• FluTrackers.com Inc. does not provide medical advice. Information on this web site is collected from various internet resources, and the FluTrackers board of directors makes no warranty to the safety, efficacy, correctness or completeness of the information posted on this site by any author or poster. The information collated here is for instructional and/or discussion purposes only and is NOT intended to diagnose or treat any disease, illness, or other medical condition. Every individual reader or poster should seek advice from their personal physician/healthcare practitioner before considering or using any interventions that are discussed on this website. By continuing to access this website you agree to consult your personal physican before using any interventions posted on this website, and you agree to hold harmless FluTrackers.com Inc., the board of directors, the members, and all authors and posters for any effects from use of any medication, supplement, vitamin or other substance, device, intervention, etc. mentioned in posts on this website, or other internet venues referenced in posts on this website.
  • We are not asking for any donations. Do not donate to any entity who says they are raising funds for us.

Wild-type poliovirus 1 transmission in Israel ? what is the risk to Europe? (ECDC, September 26 2013, extracts)

Giuseppe

Emeritus
[Source: European Centre for Disease Prevention and Control (ECDC), full PDF document: (LINK). Extracts.]


RISK ASSESSMENT

Wild-type poliovirus 1 transmission in Israel ? what is the risk to Europe?

__

Suggested citation: European Centre for Disease Prevention and Control. Wild-type poliovirus 1 transmission in Israel ? what is the risk to Europe? Stockholm: ECDC; 2013.

Stockholm, September 2013 ? European Centre for Disease Prevention and Control, 2013. Reproduction is authorised, provided the source is acknowledged.
____


Executive summary

The EU/EEA countries and the rest of the WHO European Region, have been officially polio-free since 2002. Wild-type polio virus 1 (WPV1) has been isolated in sewage and in the faeces of asymptomatic carriers in Israel since February 2013. An assessment has been made of the potential impact of this public health event on the risk of poliovirus importation and re-established circulation in EU/EEA.

Three populations have been evaluated for the risk of infection with WPV (asymptomatic infection and shedding of virus) and the risk of clinical disease (paralytic poliomyelitis) in the EU: cohorts vaccinated with OPV; cohorts vaccinated exclusively with IPV-containing vaccines and population groups with low vaccination coverage, including people for whom the vaccine has failed or who have waning immunity.


Risk assessment

Based on the evidence, there is a risk of importation and re-establishment of WPV into the EU via a recently infected person shedding the virus, if we consider the significant population flow from and to countries where WPV is still circulating, as well as the sub-optimal potential for early detection of the virus in both the environment and the population.

The overall threat posed by poliovirus re-establishment can be considered to be very low in OPV vaccinees for both poliovirus infection and disease; moderate in IPV-only cohorts for poliovirus infection and low for disease; and high in low or unvaccinated groups for poliovirus infection and moderate for disease.

The highest level of risk is posed by the proximity of clustered un- or under-immunised population groups to large populations vaccinated using IPV-only schemes. Sub-optimal hygiene and crowded living conditions may also play a role in facilitating the spread of infection.


Summary of recommendations

Thorough assessment of polio vaccination uptake (in the general population and specific sub-groups), and strengthening of surveillance and laboratory capacity, should be a high priority.

Environmental surveillance, enterovirus surveillance and other types of supplementary surveillance should be strengthened, and EU-level standards and performance indicators should be agreed.

EU/EEA Member States should recommend that all travellers to areas where WPV circulates have an up-to-date polio vaccination status.

Operational and contingency plans are needed in the EU/EEA to mobilise polio vaccine stockpiles in case of evidence of WPV transmission. The availability of poliovirus vaccines for use in the context of an outbreak should be assessed.


Source and date of request

Internal ECDC request ? 20 August 20131


Public health issue

Wild-type polio virus 1 (WPV1) has been isolated from sewage water and subsequently in faeces from asymptomatic cases in Israel since February 2013. We need to ascertain the impact of this public health event on:
  • the risk of wild-type poliovirus importation into the EU
  • the risk of re-establishment of wild-type poliovirus circulation in the EU, and
  • the risk of paralytic poliomyelitis in the EU.
In addition, we need to determine the capacity of the polio surveillance systems in the EU/EEA Member States for detecting wild-type poliovirus transmission in a timely manner, and their ability to respond effectively to outbreaks.


Consulted experts

ECDC internal response team

ECDC staff (in alphabetical order):

Elizabeth Bancroft; Arnold Bosman; Paloma Carrillo-Santisteve; Denis Coulombier; Ida Czumbel; Niklas Danielsson; Tarik Derrough; Isabelle Devaux; Ana-Belen Escriva; Johan Giesecke; Emma Huitric; Romit Jain; Kari Johansen; Verena Kessler; Piotr Kramarz; Peter Kreidl; Pierluigi Lopalco; Irene Mu?oz; Daniel Palm; Lucia Pastore Celentano; Pasi Penttinen; Emmanuel Robesyn; Marybelle Stryk; Therese Westrell.

External experts

The following individuals provided information and comments:

Donato Greco; Darina O?Flanagan; David Salisbury; Hanna Nohynek; Tapani Hovi; Anton van Loon.
__

ECDC acknowledges the valuable contributions from the above-mentioned experts and institutions. All external experts have made declarations of interest. It should be noted that while these experts have made comments on the draft text of this document, the final decisions on the content of the risk assessment were made by ECDC?s inhouse experts. ECDC would also like to acknowledge the valuable contribution of the European Medicines Agency (EMA) , WHO Regional Office for Europe, European Food Safety Authority and the Ministry of Health for Israel.


Event background information

Wild-type poliovirus 1(WPV1) was first isolated from sewage samples collected on 9 April 2013 in Rahat, southern Israel. The isolated strain is related to strains circulating in Pakistan and to the strain detected in sewage in Cairo in December 2012. It is unrelated to the strain currently affecting the Horn of Africa. WPV1 has been detected in a total of 91 sewage samples from 27 sampling sites in southern and central Israel, collected from 3 February to 25 August 2013 [1]. In addition, WPV1 has been isolated in stool samples from 42 people (4.4% of the sampled population) tested in the area [2]. Detailed information about the carriers is missing but all the 42 cases are reported to have been vaccinated with IPV-only schedules, according to Israeli national recommendations (personal communication). Three positive samples were collected from the West Bank and Gaza on 20 August 2013. No cases of paralytic poliomyelitis have been reported. This event is significant as it is the first record of widespread wild polio virus circulation with, to date, no identified cases of clinical disease.

Israel implemented a combined IPV + OPV immunisation schedule from 1990 to 2004 and switched to universal IPV-only vaccination in 2005 [3].
The primary series of IPV is given at two, four, six, and 12 months of age and a booster dose is given at seven years. The country has been free of indigenous WPV transmission since 1988 when an outbreak of WPV1 in the Hadera district resulted in 15 cases of paralytic poliomyelitis [4]. Wild-type poliovirus has occasionally been detected in environmental samples collected between 1991 and 2002, without the occurrence of paralytic poliomyelitis cases or evidence of sustained transmission. Environmental surveillance samples from Gaza and the West Bank have consistently tested negative for WPV1 from 2002 until the recent isolations.

