• 1.

    Troeger C et al., 2018. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of diarrhoea in 195 countries: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect Dis 18: 12111228.

    • Search Google Scholar
    • Export Citation
  • 2.

    Gall AM, Mariñas BJ, Lu Y, Shisler JL, 2015. Waterborne viruses: a barrier to safe drinking water. PLoS Pathog 11: e1004867.

  • 3.

    Devault DA, Maguet H, Merle S, Péné-Annette A, Lévi Y, 2018. Wastewater-based epidemiology in low Human Development Index states: bias in consumption monitoring of illicit drugs. Environ Sci Pollut Res Int 25: 2781927838.

    • Search Google Scholar
    • Export Citation
  • 4.

    Sims N, Kasprzyk-Hordern B, 2020. Future perspectives of wastewater-based epidemiology: monitoring infectious disease spread and resistance to the community level. Environ Int 139: 105689.

    • Search Google Scholar
    • Export Citation
  • 5.

    Mao K, Zhang K, Du W, Ali W, Feng X, Zhang H, 2020. The potential of wastewater-based epidemiology as surveillance and early warning of infectious disease outbreaks. Curr Opin Environ Sci Health 17: 17.

    • Search Google Scholar
    • Export Citation
  • 6.

    Hellmér M, Paxéus N, Magnius L, Enache L, Arnholm B, Johansson A, Bergström T, Norder H, 2014. Detection of pathogenic viruses in sewage provided early warnings of hepatitis A virus and norovirus outbreaks. Appl Environ Microbiol 80: 6771–6781.

  • 7.

    Xagoraraki I, O’Brien E, 2020. Wastewater-based epidemiology for early detection of viral outbreaks. O’Bannon DJ, ed. Women in Water Quality. Basingstoke, United Kingdom: Springer Nature, 75–97.

  • 8.

    Hovi T, Shulman LM, Van der Avoort H, Deshpande J, Roivainen M, De Gourville EM, 2012. Role of environmental poliovirus surveillance in global polio eradication and beyond. Epidemiol Infect 140: 113.

    • Search Google Scholar
    • Export Citation
  • 9.

    World Health Organization (WHO) , 2003. Guidelines for Environmental Surveillance of Poliovirus Circulation. Geneva, Switzerland: WHO.

  • 10.

    La Rosa G, Bonadonna L, Lucentini L, Kenmoe S, Suffredini E, 2020. Coronavirus in water environments: occurrence, persistence and concentration methods: a scoping review. Water Res 179: 115899.

    • Search Google Scholar
    • Export Citation
  • 11.

    Randazzo W, Truchado P, Cuevas-Ferrando E, Simón P, Allende A, Sánchez G, 2020. SARS-CoV-2 RNA in wastewater anticipated COVID-19 occurrence in a low prevalence area. Water Res 181: 115942.

    • Search Google Scholar
    • Export Citation
  • 12.

    Haramoto E, Kitajima M, Hata A, Torrey JR, Masago Y, Sano D, Katayama H, 2018. A review on recent progress in the detection methods and prevalence of human enteric viruses in water. Water Res 135: 168186.

    • Search Google Scholar
    • Export Citation
  • 13.

    Chacón L, Barrantes K, Santamaría-Ulloa C, Solano M, Reyes L, Taylor L, Valiente C, Symonds EM, Achí R, 2020. A somatic coliphage threshold approach to improve the management of activated sludge wastewater treatment plant effluents in resource-limited regions. Appl Environ Microbiol 86: e00616-20.

  • 14.

    Coulliette-salmond AD et al., 2019. Haiti poliovirus environmental surveillance. Am J Trop Med Hyg101: 12401248.

  • 15.

    Troy SB, Ferreyra-Reyes L, Huang C, Mahmud N, Lee Y-J, Canizales-Quintero S, Flaster H, Baez-Saldana R, Garcia-Garcia L, Maldonado Y, 2011. Use of a novel real-time PCR assay to detect oral polio vaccine shedding and reversion in stool and sewage samples after a Mexican national immunization day. J Clin Microbiol 49: 17771783.

    • Search Google Scholar
    • Export Citation
  • 16.

    González MM, Fonseca MC, Rodríguez CA, Giraldo AM, Vila JJ, Castaño JC, Padilla L, Sarmiento L, 2019. Environmental surveillance of polioviruses in Armenia, Colombia before trivalent oral polio vaccine cessation. Viruses 11: 775.

    • Search Google Scholar
    • Export Citation
  • 17.

    de Oliveira Pereira JS, da Silva LR, de Meireles Nunes A, de Souza Oliveira S, da Costa EV, da Silva EE, 2016. Environmental surveillance of polioviruses in Rio de Janeiro, Brazil, in support to the activities of Global Polio Eradication Initiative. Food Environ Virol 8: 2733.

    • Search Google Scholar
    • Export Citation
  • 18.

    World Bank Group , 2020. PIB (US$a precios actuales) - Costa Rica. Available at: https://datos.bancomundial.org/indicador/NY.GDP.MKTP.CD?end=2019&locations=CR&start=1960. Accessed October 2, 2020.

  • 19.

