton WD, Lee RG (1991) Occurrence of Giardia and Cryptosporidium spp. in surface water supplies. Applied and Environmental Microbiology 57:2610–2616

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leclerc H (2002) Relationships between common water bacteria and pathogens in drinking water. In: Heterotrophic Plate Counts and Drinking-Water Safety, Bartram J, Cotruvo J, Exner M, Fricker C, Glasmacher A (editors), London: WHO/IWA Publishing, pp 80–118

    Google Scholar 

  • Lesser-Carrillo LE, Lesser-Illades JM, Arellano-Islas S, González-Posadas D (2011) Balance hídrico y calidad del agua subterránea en el acuífero del Valle del Mezquital, México central. Revista Mexicana de Ciencias Geológicas 28:323–336

    Google Scholar 

  • Mara D, Cairncross S (1989) Guidelines for the Safe Use of Wastewater and Excreta in Agriculture and Aquaculture: Measures for Public Health Protection, Geneva, Switzerland: World Health Organization

    Google Scholar 

  • Mazari-Hiriart M, de la Torre L, Mazari-Menzer M, Ezcurra E (2001) Ciudad de México: Dependiente de sus recursos hídricos. Ciudades. Revista Trimestral de la Red de Planeación Urbana 51:42–51

    Google Scholar 

  • Mckenzie C (2005) Wastewater Reuse Conserves Water and Protects Waterways, The National Environmental Services Center (NESC). Available at: www.nesc.wvu.edu/nsfc_manufacturers.html (accessed January 18, 2014)

  • Mena KD, Gerba CP (2009) Risk assessment of Pseudomonas aeruginosa in water. Reviews of Environmental Contamination and Toxicology 201:71–115

    CAS  PubMed  Google Scholar 

  • Montgomery DC (2012) Design and Analysis of Experiments, Hoboken, NJ: Wiley

    Google Scholar 

  • Mood AM, Graybill FA, Boes DC (1987) Introduction to the theory of statistics, México City: McGraw Hill

    Google Scholar 

  • Navarro I, Chávez A, Jiménez B (2011) Risk assessment of the unplanned reuse of an aquifer recharged with wastewater as a source of drinking water. In: 8th IWA International Conference in Water Reclamation and Reuse, Barcelona, Spain: Universidad Nacional Autónoma de México, Instituto de Ingeniería

  • Olivas E, Flores JP, Di Giovanni G, Corral B, Osuna P (2013) Contaminación fecal en agua potable del Valle de Juárez. Terra Latinoamericana 31:135–143

    Google Scholar 

  • Polaczyk A, Narayanan J, Cromeans T, Hahn D, Roberts J, Amburgey J, Hill V (2008) Ultrafiltration-based techniques for rapid and simultaneous concentration of multiple microbe classes from 100-L tap water samples. Journal of Microbiological Methods 73:92–99

    CAS  Article  PubMed  Google Scholar 

  • Pseudomonas aeruginosa (ATCC 27853™)

  • Putignani L, Menichella D (2010) Global distribution, public health and clinical impact of the protozoan pathogen Cryptosporidium. Interdisciplinary Perspectives on Infectious Diseases 2010:1–39 (DOI: 10.1155/2010/753512, online May 2010)

  • Rangel-Martínez C (2010) Identificación de Blastocytis hominis en muestras de agua obtenidas de Ciudad Universitaria en la Ciudad de México. Tesis de Licenciatura, Universidad Simón Bolívar, México

  • Rendtorff RC (1979) The experimental transmission of Giardia lamblia among volunteer subjects. In: Waterborne Transmission of Giardiasis, US Environmental Protection Agency, Jakubowski W, Hoff JC (editors), Report No. EPA-600/9-79-001, Cincinnati, OH: Environmental Research Center, pp 64–81

  • Rojas C (2011) Criptosporidiosis: Cryptosporidium spp. In: Parásitos Emergentes. Conceptos Básicos y de Diagnóstico, Rojas C, Zapata J (editores), Cali: Universidad del Valle, pp 27–37

    Google Scholar 

  • Romero-Álvarez H (1997) Case study VII—the Mezquital Valley, Mexico. In: Water Pollution Control. A Guide to the Use of Water Quality Management Principles, Helmer R, Hespanhol I (editors), Bury St Edmunds, Suffolk, Great Britain: St Edmundsbury Press, pp V1–V7

    Google Scholar 

  • Sardin TR, Dowd SE, Herman DC, Maier RM (2009) Aquatic environments. In: Environmental Microbiology, Maier R, Pepper I, Gerba CP (editors), Shanghai, China: Elsevier Academic, pp 103–119

    Google Scholar 

  • Sharma VA (2009) Sustainability and water. In: Sustainability 2009: The Next Horizon. Conference Proceedings. AIP Conference Proceedings, Hronzsky I, Gordon LN (editors), Melbourne: American Institute of Physics, pp 128–137

  • Siebe C, Cifuentes E (1995) Environmental impact of wastewater irrigation in central Mexico: an overview. International Journal of Environmental Health Research 5:161–173

    CAS  Article  Google Scholar 

  • Siemens J, Huschek G, Siebe C, Kaupenjohann M (2008) Concentrations and mobility of human pharmaceuticals in the world’s largest wastewater irrigation system, Mexico City-Mezquital Valley. Water Research 42:2124–2143

    CAS  Article  PubMed  Google Scholar 

  • Sinton LW, Finlay RK, Lynch PA (1999) Sunlight inactivation of fecal bacteriophages and bacteria in sewage-polluted seawater. Applied and Environmental Microbiology 65:3605–3613