Supplementary immunisation activities (SIA) with bivalent oral polio vaccine type 1 and 3 started on 5 August in parts of southern Israel and escalated to a nationwide campaign targeting all children below 10 years of age from 18 August 2013 [5]. To date 800,000 of the potential 1.3 million (ages 0-9) are reported to have been vaccinated in the campaign (personal communication). The objective of the OPV SIA is to rapidly boost mucosal immunity in OPV-na?ve children vaccinated with IPV in an attempt to interrupt virus circulation.


ECDC threat assessment for the EU

In order to assess the overall threat posed by poliovirus importation and re-establishment in the EU/EEA, the following risks were assessed:
  • risk of poliovirus infection and disease according to the immunisation status of the EU/EEA population;
  • likelihood of poliovirus importation and re-establishment to the EU/EEA;
  • impact on public health in the event of WPV re-establishment in the EU/EEA; and
  • availability of operational plans including OPV availability in EU/EEA.
More information on the methods applied and a detailed description of the evidence collected and considered in the risk assessment are available in the annexes and in the ?Supporting evidence? section.


Risk of poliovirus infection and disease according to the immunisation status of the population

Susceptibility of the EU/ EEA population to poliovirus

Based on the evidence presented in the Supporting evidence section, the following populations have been evaluated for the risk of infection with WPV (carriage and shedding) and clinical disease:
  • Populations vaccinated with OPV;
  • Cohorts of the EU population only vaccinated with IPV-containing vaccines;
  • Low- or unvaccinated population groups in the EU including those for whom vaccine has failed and those with waning immunity.
Given that countries have different vaccination programme histories, the three population groups considered vary in size. To assess the situation at the Member State level, the following parameters need to be taken into account:
  • Year of initiation of the polio vaccination programme;
  • Historical use of OPV and IPV;
  • Historical vaccination coverage by birth cohort;
  • Current vaccine coverage at national and sub-national level.
In addition, possible pockets of unvaccinated populations (clustering) should be taken into account.
____

Box 1. Risk of poliovirus infection and disease according to the immunisation status of the population

As presented in Table 1, the following evaluation assesses the risk of the three populations becoming infected and shedding virus or developing disease, if exposed to the WPV.
  • OPV vaccinated are not at risk of getting infected and shedding the virus, or developing the disease.
  • Cohorts of the EU population only vaccinated with IPV-containing vaccines are at risk of getting infected and shedding the virus (see Supporting documentation on population susceptibility and identification of potential risk groups in the EU/EEA). Moreover, the recent findings in Israel confirm that IPV recipients can carry and sustain the circulation of polio virus in the population. The risk of developing disease is the same as for those vaccinated with OPV.
  • Low- or unvaccinated population groups, including those for whom the vaccine has failed and those with waning immunity, may carry and shed the virus and be at increased risk of developing the disease.
The evidence that IPV-vaccinated individuals can become re-infected and shed the virus comes from studies where vaccinated people have been given a challenge dose of OPV vaccine. The main limitation to such OPV challenge studies is that natural exposure to polioviruses may involve different amounts of ingested virus (generally lower) and different media (e.g. contaminated food and water or aerosol droplets). Moreover there is limited knowledge on OPV and IPV vaccines and waning immunity.


Table 1. Probability of infection and/or disease in the three population groups

[Population groups at risk by immunisation status - Probability of infection - Probability of disease]
  • OPV vaccinees ? Very low - Very low
  • IPV-only cohorts ? Moderate - Very low
  • Low- or unvaccinated groups ? High ? Moderate
____


Likelihood of poliovirus importation and re-establishment into the EU/EEA

Potential routes of importation from countries where WPV is still circulating

Because humans are the only reservoir for polioviruses, travel and migration patterns between the EU/EEA and countries in which WPV circulates will largely determine the risk of the virus being imported into the EU/EEA.

Europe has continuously been at risk since it was declared polio-free in 2002.

Countries where WPVs are currently circulating can be grouped into:
  • Countries with endemic transmission: Nigeria, Pakistan and Afghanistan
  • Countries with recently re-established transmission and paralytic disease: Somalia, Kenya and Ethiopia
  • Countries with evidence of transmission but no disease: Israel.
Based on national statistics, 1 778 437 migrants from the six countries with reported polio outbreaks and Israel were living in the EU/EEA in 2010. The countries with the largest expatriate populations were the UK, Germany, Italy, Spain and the Netherlands [6].

Migration for permanent settlement to the UK was at its highest level in 2010, with an estimated 951 191 migrants from the countries in question living in the UK at the time. The largest groups originated from Pakistan (451 712), Kenya (152 999), Nigeria (150 918) and Somalia (110 326).

In Germany, there were 202 638 migrants from polio-affected countries in 2010, the largest groups originating from Afghanistan (79 444), Pakistan (46 253), Nigeria (22 987) and Ethiopia (21 085).

In Italy, the resident population from the countries in question was 148 416 in 2010, the largest groups originating from Pakistan (64 161), Nigeria (52 845), Ethiopia (17 226) and Somalia (8 110).

In 2010, the resident population from the countries in question in Spain was 99 982, the largest groups originating from Pakistan (54 576), Nigeria (38 775) and Israel (2 972).

The resident population from the countries in question in the Netherlands in 2010 was 76 713, the largest groups originating from Afghanistan (30 986), Somalia (13 521), Pakistan (11 113) and Ethiopia (8 144).

Israel is a popular destination for EU travellers and vice versa, and the circulation of WPV1 in Israel is likely to have increased the risk of WPV importation into the EU.


Previous experience and evidence of poliovirus circulation in the EU/ EEA

In the recent past, poliovirus, both vaccine-derived (VDPV) and wild (WPV), have been detected in sewage and stool samples in various EU/EEA countries (see Supporting documentation on the situation in Europe). The last outbreak in the EU/EEA was in 1992 in the Netherlands, in a religious community opposed to vaccinations. This WPV3 outbreak resulted in two deaths and 71 cases of paralysis. All cases were unvaccinated and there was limited spread of polioviruses outside of the religious community [7].

Another smaller outbreak occurred in Finland 1984 with ten individuals developing clinical disease due to WPV3 and at least 100 000 people estimated to have been poliovirus excretors. The virus was identified in both faecal samples of healthy, fully IPV vaccinated excretors from Finland (adults and children), and in sewage water collected in fourteen cities geographically spread throughout the country [8,9]. However, both the Netherlands and Finland have used inactivated poliovirus vaccine produced by different manufacturers for the elimination of poliomyelitis in their respective countries. The Netherlands used IPV vaccine produced in-country from 1957 and Finland used IPV vaccine manufactured by RIT in Belgium from 1960 to 1985, when they changed to the more potent IPV vaccine produced in the Netherlands.

Based on the latest surveillance data, the European Regional Certification Commission for Poliomyelitis Eradication (RCC) recently concluded that evidence suggests there was no circulation of WPV and VDPV in the European Region in 2012, confirming the polio-free status [10].


