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MOLECULAR EPIDEMIOLOGY OF SILENT INTRODUCTION AND SUSTAINED TRANSMISSION OF WILD POLIOVIRUS TYPE 1, ISRAEL, 2013

Friday, 21st of February 2014

MOLECULAR EPIDEMIOLOGY OF SILENT INTRODUCTION AND SUSTAINED TRANSMISSION OF WILD POLIOVIRUS TYPE 1, ISRAEL, 2013

Eurosurveillance, Volume 19, Issue 7, 20 February 2014

Research articles

L M Shulman ()^1,2,3, E Gavrilin^3,4, J Jorba^3,5, J Martin^3,6, C C Burns^3,5, Y Manor¹, J Moran-Gilad^7,8, D Sofer¹, M Y Hindiyeh¹, R Gamzu^2,7, E Mendelson^1,2, I Grotto^7,9, for the Genotype - Phenotype Identification (GPI) group¹⁰

1. Public Health Services, Israel Ministry of Health, Central Virology Laboratory (CVL), Sheba Medical Center, Tel Hashomer, Israel
2. School of Public Health, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
3. These authors contributed equally to the manuscript
4. World Health Organization Regional Office for Europe, Regional Polio Laboratory Network, Copenhagen, Denmark
5. Polio and Picornavirus Laboratory Branch, Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, GA, United States
6. Division of Virology, National Institute for Biological Standards and Control, South Mimms, Potters Bar, United Kingdom
7. Israel Ministry of Health, Jerusalem, Israel
8. European Society of Clinical Microbiology and Infectious Diseases ESCMID Study Group for Molecular Diagnostics (ESGMD)
9. Department of Public Health, Faculty of Health Sciences, Ben Gurion University of the Negev, Beer Sheva, Israel
10. Members of the group are listed at the end of the article

Abstract and introduction below; full text, with figures, is at http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20709

Citation style for this article: Shulman LM, Gavrilin E, Jorba J, Martin J, Burns CC, Manor Y, Moran-Gilad J, Sofer D, Hindiyeh MY, Gamzu R, Mendelson E, Grotto I, for the Genotype - Phenotype Identification (GPI) group. Molecular epidemiology of silent introduction and sustained transmission of wild poliovirus type 1, Israel, 2013. Euro Surveill. 2014;19(7):pii=20709. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20709 
Date of submission: 10 January 2014

Poliovirus vaccine coverage in Israel is over 90%. The last nine birth cohorts have been vaccinated exclusively with inactivated polio vaccine (IPV). However, between February and July 2013 type 1 wild poliovirus (WPV1) was detected persistently in 10 and intermittently in 8 of 47 environmental surveillance sites in southern and central Israel and in 30 stool samples collected during July from healthy individuals in southern Israel. We report results of sequence and phylogenetic analyses of genes encoding capsid proteins to determine the source and transmission mode of the virus. WPV1 capsid protein 1 nucleotide sequences were most closely related to South Asia (SOAS) cluster R3A polioviruses circulating in Pakistan in 2012 and isolated from Egyptian sewage in December 2012. There was no noticeable geographical clustering within WPV1-positive sites. Uniform codon usage among isolates from Pakistan, Egypt and Israel showed no signs of optimisation or deoptimisation. Bayesian phylogenetic time clock analysis of the entire capsid coding region (2,643 nt) with a 1.1% evolutionary rate indicated that Israeli and Egyptian WPV1-SOAS lineages diverged in September 2012, while Israeli isolates split into two sub-branches after January 2013. This suggests one or more introduction events into Israel with subsequent silent circulation despite high population immunity.

Introduction

Two major lineages of type 1 wild poliovirus (WPV1) are currently circulating in endemic countries: the South Asia (SOAS) lineage in Pakistan and Afghanistan, and a West African lineage (WEAFB1 and WEAFB2) in Nigeria [1]. Both of these lineages occasionally spread to other countries with a high percentage of non-immunised children and have caused cases of acute flaccid paralysis (AFP) [2]. Individuals in populations with high vaccination coverage are generally protected from disease [3,4]. In such countries, detection of poliovirus importation, subsequent transmission and interruption of chains of transmission requires a high level of integration of multiple surveillance strategies performed in parallel over extended periods of time to increase reliability and strengthen interpretation of data [5].

The World Health Organization (WHO) European Region, which includes Israel, was declared poliovirus-free on 21 June 2002 [6]. Afterwards, there was only a single importation of WPV1 to the region – into Tajikistan in April 2010 from a reservoir in India. This introduction resulted in a local outbreak of poliomyelitis that subsequently spread to central Asia and Russia [7].

The last cases of poliomyelitis in Israel occurred during an outbreak in 1987–88 [8,9]. Israel has been free of poliomyelitis since 1989, as a consequence of high immunisation coverage [9,10]. Between 1990 and 2005, infants in Israel received three doses of enhanced inactivated polio vaccine (eIPV) and three doses of live-trivalent attenuated oral polio vaccine (OPV) by the age of 15 months [11], followed by an OPV booster at age five to six years (first grade of school). After 2005, the routine immunisation schedule was changed, consisting of four eIPV doses by 15 months and an eIPV booster at age five to six years. Vaccination coverage since 1990 has ranged between 92% and 95% and within individual health districts from 81% to 100% (Emelia Anis, Epidemiology Division, Israel Ministry of Health, personal communication, 31 December 2013).

Classical AFP surveillance [12] and routine monthly environmental (sewage) surveillance in catchment areas covering 30–40% of the entire population [13,14] performed routinely since 1989 revealed silent importation of WPV1 into Ashdod, Israel, in 1996 and routine surveillance samples  supplied by the Palestinian Ministry of Health, in 1994–96, 1999 and 2002, revealed repeated introductions of WPV1 into nearby Gaza [5,10].

In May 2013, a virus isolated from a sewage sample collected on 19 April from Rahat, Israel, was identified as WPV1 [15,16]. A sensitive quantitative reverse transcription polymerase chain reaction (qRT-PCR) assay [17] was used for retrospective and prospective screening of sewage. A sample collected from Beer Sheva in February 2013 was the earliest to contain WPV1. In June 2013, the frequency of sampling and the number of environmental surveillance sites was expanded to 80 (from fewer than 15), especially in catchment areas in southern Israel near sites that were found to be positive for WPV1 [15,16]. Between February and July 2013, a total of 10 sites in south and central Israel were persistently positive for WPV1. In addition, WPV1 was found intermittently in an additional eight sites out of 47 environmental surveillance sites in southern and central Israel and in some stool suspensions from stool samples collected in July 2013 in southern Israel from healthy individuals (data not shown).

The first response to these findings targeted completing immunisation with IPV of all children in the southern districts, raising full coverage from 90% to above 99%. This was followed, from 8 August 2013 onwards, by one round of supplementary immunisation with bivalent OPV (types 1 and 3) targeting all children up to the age of nine years, i.e. those previously immunised exclusively with IPV. As of 15 September 2013, approximately 750,000 of about 1,200,000 children eligible for bivalent OPV (63%, interhealth district range: 45–83%) had been vaccinated nationwide [12].

Here we report on the genotype of WPV1 isolated between February and July of 2013 and its ability to circulate in the highly immunised population of Israel, and assess the possible impact of such isolates on polio eradication in Israel and other countries using an IPV-only vaccination programme. To the best of our knowledge, this is the first in-depth molecular analysis of a wild poliovirus responsible for introduction and sustained silent circulation in a highly vaccinated population.