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      Surveillance to Track Progress Toward Polio Eradication — Worldwide, 2017–2018

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          Abstract

          When the Global Polio Eradication Initiative (GPEI) began in 1988, cases of poliomyelitis were reported from 125 countries. Since then, only Afghanistan, Nigeria, and Pakistan have experienced uninterrupted transmission of wild poliovirus (WPV). The primary means of detecting poliovirus is through surveillance for acute flaccid paralysis (AFP) among children aged <15 years with testing of stool specimens for WPV and vaccine-derived polioviruses (VDPVs) in World Health Organization (WHO)–accredited laboratories of the Global Polio Laboratory Network (GPLN) ( 1 , 2 ). AFP surveillance is supplemented by environmental surveillance for polioviruses in sewage at selected locations. Analysis of genomic sequences of isolated polioviruses enables assessment of transmission by time and place, potential gaps in surveillance, and emergence of VDPVs ( 3 ). This report presents 2017–2018 poliovirus surveillance data, focusing on 31 countries* identified as high-priority countries because of a “high risk of poliovirus transmission and limited capacity to adequately address those risks” ( 4 ). Some of these countries are located within WHO regions with endemic polio, and others are in regions that are polio-free. In 2018, 26 (84%) of the 31 countries met AFP surveillance indicators nationally; however, subnational variation in surveillance performance was substantial. Surveillance systems need continued strengthening through monitoring, supervision, and improvements in specimen collection and transport to provide sufficient evidence for interruption of poliovirus circulation. Acute Flaccid Paralysis Surveillance Two surveillance performance indicators assess the quality of AFP surveillance. The first is the nonpolio AFP (NPAFP) rate (the number of NPAFP cases per 100,000 children aged <15 years per year); an NPAFP rate ≥2 is considered sufficiently sensitive to detect circulating poliovirus. The second indicator is the collection of adequate stool specimens (i.e., two stool specimens collected ≥24 hours apart and within 14 days of paralysis onset) and arrival at a WHO-accredited laboratory by reverse cold chain and in good condition (i.e., without leakage or desiccation) from ≥80% of persons with AFP, which ensures sensitivity and provides the specificity to track poliovirus circulation ( 2 ). Among the 47 countries in the WHO African Region (AFR), the NPAFP rate in 2017 was 7.0 per 100,000 children aged <15 years, and 92% of AFP cases had adequate stool specimens; in 2018, the NPAFP rate was 5.4 per 100,000 children aged <15 years, and 89% of the AFP cases had adequate stool specimens. Among the 18 high-priority AFR countries assessed, 15 (83%) met both surveillance indicators nationally in 2018, compared with 13 (72%) in 2017 (Table 1). However, national indicators obscure subnational underperformance (Figure). During 2017–2018, no WPV cases were reported in AFR; however, circulating VDPV type 2 (cVDPV2) cases were reported in four countries. In 2017, the Democratic Republic of the Congo accounted for all 22 reported cVDPV2 cases in AFR; in 2018, 65 cVDPV2 cases were reported in the region, including 20 in the Democratic Republic of the Congo, one in Mozambique, 10 in Niger, and 34 in Nigeria (Table 1). TABLE 1 National and subnational acute flaccid paralysis (AFP) performance surveillance indicators and number of confirmed wild poliovirus (WPV) and circulating vaccine-derived poliovirus (cVDPV) cases, by country — 31 Global Polio Eradication Initiative 2018–2020 high-priority countries, World Health Organization (WHO) African, Eastern Mediterranean, South-East Asia, and Western Pacific regions, 2017–2018* WHO region/Country/Year No. of AFP cases (all ages) Regional/National NPAFP rate† Subnational areas with NPAFP rate ≥2 (%)§ Regional or national AFP cases with adequate specimens (%)¶ Subnational areas with ≥80% adequate specimens (%) Population living in areas meeting both indicators (%)** No. of confirmed WPV cases* No. of confirmed cVDPV cases*,†† 2017 African Region 31,538 7 N/A 92 N/A N/A —¶¶ 22 Burkina Faso 309 3.6 92 85 77 58 —¶¶ —¶¶ Burundi 145 2.8 53 83 65 11 —¶¶ —¶¶ Cameroon 970 9.0 100 86 90 75 —¶¶ —¶¶ Central African Republic 167 8.0 100 80 43 0 —¶¶ —¶¶ Chad 703 10.0 100 79 52 56 —¶¶ —¶¶ Democratic Republic of the Congo 2,148 5.1 100 79 42 32 —¶¶ 22 Equatorial Guinea 12 2.5 57 17 14 0 —¶¶ —¶¶ Ethiopia 1,096 2.6 73 86 100 49 —¶¶ —¶¶ Guinea 452 8.4 100 88 100 86 —¶¶ —¶¶ Guinea Bissau 83 10.6 100 82 67 35 —¶¶ —¶¶ Kenya 479 2.3 66 83 68 36 —¶¶ —¶¶ Liberia 81 4.0 100 81 60 63 —¶¶ —¶¶ Mali 259 2.9 100 86 89 91 —¶¶ —¶¶ Mozambique 385 2.8 82 85 55 39 —¶¶ —¶¶ Niger 682 6.2 100 70 0 0 —¶¶ —¶¶ Nigeria 16,468 19.6 100 98 100 100 —¶¶ —¶¶ Sierra Leone 78 2.5 100 77 75 57 —¶¶ —¶¶ South Sudan 388 7.3 90 84 60 67 —¶¶ —¶¶ Eastern Mediterranean Region 19,192 8.4 N/A 88 N/A N/A 22 74 Afghanistan 3,094 20.0 100 94 100 97 14 —¶¶ Djibouti 4 1.3 17 100 17 0 —¶¶ —¶¶ Iraq 699 4.5 95 87 79 74 —¶¶ —¶¶ Jordan 116 3.3 100 100 100 100 —¶¶ —¶¶ Lebanon 75 5.3 100 80 83 90 —¶¶ —¶¶ Libya 88 4.9 100 97 100 100 —¶¶ —¶¶ Pakistan 10,330 15.0 100 85 100 99 8 —¶¶ Somalia 345 5.0 100 99 100 100 —¶¶ —¶¶ Sudan 570 3.5 100 96 100 100 —¶¶ —¶¶ Syria 364 4.3 79 76 50 38 —¶¶ 74 Yemen 713 6.3 100 82 70 68 —¶¶ — South-East Asia Region 43,390 8.1 N/A 86 N/A N/A —¶¶ — Indonesia 1,740 2.4 71 82 47 22 —¶¶ — Western Pacific Region 6,634 2.0 N/A 90 N/A N/A —¶¶ — Papua New Guinea 28 0.9 10 46 15 0 —¶¶ — 2018 African Region 24,849 5.4 N/A 89 N/A N/A —¶¶ 65 Burkina Faso 357 4.0 100 86 77 58 —¶¶ —¶¶ Burundi 123 2.4 53 89 71 11 —¶¶ —¶¶ Cameroon 778 7.2 100 83 80 73 —¶¶ —¶¶ Central African Republic 133 6.5 86 68 14 0 —¶¶ —¶¶ Chad 650 9.0 96 90 78 56 —¶¶ —¶¶ Democratic Republic of the Congo 2,742 6.6 96 78 58 29 —¶¶ 20 Equatorial Guinea 30 6.2 86 93 71 0 —¶¶ —¶¶ Ethiopia 1,083 2.5 73 83 55 49 —¶¶ —¶¶ Guinea 232 4.2 100 89 88 81 —¶¶ —¶¶ Guinea Bissau 96 12.0 100 78 44 35 —¶¶ —¶¶ Kenya 644 3.1 85 87 74 36 —¶¶ —¶¶ Liberia 72 3.6 100 85 67 43 —¶¶ —¶¶ Mali 292 3.2 100 87 78 91 —¶¶ —¶¶ Mozambique 463 3.4 91 87 73 39 —¶¶ 1 Niger 973 8.5 100 81 75 0 —¶¶ 10 Nigeria 9,400 10.9 100 95 100 100 —¶¶ 34 Sierra Leone 114 3.5 100 83 75 57 —¶¶ —¶¶ South Sudan 430 8.0 100 83 60 67 —¶¶ —¶¶ Eastern Mediterranean Region 21,834 9.5 N/A 90 N/A N/A 33 12 Afghanistan 3,376 21.6 100 94 97 98 21 —¶¶ Djibouti 0 0 N/A N/A N/A N/A —¶¶ —¶¶ Iraq 1,023 6.5 100 90 95 78 —¶¶ —¶¶ Jordan 115 3.3 100 100 100 100 —¶¶ —¶¶ Lebanon 89 6.5 100 97 100 94 —¶¶ —¶¶ Libya 122 6.8 100 96 100 100 —¶¶ —¶¶ Pakistan 12,190 17.5 100 87 88 99 12 —¶¶ Somalia 354 4.9 100 98 100 100 —¶¶ 12 Sudan 579 3.4 100 97 100 100 —¶¶ —¶¶ Syria 362 5.5 93 85 86 44 —¶¶ —¶¶ Yemen 730 6.4 100 92 100 66 —¶¶ —¶¶ South-East Asia Region 40,493 7.6 N/A 85 N/A N/A —¶¶ 1 Indonesia 1,636 2.3 62 82 44 22 —¶¶ 1 Western Pacific Region 6,828 2.0 N/A 88 N/A N/A —¶¶ 26 Papua New Guinea 282 8.1 82 46 18 0 —¶¶ 26 Abbreviations: N/A = not applicable; NPAFP = nonpolio acute flaccid paralysis. * Data as of February 21, 2019. † Per 100,000 children aged <15 years per year. § For all subnational areas regardless of population size. ¶ Standard WHO target is adequate stool specimen collection from ≥80% of AFP cases, assessed by timeliness and condition. For this analysis, timeliness was defined as two specimens collected ≥24 hours apart (≥1 calendar day in this data set) and within 14 days of paralysis onset. Good condition was defined as arrival of specimens in a WHO-accredited laboratory with reverse cold chain maintained and without leakage or desiccation. ** Percentage of the country’s population living in subnational areas that met both surveillance indicators (NPAFP rates ≥2 per 100,000 children aged <15 years per year and ≥80% of AFP cases with adequate specimens). †† cVDPV was associated with at least one case of AFP with evidence of community transmission and genetically linked. Guidelines for classification of cVDPV can be found at http://polioeradication.org/wp-content/uploads/2016/09/Reporting-and-Classification-of-VDPVs_Aug2016_EN.pdf. ¶¶ Dashes indicate that no confirmed cases were detected. FIGURE Combined performance indicators for the quality of acute flaccid paralysis surveillance in subnational areas of 31 countries identified as Global Polio Eradication Initiative high-priority countries during 2018–2020 — World Health Organization African, Eastern Mediterranean, South-East Asia, and Western Pacific regions, 2018 Abbreviation: NPAFP = nonpolio acute flaccid paralysis. The figure is a map showing the combined performance indicators for the quality of acute flaccid paralysis surveillance during 2018 in subnational areas of 31 countries identified as Global Polio Eradication Initiative high-priority countries during 2018–2020 in the World Health Organization African, Eastern Mediterranean, Western Pacific, and South-East Asia regions. Among the 21 WHO Eastern Mediterranean Region (EMR) countries, the NPAFP rates in 2017 and 2018 were 8.4 and 9.5 per 100,000 children aged <15 years, respectively, and the respective percentages of AFP cases with adequate stool specimens in 2017 and 2018 were 88% and 90%. In the two countries with endemic WPV transmission, the number of WPV1 cases increased in Afghanistan (from 14 in 2017 to 21 in 2018) and Pakistan (from eight in 2017 to 12 in 2018). In 2017, Syria accounted for all 74 reported cVDPV2 cases in EMR. In 2018, 12 cVDPV cases were reported in Somalia, including five cVDPV2 cases, six cVDPV type 3 (cVDPV3) cases, and one coinfection of both cVDPV type 2 and type 3. Among the 11 high-priority EMR countries evaluated, nine (82%) countries in 2017 and 10 (91%) countries in 2018 met both surveillance indicators nationally; however, as in AFR, national indicators masked subnational underperformance (Table 1) (Figure). In the WHO Western Pacific Region, 26 cVDPV type 1 (cVDPV1) cases were reported in Papua New Guinea in 2018. Papua New Guinea did not meet either surveillance indicator nationally in 2017, and although the NPAFP rate improved in 2018 (mainly related to implementation of enhanced AFP surveillance as part of the outbreak response), collection of adequate stool specimen remained low. In the WHO South-East Asia Region, one cVDPV1 case was reported in Indonesia in 2018. Although Indonesia met both surveillance indicators nationally in 2017 and 2018, subnational weaknesses in surveillance were substantial (Table 1) (Figure). Environmental Surveillance Environmental surveillance (testing of sewage samples) supplements AFP surveillance by identifying poliovirus transmission in the absence of detected AFP cases ( 3 ). The number of environmental surveillance sites increased in Afghanistan, Nigeria, and Pakistan from 143 in 2017 to 185 in 2018. Environmental surveillance detected no WPV or cVDPV in Nigeria in 2017; however, 46 cVPDV2 isolates were detected in 2018. Some had been isolated weeks before cases were confirmed. In 2017, four genetic clusters (isolates with ≥95% genetic relatedness) of WPV1 were detected in sewage samples from five provinces in Afghanistan, and seven genetic clusters were