4,350
Views
25
CrossRef citations to date
0
Altmetric
Research Paper

Polio elimination in Nigeria: A review

, , , , , & show all
Pages 658-663 | Received 29 Jun 2015, Accepted 25 Aug 2015, Published online: 05 May 2016

abstract

Nigeria has made tremendous strides towards eliminating polio and has been free of wild polio virus (WPV) for more than a year as of August 2015. However, sustained focus towards getting rid of all types of poliovirus by improving population immunity and enhancing disease surveillance will be needed to ensure it sustains the polio-free status. We reviewed the pertinent literature including published and unpublished, official reports and working documents of the Global Polio Eradication Initiative (GPEI) partners as well as other concerned organizations. The literature were selected based on the following criteria: published in English Language, published after year 2000, relevant content and conformance to the theme of the review and these were sorted accordingly. The challenges facing the Polio Eradication Initiative (PEI) in Nigeria were found to fall into 3 broad categories viz failure to vaccinate, failure of the Oral Polio Vaccine (OPV) and epidemiology of the virus. Failure to vaccinate resulted from insecurity, heterogeneous political support, programmatic limitation in implementation of vaccination campaigns, poor performance of vaccination teams in persistently poor performing Local Government areas and sporadic vaccine refusals in Northern Nigeria. Sub optimal effectiveness of OPV in some settings as well as the rare occurrence of VDPVs associated with OPV type 2 in areas of low immunization coverage were also found to be key issues. Some of the innovations which helped to manage the threats to the PEI include a strong government accountability frame work, change from type 2 containing OPV to bi valent OPVs for supplementary immunization activities (SIA), enhancing environmental surveillance in key states (Sokoto, Kano and Borno) along with an overall improvement in SIA quality. There has been an improvement in coverage of routine immunization and vaccination campaigns, which has resulted in Nigeria being removed from the list of endemic countries following an absence of new cases for an entire year as of September 2015. However, the last mile remains to be crossed and there is need to further improve and sustain the momentum to complete the journey toward polio elimination.

Introduction/Background

A large proportion of importation of polio cases into polio-free countries following elimination has been from Nigeria.Citation1

Outbreaks linked to increased circulation of WPV1 and 3 in Nigeria during 2008 and 2009 also occurred in 12 countries in 2009 including Senegal, Liberia, Mali, Niger and Chad republic.Citation2 There were about 25 exportations to other countries between 2003 and 2012,Citation3; some of these countries like Cameroun and Chad have re-established transmission and Cameroun persists as a source of exportation. The gaps in surveillance in most African countries make it even more important to eliminate Nigeria as a source of exportation.

This review was carried out to identify the progress toward elimination of polio from Nigeria, ongoing and historic challenges related to elimination strategy facing the PEI in Nigeria and innovations put in place to manage these threats.

Methodology

This is a review of the existing literature: publications, official documents, working plans and policy statements of the relevant organizations responsible for polio eradication including the World Health Organization (WHO), United Nations International Children Emergency Fund (UNICEF), Rotary international and United States Center for Disease Control and Prevention (CDC).

Search strategy

A ‘free word’ internet search was conducted on Pubmed using the mesh terms “Global polio eradication and (vaccin*] and Nigeria.” Other sources included the official reports of Global Polio Eradication Initiative (GPEI) partners and other important partners such as the Bill and Melinda Gates Foundation. Finally, reports of vaccination activities carried out within Nigeria by the National Primary Health Care Development Agency (NPHCDA) either alone or with partners, published or unpublished, were included, obtained by contacting the NPCHDA.

Selection criteria

The abstracts of all the articles retrieved were examined for relevance under the following topics.

Time

For articles relating to the progress toward polio eradication, the latest reports were used for each relevant country or region. Articles selected were those from 1st January 2000, the original timeline for eradication which has since been revised.

Content availability

Only Articles with full content available and that could be accessed were included.

Theme

The content of the articles was scanned for relatedness to the thematic areas covered in this review as including: i) Nigeria's polio situation, ii) challenges and iii) innovations made to eliminate polio from Nigeria.

Language

Only articles in English language were extracted, those with only the abstract in English were excluded.

Duplication

Articles which reported findings from the same event or covering the same scope were also excluded. (2 articles)

Review strategy

The articles were summarized using a concept map (inspiration®) and a thematic classification was carried out under the themes explained earlier.