Likelihood of detecting circulating poliovirus in the EU/ EEA

Poliovirus may be released into the environment through urban sewage (including sewage from healthcare facilities) in areas where poliovirus is shed. Depending on the initial virus concentration and the type of wastewater treatment applied, the probability of finding infectious virus particles in the effluent varies [11-13]. However, once released into the environment, poliovirus is able to survive well in soil or on crops [13-15].

The potential risk of transmission to humans occurs at critical points in the water cycle, depending on the possible usage of treated wastewater.

Scenarios for potential transmission across the water cycle are displayed in Table 6. Poliovirus detection in Europe and Israel (2002?2013) [42] (under Supporting documentation on poliovirus circulation in the environment). According to EU legislation on water quality, it is not necessary to monitor for poliovirus or Enteroviruses, either in relation to the discharge of wastewater in the environment after treatment, bathing water, or drinking water [16-18]. In areas with potential exposure, such as Israel, environmental surveillance of wild poliovirus can be essential to prevent re-transmission to humans. If such environmental surveillance systems were to be set up in European countries, they would need to target specific populations/areas/practices.

Surveillance programmes for polio in non-endemic or polio-free regions, such as the EU/EEA, are important to detect re-introduction of the virus, prevent further spread of the virus, and prevent new cases of paralytic disease.

Regional certification of polio-free status only occurs when all Member States demonstrate the absence of WPV transmission for three consecutive years with agreed performance targets [19]. In 2010?2011, 27 out of 29 EU/EEA countries had compulsory comprehensive reporting for polio cases [20]. However, since Europe has been a polio-free region since 2002, and no cases have been reported in the EU/EEA since 1998, other indicators are used to determine the sensitivity of surveillance for polio. The RCC uses several criteria to assess the performance of polio surveillance [10,21]. These include a health services criterion; the reported rate and completeness of investigation of acute flaccid paralysis cases; timeliness of AFP reporting and the use of supplemental surveillance (enterovirus and/or environmental sampling). The latter three criteria are discussed in Supporting documentation on surveillance systems for polioviruses in the EU/EEA countries.

There are many limitations on evaluating the surveillance of polio in the EU/EEA including; the heterogeneity of surveillance systems in terms of sensitivity, timeliness and completeness; the fact that numerous countries do not have a sensitive AFP surveillance system and the lack of supplementary surveillance systems (enterovirus and/or environmental) in some countries. Surveillance for AFP to identify polio cases is currently considered to be the ?gold standard? [22]. A total of 20 out of 30 EU/EEA Member States use AFP surveillance. However, as reported by WHO, only four of 20 EU/EEA Member States had a calculated AFP rate of > 1/100 000 persons in 2012 and only three had a calculated surveillance index of >0.8 (Latvia, Lithuania and Cyprus) [23]. In 2012 only seven of the countries reported data in a timely fashion more than 80% of the time [24].

Given the poor quality of AFP surveillance in the EU/EEA, the RCC has encouraged the use of supplementary surveillance [10]. The ten EU/EEA countries electing not to use AFP surveillance use supplementary surveillance for Enteroviruses, environmental samples (primarily sewage), or a combination to detect polio (other AFP surveillance countries may also use some combination of supplementary surveillance). In 2011, WHO European Regional Office determined that Denmark, Finland, France, Iceland, Luxembourg, Netherlands, Sweden, and the UK (all of which did not have AFP surveillance) had ?high quality? supplementary surveillance [24]. There are currently no standards to evaluate the supplemental surveillance used by the other 10 EU/EEA Member States for polio surveillance.

A minority of EU/EEA Member States currently use supplemental surveillance. From varying sources, there are at least six Member States using environmental surveillance and ten using enterovirus surveillance (see Table 8 under Supporting documentation on surveillance systems for polioviruses in the EU/EEA countries and personal communication WHO Regional Office for Europe).

Environmental surveillance can be an important tool for shortening the response time between awareness of a PV re-emergence event and response. It plays a critical role during the period between interruption of WPV transmission and certification of polio eradication. Ideally it should also continue to monitor for the emergence of VDPVs, re-emergence of WPVs, or disappearance of all OPV-related strains during the post-eradication and OPV cessation periods [25].

Based on the surveillance data and the reports submitted by Member States, the RCC concluded that the evidence gave no indication of WPV and VDPV circulation in the European Region in 2012 [10]. At the same time, however, RCC expressed increasing concern about the deteriorating quality of AFP surveillance in the European Region and the lack of reports from several Member States [26]. The RCC called upon Member States to improve surveillance for polio. Improving adherence to standard methods of surveillance is critical while developing new, more sensitive methods of surveillance for polio.

In response to the Global Polio Eradication Initiative in 1988, WHO initiated a global laboratory network to support surveillance activities in polio endemic and non-endemic regions. As of 2013, 145 laboratories participate as accredited members of the Global Polio Laboratory Network (GPLN) [27]. The network is coordinated by WHO and through standardised methodology has the primary task of supporting the detection of poliovirus in AFP screening specimens as well as in environmental samples.

Based on the above considerations (potential routes of importation; previous experience and likelihood of detecting circulating poliovirus), there is a likelihood that poliovirus may be imported and re-established in the EU/EEA. Furthermore, based on the limited evidence collected on existing surveillance systems, there is a risk that poliovirus circulation will go undetected if it is imported.


Impact assessment on public health in the event of WPV reestablishment

The following assessment estimates the public health impact in the event that WPV is re-introduced into the EU Member States, depending on the immunity status of the population. The elements considered in the algorithm are: immunisation status of the population (OPV vaccinees, IPV-only cohorts, and low- or unvaccinated groups); vaccination coverage; modes of transmission (oral-oral; faecal-oral); type of immunity induced by OPV vaccines versus IPV vaccines; severity of the disease; ratio of inapparent infection to clinically recognised polio infection and availability of operational plans.


Immunity to polioviruses in EU/ EAA populations

Assessing immunity to polioviruses in EU/EEA populations is complex and dependent on a variety of factors such as genetics, previous environmental exposure to one or several wild-type or vaccine-type polioviruses, previous exposure to other Enteroviruses, type/s of vaccine offered throughout life, number of doses and timing of earlier vaccinations and (in infants) presence of maternal antibodies. The current EU/EEA population is a mix of individuals born in an EU/EEA Member State or elsewhere. Wild-type viruses circulated widely in Europe and worldwide until the early 1960s and large populations living in the EU/EEA may therefore have been exposed to wildtype polioviruses (one or several serotypes) in Europe or elsewhere.


Poliovirus shedding in OPV & IPV recipients

Polio virus (PV) is highly contagious: infected individuals shed virus in faeces and from naso-pharyngeal mucosa. The mode of transmission is person-to-person, both via the faecal-oral and the oral-oral routes (the latter being most probable in developed countries with high hygiene standards). Poliovirus excreted through the faecal route may be identified in sewage water. The period of communicability lasts for as long as virus is excreted (also from asymptomatic persons).