detected from 19 districts in Pakistan. In 2018, three WPV1 genetic clusters were detected in sewage samples from seven provinces in Afghanistan and in five clusters from 27 districts in Pakistan. In Pakistan, 16% of sewage samples from 19 districts tested positive for WPV1 in 2017, and 20% from 27 districts tested positive in 2018. Also in 2018, environmental surveillance detected one cVDPV2 isolate in Kenya as well as 19 cVDPV2 and 11 cVDPV3 isolates in Somalia. In Papua New Guinea, environmental surveillance detected seven cVDPV1 isolates from two provinces in 2018. As part of the GPEI’s global environmental surveillance expansion plan, † environmental surveillance is conducted in 44 countries without active WPV transmission, including 24 in AFR. Global Polio Laboratory Network GPLN consists of 146 quality-assured poliovirus laboratories in the six WHO regions. GPLN laboratories implement standardized protocols to 1) isolate and identify polioviruses; 2) conduct intratypic differentiation (ITD) to identify WPV, Sabin (vaccine) poliovirus, and VDPV; and 3) conduct genomic sequencing. Poliovirus transmission pathways are monitored through analysis of the viral capsid protein (VP1) coding region sequences from isolates. Standard timeliness indicators specify that laboratories should report ≥80% of poliovirus culture results within 14 days of specimen receipt, ≥80% of ITD results within 7 days of isolate receipt, and ≥80% of sequencing results within 7 days of ITD result. The combined field and laboratory performance indicator is to report ITD results for ≥80% of isolates within 60 days of paralysis onset in AFP cases. The accuracy and quality of testing at GPLN laboratories are monitored through an annual accreditation program of onsite reviews and proficiency testing ( 5 ). An accreditation checklist was implemented in 2017 for laboratories testing sewage samples. GPLN tested 201,546 stool specimens from AFP cases in 2017 and 190,055 in 2018 (Table 2). WPV1 was isolated in specimens from 22 AFP patients in 2017 and 33 patients in 2018. cVDPVs were isolated from 96 patients in 2017 and 104 patients in 2018. GPLN laboratories in all regions met timeliness indicators for poliovirus isolation and ITD. All regions met the overall timeliness indicator for onset to ITD results in both years except the European and Western Pacific Regions in 2018. TABLE 2 Number of poliovirus isolates from stool specimens of persons with acute flaccid paralysis (AFP) and timing of results, by World Health Organization (WHO) region — 2017 and 2018* WHO region/Year No. of specimens No. of poliovirus isolates % Poliovirus isolation results within 7 days of receipt at laboratory % ITD results within 7 days of receipt of specimen % ITD results within 60 days of paralysis onset Wild† Sabin§ cVDPV¶ African Region 2017 65,245 0 1,663 22 97 80 98 2018 51,292 0 2,547 65 94 98 96 Americas Region 2017 1,755 0 14 0 83 100 100 2018 1,866 0 47 0 86 100 100 Eastern Mediterranean Region 2017 35,602 22 2,521 74 98 99 97 2018 40,419 33 1,749 12 92 99 97 European Region 2017 3,480 0 73 0 83 92 90 2018 3,274 0 71 0 84 92 62 South-East Asia Region 2017 82,292 0 2,251 0 91 96 99 2018 79,566 0 1,970 1 97 100 99 Western Pacific Region 2017 13,370 0 140 0 96 97 90 2018 13,638 0 348 26 97 99 68 Total** 2017 201,546 22 6,662 96 94 91 98 2018 190,055 33 6,732 104 95 99 95 Abbreviations: cVDPV = circulating vaccine-derived poliovirus; ITD = intratypic differentiation; VP1 = viral capsid protein. * Data as of March 4, 2019. † Number of AFP cases with wild poliovirus isolates. § Either 1) concordant Sabin-like results in ITD test and vaccine-derived poliovirus screening or 2) ≤1% VP1 nucleotide sequence difference compared with Sabin vaccine virus (≤0.6% for type 2). ¶ For poliovirus types 1 and 3, ≥10 VP1 nucleotide differences from the respective poliovirus; for poliovirus type 2, ≥6 VP1 nucleotide differences from Sabin type 2 poliovirus. ** For the last three indicators, total represents weighted percentage of regional performance. In 2018, South Asia genotype (the only WPV1 genotype circulating globally since 2016) was detected in Afghanistan and Pakistan, with frequent cross-border transmission between the two countries. Compared with the previous report ( 1 ), sequence analysis indicates a reduction in the number of orphan WPV1 isolates (those with less genetic relatedness [≤98.5% in VP1] to other isolates) from AFP patients, from three in 2017 to zero in 2018, indicating that gaps in AFP surveillance might be closing; sensitive surveillance identifies AFP cases with isolates that are closely related. However, the net genetic diversity of WPV1 isolates in Afghanistan and Pakistan has remained constant for the last 3 years because of the persistent circulation of many poliovirus lineages in the reservoirs of these countries. In 2018, cVDPVs, most with extended divergence from the Sabin strain (genetic relatedness = 94%–98.5% identity), were isolated from stool specimens of AFP patients and from sewage samples, identifying nine cVDPV emergences during 2018 in seven countries (Democratic Republic of the Congo, Indonesia, Mozambique, Niger, Nigeria, Papua New Guinea, and Somalia) ( 6 , 7 ). Discussion Although most of the 31 GPEI high-priority countries evaluated met national-level AFP performance indicators, considerable variation and deficiencies existed at subnational levels. No substantial improvements were noted in surveillance indicators for these 31 countries from 2017 to 2018. For most of the evaluated AFR countries, the primary deficiency was the low percentage of AFP cases with adequate specimens, which is