Results

Literature

50 literature were found to be relevant for the global polio situation while 43 were reviewed particularly concerning Nigeria, with most of the literature relevant for the 3 thematic areas of progress toward elimination, challenges and innovations to deal with these challenges.

Progress toward polio elimination from Nigeria

There has been steady progress toward interrupting transmission. There were 541 cases of WPV in 2009,Citation4 but only 6 cases as of June 2010. There was a new surge in the number of cases in 2011. In 2012, there were 122 cases of WPV in 60 districts, 53 cases in 30 districts in 2013.Citation5 Year 2013 marked a turning point of the Polio Eradication Initiative (PEI) in Nigeria: there was at least a 58% reduction in the number of WPV 1 cases compared to 2012; 50% reduction in the number of affected Local Government Areas (LGAs), with 4 states - Kano, Borno, Yobe and Bauchi, accounting for 84% of the cases. The year 2013 also saw an 80% reduction in the number of circulating genetic clusters (2 clusters) versus 2012 (8 clusters).

The progress towards reduction in virus circulation was maintained in 2014 with a massive decrease of up to 88% in the number of cases as at May 2014 when the country had witnessed only 3 cases of WPV1.Citation6 Since September 3 2013, circulation in Nigeria has been restricted to Kano and Borno states of Northern Nigeria although surveillance gaps have persisted.Citation7

cVDPVs have also declined. They were first noticed in Northern Nigeria in 2005 when a CDC laboratory technician at a polio laboratory noticed a preponderance of type 2 polio virus in samples from Northern Nigeria. As at September 2007, 69 cases had been discovered.Citation8 Between July 2005 and June 2010, there were 315 cVDPV 2 cases.Citation9 Since then, there was a spike, with 32 cases in 2012, from 18 in 2011, but eventually declined to 3 in 2013; all cases were reported in Borno state; the last of the 6 cases reported in 2014 was recorded on the 9th of February 2014.

There have been no reports of cases of WPV2 since 1999 and WPV3 since November 2012.Citation10

In July 2015, Nigeria celebrated a year without new cases of wild polio acute flaccid paralysis (AFP). Although it came 6 months after the latest target date, it is still worthy of commendation, and a major milestone seeing as the elimination program has been bedeviled by a myriad of challenges as discussed subsequently.

Challenges

The problems facing the program in Nigeria could be classified into 3 main classes: i) failure to vaccinate, ii) failure of the vaccine and iii) problems related to the epidemiology of the virus.Citation4

Long standing weakness in health infrastructure is the main limitation in the vaccination program, along with programmatic limitations in implementation of vaccination campaigns, weak accountability mechanisms and loss of public confidence in Oral Polio Vaccine (OPV), since 2003 in some areas.Citation3

The conflict in Northern Nigeria, particularly in North Eastern Nigeria has posed a challenge for delivery of vaccines in the PEI. Supplementary Immunisation Activities (SIAs) were temporarily suspended in 2013 as a result of the conflict, with limited access to children. This had improved as of March 2014, with about 84% of the target population accessibleCitation5).

The challenges facing the PEI in Nigeria were summarized by the NPHCDA as follows:Citation10

  • – Heterogeneous political support and commitment at the state and LGA levels, with slow release of counterpart funds for eradication related activities.

  • – Insecurity and killing of vaccination teams in Kano and Borno.

  • – Poor performance of vaccination teams due to interference in several persistently poor performing, very high risk LGAs.

  • – Localized noncompliance, which was exacerbated by anti-OPV campaigns, messages by institutions of higher learning and religious clerics.

  • – Delays to mount timely and adequate polio outbreak response due to global shortage of vaccines and non-availability of operational funds in some instances.

  • – At national level, statistical modeling and lot quality assurance sampling data are not used to define high –risk LGAs and wards to prioritize intervention.

Others challenges are the existence of polio sanctuaries in Northern Nigeria; in the North western states of Kano, Katsina, Kaduna and Jigawa, and the North Eastern states, Borno and Yobe. In the North West, there are also risk areas in Sokoto and Zamfara states.Citation7

Innovations

To tackle the challenges as enumerated earlier, there have been several strategic changes in the polio eradication plans globally. In Nigeria there has also been an evolution of the end game approach. These measures described below are responsible for the gains which have driven polio to the brink of elimination from Nigeria.