Both IPV and OPV induce an immune response that protects individuals from disease, including paralytic poliomyelitis. A significant difference between the two vaccines is that the IPV induces weaker gut mucosal immunity compared to OPV. This means that IPV-vaccinated individuals are at higher risk of asymptomatic intestinal infection and shedding of virus than OPV-vaccinated individuals. IPV-vaccinated individuals are therefore more likely than OPV-vaccinated individuals to contribute to the circulation of poliovirus [28,29]. However, during the outbreak in the Netherlands in 1992 no poliovirus excretors were identified in healthy IPV-vaccinated (produced in the Netherlands) individuals [30]. No evaluation has been conducted comparing mucosal immunity and or excretion following different IPV vaccines. Therefore, although infection in individuals with prior immunity through vaccination does not lead to disease, prior immunisation with IPV may not protect individuals from the infection itself and may potentially play a role in poliovirus transmission (Supporting documentation on population susceptibility and identification of potential risk groups in the EU/EEA) [31].


Vaccination coverage in the EU/EEA

Vaccination coverage levels in the EU/EEA can be considered satisfactory as a whole (>90% for three doses of either IPV or OPV) and can largely justify the absence of WPV circulation in the region so far. However, in the EU/EEA there are significantly large pockets of population sub-groups that are under-immunised or not immunised at all. Moreover, a gradual accumulation of unvaccinated children (from 5% up to 20% every year in some EU countries) progressively increases the overall susceptible population. A rough estimate, based on officially reported vaccine coverage data indicates that in the EU/EEA population aged of 0?29 years, up to 12 million people are not vaccinated against polio (see Table 2). These calculations represent a two-year coverage period and may therefore over-estimate the number of people susceptible as they do not take into account late immunisation. According to historical changes in the polio vaccination programmes, a large proportion of the EU/EEA population can be considered OPV-na?ve. In fact, in most of the Nordic countries and the Netherlands, IPV has been used for the universal routine programme since polio vaccination was introduced (and OPV was only used when facing outbreak situations). Several EU countries adopted IPV-only vaccination in the 1990s and as of 2010, all EU/EEA2 countries had switched to IPV-only schedules for the primary vaccination series. Only one EU/EEA Member State, Poland, uses a mixed schedule and provides OPV as a booster dose. In the age group 0?29 years up to 70 million people have been vaccinated using an IPV-only schedule. This population represents a large potential reservoir for sustaining wild poliovirus circulation in the event of a re-introduction of polio into the environment. The highest risk of re-introduction and sustained circulation of WPV occurs where susceptible populations are clustered together with a large potential reservoir.

__

Table 2. Polio immunisation status in the age groups 0?29 years among the EU/EEA population (in millions). Estimate based on WHO/CISID vaccine coverage and Eurostat population data

[Age groups ? Unvaccinated - IPV-only ? OPV]
  • 0-9 - 2.3 - 43.7 - 7.1
  • 10-19 - 2.7 - 17.7 - 34.2
  • 20-29 - 6.5 - 7.4 - 51.0
  • Total 0?29 - 11.5 - 68.8 - 92.3
____

Box 2. Main conclusions from the impact algorithm

In the event of WPV being re-introduced, based on the evidence, the following conclusions can be drawn from the impact algorithm:
  • As OPV vaccinees are unlikely to become infected, the impact is considered to be very low;
  • Although IPV vaccinees are protected against disease, they are more likely to be susceptible to gut mucosal infection and therefore more likely than OPV vaccinees to contribute to the circulation of virus, even if they are unlikely to develop the disease. For these reasons the impact is considered to be low;
  • Unvaccinated individuals are at high risk of becoming infected and at moderate risk of developing the disease. However, the presence of control measures and operational plans in numerous EU/EEA Member States reduces the impact to moderate.
(...)
____


Operational plans including OPV availability in EU

The Global Polio Eradication Initiative Strategic Plan 2013?2018 [32] includes:
  • Strategic approaches to end all polio disease (wild and vaccine-related);
  • An urgent emphasis on improving immunisation systems in key areas;
  • The introduction of new, affordable inactivated polio vaccine;
  • Options for managing long-term poliovirus risks and potentially accelerating wild poliovirus eradication, risk mitigation strategies to address new threats, particularly insecurity in some endemic areas;
  • Contingency plans, should there be a delay in interrupting transmission in such reservoirs;
  • A specific timeline to complete the programmes and a legacy planning process to extrapolate lessons learned from the Global Polio Eradication Initiative and put in place the infrastructure to deliver other critical health and development resources and ultimately, complete the Global Polio Eradication Initiative programme.
The four main objectives of the new plan are:
  • Poliovirus detection and interruption (by 2014);
  • Strengthening of immunisation systems and the withdrawal of oral poliovirus vaccine (OPV) (by 2016);
  • Containment and certification (by 2018);
  • Legacy planning.
To map the current availability of IPV stockpiles in the event of an outbreak and the existence of outbreak control plans in EU/EEA Member States, the ECDC carried out a rapid inquiry through the EPIS-VPD platform. Of the fifteen responding Member States, five reported having IPV stockpiles, albeit limited, and 13 reported having an updated outbreak control plan for poliovirus outbreaks (see Table 5 and Table 10 in the section Supporting documentation on operational plans including OPV availability in the EU).

In order to assess the availability of and access to OPV outbreak control, EMA (the European Medicines Agency) and ECDC conducted a joint rapid survey through their official contact points in the EU/EEA Member States (see Table 5 and Table 10 under Supporting documentation for operational plans including OPV availability in the EU).

From the two surveys mentioned we can conclude that IPVs are authorised in all EU/EEA Member States and readily available for use in universal childhood vaccination programmes. Furthermore, trivalent oral polio vaccines (tOPV) are authorised in eight Member States but no country maintains OPV stockpiles for possible outbreak response. Poland uses OPV in its routine immunisation schedule as a booster dose at the age of six years after primary IPV vaccination during the first year of life and therefore only has limited OPV stocks for supplying the vaccination programme. Italy has authorised trivalent OPV, bivalent OPV (PV1 and 3), monovalent OPV (PV1) and monovalent (PV3) produced by Novartis, a supplier to UNICEF. However, although OPV vaccines have national marketing authorisation in Italy (according to Dir. 2001/838/EC), the products are not available on the market as they are not part of the current national immunisation schedule. All countries that responded to the survey plan to use IPV as their first choice for outbreak control.
In the event of extensive transmission not being controlled by IPV vaccination, the use of monovalent OPV (mOPV) is considered to be the standard response to an outbreak, according to WHO guidance [33].

However, mOPV is currently not available on the EU market, and would therefore have to be used as an unlicensed product or licensed by means of an emergency procedure to rapidly authorise the use of a non-licensed OPV vaccine in response to an outbreak.

The experience from Finland in 1984 and from the current situation in Israel suggest that OPV may be necessary to clear the transmission of polioviruses in the respective populations. In addition, the impact of IPV vaccines in an outbreak setting needs to be further explored since there appear to be countries where no WPV transmission into the vaccinated populations has been observed (e.g. the Netherlands).