most often the result of delayed case detection after paralysis onset. In the three countries with endemic WPV transmission, subnational surveillance performance indicators have been high for several years, even at the district level. In Nigeria, no WPV1 was detected during August 2014–July 2016; however, during August–September 2016, WPV1 cases were detected in Borno State. Effective AFP surveillance did not take place in vast insurgent-held areas of Borno during 2013–2016. Since 2016, more areas have become accessible, and Nigeria has enhanced case detection and reporting by community-based informants residing in currently inaccessible areas ( 8 ). AFR will be considered for WPV-free certification in early 2020, and careful examination of the extent of quality surveillance will be needed to certify the region WPV-free. Genomic analyses indicated that the cVDPV1s in Indonesia and Papua New Guinea were circulating several years before detection. Papua New Guinea has experienced chronic national and subnational deficiencies in AFP case detection and adequate specimen collection and transport. Subnational surveillance gaps in Indonesia have been identified previously ( 9 ). cVDPV outbreaks in regions with endemic polio and those that are polio-free underscore the need to maintain sensitive poliovirus surveillance everywhere to rapidly detect and respond to outbreaks. AFP surveillance has been complemented by environmental surveillance in high-risk areas, which has allowed detection of cVDPVs before identification of paralyzed patients, as well as documentation of continued circulation of WPV1 in the reservoir areas of Afghanistan and Pakistan despite low-level WPV1 case confirmation. In the long term, continued environmental surveillance will be needed to monitor for poliovirus circulation in high-risk areas. The findings in this report are subject to at least two limitations. First, issues relating to security, hard-to-reach populations, and other factors could affect AFP surveillance indicators and limit their interpretation. Second, high NPAFP rates do not necessarily indicate highly sensitive surveillance because not all cases reported as AFP cases meet the AFP definition and some actual AFP cases might not be detected by weak surveillance systems. Strong AFP surveillance, which is essential for global certification of polio eradication, includes timely case detection, notification, and investigation as well as adequate stool collection and transport ( 10 ). External technical and financial support to enhance surveillance has been provided to all seven countries with cVDPV outbreaks and to the other 24 high-priority countries. The Global Polio Surveillance Action Plan, 2018–2020 ( 4 ), specifies which tasks are to be undertaken at the country level; support is tailored to countries’ needs. Routine monitoring of AFP surveillance performance indicators at subnational levels and supervision of active surveillance by field personnel are critical to achieving sensitive poliovirus surveillance. Leading up to certification of WPV eradication, integrating AFP surveillance with surveillance for other vaccine-preventable and outbreak-prone diseases will have the advantage of maximizing field surveillance capacity and performance ( 10 ). Summary What is already known about this topic? Sensitive acute flaccid paralysis surveillance is the cornerstone of polio eradication programs. What is added by this report? This report presents 2017–2018 poliovirus surveillance data, focusing on 31 countries identified as high-priority countries by the Global Polio Eradication Initiative. In 2018, 26 (84%) of the 31 countries met acute flaccid paralysis surveillance indicators nationally; however, subnational variation in surveillance performance was substantial, and no improvements were noted from 2017 to 2018. What are the implications for public health practice? Surveillance systems need continued strengthening through monitoring, supervision, and improvements in specimen collection and transport to provide sufficient evidence for interruption of poliovirus circulation.

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          Environmental surveillance for polioviruses in the Global Polio Eradication Initiative.

          This article summarizes the status of environmental surveillance (ES) used by the Global Polio Eradication Initiative, provides the rationale for ES, gives examples of ES methods and findings, and summarizes how these data are used to achieve poliovirus eradication. ES complements clinical acute flaccid paralysis (AFP) surveillance for possible polio cases. ES detects poliovirus circulation in environmental sewage and is used to monitor transmission in communities. If detected, the genetic sequences of polioviruses isolated from ES are compared with those of isolates from clinical cases to evaluate the relationships among viruses. To evaluate poliovirus transmission, ES programs must be developed in a manner that is sensitive, with sufficiently frequent sampling, appropriate isolation methods, and specifically targeted sampling sites in locations at highest risk for poliovirus transmission. After poliovirus ceased to be detected in human cases, ES documented the absence of endemic WPV transmission and detected imported WPV. ES provides valuable information, particularly in high-density populations where AFP surveillance is of poor quality, persistent virus circulation is suspected, or frequent virus reintroduction is perceived. Given the benefits of ES, GPEI plans to continue and expand ES as part of its strategic plan and as a supplement to AFP surveillance.
