Abstract
To enhance our ability to monitor poliovirus circulation and certify eradication, we evaluated the performance of the bag-mediated filtration system (BMFS) against the two-phase separation (TPS) method for concentrating wastewater samples for poliovirus detection. Sequential samples were collected at two sites in Mexico; one L was collected by grab and ~ 5 L were collected and filtered in situ with the BMFS. In the laboratory, 500 mL collected by grab were concentrated using TPS and the sample contained in the filter of the BMFS was eluted without secondary concentration. Concentrates were tested for the presence of poliovirus and non-poliovirus enterovirus (NPEV) using Global Poliovirus Laboratory Network standard procedures. Between February 16, 2016, and April 18, 2017, 125 pairs of samples were obtained. Collectors spent an average (± standard deviation) of 4.3 ± 2.2 min collecting the TPS sample versus 73.5 ± 30.5 min collecting and filtering the BMFS sample. Laboratory processing required an estimated 5 h for concentration by TPS and 3.5 h for elution. Sabin 1 poliovirus was detected in 37 [30%] samples with the TPS versus 24 [19%] samples with the BMFS (McNemar’s mid p value = 0.004). Sabin 3 poliovirus was detected in 59 [47%] versus 49 (39%) samples (p = 0.043), and NPEV was detected in 67 [54%] versus 40 [32%] samples (p < 0.001). The BMFS method without secondary concentration did not perform as well as the TPS method for detecting Sabin poliovirus and NPEV. Further studies are needed to guide the selection of cost-effective environmental surveillance methods for the polio endgame.
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References
Abedi, G. R., Watson, J. T., Pham, H., Nix, W. A., Oberste, M. S., & Gerber, S. I. (2015). Enterovirus and human parechovirus surveillance—United States, 2009–2013. Morbidity and Mortality Weekly Report,64(34), 940–943. https://doi.org/10.15585/mmwr.mm6434a3.
Asghar, H., Diop, O. M., Weldegebriel, G., Malik, F., Shetty, S., El Bassioni, L., et al. (2014). Environmental surveillance for polioviruses in the Global Polio Eradication Initiative. Journal of Infectious Diseases,210(Suppl 1), S294–S303. https://doi.org/10.1093/infdis/jiu384.
Blomqvist, S., Savolainen, C., Laine, P., Hirttio, P., Lamminsalo, E., Penttila, E., et al. (2004). Characterization of a highly evolved vaccine-derived poliovirus type 3 isolated from sewage in Estonia. Journal of Virology,78(9), 4876–4883. https://doi.org/10.1128/JVI.78.9.4876-4883.2004.
Burns, C. C., Kilpatrick, D. R., Iber, J. C., Chen, Q., & Kew, O. M. (2016). Molecular properties of poliovirus isolates: nucleotide sequence analysis, typing by PCR and real-time RT-PCR. In J. Martin (Ed.), Poliovirus: methods and protocols, methods in molecular biology (Vol. 1387, pp. 177–212). New York: Springer.
Cowger, T. L., Burns, C. C., Sharif, S., Gary, H. E., Jr., Iber, J., Henderson, E., et al. (2017). The role of supplementary environmental surveillance to complement acute flaccid paralysis surveillance for wild poliovirus in Pakistan—2011–2013. PLoS ONE,12(7), e0180608. https://doi.org/10.1371/journal.pone.0180608.
Deshpande, J., Shetty, S., & Siddiqui, Z. (2003). Environmental surveillance system to track wild poliovirus transmission. Applied and Environmental Microbiology,69(5), 2919–2927. https://doi.org/10.1128/AEM.69.5.2919-2927.2003.
Dhole, T. N., Ayyagari, A., Chowdhary, R., Shakya, A. K., Shrivastav, N., Datta, T., et al. (2009). Non-polio enteroviruses in acute flaccid paralysis children of India: vital assessment before polio eradication. Journal of Paediatrics and Child Health,45(7–8), 409–413. https://doi.org/10.1111/j.1440-1754.2009.01529.
Dowdle, W., van der Avoort, H., de Gourville, E., Delpeyroux, F., Desphande, J., Hovi, T., et al. (2006). Containment of polioviruses after eradication and OPV cessation: characterizing risks to improve management. Risk analysis,26(6), 1449–1469. https://doi.org/10.1111/j.1539-6924.2006.00844.x.