Threat posed by poliovirus re-establishment in the EU/EEA

The threat posed by poliovirus importation and re-establishment in the EU/EEA has been assessed combining the probability of infection/disease and the impact on public health (see Figure 1). This was done for the three population groups at risk. In case of uncertainty and identified knowledge gaps, the algorithm adopts a precautionary approach, stepping up the level of risk by one (see Annex ? Methodology)

__

Box 3. Assessed threat posed by poliovirus importation and reestablishment into the EU/EEA

Using the algorithm (Figure 3 in the annexes), the overall threat posed by re-establishment of poliovirus into the EU/EEA can be assessed as follows:
  • Very low in OPV vaccinees for both poliovirus infection and disease;
  • Moderate in IPV-only cohorts for poliovirus infection and low for disease;
  • High in low-or unvaccinated groups for poliovirus infection and moderate for disease.
____


Conclusions

Europe has been polio-free since 2002 and the latest assessment by the RCC concludes that in 2012 there was no evidence of wild-type or vaccine-derived polio viruses circulating in the region. Detection of WPV in environmental samples is a signal of WPV transmission in the population and consequently a potential risk of paralytic poliomyelitis. A risk of asymptomatic gut mucosal infection and virus shedding remains after both IPV and OPV vaccination, although the risk is higher for those who are IPV-vaccinated. Israel is a popular destination for EU travellers and vice versa, and the circulation of WPV1 in Israel is likely to have increased the risk of WPV importation into the EU.

Given the significant population flow from and to countries where WPV is still circulating, the existence of areas with low vaccine coverage and the sub-optimal potential for early detection of the virus in both the environment and the population there is risk that WPV could be imported and re-established in the EU via a recently infected person shedding the virus.

However, lack of observed WPV circulation in the EU/EEA to date may be due to the limited number of locations in the world where WPV circulates; the fact that infected persons do not shed much virus, or for a very long time, and the high vaccination uptake of visitors to these areas.

Moreover, proper sewage treatment in EU countries may contribute to mitigating the risk. In support of this statement, although there are large migrant populations in EU countries that have frequent contact with polio endemic countries (Pakistan, Nigeria) or countries with recent onset of large outbreaks (Somalia), importation of WPV has to date not been documented in such populations.

Consequently, assuming that WPV is imported and re-established in the EU/EEA, the overall threat posed by poliovirus re-establishment can be considered:
  • Very low in OPV vaccinees for both poliovirus infection and disease
  • Moderate in IPV-only cohorts for poliovirus infection and low for disease
  • High in low- or unvaccinated groups for poliovirus infection and moderate for disease.
If WPV is imported into the EU/EEA, the highest risk for establishment of circulation is within unvaccinated groups. The risk is also high in geographically clustered, under-vaccinated groups and in groups that live in poor sanitary conditions. If WPV were to be introduced into an unvaccinated group with close social contact among the members, then it is likely that the virus would spread quickly through a large proportion of the group, and that the circulation would result in paralytic cases.

There are several under-vaccinated groups at particular risk of polio in the EU. Orthodox religious groups, among whom low vaccination coverage is often reported, are likely to be at increased risk of exposure to the WPV1 currently circulating in Israel as a result of frequent direct or indirect contacts with that country.

Other potentially under-vaccinated groups in the EU at increased risk of exposure to poliovirus through contacts with family and friends in polio transmission areas include those linked to countries with sustained poliovirus circulation. In addition, ethnic Roma represent a large, under vaccinated risk group often living under socioeconomic conditions that increase the risk of imported poliovirus being transmitted.

Vaccination uptake of IPV, and previously of OPV, is high in the EU and both vaccines effectively prevent disease. The risk of asymptomatic WPV infection is likely to be higher among IPV-vaccinated individuals than among OPVvaccinated, but both vaccines significantly reduce the risk of infection and the overall quantity of viruses shed in the event of infection. The use of either vaccine has resulted in the elimination of WPV circulation in the EU countries.

Satisfactory levels of vaccination coverage (>90% for three doses of either IPV or OPV) can largely justify the absence of disease in the EU/EEA (see Figure 5 and Table 14 in the annexes). On the other hand, the recent events in Israel raise new questions on the potential for the importation and re-establishment of WPV in the general population or in selected population subgroups, fully immunised with IPV.

Interventions aimed at preventing poliomyelitis cases and the re-establishment of WPV circulation in the EU are likely to reduce the risk of established virus transmission in low or unvaccinated population groups. A reduction in the risk of virus circulation in under-vaccinated groups can, in the short term, be achieved by increasing vaccination uptake in these risk groups and through the early detection of WPV transmission. All EU travellers to areas where WPV is circulating should be up-to-date with their polio vaccination status.

Experiences from the Netherlands show that people who object to vaccination on religious grounds are unlikely to change their opinion and accept vaccination unless an outbreak has been established. However, once the outbreak is a fact, uptake often increases even among vaccine opponents.

AFP surveillance is a blunt instrument for detecting WPV circulation because of the high ratio of asymptomatic-tosymptomatic polio cases and the fact that few EU/EEA countries meet current guidelines for APF surveillance. By the time a case of polio is detected through AFP surveillance, the WPV virus is likely to have spread widely in an unvaccinated population. Environmental surveillance has the advantage of potentially signalling WPV circulation before cases of poliomyelitis have occurred, as exemplified by the developments in Israel. However, although a limited number of EU/EEA Member States (at least five) conduct environmental surveillance, there are no agreed standards for routine environmental surveillance in polio-free areas, and the chance of environmental surveillance identifying just one imported case is considered to be very low [22].

Established outbreak guidelines have the potential to improve the timeliness and effectiveness of outbreak control measures. The number of EU/EEA Member States with outbreak control guidelines is sub-optimal (see Supporting documentation for operational plans including OPV availability in the EU ).

Therefore, international cooperation can be the key to an effective outbreak response. Prior information on stockpile availability (in Member States and at UNICEF) is needed, as well as the existence of political approval processes for exchanging the existing stockpile between donor and recipient countries (shipment procedures, customs clearance and product liability issues). Outbreak management is the responsibility of the EU/EEA Member State and careful monitoring of the outbreak response is crucial.