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            Update on Vaccine-Derived Poliovirus Outbreaks — Democratic Republic of the Congo and Horn of Africa, 2017–2018

            Widespread use of live attenuated (Sabin) oral poliovirus vaccine (OPV) has resulted in marked progress toward global poliomyelitis eradication ( 1 ). However, in underimmunized populations, extensive person-to-person transmission of Sabin poliovirus can result in genetic reversion to neurovirulence and paralytic vaccine-derived poliovirus (VDPV) disease ( 1 ). This report updates (as of February 26, 2019) previous reports on circulating VDPV type 2 (cVDPV2) outbreaks during 2017–2018 in the Democratic Republic of the Congo (DRC) and in Somalia, which experienced a concurrent cVDPV type 3 (cVDPV3) outbreak* ( 2 , 3 ). In DRC, 42 cases have been reported in four cVDPV2 outbreaks; paralysis onset in the most recent case was October 7, 2018 ( 2 ). Challenges to interrupting transmission have included delays in outbreak-response supplementary immunization activities (SIAs) and difficulty reaching children in all areas. In Somalia, cVDPV2 and cVDPV3 were detected in sewage before the detection of paralytic cases ( 3 ). Twelve type 2 and type 3 cVDPV cases have been confirmed; the most recent paralysis onset dates were September 2 (cVDPV2) and September 7, 2018 (cVDPV3). The primary challenge to interrupting transmission is the residence of >300,000 children in areas that are inaccessible for vaccination activities. For both countries, longer periods of surveillance are needed before interruption of cVDPV transmission can be inferred. Vaccine-Derived Polioviruses VDPV types 1 or 3 are polioviruses that are >1% divergent (≥10 nucleotide differences in the genetic sequence) from the corresponding Sabin OPV strain in the viral protein 1 (VP1) genomic coding region ( 1 , 4 ). VDPV2s are >0.6% divergent (≥6 nucleotide differences in the VP1 coding region) ( 1 , 4 ). When polioviruses replicate during transmission, nucleotide substitutions in the viral genome accumulate at approximately 1.1% (10 nucleotides of the VP1 coding region) per year, which can provide the means to determine how long a strain has been circulating. VDPVs are classified as circulating (cVDPVs) when community transmission is demonstrated by genetic linkages of VDPVs isolated from paralytic cases, community contacts, or environmental (sewage) samples ( 4 ). 2016 Global Switch from Trivalent OPV to Bivalent OPV The type 2 component of trivalent OPV (tOPV) (containing vaccine virus types 1, 2, and 3) was responsible for >90% of cVDPV cases occurring during 2006–2015 ( 5 – 7 ). After the declaration of eradication of wild poliovirus type 2 in 2015 ( 6 , 7 ), a globally synchronized switch from tOPV to bivalent OPV (bOPV) (containing types 1 and 3) occurred in all OPV-using countries by May 1, 2016 ( 6 , 7 ). A single dose of inactivated poliovirus vaccine (IPV), which includes all three poliovirus serotypes, was introduced into routine immunization schedules in OPV-using countries to mitigate the risk for a gap in immunity to poliovirus type 2 ( 6 ). Children who seroconvert after IPV administration are protected from paralytic disease but still can contribute to the transmission of poliovirus. Monovalent type 2 OPV (mOPV2) is held in a global stockpile for implementation of outbreak response SIAs for poliovirus type 2 outbreaks after the switch ( 8 ). cVDPV2 Outbreaks in the Democratic Republic of the Congo Maniema province outbreak (two cases): The first patient in this outbreak had paralysis onset on March 26, 2017, and the second had paralysis onset on April 18, 2017 ( 2 ). Genetic analyses of the cVDPV2 isolates identified a 7-nucleotide difference from the Sabin type 2 strain, suggesting recent emergence. After the onset of the most recent case, four to five mOPV2 supplementary immunization activities (SIAs) were conducted in the health zones (subprovince areas) nearest to the identified cases and two in the remainder of the province (Figure 1). FIGURE 1 Circulating vaccine-derived poliovirus type 2 (cVDPV2) cases, by location and number of response supplementary immunization activities (SIAs) with monovalent oral poliovirus vaccine type 2 (mOPV2) — Democratic Republic of Congo, 2017–2018* * Each dot represents one confirmed paralytic cVDPV2 case. Dots are randomly positioned within health zones and do not represent exact locations where cases occurred. The figure is a map with insets indicating geographic distribution of circulating vaccine-derived poliovirus type 2 cases, by location and number of response supplementary immunization activities with monovalent oral poliovirus vaccine type 2, in the Democratic Republic of Congo during 2017–2018. Four-province outbreak originating in Haut Lomami (27 cases): The first patient had paralysis onset on February 20, 2017, in Haut Lomami province; the VDPV2 isolate from this case had a 15-nucleotide difference from Sabin 2, indicating >1 year of undetected circulation. Subsequent to this case, 26 additional cases with genetically linked cVDPV2 isolates were identified, with paralysis onset from March 8, 2017, to May 27, 2018, in Haut Lomami province (eight cases), in two adjacent provinces (Haut Katanga [two] and Tanganyika [15]), and in Ituri province in northeastern DRC (one). In response to these cases, up to 10 mOPV2 SIAs were conducted in the outbreak area; three mOPV2 SIAs were conducted in the broader outbreak area after the onset of the most recent case (Figure 1) ( 2 ). The isolate from the Ituri patient was genetically linked to the Haut Lomami outbreak area; however, no epidemiologic link was established. Up to three mOPV2 SIAs were conducted after the onset of the single case in Ituri province, except in health zones where Ebola virus transmission had been confirmed or suspected in 2018 ( 9 ). Mongala province outbreak (11 cases): The first case of paralysis onset associated with this outbreak occurred on April 26, 2018, and the patient’s VDPV2 isolate had a 19-nucleotide difference from Sabin 2, indicating nearly 2 years of undetected circulation. Ten additional cases with genetically linked viruses were reported, with paralysis onset during June 14–September 13, 2018. Four mOPV2 SIAs were conducted in health zones with identified cases and two to four in the remainder of Mongala and neighboring provinces; two mOPV2 SIAs have been conducted in the entirety of the outbreak area after the onset of the most recent case (Figure 1). Haut Katanga province outbreak (two cases): In this outbreak, the first patient had paralysis onset on October 6, 2018, and the second on October 7. The VDPV2 isolates had 7- and 8-nucleotide differences from the Sabin 2 strain, indicating emergence in 2018 after use of mOPV2 for SIAs in response to the Haut Lomami area outbreak, with suboptimal coverage achieved. Two SIAs were conducted after the onset of these cases (Figure 1). cVDPV2 and cVDPV3 Outbreaks in the Horn of Africa Environmental surveillance, the testing of sewage samples for polioviruses, detected genetically linked cVDPV2 in samples taken from two different environmental surveillance sites in Banadir province, Somalia, in October 2017 and January 2018 and genetically linked cVDPV3 from two different sites in April 2018. Genetic analyses of the viruses indicated