In 2006 and 2007, Nigeria utilized monovalent OPV 1 and 3 respectively in SIAs, as it was recommended for use in areas with a low vaccine coverage. Subsequently for sub national immunization activities, bivalent OPV (bOPV) is used with utilization of trivalent OPV (tOPV) reserved for national immunization days. This strategy has been effective in reducing the circulation of both wild viruses and VDPV.Citation11 Revertant vaccine derived polio viruses are vaccine type viruses which regain virulence transmissibility and have potential to cause outbreaks. They are primarily seen in areas of low vaccination coverage with OPV and about 95% of cases are due to type 2 vaccine virus.Citation12

It has been estimated that there is a likelihood of 60–95% that there will be at least one cVDPV outbreak somewhere in the world, in the 12 months following OPV cessation.Citation13 In view of these, the end game plan stipulates the introduction of at least 1 dose of IPV into countries which are using only OPV in routine immunisation to be administered at the point of administering the third dose of DPT/Pentavalent vaccine. This is meant to enable a switch from the use of trivalent to bivalent OPV with an elimination of the type 2 antigen, insuring against an outbreak of VDPV 2 and stopping the emergence of VDPVs and also reducing vaccine associated paralytic polio (VAPP) due to type 2.Citation30 Thereafter, only type 1 and 3 polio viral antigens would be administered either singly or combined as bivalent OPV. IPV campaigns have been held in the high risk polio areas of Northern Nigeria in limited campaigns, as recommended under the end game plan for polio eradication, with high coverage rates. It has also been introduced into routine immunization in pilot projects around the country in April 2015.

Building on the achievements of those campaigns, there was an emergency plan for polio eradication in Nigeria for 2012 that contained several initiatives including:Citation3

  • – Senior Government oversight, new program management and strategic initiatives, accountability framework and a surge in human resources.

  • – Improved surveillance with recall and vaccination cards of children 6–35 months with non-polio Acute Flaccid Paralysis (AFP).

  • – Increase in routine OPV3 immunisation coverage from 54 to 73%

  • – Plan for 1 national and 10 sub national SIAs for 2012 targeting children under 5 y of age, using bivalent OPV 1 and 3. Also 3 national and 4 sub national SIAs with tOPV.

  • – Sustaining and expanding environmental surveillance which is ongoing in Sokoto and Kano.

The accountability dashboard tool was also developed and implemented, based on the presidential task force directive established in March 2012. This is useful for SIA preparation and execution at LGA level. And clearly stipulates the responsible parties for all actions in the planning and implementation of immunization activities. This ensures that tasks missed are readily identified and there is a continuous cycle of improvement in immunization activities.

Under the plan for 2013–2015, improvement in SIA quality was noted in 2013 when 74% (from 64%) of the LGAs achieved Lot Quality Assurance Survey estimated coverage of at least 80%.

The plan had a goal of interrupting polio virus transmission by December 2014, expecting no new cases to be reported from the end of June 2015. More specific targets included increasing SIA quality by March 2014, in which 80% of LGAs are expected to achieve 80% coverage, with the underperforming wards expected to achieve at least 90%.

The strategic priorities were on:Citation10

  • – Improvement of immunisation plus days' (IPDs) quality in the persistent poor performing (PPP) LGAs. This has remarkably increased with latest estimates (unpublished) showing all LGAs achieving more than 80% immunization coverage of their target population.

  • – Increasing the reach of campaigns to children in security compromised areas. Which has also been successful with improving access to children within the target age group during immunization activities, directly as a result of measures elucidated subsequently.

  • – Rapidly containing circulation, in the breakthrough transmission zones.

  • – Mounting timely and adequate polio outbreak responses.

  • – Reaching underserved populations (hard to reach), these communities are inaccessible either due to the geography of their place of residence or cultural factors such as nomads.

  • – Intensifying both Acute Flaccid Paralysis (AFP) and environmental surveillance and improvements in its quality.

  • – Expanding technologies to aid the eradication effort.

  • – Innovations to further improve micro planning and team performance.

  • – Intensifying communication and demand creation.

  • – Boosting child immunity in between rounds and in polio-free states.

  • – Optimising resources and implementation of the accountability framework.

  • – Focused activities in polio-free states and neighboring countries in between rounds.

  • – Using OPV and non-polio SIAs like measles and meningitis. These should incorporate other activities like community management of acute malnutrition and outpatient therapeutic programmes in Northern endemic states.

  • – Advocacy activities using traditional rulers (maiangwas) and doctors against polio.