Esteves-Jaramillo, A., Estivariz, C. F., Peñaranda, S., Richardson, V. L., Reyna, J., Coronel, D. L., et al. (2014). Detection of vaccine-derived polioviruses in Mexico using environmental surveillance. Journal of Infectious Diseases,210(Suppl 1), S315–S323. https://doi.org/10.1093/infdis/jiu183.
Fagnant, C. S., Beck, N. K., Yang, M. F., Barnes, K. S., Boyle, D. S., & Meschke, J. S. (2014). Development of a novel bag-mediated filtration system for environmental recovery of poliovirus. Journal of Water and Health,12(4), 747–754. https://doi.org/10.2166/wh.2014.032.
Fagnant, C. S., Kossik, A. L., Zhou, N. A., Sanchez-Gonzalez, L., Falman, J. C., Keim, E. K., et al. (2017a). Use of preservative agents and antibiotics for increased poliovirus survival on positively charged filters. Food and Environmental Virology,9(4), 383–394. https://doi.org/10.1007/s12560-017-9306-4.
Fagnant, C. S., Sanchez-Gonzalez, L. M., Zhou, N. A., Falman, J. C., Eisenstein, M., Guelig, D., et al. (2018). Improvement of the bag-mediated filtration system for sampling wastewater and wastewater-impacted waters. Food and Environmental Virology,10(1), 72–82. https://doi.org/10.1007/s12560-017-9311-7.
Fagnant, C. S., Toles, M., Zhou, N. A., Powell, J., Adolphsen, J., Guan, Y., et al. (2017b). Development of an elution device for ViroCap virus filters. Environmental Monitoring and Assessment,189(11), 574. https://doi.org/10.1007/s10661-017-6258-y.
Falman, J. C., Fagnant-Sperati, C. S., Kossik, A. L., Boyle, D. S., & Meschke, J. S. (2019). Evaluation of secondary concentration methods for poliovirus detection in wastewater. Food and Environmental Virology,11(1), 20–31. https://doi.org/10.1007/s12560-018-09364-y.
Gerloff, N., Sun, H., Mandelbaum, M., Maher, C., Nix, W. A., Zaidi, S., et al. (2018). Diagnostic assay development for poliovirus eradication. Journal of Clinical Microbiology,56(2), e01624. https://doi.org/10.1128/jcm.01624-17.
Global Polio Eradication Initiative (2013). Polio Eradication & Endgame Strategic Plan 2013–2018. WHO/POLIO/13.02. Retrieved from http://www.polioeradication.org/Portals/0/Document/Resources/StrategyWork/PEESP_EN_US.pdf.
Global Polio Eradication Initiative (2015). Guidelines on environmental surveillance for detection of polioviruses. March, 2015. Retrieved from http://polioeradication.org/wp-content/uploads/2016/07/GPLN_GuidelinesES_April2015.pdf.
Hampton, L. M., Farrell, M., Ramirez-Gonzalez, A., Menning, L., Shendale, S., Lewis, I., et al. (2016). Cessation of trivalent oral poliovirus vaccine and introduction of inactivated poliovirus vaccine—Worldwide, 2016. Morbidity & Mortality Weekly Report,65(35), 934–938. https://www.cdc.gov/mmwr/volumes/65/wr/mm6535a3.htm?s_cid=mm6535a3_w.
Hovi, T., Blomqvist, S., Nasr, E., Burns, C. C., Sarjakoski, T., Ahmed, N., et al. (2005). Environmental surveillance of wild poliovirus circulation in Egypt—Balancing between detection sensitivity and workload. Journal of Virological Methods,126(1–2), 127–134. https://doi.org/10.1016/j.jviromet.2005.02.002.
Hovi, T., Shulman, L. M., van der Avoort, H., Deshpande, J., Roivainen, M., & De Gourville, E. M. (2012). Role of environmental poliovirus surveillance in global polio eradication and beyond. Epidemiology and Infection,140(1), 1–13. https://doi.org/10.1017/S095026881000316X.
Khetsuriani, N., Lamonte-Fowlkes, A., Oberste, S., & Pallansch, M. A. (2006). Enterovirus surveillance—United States, 1970–2005. MMWR: Surveillance Summaries,55(8), 1–20.
