Stool screening of Syrian refugees and asylum seekers in Germany, 2013/2014: Identification of Sabin like polioviruses

https://doi.org/10.1016/j.ijmm.2015.08.008Get rights and content

Abstract

Germany is a partner of the Global Polio Eradication Initiative. Assurance of polio free status is based on enterovirus surveillance, which focuses on patients with signs of acute flaccid paralysis or aseptic meningitis/encephalitis, representing the key symptoms of poliovirus infection. In response to the wild poliovirus outbreak in Syria 2013 and high number of refugees coming from Syria to Germany, stool samples from 629 Syrian refugees/asylum seekers aged <3 years were screened for wild poliovirus between November 2013 and April 2014. Ninety-three samples (14.8%) were positive in an enterovirus specific PCR. Of these, 12 contained Sabin-like polioviruses. The remaining 81 samples were characterized as non-polio enteroviruses representing several members of groups A–C as well as rhinovirus. Wild-type poliovirus was not detected via stool screening involving molecular and virological methods, indicating a very low risk for the importation by Syrian refugees and asylum seekers at that time.

Introduction

Human enteroviruses (EV) belong to the Picornaviridae family and constitute a large genus of viruses containing more than 110 different types that can be classified into four species (EV-A, -B, -C, and -D). Three species of rhinoviruses have also been included recently into this genus (Knowles et al., 2012). EV are small non-segmented viruses with a positive-strand RNA genome of about 7500 kb, surrounded by an icosahedral capsid composed of VP1–VP4 proteins (Wimmer et al., 1993).

Enteroviruses can cause a wide spectrum of acute diseases, ranging from mild fever and respiratory illness to severe neurologic diseases with involvement of central nervous system such as aseptic meningitis and poliomyelitis (Melnick, 1983). The latter is a severe, but vaccine-preventable disease that is caused by polioviruses (PV) types 1–3 which are members of EV-C species (Minor, 2014).

Only 0.1–1% of polio infections result in acute flaccid paralysis (AFP) of the limbs. Person-to-person spread of PV via the faecal–oral route is the most important way of transmission, although the oral–oral route may account for some cases. The virus can be shed in the stool from three to six weeks (Melnick, 1996). Persons with primary immune deficiencies can excrete the virus for several months and even years (Burns et al., 2014), leading to accumulation of mutations characteristic for wild type virus genotype.

Worldwide concerted efforts under the leadership of the World Health Organization (WHO) and its partners have been successful in reducing the incidence of poliomyelitis which is now targeted for global eradication by the year 2018 (Dowdle and Birmingham, 1997, Global Polio Eradication Initiative, 2014). The transmission of wild-type polioviruses (WPV) has been interrupted in four of the six WHO regions and now more than 80% of the world's population lives in certified polio-free regions. There are only three countries with endemic WPV circulation left, namely Pakistan, Afghanistan and Nigeria (http://www.polioeradication.org/).

As humans are the only reservoir for PV, travel between polio-free countries and those where WPV circulates will largely determine the risk of the virus being re-imported.

Although the WHO European region was officially declared polio-free in 2002, importations of WPV have occurred and resulted in an outbreak as recently as 2010 in Tajikistan (Yakovenko et al., 2014) or a silent circulation with detection in sewage in 2013–2014 in Israel (Manor et al., 2014).

The lowest number of global polio cases ever reported was in 2012 with 223 confirmed cases. In 2013, this number increased to 416. To protect the overall global progress, WHO declared WPV spread as a Public Health Emergency of International Concern under the International Health Regulations. The rationale was the observation that in 2013 about 60% of polio cases were the result of international spread of WPV. Even during the low-transmission season for polio, the virus has been exported to three countries in three major epidemiological zones: in central Asia (from Pakistan to Afghanistan), in Central Africa (Cameroon to Equatorial Guinea) and in the Middle East (Syria to Iraq).

After being polio-free since 1999, a polio outbreak with 36 confirmed cases occurred in Syria from October 2013 to January 2014. WPV type 1 originating from Pakistan was found in all stool samples investigated (Aylward and Alwan, 2014). Because of the civil war in Syria, the vaccination has been discontinued since 2011 and the officially reported polio vaccination coverage decreased from 99% in 2010 to 68% in 2012 (http://www.who.int/immunization/monitoring_surveillance/data/syr.pdf). This puts children born after 2010 at the highest risk of acquiring polio or transmitting WPV.