  • – Key technological advances including the use of GIS for tracking vaccinators.

  • – Two nationwide and 7 sub national SIAs were scheduled and executed successfully in 2014.

In 2014, the report showed improved quality of SIAs in Q4 2013 and Q1 2014, with more than 80% of LGAs in high-risk states exceeding the 80% threshold. Results for 2015 are yet to be published, but early pointers indicate a further improvement on the 2014 indicators.

Permanent health teams were established in Borno State to cope with insecurity from the ongoing insurgency, and Emergency operation centers were formed and deployed; these are management support teams sent to the poorest performing LGAs ahead of SIAs to assist in planning and microplanning and to ensure smooth implementation of these plans.

Volunteer community mobilization (VCM) network was set up and achieved impressive results in a short time. Refusals and missed children have reduced in all areas of their deployment by at least 70%. VCMs are groups of about 1600 religious focal persons, 1320 polio survivors and hundreds of doctors and journalists against polio who aid in community mobilization in their residential communities.

Health camps are also being run for underserved communities to provide routine immunization services, with free anti malaria medicines and diarrhea management. Children attending the camps with acute malnutrition are referred to Community Management of Acute Malnutrition (CMAM) sites after screening. They have permanent workers covering about 200 households each, in their area of catchment.Citation7

To restore vaccine confidence in Nigeria social mobilization was carried out with intensified and simplified communication strategies. Majigi which is a local documentary viewing usually at the village square was one way that resonated with the local people as well as direct contact with the traditional rulers in vaccination exercises.Citation14

The plan for 2014 included an aim to administer Inactivated Polio Vaccine (IPV) with tOPV to 200,000 often missed children in Borno state in June 2014, with more children planned for August 2014. The first goal was aborted due to the ongoing insurgency in North Eastern Nigeria but the second one was largely successful, even if restricted to internally displaced persons' (IDP) camps.Citation15

To circumvent the problem of access in areas where security is a challenge, there are some strategies being implemented such as:

Hit and run- this entails conducting the National immunization Days (NIDs) over a shorter period (e.g., 1-2 days) instead of 3 days to a week.

Fire walling or wall fencing- in this case, vaccinations are given at border crossing points, using fixed posts as well as in bordering communities as part of intensified outreach services.

Deployment of permanent health teams - Teams including discreet old women.Citation10 These ‘women’ are usually traditional birth attendants with many years of experience, resident within the community and providing services as deliveries, reproductive health counselling for married women and care of infants and children. They are well regarded in the communities, which makes it easier for them to enter households within the community without arousing suspicion. This is especially important because in some parts of Nigeria particularly in hotspots of insecurity, vaccinators have been targeted in the past and that risk lingers in the face of an ongoing insurgency. The team members are paid tokens on a regular basis for their activities during supplemental immunization activities.

Other possible measures include the implementation of recommendations under the Global vaccine action plan (GVAP) that was signed by leaders of worldwide countries including African countries.Citation16 The plan has 5 goals:

  1. Achieving a polio-free world

  2. Meeting vaccination coverage targets in every region, country and community.

  3. Exceeding MDG 4 targets on reducing child mortality.

  4. Meeting global and regional elimination targets

  5. Developing and introducing new and improved vaccines and technologies.

One such technology is the use of Geographic Information systems (GIS). It has a wide range of application in health including disaster management, research, outbreak response, emergency preparedness, research and humanitarian crises. All of these applications are relevant to polio vaccination and PEI. An example was the use of Google earth in Congo during a polio outbreak: it provided numerous benefits including more efficient use of resources, improved social mobilization, supervision and monitoring.Citation17

OPV campaigns in Nigeria

To ensure successful introduction of IPV, lessons need to be learned from previous campaigns with OPV in Nigeria and other parts of the globe. Mass vaccinations have been shown to be highly effective in raising the dose-related specific immunity of the population above that achieved by routine immunisation. These findings suggest campaigns should continually be used as an adjunct to routine immunisation especially in countries with low routine coverage.Citation18

Although detailed information on the conduct of these vaccination campaigns is not readily available publicly, bits of information relating to the key outcomes and challenges can be explored.