Recommendations
  • EU/EEA Member States should give high priority to the assessment of polio vaccination uptake at national, subnational and local level, and to the identification of vulnerable and under-vaccinated populations.
  • Countries where the overall national vaccination coverage is below 90% should increase efforts towards improving vaccination coverage under the national schedule.
  • The highest level of risk is posed by the proximity of low- or unimmunised population clusters to large populations vaccinated using IPV-only schemes, however suboptimal hygiene and crowded living conditions may also play a role in facilitating the spread of infection. In particular, religious groups having contact with Israel, migrant residents visiting family and friends in countries where WVP is circulating, and vulnerable groups living in poor sanitary conditions are key risk groups. Countries with groups living in such conditions should urgently consider implementing targeted action and improving vaccine coverage in these groups.
  • EU/EEA Member States should recommend all travellers to areas where WPV is in circulation to have an up-todate polio vaccination status.
  • Member States not meeting the polio surveillance requirements established by the Regional Certification Commission for Polio Eradication should urgently consider strengthening their surveillance systems, and to at least comply with the minimum AFP surveillance standards if this is the only surveillance system in place.
  • Member States with pockets of unvaccinated individuals should consider strengthening or establishing environmental and enterovirus surveillance in these areas, as a complement to AFP surveillance.
  • Member States should consider assessing their current laboratory capacity for polio virus detection.
  • The role of environmental and enterovirus surveillance should be further discussed at the EU/EEA-level with a view to agreeing on common standards and indicators. ECDC and the Member States, in close collaboration with WHO, should engage in the development of guidance for the establishment of environmental and enterovirus surveillance.
  • Member States identifying positive environmental or enterovirus samples should be prepared to use WHO guidelines to assess WPV circulation in the affected areas.
  • Member States that have not yet developed national response plans should develop these plans and consider requesting support from ECDC and WHO.
  • In the event that positive human samples are detected, Member States should implement their national poliomyelitis response plan. In the unfortunate event that a national plan is not yet available, an emergency plan should be developed on the basis of WHO guidance and recommendations.
  • Member States should be undertaking exercises to test their poliomyelitis response plans.
  • Operational and contingency plans are needed in the EU/EEA for the possible mobilisation of IPV and OPV stockpiles in case of evidence of WPV transmission.
  • The availability of poliovirus vaccines to be used in the context of an outbreak should be assessed.
(...)