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sistema Meteorológico Nacional (SMN, 2012) Resúmenes mensuales de temperatura y lluvia. Available at: http://smn.cna.gob.mx/index.php?option=com_content&view=article&id=12&Itemid=77 (accessed September 10, 2013)

  • Smith HV, Caccio SM, Cook N, Nichols RA, Tait A (2007) Cryptosporidium and Giardia as foodborne zoonoses. Veterinary Parasitology 149:29–40

    CAS  Article  PubMed  Google Scholar 

  • Solarte Y, Peña M, Madera C (2006) Transmisión de protozoarios patógenos a través del agua para consumo humano. Colombia Médica 37:74–82

    Google Scholar 

  • Tapia-Palacios MA (2012) Detección de Cryptosporidium parvum y Giardia lamblia en agua del río Cuitzmala, Jalisco. Tesis de Licenciatura, Facultad de Ciencias-Instituto de Ecología, Universidad Nacional Autónoma de México, México

  • Toranzos GA (2002) Pseudomonas. In: Encyclopedia of Environmental Microbiology, Bitton G (editor), New York: Wiley, pp 2632–2639

    Google Scholar 

  • United Nations Department of Economic and Social Affairs (UNDESA, 2013) International Decade for Action ‘Water for life’ 2005–2015: Water Quality. Available at: http://www.un.org/waterforlifedecade/quality.shtml (accessed September 10, 2013)

  • US-Environmental Protection Agency (EPA, 2000) Giardia: Drinking Water Fact Sheet. Available at: http://water.epa.gov/action/advisories/drinking/upload/2009_02_03_criteria_humanhealth_microbial_giardiafs.pdf (accessed October 20, 2013)

  • Volkmann H, Schwartz T, Kirchen S, Stofer C, Obst U (2007) Evaluation of inhibition and cross-reaction effects on real time PCR applied to the total DNA of wastewater samples for the quantification of the bacterial antibiotics resistance genes and taxon-specific targets. Molecular and Cellular Probes 21:125–139

    CAS  Article  PubMed  Google Scholar 

  • Wilkes G, Edge T, Gannon V, Jokinen C, Lyautey E, Medeiros D, Neumann N, Ruecker N, Topp E, Lapen DR (2009) Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural landscape. Water Research 43:2209–2223

    CAS  Article  PubMed  Google Scholar 

  • World Health Organization (WHO, 2006) WHO Guidelines for the Safe Use of Wastewater, Excreta and Greywater, Vol. 1, Geneva: WHO

    Google Scholar 

  • World Health Organization (WHO, 2013) Water Quality and Health Strategy 2013–2020. Available at: http://www.zaragoza.es/ciudad/medioambiente/onu/en/detallePer_Onu?id=633 (accessed March 6, 2014)

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Acknowledgments

We are grateful to the Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México (UNAM) for the Scholarship assigned to María Alejandra Fonseca-Salazar; to Dr. Christina D. Siebe-Grabach and Dr. Jan Siemens, for inviting us to collaborate in the Project entitled “Scale dependency of formation of resistances and their transfer to human pathogens during wastewater reuse,” which was funded by the DFG (Deutsche Forschungsgemeinschaftand) and CONACyT (Consejo Nacional de Ciencia y Tecnología) México I0110/193/10; are especially grateful to all of the researchers and students who participated in this Project, Dr. Melanie Broszat, Dr. Elisabeth Grohmann, from Department of Infectious Diseases, University Hospital Freiburg, Freiburg, Germany, for the bacteria concentration method; to Dr. Yolanda López-Vidal, from the Laboratorio of the Programa de Inmunología Molecular Microbiana, Facultad de Medicina, UNAM, for providing Pseudomonas aeruginosa ATCC 27853; to the Faculty and students of the Laboratorio Nacional de Ciencias de la Sostenibilidad, especially Gustavo Pérez-Ortíz, Rosa Solano-Ortiz, Jannice Alvarado, Víctor Jesús García-Luna, Marco Antonio Tapia; and to Mirsha Quito for the elaboration of Fig. 2.

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Affiliations

  1. Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Mexico City, Mexico

    María Alejandra Fonseca-Salazar & Marco Antonio Tapia-Palacios

  2. Laboratorio Nacional de Ciencias de la Sostenibilidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275, Tercer Circuito Exterior Ciudad Universitaria, Coyoacán, 04510, Mexico City, DF, Mexico

    María Alejandra Fonseca-Salazar, María Teresa Castañón-Martínez, Marco Antonio Tapia-Palacios & Marisa Mazari-Hiriart

  3. Instituto de Investigaciones en Matemáticas Aplicadas y en Sistemas, Universidad Nacional Autónoma de México, Mexico City, Mexico

    Carlos Díaz-Ávalos

  4. Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City, Mexico

    María Teresa Castañón-Martínez

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  1. María Alejandra Fonseca-Salazar
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  2. Carlos Díaz-Ávalos
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  3. María Teresa Castañón-Martínez
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  4. Marco Antonio Tapia-Palacios
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  5. Marisa Mazari-Hiriart
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Correspondence to Marisa Mazari-Hiriart.

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Fonseca-Salazar, M.A., Díaz-Ávalos, C., Castañón-Martínez, M.T. et al. Microbial Indicators, Opportunistic Bacteria, and Pathogenic Protozoa for Monitoring Urban Wastewater Reused for Irrigation in the Proximity of a Megacity. EcoHealth 13, 672–686 (2016). https://doi.org/10.1007/s10393-016-1172-2

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Keywords

  • wastewater reuse
  • pathogens
  • sustainability
  • planning
  • public health
  • megacity