379 million doses of OPV were administered in Nigeria in 2013 during 22 SIAs and at least 200 million doses in 11 SIAs as at April 2014; this was necessary because OPV 3 coverage in 2012 was low at 59%.Citation5

Campaigns are usually conducted without screening for immunodeficient states like HIV, and although it has been proven that HIV positive children shed OPV virus for a longer time than immunocompetent children, studies suggest there is minimal risk of outbreaks of Vaccine derived polio viruses (VDPVs) and as such pose little threat post-elimination.Citation19,Citation20 Another common cause of immunodeficiency in African and Nigerian children is malnutrition, and this has been shown not to affect the seropositivity for antibodies to polio viruses.

The vaccines used for vaccination campaigns in Nigeria are trivalent OPV (tOPV) in SIAs and for outbreak response, monovalent OPV (mOPV) 1 and 3 since 2006, whereas bivalent OPV (bOPV) was introduced in 2010. While there is a fear that immunisation campaigns cause VDPVs to persist and circulate, studies have shown that they do not persist for extended periods and with concomitant IPV administration, this risk is offset. More importantly, low immunization coverage due to poor routine or supplemental immunization activities have been established to be the primary reasons of emergence of VDPVs.Citation21,Citation22

The choice of vaccines has also been found to impact on the seroprevalence among children, of antibodies against the WPV. A study in Zaria, North Western Nigeria found seroprotective titres (a titre of >1:8) in 86.4, 76.1 and 77.3% of children against WPV 1, 2 and 3 respectively. Less than 2 thirds of the children assessed had antibodies against all 3 polio viruses.Citation23 The findings were similar to those in Kano where 2 age groups were studied; infants 6 to 9 months; and children 36–47 months of age. The children had seroprotection of 91%, 87 and 86% against type 1,2 and 3 respectively while for infants it was lower although the pattern of protection was similar, type 1 having the highest protection with type 3 the lowest.Citation1 But what factors are responsible for these sub optimal levels of protection?

The key issues in polio persistence in Nigeria were elucidated by Mangal et al in the Lancet, mainly:Citation24

  • Higher incidence in the north of Nigeria of enteric infections, including other enteroviruses, which might interfere with the response to the vaccine

  • Lack of availability of immunization via the routine Expanded Program on Immunization

  • Ignorance of the importance of routine immunisations.

According to authors, Nigeria was key to poliomyelitis elimination in Africa and possibly the world. The introduction of IPV might help to sustain immunity against serotype 2, while accelerating the eradication of the remaining type 1 and 3 wild polioviruses.Citation24

At a population level, however, prominent among the reasons for low vaccination coverage was the spate of vaccine refusals in Northern Nigeria.Citation24

Vaccine refusal in Northern Nigeria

Vaccine refusal is a challenge that is not unique to Northern Nigeria. This has been the case for Tetanus Toxoid in other parts of the world and rejection of vaccines containing thiomersal in Europe.Citation25 However, a high rate of vaccine scepticism and hesitancy from vaccine rumours led to suspension of polio vaccination in Kano state of Northern Nigeria in 2003, resulting in massive outbreaks up till 2006 and importation into at least 20 previously polio free countries. These set the GPEI back at least 500 million dollars in additional SIA funding and other outbreak activities. Another such event would be devastating for the polio end game which is why lessons need to be learnt from those events.

Muslim religious and political leaders in Northern Nigeria brought the polio eradication drive to a stand-still in 2003 in response to fears from some communities that the vaccines were deliberately contaminated with anti-fertility agents and the HIV virus. The allegations were made by the Supreme Council for Sharia in Nigeria (SCSN) which was established by the Zamfara state legislature in Nigeria, following the adoption of the sharia legal code in the state in 1999. They alleged that the PEI was a plot by western governments to reduce Muslim populations worldwide. However none of such allegations and rumors were found to be true or based on any scientific merit.

They investigated and found traces of estradiol in the vaccines, although this was contrary to the findings of a team by the Nigerian Federal government. Sixteen months later however, vaccinations were resumed after procurement was made from Biopharma; an Indonesian vaccine company, and pressure from the international Muslim community including the organization of Islamic countries (OIC), Islamic fiqh council and the Arab league.Citation26

The process involved extensive diplomacy driven by the World Health Organization, where public health was enmeshed with thorny ethno religious and political issues. While the boycott was officially ended, it was only part of the job done, as sections of the population remained disaffected.Citation27 Part of the reasons they adduced were questions from the largely uneducated populace on the reasons for enormous expenditure on polio where basic necessities of life are lacking, and the focus on polio when presumably more deadly diseases like malaria and measles abound.Citation28

Among the lessons learned from the episode in Nigeria as analyzed by Ghinnai et alCitation29 include:

  • The role of prominent people and opinion leaders in the society in public health debates cannot be underestimated.