References
  1. Global Polio Eradication Initiative. Polio this week: 28 August 2013 [cited 3 September 2013]. Available from: http://www.polioeradication.org/Dataandmonitoring/Poliothisweek.aspx.
  2. State of Israel: Ministry of Health. Polio update August 18, 2013 [cited 17 September 2013]. Available from: http://www.health.gov.il/English/News_and_Events/Spokespersons_Messages/Pages/18082013_2.aspx.
  3. State of Israel: Ministry of Health - Two drops - polio vaccination campaign. [cited 3 September 2013]. Available from: http://www.health.gov.il/English/Topics/Vaccination/two_drops/Pages/Vaccination.aspx
  4. Slater PE, Orenstein WA, Morag A, Avni A, Handsher R, Green MS, et al. Poliomyelitis outbreak in Israel in 1988: A report with two commentaries. Lancet. 1990 May 19;335(8699):1192-5.
  5. State of Israel: Ministry of Health. Two drops for stopping polio campaign. Polio, public health, vaccination. Press release [cited 17 September 2013]. Available from: http://www.health.gov.il/English/News_and_Events/Spokespersons_Messages/Pages/04082013_1.aspx.
  6. The World Bank. Prospects - Bilateral Migration and Remittances. [cited 3 September 2013]. Available from: http://econ.worldbank.org/WBSITE/EXTERNAL/EXTDEC/EXTDECPROSPECTS/0,,contentMDK:22803131~pagePK:64165401~piPK:64165026~theSitePK:476883,00.html.
  7. Oostvogel PM, van Wijngaarden JK, van der Avoort HG, Mulders MN, Conyn-van Spaendonck MA, Rumke HC, et al. Poliomyelitis outbreak in an unvaccinated community in the Netherlands, 1992-93. Lancet. 1994 Sep 3;344(8923):665-70.
  8. Hovi T, Huovilainen A, Kuronen T. Outbreak of paralytic poliomyelitis in Finland: Widespread circulation of antigenically altered poliovirus type 3 in a vaccinated population. Lancet. 1986;1(8495):1427-32.
  9. Poyry T, Stenvik M, Hovi T. Viruses in sewage waters during and after a poliomyelitis outbreak and subsequent nationwide oral poliovirus vaccination campaign in Finland. Appl. Environ. Microbiol. 1988 Feb;54(2):371-4.
  10. World Health Organization. Report of the 27th meeting of the European Regional Certification Commission for Poliomyelitis Eradication: Copenhagen, Denmark 30?31 May 2013: WHO Regional Office for Europe; 2013. Available from: http://www.euro.who.int/__data/assets/pdf_file/0016/200752/Report-of-the-27th-Meeting-of-the-European-Regional-Certification-Commission-for-Poliomyelitis-Eradication.pdf.
  11. Boot HJ, Kasteel DT, Buisman AM, Kimman TG. Excretion of wild-type and vaccine-derived poliovirus in the faeces of poliovirus receptor-transgenic mice. J Virol. 2003 Jun;77(11):6541-5.
  12. Francy DS, Stelzer EA, Bushon RN, Brady AM, Williston AG, Riddell KR, et al. Comparative effectiveness of membrane bioreactors, conventional secondary treatment, and chlorine and UV disinfection to remove microorganisms from municipal wastewaters. Water Research. 2012 Sep 1;46(13):4164-78.
  13. Sima LC, Schaeffer J, Le Saux JC, Parnaudeau S, Elimelech M, Le Guyader FS. Calicivirus removal in a membrane bioreactor wastewater treatment plant. Appl. Environ. Microbiol. 2011 Aug;77(15):5170-7.
  14. Simmons FJ, Kuo DH, Xagoraraki I. Removal of human enteric viruses by a full-scale membrane bioreactor during municipal wastewater processing. Water Research. 2011 Apr;45(9):2739-50.
  15. Tierney JT, Sullivan R, Larkin EP. Persistence of poliovirus 1 in soil and on vegetables grown in soil previously flooded with inoculated sewage sludge or effluent. Appl. Environ. Microbiol. 1977 Jan;33(1):109-13.
  16. Council Directive, 21 May 1991 concerning urban wastewater treatment (91/27/EEC). Official Jounal of the European Communities 1991.
  17. Directive 2006/7/EC of the European Parliament and of the Council, 15 February 2006 concerning the management of bathing water quality and repealing Directive 76/160/EEC. Official Journal of the European Union 2006.
  18. Council Directive 98/83/EC, 3 November 1998 on the quality of water intended for human consumption. Official Journal of the European Communities 1998.
  19. Sein C. Evaluating surveillance indicators supporting the global polio eradication initiative, 2011?2012. Morbidity and Mortality Weekly Report. 2013;62(14):270-4.
  20. European Centre for Disease Prevention and Control. Annual epidemiological report 2012: Reporting on 2010 surveillance data and 2011 epidemic intelligence data. Stockholm: ECDC; 2013. Available from: http://ecdc.europa.eu/en/publications/Publications/Annual-Epidemiological-Report-2012.pdf.
  21. World Health Organization. Report of the 26th meeting of the European Regional Certification Commission for Poliomyelitis: Copenhagen, Denmark 18?20 June 2012. Copenhagen: WHO Regional Office for Europe; 2013. Available from: http://www.euro.who.int/__data/assets/pdf_file/0005/184739/e96806.pdf.
  22. World Health Organization. Department of Vaccines and Other Biologicals. Guidelines for environmental surveillance of poliovirus circulation. Geneva: WHO; 2003. Available from: http://whqlibdoc.who.int/hq/2003/WHO_V&B_03.03.pdf.
  23. World Health Organization. Classification of AFP cases, surveillance performance and weekly reporting to WHO EURO by country, 2012?2013. WHO European Region 2013. Available from: http://www.euro.who.int/__data/assets/pdf_file/0007/199537/EpiData6-2013-Eng.pdf
  24. World Health Organization. Epidemiological Brief No 29: A monthly publication on vaccine-preventable diseases and immunization data and analysis. December 2012 [cited 17 September 2013]. Available from: http://www.euro.who.int/__data/assets/pdf_file/0018/181800/EpiBrief-Issue-29.pdf.
  25. Hovi T, Shulman LM, van der Avoort H, Deshpande J, Roivainen M, De Gourville EM. Role of environmental poliovirus surveillance in global polio eradication and beyond. Epidemiol. Infect. 2012 Jan;140(1):1-13.
  26. World Health Organization. Press release: Polio commission calls on Europe to improve surveillance and reporting 2013 [cited 17 September 2013]. Available from: http://www.euro.who.int/en/what-we-do/health-topics/communicablediseases/poliomyelitis/news/news/2013/06/polio-commission-calls-on-europe-to-improve-surveillance-and-reporting.
  27. Global Polio Eradication Initiative. Global Polio Laboratory Network. [cited 5 September 2013]. Available from: http://www.polioeradication.org/Dataandmonitoring/Surveillance/GlobalPolioLaboratoryNetwork.aspx.
  28. Murdin AD, Barreto L, Plotkin S. Inactivated poliovirus vaccine: Past and present experience. Vaccine. 1996 Jun;14(8):735-46.
  29. Zurbriggen S, Tobler K, Abril C, Diedrich S, Ackermann M, Pallansch MA, et al. Isolation of sabin-like polioviruses from wastewater in a country using inactivated polio vaccine. Appl. Environ. Microbiol. 2008 Sep;74(18):5608-14.
  30. Conyn-van Spaendonck MA, Oostvogel PM, van Loon AM, van Wijngaarden JK, Kromhout D. Circulation of poliovirus during the poliomyelitis outbreak in the Netherlands in 1992?1993. Am. J. Epidemiol. 1996 May 1;143(9):929-35.
  31. Duintjer Tebbens RJ, Pallansch MA, Chumakov KM, Halsey NA, Hovi T, Minor PD, et al. Expert review on poliovirus immunity and transmission. Risk analysis: an official publication of the Society for Risk Analysis. 2013 Apr;33(4):544-605.
  32. Global Polio Eradication Initiative. Polio Eradication and Endgame Strategic Plan 2013?2018 [cited 17 September 2013]. Available from: http://www.polioeradication.org/resourcelibrary/strategyandwork.aspx.
  33. Global Polio Eradication Initiative. Responding to a polio outbreak: Guideline. 7 January 2011 [cited 17 September 2013] Available from: http://www.polioeradication.org/Portals/0/Document/Resources/PolioEradicators/1a.PolioOutbreakGuideline20110107.pdf.
  34. Global Polio Eradication Initiative. Polio this week: 10 September 2013 [cited 10 September 2013]. Available from: http://www.polioeradication.org/Dataandmonitoring/Poliothisweek.aspx.
  35. World Health Organization. Poliovirus detected from environmental samples in Israel - Update. [updated 26 August 2013; cited 3 September 2013]. Available from: http://www.who.int/csr/don/2013_08_15/en/index.html.
  36. UNOCHA. Humanitarian Bulletin - Somalia August 2013. [cited 17 September 2013] Available from: http://reliefweb.int/sites/reliefweb.int/files/resources/OCHA%20Somalia%20Humanitarian%20Bulletin%20August%202013.pdf.
  37. World Health Organization. Certification of poliomyelitis eradication - European Region declared ?polio-free?. Fifteenth meeting of the European Regional Certification Commission, Copenhagen, 19?21 June 2002. Denmark: WHO; 2005.
  38. Kojouharova M, Zuber PL, Gyurova S, Fiore L, Buttinelli G, Kunchev A, et al. Importation and circulation of poliovirus in Bulgaria in 2001. Bulletin of the World Health Organization. 2003;81(7):476-81.