undetected circulation of cVDPV2 for >3 years (36–44-nucleotide differences from Sabin 2) and of cVDPV3 for >1 year (15–17-nucleotide differences from Sabin 3) ( 3 ). No genetically linked paralytic cVDPV cases were detected until a coinfection with cVDPV2 and cVDPV3 was identified in a patient from the central province of Hiran, with paralysis onset on May 11, 2018 (Figure 2) ( 3 ). As of January 31, 2019, a total of 12 cVDPV cases had been identified in Somalia: five cVDPV2 cases, six cVDPV3 cases, and the cVDPV2/cVDPV3 coinfection (Figure 2) (Figure 3). The most recent paralysis onsets occurred on September 2 (cVDPV2) and September 7, 2018 (cVDPV3). Three patients resided in districts that were inaccessible for polio vaccination for >5 years, and none had ever received OPV. FIGURE 2 Circulating vaccine-derived poliovirus (cVDPV) type 2 and type 3 cases, as of February 26, 2019, by location — Somalia, 2018* * Each symbol represents one confirmed paralytic cVDPV case. Symbols are randomly positioned within districts and do not represent exact locations where cases occurred. The figure is a map indicating geographic distribution of circulating vaccine-derived poliovirus type 2 and type 3 cases, as of February 26, 2019, by location in Somalia during 2018. FIGURE 3 Circulating vaccine-derived poliovirus (cVDPV) cases and outbreak response supplementary immunization activities, by month — Somalia, 2017–2018 Abbreviations: bOPV = bivalent oral poliovirus vaccine, types 1 and 3; cVDPV2 = circulating vaccine derived poliovirus type 2; cVDPV3 = circulating vaccine derived poliovirus type 3; mOPV2 = monovalent oral poliovirus vaccine type 2. The figure is a histogram indicating circulating vaccine-derived poliovirus cases and outbreak response supplementary immunization activities, by month, in Somalia during 2017–2018. Twenty-one sewage samples from environmental surveillance sites in Banadir province tested positive for genetically linked cVDPV2, the most recent collected on October 11, 2018. One sewage sample collected in Kamakunji district, Kenya, in March 2018 tested positive for cVDPV2 genetically linked to strains circulating in Somalia ( 3 ); however, no cVDPV2 cases were detected in Kenya. Genetically linked cVDPV3 isolates were identified in 12 sewage samples from Banadir province, the most recent collected on August 23, 2018. No cVDPV3 isolates have been detected by environmental or acute flaccid paralysis (AFP) surveillance in Kenya, and neither cVDPV2 nor cVDPV3 has been detected in Ethiopia. In response to the Horn of Africa cVDPV2 outbreak, six mOPV2 outbreak response SIAs were conducted in Somalia during December 2017–November 2018, including two conducted after the most recent case onset. Two of these SIAs were synchronized with subnational mOPV2 outbreak response SIAs in Kenya and Ethiopia during July–September 2018. Before that, when cVDPV2 was identified by environmental surveillance in Kenya, a focal mOPV2 outbreak response SIA was conducted in Kamakunji district in May 2018. After cVDPV3 detection in Somalia, three bOPV outbreak response SIAs were conducted there during April–October 2018, two of which were synchronized with subnational bOPV SIAs in Kenya during September–October 2018. Both SIAs were implemented after paralysis onset of the most recent cVDPV3 case in Somalia. Discussion During 2005–2013, multiple cVDPV2 outbreaks occurred in DRC and Somalia ( 2 , 10 ). Because of chronically low childhood routine immunization coverage in both countries, preventive tOPV SIAs were implemented annually to boost immunity before the tOPV/bOPV switch in 2016 ( 2 , 10 ). The cVDPV outbreaks during 2017–2018 indicate that children residing in the outbreak-affected areas were not effectively reached with tOPV before the switch (and for type 3, with bOPV after the switch) through childhood routine immunization services or preventive SIAs. After the tOPV/bOPV switch, preventive SIAs using tOPV can no longer be implemented; although IPV can provide protection from paralytic disease to infected children who have received it, low routine immunization coverage precluded IPV serving as a substantive means of preventing cVDPV cases in both countries. In addition to DRC and Somalia, cVDPV2 outbreaks also were identified during 2017–2018 in Mozambique, Niger, Nigeria, and Syria. Although improving delivery of bOPV through routine immunization services would prevent cVDPV1 or cVDPV3 outbreaks, this would require considerable time, effort, and resources. Preventive bOPV SIAs can raise population immunity more quickly in countries and areas with low routine immunization coverage. cVDPV2 transmission in the DRC outbreaks might have ceased; however, a longer period of surveillance is needed before interruption of transmission can be inferred. Because of serious limitations in mOPV2 SIA quality (i.e., low population coverage), delays in SIA implementation, and a smaller geographic scope than that needed for some SIAs, many more SIAs were needed to achieve apparent interruption of transmission than are usually required. As well, when SIA coverage in the target population is low, there is a risk that the mOPV2 response SIAs themselves will seed new cVDPV2 outbreaks; in DRC, the Haut Katanga outbreak resulted from suboptimal outbreak response SIAs for the Haut Lomami area outbreak. In Somalia, AFP surveillance performance indicators have been met, even in insecure areas where community-based surveillance is conducted. However, undetected cVDPV2 and cVDPV3 transmission for approximately 1–3 years indicates high likelihood that the emergence and circulation of VDPVs occurred among unimmunized children residing in inaccessible areas. To extend the reach of the outbreak response as much as possible, outbreak response SIAs included vaccination of children living in inaccessible areas when they were at transit points (e.g., bus stations) and at markets, and rapid response vaccination in a few areas where children were not usually accessible for vaccination. However, >300,000 unimmunized children are estimated to reside in these areas. An extended period of AFP surveillance and environmental surveillance will be needed to indicate that cVDPV transmission has been interrupted in Somalia. In both countries, if additional response is required, programs need to ensure the quality and reach of timely SIAs. The continued use of aggressive strategies, such as transit-point vaccination, to reach underimmunized populations, should be considered. Summary What is already known about this topic? Prolonged person-to-person transmission of polio vaccine viruses in underimmunized populations can lead to emergence of outbreaks of paralysis from circulating vaccine-derived poliovirus (cVDPV). What is added by this report? During 2017–2018, four cVDPV type 2 outbreaks, with 42 cases to date, occurred in six provinces of the Democratic Republic of the Congo and required multiple response supplementary immunization activities (SIAs). In Somalia, concurrent cVDPV type 2 and cVDPV type 3 outbreaks occurred, first identified by sewage testing months before occurrence of 12 paralytic cases to date. What are the implications for public health practice? To promptly interrupt cVDPV transmission, country programs must effectively plan and implement timely response SIAs to optimize their quality and reach.