  • Locally based risk assessments should be carried out and routinely factored into vaccination programmes.

  • Vaccination programmes and other public health interventions should be devoid of political considerations.

Conclusion

The drive to eliminate polio from Nigeria is of strategic importance to the global polio eradication initiative because most importations of polio into non endemic regions from the last decade have been traced to Nigeria, leading to global spread of polio. In view of this fact, as evident in the literature review, Nigeria has overcome several unique challenges over the past several decades to finally eliminate polio from the country, but a strong vigil towards early detection and effective response to any reemergence of wild virus circulation, and stopping all vaccine derived viruses will be key to the maintenance of its polio-free status.

There have been several innovations tailored toward addressing the real world challenges with remarkable success, but the ultimate goal of sustaining elimination would require carrying the momentum forward with focus on improving quality of immunization programs and disease surveillance strategies.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

References

  • Iliyasu Z, Nwaze E, Verma H, Mustapha AO, Weldegebriel G, Gasasira A, Sutter RW. Survey of poliovirus antibodies in Kano, Northern Nigeria. Vaccine 2014; 32(12):1414-20; PMID:24041545; http://dx.doi.org/10.1016/j.vaccine.2013.08.060
  • CDC. Outbreaks following wild poliovirus importations — Europe, Africa, and Asia, January 2009 – September 2010. Morb Mortal Wkly Rep 2012; 59(43):PMID:22647710
  • WHO. WHO, Progress towards poliomyelitis eradication in Nigeria, January 2012–September 2013. Wkly Epidemiological Record 2013; 51-52(88):545-56
  • Nathanson N, Kew OM. From emergence to eradication: the epidemiology of poliomyelitis deconstructed. Am J Epidemiol 2010; 172(11):1213-29; PMID:20978089; http://dx.doi.org/10.1093/aje/kwq320
  • Moturi EK, Porter KA, Wassilak SGF, Tangermann Rudolf H, Diop OM, Burns CC, Jafari H. Progress toward polio eradication — worldwide, 2013–2014. Morb Mortal Wkly Rep 2014; 63(21):468-72; PMID:24871252
  • Mundel T, Orenstein WA. No country is safe without global eradication of poliomyelitis. New Engl J Med 2013; 369(21):2045-6; PMID:24256383; http://dx.doi.org/10.1056/NEJMe1311591
  • Global Polio Eradication Initiative (GPEI). Global polio eradication initiative status report 30 April 2014. 2014.
  • Roberts L. Vaccine-related polio outbreak in Nigeria Raises concerns. Science 2007; 317( September):2007; PMID:17901301; http://dx.doi.org/10.1126/science.317.5846.1842
  • Bhutta ZA. The last mile in global poliomyelitis eradication. Lancet 2011; 378(9791):549-52; PMID:21664681; http://dx.doi.org/10.1016/S0140-6736(11)60744-7
  • National Primary Healthcare Development Agency (NPHCDA). 2014 Nigeria polio eradication emergency plan. 2014; ( December 2013):1-69.
  • Arita I, Nakane M. Road map for polio eradication–establishing the link with Millennium Development Goal no. 4 for child survival. Jap J Infect Dis 2008; 61(3):169-74. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/18503163; PMID:18503163
  • Jenkins HE, Aylward RB, Gasasira A, Donnelly CA, Mwanza M, Corander J, Grassly NC. Implications of a circulating vaccine-derived poliovirus in Nigeria. New Engl J Med 2010; 362(25):2360-9; PMID:20573924; http://dx.doi.org/10.1056/NEJMoa0910074
  • Heymann DL, Sutter RW, Aylward RB. A vision of a world without polio: the OPV cessation strategy. Biol: J Int Assoc Biol Stand 2006; 34(2):75-9; PMID:16682224; http://dx.doi.org/10.1016/j.biologicals.2006.03.005
  • Tomori O. From smallpox eradication to the future of global health: innovations, application and lessons for future eradication and control initiatives. Vaccine 2011; 29 Suppl 4:D145-8; PMID:22185830; http://dx.doi.org/10.1016/j.vaccine.2011.09.003