In 2012, Syrians became the single largest group of persons granted protection status in the European Union. More than 70% were recorded in only two Member States: Germany and Sweden. In 2013, 11.851 asylum applicants from Syria were registered in Germany with increasing number in 2014 (http://www.bamf.de/SharedDocs/Anlagen/DE/Publikationen/Broschueren/bundesamt-in-zahlen-2013.pdf?__blob=publicationFile).

Due to the WPV outbreak in Syria and high number of refugees coming from Syria, Robert Koch Institute (RKI) as the national public health institute in Germany re-emphasized the necessity of polio vaccination using inactivated polio vaccine (IPV) for all residents and staff of asylum seeker reception centres and shelters. Additionally, after consultation with the National Certification Committee (NCC), mandatory testing of stool samples of asymptomatic Syrian refugees and asylum seekers aged less than three years was recommended. The aim of this study was to evaluate the absence of WPV. Timely identification of poliovirus transmission is critical to the control of polio. Every single clinical case of polio in a polio-free area must be addressed to prevent further cases.

The screening of stool samples for EV/PV as well as characterization of EV-positive samples and the intratypic differentiation (ITD) of all PV was performed by the National/WHO Regional Reference Laboratory for Poliomyelitis and Enteroviruses (NL/RRL) at RKI. In addition, three labs of the German EV-laboratory network also performed primary testing of stool samples using molecular assays as well as cultivation on different cell lines. The German EV-network was established for continuous monitoring the polio-free status of Germany, performed by investigation of stool samples from patients with viral meningitis or encephalitis as well as AFP.

Section snippets

Samples

During a period of six months (November 2013–April 2014) 629 stool samples from Syrian refugees and asylum seekers were screened for EV by molecular and virological methods. Samples tested positive in the EV-network labs (Hanover, Stuttgart, Oberschleissheim) were sent to the NL/RRL for further differentiation. Overall, 414 samples were analyzed at the NL/RRL. Data requested included name, date of birth, date of arrival in Germany, travel history, polio vaccination history and health status.

Results

Within one week after announcement of RKI recommendation to public health authorities, first samples arrived at RKI for stool screening (see Fig. 4). Overall, 629 stool samples were sent in by 118 asylum seeker reception centres or shelters (RC/S) and public health departments and tested for presence of EV in four participating labs out of the EV network: NL/RRL (n = 358), NLGA Hanover (n = 76), LGL Oberschleissheim (n = 111) and LGA Stuttgart (n = 84). Age distribution was as follows: 445 children

Discussion

Germany is a partner of the Global Polioeradication Initiative. Assurance of polio free status is based on enterovirus (EV) surveillance, which focuses on patients with signs of acute flaccid paralysis or aseptic meningitis/encephalitis, representing the key symptoms of poliovirus infection. Since declaration of Polio-free status of WHO region EURO in 2002, criteria for AFP surveillance are hard to fulfil by many European countries (Khetsuriani et al., 2014).

In response to the wild poliovirus

Acknowledgement

We thank all local health authorities as well as staff of asylum seeker reception centres and shelters for organization and collection of stool samples. We also thank technical staff of all four contributing labs for excellent technical assistance.

References (30)

  • S. Diedrich et al.

    The German Health Interview and Examination Survey for Children and Adolescents (KiGGS): state of immunity against poliomyelitis in German children

    Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz

    (2007)
  • W.R. Dowdle et al.

    The biologic principles of poliovirus eradication

    J. Infect. Dis.

    (1997)
  • ECDC-RRA12/2013....
  • Global Polio Eradication Initiative

    10th meeting of the Independent Monitoring Board

    Wkly. Epidemiol. Rec.

    (2014)
  • M.Y. Hindiyeh et al.

    Development and validation of a real time quantitative reverse transcription-polymerase chain reaction (qRT-PCR) assay for investigation of wild poliovirus type 1-South Asian (SOAS) strain reintroduced into Israel, 2013 to 2014

    Euro Surveill.

    (2014)
  • Cited by (23)

    • Infectious disease profiles of Syrian and Eritrean migrants presenting in Europe: A systematic review

      2018, Travel Medicine and Infectious Disease
      Citation Excerpt :

      Some studies detected enteroviruses in Syrian refugees, some of these cases with the evidence of the poliovirus (PV). Intratypic differentation of PV revealed Sabin-like Poliovirus, indicating a recent oral polio vaccination or contact to a OPV vaccinee; wild-type Poliovirus was not detected [32–35]. A seroprevalence study showed high seroprevalence against all three PV types, similar to the population living in Germany [33].

    View all citing articles on Scopus
    View full text