  39. Outbreak of poliomyelitis in Tajikistan in 2010: Risk for importation and impact on polio surveillance in Europe? Eurosurveillance: Bulletin europeen sur les maladies transmissibles = European communicable disease bulletin. 2010 Apr 29;15(17).
  40. World Health Organization. WHO Epidemiological Brief 2012 [cited 22 August 2013]. Available from: http://www.euro.who.int/__data/assets/pdf_file/0004/160789/WHO_EPI_Brief_VPD_Summary_Tables_Jan-Dec2011.pdf.
  41. World Health Organization. Tajikistan Polio Update, Monthly Newsletter, April 2011 [cited 22 August 2013]. Available from: http://www.euro.who.int/__data/assets/pdf_file/0017/141263/PolioUpdate_1_TAD.pdf.
  42. European Centre for Disease Prevention and Control. Risk assessment on the finding of Vaccine-Derived Polio Virus (VDPV) in Finland, 17 February 2009. Stockholm: ECDC; 2009.
  43. Combiescu M, Guillot S, Persu A, Baicus A, Pitigoi D, Balanant J, et al. Circulation of a type 1 recombinant vaccinederived poliovirus strain in a limited area in Romania. Arch Virol. 2007;152(4):727-38.
  44. Blomqvist S, Savolainen C, Laine P, Hirttio P, Lamminsalo E, Penttila E, et al. Characterization of a highly evolved vaccine-derived poliovirus type 3 isolated from sewage in Estonia. J Virol. 2004 May;78(9):4876-83.
  45. Maderova E, Slacikova M, Cernakova B, Sobotova Z, Nadova K. First isolation of vaccine-derived poliovirus in Slovakia. Eurosurveillance: Bulletin europeen sur les maladies transmissibles = European communicable disease bulletin. 2005 Aug;10(8):E050818 3.
  46. Hovi T, Paananen A, Blomqvist S, Savolainen-Kopra C, Al-Hello H, Smura T, et al. Characteristics of an environmentally monitored prolonged type 2 vaccine derived poliovirus shedding episode that stopped without intervention. PLoS One. 2013;8(7):e66849.
  47. World Health Organization. Polio Lab Network - Quarterly Update April 2007 13(1):4 [cited 17 September 2013] Available from: http://www.who.int/immunization_monitoring/VolIIIIssue1April07.pdf.
  48. Drake JW. Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci USA. 1993 May 1;90(9):4171-5.
  49. Global Polio Eradication Initiative. Annual Report of the Global Polio Eradication Initiative - 2006. [cited 17 September 2013] Available from: http://www.polioeradication.org/content/publications/AnnualReport2006_ENG.pdf
  50. Shulman LM, Manor Y, Sofer D, Handsher R, Swartz T, Delpeyroux F, et al. Neurovirulent vaccine-derived polioviruses in sewage from highly immune populations. PLoS One. 2006;1:e69.
  51. Centers for Disease Control and Prevention. Laboratory surveillance for wild and vaccine-derived polioviruses--worldwide. January 2007?June 2008. MMWR Morb Mortal Wkly Rep. 2008 Sep 5;57(35):967-70.
  52. Centers for Disease Control and Prevention. Update on vaccine-derived polioviruses--worldwide. July 2009-March 2011. MMWR Morb Mortal Wkly Rep2011. p. 846-50.
  53. World Health Organization. WHO EURO Polio page. Monthly AFP surveillance bulletin. November 2007 [cited 10 September 2013]. Available from: http://www.euro.who.int/__data/assets/pdf_file/0005/79394/E200711_PolioPage.pdf
  54. Centers for Disease Control and Prevention. Update on vaccine-derived polioviruses-worldwide. January 2008?June 2009. MMWR Morb Mortal Wkly Rep. 2009 Sep 18;58(36):1002-6.
  55. Roivainen M, Blomqvist S, Al-Hello H, Paananen A, Delpeyroux F, Kuusi M, et al. Highly divergent neurovirulent vaccinederived polioviruses of all three serotypes are recurrently detected in Finnish sewage. Eurosurveillance: Bulletin europeen sur les maladies transmissibles = European communicable disease bulletin. 2010 May 13;15(19):pii/19566.
  56. Mandell G. Poliovirus. In Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases. Philadelphia, PA: Churchill Livingstone/Elsevier; 2010. p. 2345-51.
  57. Heymann DL. Control of Communicable Diseases Manual. Washington DC: American Public Health Association; 2008.
  58. Yang CF, Chen HY, Jorba J, Sun HC, Yang SJ, Lee HC, et al. Intratypic recombination among lineages of type 1 vaccinederived poliovirus emerging during chronic infection of an immunodeficient patient. J Virol. 2005 Oct;79(20):12623-34.
  59. Wood DJ, David TJ, Chrystie IL, Totterdell B. Chronic enteric virus infection in two T-cell immunodeficient children. J Med Virol. 1988 Apr;24(4):435-44.
  60. Martin J. Vaccine-derived poliovirus from long term excretors and the end game of polio eradication. Biologicals. 2006 Jun;34(2):117-22.
  61. Plotkin S. Poliovirus vaccine-inactivated. Vaccines. [St. Louis, Mo.]: Elsevier Saunders; 2013. p. 573-97.
  62. Plotkin S. Poliovirus vaccine-live. Vaccines. [St. Louis, Mo.]: Elsevier Saunders; 2013. p. 598-645.
  63. Bottiger M. Experiences of vaccination with inactivated poliovirus vaccine and epidemiology round a single case of polio in 1977 in Sweden. Dev Biol Stand. 1978;41:133-6.
  64. Centers for Disease Control and Prevention. Poliomyelitis prevention in the United States: Introduction of a Sequential Vaccination Schedule of Inactivated Poliovirus Vaccine Followed by Oral Poliovirus Vaccine; Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recommendations and Reports: Morbidity and Mortality Weekly Report. January 1997 9026708; 46 RR-3):[1-25 pp.]. Available from: http://www.cdc.gov/mmwr/preview/mmwrhtml/00046568.htm.
  65. Grassly NC, Jafari H, Bahl S, Sethi R, Deshpande JM, Wolff C, et al. Waning intestinal immunity after vaccination with oral poliovirus vaccines in India. J Infect Dis. 2012;205(10):1554-61.
  66. Blumenthal UJ, Mara DD, Peasey A, Ruiz-Palacios G, Stott R. Guidelines for the microbiological quality of treated wastewater used in agriculture: Recommendations for revising WHO guidelines. Bulletin of the World Health Organization. 2000;78(9):1104-16.
  67. Asano T, Leong LYC, Rigby MG, Sakaji RH. Evaluation of the California wastewater reclamation criteria using enteric virus monitoring data. Water Sci Technol 1992;26(7-8):1513-24.
  68. World Health Organization. State of the Art Report Health Risks in Aquifer Recharge Using Reclaimed Water. WHO; 2003 [cited 24 September 2013]. Available from: http://whqlibdoc.who.int/hq/2003/who_sde_wsh_03.08.pdf
  69. Bixio D, Thoeye J, De Koning D, Joksimovic D, Savic D, Wintgens T et al. Wastewater reuse in Europe. Desalination. 2006;187(1-3):89-101.
  70. Lodder WJ, Buisman AM, Rutjes SA, Heijne JC, Teunis PF, de Roda Husman AM. Feasibility of quantitative environmental surveillance in poliovirus eradication strategies. Appl. Environ. Microbiol. 2012 Jun;78(11):3800-5.
  71. World Health Organization. Department of Immunization, Vaccines and Biologicals. Polio Laboratory Manual. Geneva: WHO; 2004. Available from: http://whqlibdoc.who.int/hq/2004/WHO_IVB_04.10.pdf.
  72. Bottiger M. Polio immunity to killed vaccine: An 18-year follow-up. Vaccine. 1990 Oct;8(5):443-5.
  73. De Melker HE, Van den Hof S, Berbers GAM, Conyn-van Spaendonck MAE. Evaluation of the national immunisation programme in the Netherlands: Immunity to diphtheria, tetanus, poliomyelitis, measles, mumps, rubella and haemophilus influenzae Type B. Vaccine. 2003;21 7-8):716-20.
  74. Kulshammer M, Winke U, Frank M, Skali-Lami U, Steudel H, Schilling G, et al. Poor immunity status against poliomyelitis in medical students: A semi-anonymous study. Med Microbiol Immun. 2013 Feb;202(1):63-5.
  75. Hird TR, Grassly NC. Systematic review of mucosal immunity induced by oral and inactivated poliovirus vaccines against virus shedding following oral poliovirus challenge. PLoS Pathogens. 2012;8(4).
  76. Gary HE Jr, Smith B, Jenks J, Ruiz J, Sessions W, Vinje J, et al. Failure to detect infection by oral polio vaccine virus following natural exposure among inactivated polio vaccine recipients. Epidemiol Infect. 2008 Feb;136(2):180-3.
  77. Swartz TA, Green MS, Handscher R, Sofer D, Cohen-Dar M, Shohat T, et al. Intestinal immunity following a combined enhanced inactivated polio vaccine/oral polio vaccine programme in Israel. Vaccine. 2008 Feb 20;26(8):1083-90.
  78. Duintjer Tebbens RJ, Pallansch MA, Chumakov KM, Halsey NA, Hovi T, Minor PD, et al. Review and assessment of poliovirus immunity and transmission: Synthesis of knowledge gaps and identification of research needs. Risk analysis: an official publication of the Society for Risk Analysis. 2013 Apr;33(4):606-46.
  79. European Centre for Disease Prevention and Control. Operational guidance on rapid risk assessment methodology. Stockholm: ECDC; 2001. Available from: http://ecdc.europa.eu/en/publications/Publications/1108_TED_Risk_Assessment_Methodology_Guidance.pdf
  80. World Health Organization. WHO Guidelines for save use of wastewater, excreta and greywater. Volume 2. Wastewater use in agriculture [cited 25 September 2013]. Available from: http://whqlibdoc.who.int/publications/2006/9241546832_eng.pdf
(...)
-
--------
 

Attachments

Back
Top Bottom