Kilpatrick, D. R., Ching, K., Iber, J., Chen, Q., Yang, S. J., De, L., et al. (2014). Identification of vaccine-derived polioviruses using dual-stage real-time RT-PCR. Journal of Virological Methods,197, 25–28. https://doi.org/10.1016/j.jviromet.2013.11.017.
Kilpatrick, D. R., Yang, C. F., Ching, K., Vincent, A., Iber, J., Campagnoli, R., et al. (2009). Rapid group-, serotype-, and vaccine strain-specific identification of poliovirus isolates by real-time reverse transcription-PCR using degenerate primers and probes containing deoxyinosine residues. Journal of Clinical Microbiology,47(6), 1939–1941. https://doi.org/10.1128/jcm.00702-09.
Kopel, E., Kaliner, E., & Grotto, I. (2014). Lessons from a public health emergency–importation of wild poliovirus to Israel. New England Journal of Medicine,371(11), 981–983. https://doi.org/10.1056/NEJMp1406250.
Mas Lago, P., Gary, H. E., Jr., Perez, L. S., Caceres, V., Olivera, J. B., Puentes, R. P., et al. (2003). Poliovirus detection in wastewater and stools following an immunization campaign in Havana, Cuba. International Journal of Epidemiology,32(5), 772–777.
Nakamura, T., Hamasaki, M., Yoshitomi, H., Ishibashi, T., Yoshiyama, C., Maeda, E., et al. (2015). Environmental surveillance of poliovirus in sewage water around the introduction period for inactivated polio vaccine in Japan. Applied and Environmental Microbiology,81(5), 1859–1864. https://doi.org/10.1128/aem.03575-14.
Shulman, L. M., Manor, Y., Sofer, D., Handsher, R., Swartz, T., Delpeyroux, F., et al. (2006). Neurovirulent vaccine-derived polioviruses in sewage from highly immune populations. PLoS ONE,1, e69. https://doi.org/10.1371/journal.pone.0000069.
Van Der Avoort, H. G., Reimerink, J. H., Ras, A. R., Mulders, M. N., & Van Loon, A. M. (1995). Isolation of epidemic poliovirus from sewage during the 1992-3 type 3 outbreak in The Netherlands. Epidemiology and Infection,114, 481–491.
World Health Organization (2004). Department of Immunization, Vaccines and Biologicals. Polio laboratory manual, 4th Edition 2004. Retrieved from http://whqlibdoc.who.int/hq/2004/WHO_IVB_04.10.pdf.
World Health Organization (2010). Department of Immunization, Vaccines and Biologicals. Supplement 1to the WHO Polio Laboratory Manual. An alternative test algorithm for poliovirus isolation and characterization. Retrieved from http://www.who.int/immunization_monitoring/Supplement_polio_lab_manual.pdf.
Zhou, N. A., Fagnant-Sperati, C. S., Shirai, J. H., Sharif, S., Zaidi, S. Z., Rehman, L., et al. (2018). Evaluation of the bag-mediated filtration system as a novel tool for poliovirus environmental surveillance: Results from a comparative field study in Pakistan. PLoS ONE,13(7), e0200551. https://doi.org/10.1371/journal.pone.0200551.
Acknowledgements
We are grateful to the local field staff at Hidalgo (Víctor Manuel Bustos Zamora, Gabriela Muños Villegas, Carlos Alberto de la Guardia Ángeles) and Mexico City (José Antonio Herrera Cobos, Jorge Morales López) for their contribution to the collection and initial processing of the environmental samples. We would also like to acknowledge Alexandra L Kossik for supporting the training of field and laboratory staff in the use of the bag-mediated filtration system; Dr. Steven G. F. Wassilak, Dr. Mark A. Pallansch and Dra. Tamara Mancero Buchelli, for their contributions to the study design and planning; Hongmei Liu and Jane Iber for sequencing; and Dr. Angela Coulliette-Salmond, and Jeff Shirai for their support to the coordination of logistics for study implementation.
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This study was supported by funding from the Centers for Disease Control and Prevention.
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Estívariz, C.F., Pérez-Sánchez, E.E., Bahena, A. et al. Field Performance of Two Methods for Detection of Poliovirus in Wastewater Samples, Mexico 2016–2017. Food Environ Virol 11, 364–373 (2019). https://doi.org/10.1007/s12560-019-09399-9
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DOI: https://doi.org/10.1007/s12560-019-09399-9