    Hewitt J, Leonard M, Greening GE, Lewis GD, 2011. Influence of wastewater treatment process and the population size on human virus profiles in wastewater. Water Res 45: 62676276.

    • Search Google Scholar
    • Export Citation
  • 20.

    Eaton A, Clsceri L, Rice E, Greenberg A, eds., 2005. Standard Methods for the Examination of Water and Wastewater, 21st edition. Washington, DC: American Public Health Association.

  • 21.

    Deshpande JM, Shetty SJ, Siddiqui ZA, 2003. Environmental surveillance system to track wild poliovirus transmission. Appl Environ Microbiol 69: 29192927.

    • Search Google Scholar
    • Export Citation
  • 22.

    Bortman M, 1999. Elaboración de corredores o canales endémicos mediante planillas de cálculo. Pan Am J Public Health 5: 1–8.

  • 23.

    de Salud M, 2015. Protocolo: Vigilancia de La Enfermedades Transmitidas Por Alimentos y Agua Paea La Detección e Intervención de Brotes, 1st edition. San José, Costa Rica: Ministerio de Salud de Costa Rica.

  • 24.

    Rodríguez-Morales F, Suárez-Cuartas MR, Ramos-Ávila AC, 2016. Canal endémico de enfermedad respiratoria aguda y enfermedad diarreica aguda en menores de 5 años en una localidad de Bogotá. Rev Salud Publica (Bogota) 18: 263274.

    • Search Google Scholar
    • Export Citation
  • 25.

    Hernández M, Arboleda D, Arce S, Benavides A, Tejada PA, Ramírez SV, Cubides Á, 2016. Metodología para la elaboración de canales endémicos y tendencia de la notificación del dengue, Valle del Cauca, Colombia, 2009–2013. Biomedica 36: 98107.

    • Search Google Scholar
    • Export Citation
  • 26.

    Ministerio de Salud de Costa Rica, 2020. Vigilancia de la Salud: Enfermedades de Notificación Colectiva. Available at: https://www.ministeriodesalud.go.cr/index.php/vigilancia-de-la-salud/estadisticas-y-bases-de-datos/notificacion-colectiva. Accessed August 18, 2020.

  • 27.

    Instituto Nacional de Estadística y Censos (INEC) , 2015. Anuario Estadístico 2012–2013. Available at: https://www.inec.cr/sites/default/files/documetos-biblioteca-virtual/12._anuario_2012-2013.pdf. Accessed July 6, 2021.

  • 28.

    Salas Peraza D, Torres Alvarado G, Obando Rodríguez A, Ramírez Espinoza F, 2015. Boletín Estadístico de Enfermedades o Eventos de Notificación Colectiva En Costa Rica de Año 2015. Available at: https://www.ministeriodesalud.go.cr/index.php/vigilancia-de-la-salud/indicadores-de-salud-boletines/boletin-de-morbilidad/3172-registro-colectivo-2015-4/file. Accessed July 6, 2021.

  • 29.

    Mata L, Simhon A, Padilla R, del Mar Gamboa M, Vargas G, Hernández F, Mohs E, Lizano C, 1983. Diarrhea associated with rotaviruses, enterotoxigenic Escherichia coli, Campylobacter, and other agents in Costa Rican children, 1976–1981. Am J Trop Med Hyg 32: 146153.

    • Search Google Scholar
    • Export Citation
  • 30.

    Patel MM, Pitzer V, Alonso W, Vera D, Lopman B, Tate J, Viboud C, Parashar UD, 2013. Global seasonality of rotavirus disease. Pediatr Infect Dis J 130: 15141523.

    • Search Google Scholar
    • Export Citation
  • 31.

    da Silva Poló T, Peiró JR, Mendes LCN, Ludwig LF, de Oliveira-Filho EF, Bucardo F, Huynen P, Melin P, Thiry E, Mauroy A, 2016. Human norovirus infection in Latin America. J Clin Virol 78: 111119.

    • Search Google Scholar
    • Export Citation
  • 32.

    Farfán-García AE, Imdad A, Zhang C, Arias-Guerrero MY, Sánchez-álvarez NT, Iqbal J, Hernández-Gamboa AE, Slaughter JC, Gómez-Duarte OG, 2020. Etiology of acute gastroenteritis among children less than 5 years of age in Bucaramanga, Colombia: a case-control study. PLoS Negl Trop Dis 14: 120.

    • Search Google Scholar
    • Export Citation
  • 33.

    Bányai K, Estes MK, Martella V, Parashar UD, 2018. Viral gastroenteritis. Lancet 392: 175186.

  • 34.

    Gaensbauer JT et al., 2019. Identification of enteropathogens by multiplex PCR among rural and urban Guatemalan children with acute diarrhea. Am J Trop Med Hyg 101: 534540.

    • Search Google Scholar
    • Export Citation
  • 35.

    Banco Interamericano de Desarrollo , 2019. ¿Cómo está America Latina en Términos de Saneamiento? Available at: https://www.iadb.org/es/mejorandovidas/como-esta-america-latina-en-terminos-de-saneamiento. Accessed August 19, 2020.

  • 36.