  • National Primary Health Care Development Agency. (2012). National routine immunization strategic plan:12-14.
  • Okeibunor JC, Akanmori BD, Balcha GM, Mihigo R, Vaz RM, Nshimirimana D. Enhancing access to immunization services and exploiting the benefits of recent innovations in the African region. Vaccine 2013; 31(37):3772-6; PMID:23800541; http://dx.doi.org/10.1016/j.vaccine.2013.06.038
  • Kamadjeu R. Tracking the polio virus down the Congo River: a case study on the use of Google Earth in public health planning and mapping. Int J Health Geographics 2009; 8:4; PMID:19161606; http://dx.doi.org/10.1186/1476-072X-8-4
  • Richardson G, Linkins RW, Eames MA, Wood DJ, Campbell PJ, Ankers E, Minor PD. Immunogenicity of oral poliovirus vaccine administered in mass campaigns versus routine immunization programmes. Bull World Health Org 1995; 73(6):769-77. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2486680&tool=pmcentrez&rendertype=abstract; PMID:8907770
  • Hennessey KA, Lago H, Diomande F, Akoua-koffi C, Caceres VM, Pallansch MA, Zuber PLF. Poliovirus vaccine shedding among persons with HIV in Abidjan. J Infect Dis 2005; 192(12):2124-2128
  • Manirakiza A, Picard E, Ngbale R, Menard D, Gouandjika-Vasilache I. OPV strains circulation in HIV infected infants after National Immunisation Days in Bangui, Central African Republic. BMC Res Notes 2010; 3( October 2001):136; PMID:20482773; http://dx.doi.org/10.1186/1756-0500-3-136
  • Troy SB, Ferreyra-Reyes L, Huang C, Mahmud N, Lee Y-J, Canizales-Quintero S, Maldonado Y. Use of a novel real-time PCR assay to detect oral polio vaccine shedding and reversion in stool and sewage samples after a mexican national immunization day. J Clin Microbiol 2011; 49(5):1777-83; PMID:21411577; http://dx.doi.org/10.1128/;JCM.02524-10
  • Más Lago P, Cáceres VM, Galindo MA, Gary HE, Valcarcel M, Barrios J, de Quadros CA. Persistence of vaccine-derived poliovirus following a mass vaccination campaign in Cuba: implications for stopping polio vaccination after global eradication. Int J Epidemiol 2001; 30(5):1029-34. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11689516; PMID:11689516; http://dx.doi.org/10.1093/ije/30.5.1029
  • Giwa FJ, Olayinka AT, Ogunshola FT. Seroprevalence of poliovirus antibodies amongst children in Zaria, Northern Nigeria. Vaccine 2012; 30(48):6759-65; PMID:23000220; http://dx.doi.org/10.1016/j.vaccine.2012.09.023
  • Mangal TD, Aylward RB, Mwanza M, Gasasira A, Abanida E, Pate MA, Grassly NC. Key issues in the persistence of poliomyelitis in Nigeria: a case-control study. Lancet Glob Health 2014; 2:e90-97; PMID:25104665; http://dx.doi.org/10.1016/S2214-109X(13)70168-2
  • Clements CJ, Greenough P, Shull D. How vaccine safety can become political–the example of polio in Nigeria. Current Drug Safety 2006; 1(1):117-9. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/18690921; PMID:18690921; http://dx.doi.org/10.2174/157488606775252575
  • Yahya M. Polio vaccines- no thank you! Barriers to polio eradication in Northern Nigeria. African Affairs 2007; 106(423):185-204; http://dx.doi.org/10.1093/afraf/adm016
  • Kaufmann JR, Feldbaum H. Diplomacy and the polio immunization boycott in Northern Nigeria. Health Affairs (Project Hope) 2009; 28(4):1091-101; PMID:19597208; http://dx.doi.org/10.1377/hlthaff.28.4.1091
  • Renne E. Perspectives on polio and immunization in Northern Nigeria. Social Science & Medicine (1982) 2006; 63(7):1857-69; PMID:16765498; http://dx.doi.org/10.1016/j.socscimed.2006.04.025
  • Ghinai I, Willott C, Dadari I, Larson HJ. Listening to the rumours: what the northern Nigeria polio vaccine boycott can tell us ten years on. Global Public Health 2013; 8(10):1138-50; PMID:24294986; http://dx.doi.org/10.1080/17441692.2013.859720
  • Bandyopadhyay, Ananda S., et al. Polio vaccination: past, present and future. Future Microbiology 2015; 10(5):791-808.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.