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              Progress Toward Poliomyelitis Eradication — Nigeria, January–December 2017

              Nearly three decades after the World Health Assembly launched the Global Polio Eradication Initiative in 1988, four of the six World Health Organization (WHO) regions have been certified polio-free ( 1 ). Nigeria is one of three countries, including Pakistan and Afghanistan, where wild poliovirus (WPV) transmission has never been interrupted. In September 2015, after >1 year without any reported WPV cases, Nigeria was removed from WHO’s list of countries with endemic WPV transmission ( 2 ); however, during August and September 2016, four type 1 WPV (WPV1) cases were reported from Borno State, a state in northeastern Nigeria experiencing a violent insurgency ( 3 ). The Nigerian government, in collaboration with partners, launched a large-scale coordinated response to the outbreak ( 3 ). This report describes progress in polio eradication activities in Nigeria during January–December 2017 and updates previous reports ( 3 – 5 ). No WPV cases have been reported in Nigeria since September 2016; the latest case had onset of paralysis on August 21, 2016 ( 3 ). However, polio surveillance has not been feasible in insurgent-controlled areas of Borno State. Implementation of new strategies has helped mitigate the challenges of reaching and vaccinating children living in security-compromised areas, and other strategies are planned. Despite these initiatives, however, approximately 130,000–210,000 (28%–45%) of the estimated 469,000 eligible children living in inaccessible areas in 2016 have not been vaccinated. Sustained efforts to optimize surveillance and improve immunization coverage, especially among children in inaccessible areas, are needed. Security Situation During the past 8 years, Borno State in northeastern Nigeria has been at the center of an insurgency that has affected other Nigerian states including Adamawa, Gombe, and Yobe and the neighboring Lake Chad Basin countries of Cameroon, Chad, and Niger. Insecurity in this region has led to a major humanitarian emergency, with forced displacement of an estimated 2.1 million persons within Nigeria and 200,000 refugees seeking shelter in other countries ( 6 ). At the height of the insurgency in 2015, 60% of settlements were inaccessible for implementation of vaccination and surveillance activities (Figure 1). Security assessments conducted during December 2017 in Borno State indicate that of the 27 districts (local government areas [LGAs]), eight (30%) are fully accessible to polio eradication program personnel, 17 (63%) are accessible only by polio eradication program personnel with military escorts, and two (7%) are accessible only by combat-ready military personnel. Overall, an estimated 30% of subdistrict level communities (settlements) in Borno State were fully inaccessible to personnel in the Nigeria polio eradication program. Analyses of satellite imagery conducted in October 2017 estimated that approximately 130,000–210,000 (28%–45%) of the estimated 469,000 children aged ≤5 years living in inaccessible areas in Borno State in 2016 had not been reached by polio vaccination or surveillance efforts. Figure 1 Accessibility of local government areas to polio eradication program personnel, by ward — Borno State, Nigeria, September 2015 The figure above is a map of Nigeria showing the accessibility of local government areas, by ward, to polio eradication program personnel in the country’s Borno State in September 2015. Poliovirus Surveillance Acute Flaccid Paralysis Surveillance. During 2016 and 2017, Nigeria met major acute flaccid paralysis (AFP) performance indicators for all states, including the nonpolio AFP (NPAFP) rate (which assesses surveillance system sensitivity) and stool adequacy (which assesses the timeliness and appropriateness of investigation of suspected cases) ( 7 ). In Borno State, NPAFP rates of 27.0 (2016) and 24.5 (2017) cases per 100,000 children aged 90% of LGAs surveyed passed the 80% LQAS threshold. TABLE Polio supplementary immunization activity dates, antigen types, coverage, and reported lot quality assurance sampling results — Nigeria, 2017 SIA date in 2017 Vaccine antigen type Target area No. children vaccinated LGAs achieving ≥90% coverage on LQAS* (%) Jan 28–31 mOPV2 18 northern states† 32,360,489 89 Feb 25–28 bOPV 14 states at the highest risk for polio§ 25,350,055 87 Mar 25–28 bOPV All 36 states + FCT 57,937,250 75 Apr 29–Aug 22¶ bOPV All 36 states + FCT 57,928,320 77 May 20–30** IPV + mOPV2 Sokoto 463,963 (IPV)
1,893,914 (mOPV2) 91 Jul 8–11 bOPV 18 northern states† 32,449,576 85 Oct 6–24†† bOPV 18 northern states† 31,242,217 78 Nov 4–14 bOPV 7 highest priority states§§ 9,847,162 89 Abbreviations: bOPV = bivalent oral poliovirus types 1 and 3; FCT = federal capital territory; IPV = inactivated polio vaccine; LGAs = local government areas; LQAS = lot quality assurance sampling; mOPV2 = monovalent oral poliovirus type 2; SIA = supplemental immunization activity. * ≥90% coverage achievement pass mark on LQAS set by Nigeria polio program. † 18 states included Abuja and the Federal Capital Territory, Adamawa, Bauchi, Borno State, Gombe, Jigawa, Kaduna, Kano, Katsina, Kebbi, Kogi, Nasarawa, Niger, Plateau, Sokoto, Taraba, Yobe, and Zamfara. § 14 states included Abuja and the Federal Capital Territory, Adamawa, Bauchi, Borno State, Gombe, Jigawa, Kaduna, Kano, Katsina, Nasarawa, Sokoto, Taraba, Yobe, and Zamfara. ¶ Campaign staggered across states to improve effectiveness and quality. ** Response to vaccine-derived poliovirus isolation. †† Campaign in Borno State coordinated with other Lake Chad Basin countries. §§ Seven states included Adamawa, Bauchi, Borno, Gombe, Sokoto, Taraba, and Yobe. In collaboration with the Nigerian military, two measures have been employed to increase poliovirus immunity among children in insecure areas of Borno and Yobe states. The Reaching Every Settlement initiative engages civilian vigilante and military support to reach children in settlements in which vaccinators require security escorts. During 2017, approximately 251,000 children in 2,921 settlements were vaccinated during 16 Reaching Every Settlement rounds. The Reaching Inaccessible Children initiative deploys military personnel with basic vaccination training to vaccinate children living in settlements that can only be accessed by combat-ready military personnel. During 2017, six Reaching Inaccessible Children rounds vaccinated 50,196 children in 1,412 inhabited settlements. Assessment of vaccination status of children arriving in camps for internally displaced persons from insurgent-held areas is conducted to help monitor progress in vaccinating children living in inaccessible areas. Other efforts aimed at