    Instituto Metereológico Nacional , 2013. Boletín Meteorológico. Available at: https://www.imn.ac.cr/boletin-meteorologico. Accessed July 6, 2021.

  • 37.

    Sarmiento L, Mas P, Goyenechea A, Palomera R, Morier L, Capó V, Quintana I, Santin M, 2001. First epidemic of echovirus 16 meningitis in Cuba. Emerg Infect Dis 7: 887889.

    • Search Google Scholar
    • Export Citation
  • 38.

    Arauz-Ruiz P, Sundqvist L, García Z, Taylor L, Visoná K, Norder H, Magnius LO, 2001. Presumed common source outbreaks of hepatitis A in an endemic area confirmed by limited sequencing within the VP1 region. J Med Virol 65: 449456.

    • Search Google Scholar
    • Export Citation
  • 39.

    Pang X, Cao M, Zhang M, Lee B, 2011. Increased sensitivity for various rotavirus genotypes in stool specimens by amending three mismatched nucleotides in the forward primer of a real-time RT-PCR assay. J Virol Methods 172: 8587.

    • Search Google Scholar
    • Export Citation
  • 40.

    Japhet MO, Adesina OA, Famurewa O, Svensson L, Nordgren J, 2012. Molecular epidemiology of rotavirus and norovirus in Ile-Ife, Nigeria: high prevalence of G12P[8] rotavirus strains and detection of a rare norovirus genotype. J Med Virol 84: 14891496.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 1582 920 36
Full Text Views 236 82 19
PDF Downloads 253 95 20
 
 
 
 
 
 
 
 
 
 
 

Wastewater-Based Epidemiology of Enteric Viruses and Surveillance of Acute Gastrointestinal Illness Outbreaks in a Resource-Limited Region

Luz ChacónInstituto de Investigaciones en Salud (INISA), Universidad de Costa Rica, San José, Costa Rica;

Search for other papers by Luz Chacón in
Current site
Google Scholar
PubMed
Close
,
Eric MoralesInstituto de Investigaciones en Salud (INISA), Universidad de Costa Rica, San José, Costa Rica;

Search for other papers by Eric Morales in
Current site
Google Scholar
PubMed
Close
,
Carmen ValienteLaboratorio Nacional de Aguas (LNA), Instituto Costarricense de Acueductos y Alcantarillados, San José, Costa Rica

Search for other papers by Carmen Valiente in
Current site
Google Scholar
PubMed
Close
,
Liliana ReyesInstituto de Investigaciones en Salud (INISA), Universidad de Costa Rica, San José, Costa Rica;

Search for other papers by Liliana Reyes in
Current site
Google Scholar
PubMed
Close
, and
Kenia BarrantesInstituto de Investigaciones en Salud (INISA), Universidad de Costa Rica, San José, Costa Rica;

Search for other papers by Kenia Barrantes in
Current site
Google Scholar
PubMed
Close
View More View Less
Restricted access

ABSTRACT.

Acute gastrointestinal illness (AGI) continues to be an important cause of morbidity and mortality among all ages. This study applied the principles of wastewater-based epidemiology for the preventive identification of potential outbreaks of acute viral gastroenteritis and hepatitis A by analyzing the presence of human enteric viruses in influents of small municipal wastewater treatment plants (WWTPs) handling domestic sewage, together with public health reports of acute diarrheal and hepatitis A disease in Costa Rica during 2013. Raw wastewater samples were collected during four seasonal periods with different rainfall levels. The presence of five human enteric viruses (rotavirus A, norovirus GI, norovirus GII, enterovirus, and hepatitis A virus) was studied by endpoint and real-time polymerase chain reaction in influents of five WWTPs. Cases of AGI were analyzed using historical public health reports of endemic levels and quartile ranges for each administrative and territorial area where the WWTPs are located and for its surrounding counties. A tendency for a higher rate of positive viral tests was present 1 week before an increase of AGI cases. Epidemiological weeks categorized as Outbreak (above the 75th percentile) and Success (below the 25th percentile) showed statistically significant differences in terms of positive viral test rates (Wilcoxon test, P = 0.05). Virological monitoring of wastewater in small WWTPs is an appropriate model for epidemiological surveillance of diarrheal and hepatitis A diseases in low- and middle-resource countries.

Author Notes

Address correspondence to Luz Chacón, Instituto de Investigaciones en Salud (INISA), Universidad de Costa Rica, San José, Costa Rica. E-mail: luz.chacon@ucr.ac.cr

Authors’ addresses: Luz Chacón, Eric Morales, Liliana Reyes, and Kenia Barrantes, Universidad de Costa Rica, Instituto de Investigaciones en Salud (INISA), Montes de Oca, San Jose, Costa Rica, E-mails: luz.chacon@ucr.ac.cr, eric.morales@ucr.ac.cr, lilliana.reyes@ucr.ac.cr, and kenia.barrantes@ucr.ac.cr. Carmen Valiente, Instituto Costarricense de Acueductos y Alcantarillados, Laboratorio Nacional de Aguas, San Jose, San José, Costa Rica, E-mail: civaliente@gmail.com.

Save