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. 2020 Jul 20;86(15):e00702-20.
doi: 10.1128/AEM.00702-20. Print 2020 Jul 20.

Environmental Surveillance Complements Case-Based Surveillance of Acute Flaccid Paralysis in Polio Endgame Strategy 2019-2023

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Environmental Surveillance Complements Case-Based Surveillance of Acute Flaccid Paralysis in Polio Endgame Strategy 2019-2023

Peng Chen et al. Appl Environ Microbiol. .

Abstract

The Polio Endgame Strategy 2019-2023 has been developed. However, more effective and efficient surveillance activities should be conducted with the preparedness of emergence for vaccine-derived poliovirus (VDPV) or wild poliovirus (WPV). We reviewed the impact of the case-based acute flaccid paralysis (AFP) surveillance (1991 to 2018) and environmental surveillance (2011 to 2018) in polio eradication in Shandong province of China. Clinical characteristics of AFP cases and enterovirus (EV) investigation of research samples were assessed. During the period, 10,224 AFP cases were investigated, and 352 sewage samples were collected. The nonpolio AFP rate sustained at over 2.0/100,000 since 1997. Of 10,224 cases, males and young children experienced a higher risk of severe diseases, and 68.5% suffered lower limb paralysis. We collected 1,707 EVs from AFP cases, including 763 polioviruses and 944 nonpolio enteroviruses (NPEVs). No WPV was isolated since 1992. The AFP surveillance showed high sensitivity in detecting 143 vaccine-associated paralytic poliomyelitis (VAPP) cases and 6 VDPVs. For environmental surveillance, 217 (61.6%) samples were positive for poliovirus, and altogether, 838 polioviruses and 2,988 NPEVs were isolated. No WPV was isolated in environmental surveillance, although one VDPV2 was identified. Phylogenetic analysis revealed environmental surveillance had the capacity to detect a large scope of NPEVs. The case-based AFP surveillance will be indispensable for detecting VAPP cases and VDPV circulation in countries using oral polio vaccine. Environmental surveillance is advantageous in identifying EV circulation and responding to ongoing circulating VDPV outbreaks and should be expanded to complement the AFP surveillance.IMPORTANCE Interrupting wild poliovirus transmission and stopping circulating vaccine-derived poliovirus (cVDPV) outbreaks have been proposed as two global goals by the World Health Organization in the Global Polio Eradication Initiative (GPEI). This analysis, based on the 28-year acute flaccid paralysis (AFP) surveillance and 8-year environmental surveillance, provides continued high-quality surveillance performance in achieving the GPEI and detecting the circulation of enterovirus. Given the ongoing cVDPV outbreaks in the world, we present the surveillance capacity of environmental surveillance in capturing enterovirus circulation. The final poliovirus (especially VDPV) elimination has become increasingly complex, and the case-based AFP surveillance alone will lead to difficulties in early detecting dynamics of poliovirus transmission and monitoring the extent of environmental circulation. This study goes beyond previous work to provide a detailed comprehensive evaluation of the enterovirus surveillance and can be used to formulate a set of implementation plan and performance indicators for environmental surveillance.

Keywords: acute flaccid paralysis surveillance; enterovirus; environmental surveillance; oral polio vaccine; poliomyelitis.

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Figures

FIG 1
FIG 1
Timeline of poliomyelitis eradication process in Shandong province, China from 1956 to 2018. Abbreviations: AFP, acute flaccid paralysis; bOPV, bivalent oral polio vaccine; cVDPV, circulating vaccine-derived poliovirus; EPI, Expanded Program on Immunization; ES, environmental surveillance; GPEI, Global Polio Eradication Initiative; IPV, inactivated polio vaccine; NIDs, National Immunization Days; NNDRS, National Notifiable Disease Reporting System; OPV, oral polio vaccine; SIAs, supplementary immunization activities; SNIDs, Subnational Immunization Days; tOPV, trivalent oral polio vaccine; WPV, wild poliovirus.
FIG 2
FIG 2
Data for AFP cases, VAPP cases, nonpolio AFP rates, and vaccination doses in Shandong province (1991 to 2018). (A) Monthly numbers of reported AFP cases and annual nonpolio AFP rates. The red dotted line indicates the target recommended by the WHO. (B) Annual numbers of VAPP cases positive for poliovirus and vaccination doses. A square represents one VAPP case. Abbreviations: AFP, acute flaccid paralysis; VAPP, vaccine-associated paralytic poliomyelitis.
FIG 3
FIG 3
Numbers of polioviruses (A), NPEVs (B) and EV-A71 strains (C) isolated from the case-based AFP surveillance in Shandong province (1991 to 2018). (A) Annual numbers of three poliovirus types from 1991 to 2018. The color-coded stars indicate the numbers of three VDPV types detected from the AFP cases. The arrow indicates Shandong province achieves a switch from tOPV to bOPV and IPV in May 2016. (B) Monthly number of NPEV from January 1991 to December 2018. (C) Annual number of EV-A71 from 1991 to 2018. Abbreviations: EV-A71, enterovirus A71; NPEV, nonpolio enterovirus; VDPV, vaccine-derived poliovirus.
FIG 4
FIG 4
Poliovirus and NPEV isolated from the environmental surveillance in Shandong province (2011 to 2018). (A) Annual numbers of three poliovirus types and vaccination doses inoculated at three environmental surveillance sites from 2011 to 2018. A color-coded star indicates one VDPV2 is detected from a sewage sample. The arrow indicates Shandong province achieves a switch from tOPV to bOPV and IPV in May 2016. (B) Monthly distribution of three poliovirus types in environmental surveillance. The solid brown line with triangles indicates the positivity rate of poliovirus in sewage samples every year. The green star indicates one VDPV2 was isolated from sewage samples in December 2012. (C) Monthly distribution of NPEV in environmental surveillance. Abbreviations: NPEV, nonpolio enterovirus; bOPV, bivalent oral polio vaccine; IPV, inactivated polio vaccine; tOPV, trivalent oral polio vaccine; VDPV, vaccine-derived poliovirus.
FIG 5
FIG 5
Phylogenetic relationship and genetic divergence of E-11 from AFP surveillance and environmental surveillance in Shandong province in 2018. (A) Phylogenetic tree of E-11 based on complete VP1 sequences. Circles indicate strains detected from AFP cases; squares indicate prototype strains. (B) Density curve of the genetic distance for E-11. The red line indicates the genetic divergence of strains from AFP cases, the blue line indicates the genetic divergence of strains from sewage, and the green line indicates the genetic divergence of strains between cases and sewage. Abbreviations: AFP, acute flaccid paralysis; E-11, echovirus 11; ES, environmental surveillance.

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