improving population immunity include vaccination at markets and international borders and outreach to nomadic and migrant populations. In-depth analysis of satellite imagery to identify inaccessible areas ( 9 ) has facilitated identification and characterization of settlements and populations in areas inaccessible to polio program personnel (Figure 2), helping guide the implementation of targeted approaches to reach and immunize eligible children in these areas. Figure 2 Polio vaccination coverage, by area — Borno State, Nigeria, August 2016–October 2017 The figure above is a map of Nigeria showing polio vaccination coverage, by area, in the country’s Borno State during August 2016–October 2017. The routine immunization schedule for Nigeria includes bOPV at birth, followed by 3 additional bOPV doses at ages 6, 10, and 14 weeks. In 2015, a single dose of inactivated poliovirus vaccine was also included in the routine immunization schedule at age 14 weeks. During 2016–2017, a national coverage survey estimated that overall, 33% of children aged 12–23 months were fully vaccinated against polio, although large variations were observed by state, ranging from 7% in Sokoto and Yobe to 75% in Lagos. Discussion Since the identification of four WPV cases in Borno State in 2016, the Nigerian polio program has intensified polio eradication activities, especially in areas experiencing insurgency. However, the ability of program personnel to implement eradication activities, including high quality surveillance and vaccination, has been limited because of ongoing insurgency-related inaccessibility to areas in Borno State and other states in the country’s northeast and northwest areas. Because of military interventions against the insurgency, the percentage of settlements that are inaccessible to polio eradication personnel has been reduced from 60% in September 2015 to approximately 30% in December 2017. Implementation of the Reaching Every Settlement and Reaching Inaccessible Children strategies has helped reach some of the children living in areas inaccessible to house-to-house vaccination teams, and at least five contacts with children eligible for immunization in these areas are planned. Children reached by these initiatives need to be tracked to ensure receipt of the multiple OPV doses needed to complete the immunization series. Increased involvement of the military in implementing Reaching Every Settlement and Reaching Inaccessible Children strategies is planned in 2018 to reach as many children as possible in inaccessible areas. The low OPV3 coverage among children aged 12–23 months in the 2016–2017 national vaccination survey reflects persistently poor delivery of routine immunization services, particularly in states in northeast and northwest Nigeria ( 10 ). A National Emergency Routine Immunization Coordinating Center has been commissioned to identify and implement strategies to increase vaccination coverage, starting in the poorest performing states. Understanding reasons for the persistently low coverage in the northeast and northwest areas despite years of investment is a major focus in planning remedial activities. Surveillance activities have been strengthened since the last reported WPV case in Nigeria in September 2016, including expanding the number of environmental surveillance sites and increasing the number of surveillance community informants who reside in areas with limited access for polio program personnel in the states of Borno and Yobe to alert the program of potential AFP cases. Although national surveillance performance indicators are high, there are concerns about ongoing undetected poliovirus circulation in inaccessible areas; ongoing undetected poliovirus circulation is also possible in some accessible areas of Borno and other states where concerns about case investigation quality were identified. Efforts to address the impediments created by insecurity and geographic access limitations continue to be implemented and expanded. Searching for recent AFP cases in security-compromised areas is one objective of the Reaching Every Settlement and Reaching Inaccessible Children initiatives. A commitment to strengthening routine and supplementary immunization coverage in all areas of the country is needed, as are efforts to ensure high quality surveillance. Summary What is already known about this topic? In August 2015, the World Health Organization removed Nigeria from the list of polio-endemic countries because of the high likelihood that endemic wild poliovirus (WPV) circulation had been interrupted in Nigeria. However, during August and September 2016, four WPV cases were reported in Borno State, a northeastern Nigerian state experiencing protracted insurgency. What is added by this report? No WPV cases have been reported since September 2016. New strategies implemented by the Nigeria polio program have helped improve polio eradication activities, including those in areas with security challenges. However, approximately 28%–45% of eligible children living in the inaccessible areas have not been vaccinated, and surveillance has not been feasible in insurgent-controlled areas of Borno State. What are the implications for public health practice? Although access to communities for polio eradication activities continues to improve, approximately 30% of subdistrict level communities in Borno State remain inaccessible because of insurgency-related insecurity. Sustained efforts are needed to optimize surveillance and improve immunization coverage, especially among children in inaccessible areas.
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                Author and article information

                Journal
                MMWR Morb Mortal Wkly Rep
                MMWR Morb. Mortal. Wkly. Rep
                WR
                Morbidity and Mortality Weekly Report
                Centers for Disease Control and Prevention
                0149-2195
                1545-861X
                05 April 2019
                05 April 2019
                : 68
                : 13
                : 312-318
                Affiliations
                Global Immunization Division, CDC; Polio Eradication Department, World Health Organization, Geneva, Switzerland; Division of Viral Diseases, CDC.
                Author notes
                Corresponding author: Jaymin C. Patel, isr0@ 123456cdc.gov , 404-718-5539.
                Article
                mm6813a4
                10.15585/mmwr.mm6813a4
                6611474
                30946737
                b7d9d7fd-0d30-4252-871c-68e1bb383550

                All material in the MMWR Series is in the public domain and may be used and reprinted without permission; citation as to source, however, is appreciated.

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