Sero-prevalence study to determine the effectiveness of Peste de Petits Ruminants vaccination in Somalia

Sero-prevalence study to determine the effectiveness of Peste de Petits Ruminants vaccination in... Peste de Petits Ruminants (PPR) is an acute or sub-acute highly contagious viral disease of small ruminants caused by morbillivirus and associated with high mortality and morbidity rates in naïve populations, colossal economic losses, reduced production and productivity as well as high control costs. Sero-surveys conducted in Somalia between 2006 and 2009 revealed sero-prevalence of 6.5% in north-western Somalia, 28.7% in north-eastern Somalia, 32.6% in central Somalia and 37.6% in southern Somalia. Somalia, like other countries in conflict, has limited capacity to control PPR. In this regard, Food and Agriculture Organisation of the United Nations (FAO) conducted country-wide PPR vaccination campaigns covering the five zones of Somalia, namely, Banadir, central, north-eastern, north-western and southern using a public-private partnership approach. Approximately 20 million sheep and goats constituting 60% of the estimated Somalia national small ruminant population were targeted for vaccination in entire Somalia in 2012. Data on vaccination was captured using FAO’s Form Monitoring Tool (FMT) software. The overall unit cost of PPR vaccination was estimated to be USD 0.28 per animal. Two serological surveys were conducted before and after the vaccination campaigns where a two-stage cluster sampling methodology was used to collect sera samples for analysis. The results showed an overall increase in individual animal sero-prevalence from 62 to 76% after PPR vaccination campaign. This paper primarily focuses on practicality of PPR control in Somalia, a conflict-affected and fragile zone, which can be adopted by other countries. Keywords: Somalia, PPR, Vaccination, Sero-prevalence, Cost of disease control Introduction increased vulnerability to shocks as reported during the Peste de Petits Ruminants (PPR) is an acute or sub-acute PPR outbreak in Kenya (FAO 2009a, b). In addition, the highly contagious viral disease of small ruminants disease is a major impediment to attaining a major glo- caused by morbillivirus. The disease affects both goats bal development objective to eradicate extreme poverty and sheep; however, goats are considered more suscep- and hunger. tible than sheep (Gargadennac and Lalanne 1942). The PPR was first recorded by Gargadennac and Lalanne disease is associated with high mortality and morbidity (1942) in Cote d’Ivoire, West Africa, and has since rates in naïve populations (Kaukarbayevich 2009), colos- widely spread in other parts of Africa and Asia (Taylor sal economic losses (Couacy-Hymann et al. 1995), et al. 1990; Banyard et al. 2010; Munir et al. 2013). In reduced production, productivity as well as high control the Greater Horn of Africa region, PPR outbreaks were costs (FAO 2010). PPR negatively affects livelihoods reported in Sudan, Ethiopia, Somalia and Kenya (Diallo through diminished and complete loss of incomes and 1988; Roeder et al. 1994; Karimuribo et al. 2008 and Kihu et al. 2012). In Somalia, there were unconfirmed PPR outbreaks but sero-surveys conducted between 2006 * Correspondence: Sophycate.Njue@fao.org and 2009 (SAHSP 2006a, b, 2009) revealed sero-prevalence Food and Agriculture Organisation of the United Nations (FAO), Somalia Country Office, P.O Box 30470-00100, Nairobi, Kenya of 6.5% in north-western Somalia, 28.7% in north-eastern Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 2 of 11 Somalia, 32.6% in central Somalia and 37.6% in southern In response to the country’s needs and in line with Somalia. Although these results are inconclusive on the its mandate, FAO supported the Somalia Government frequency and distribution of PPR in Somalia, they are a in developing a 15-year phased strategy for control of good indicator of PPR virus circulation and hence PPR PPR with possible eradication (FAO 2011a, b, c) infection as reported by Waret-Szkuta et al. (2008)in under a livelihood support programme. The strategy other studies. is in line with the FAO/World Animal Health Organ- Somalia, like other countries in conflict, has limited isation (OIE) global strategy for the control and eradi- capacity to control PPR. The country is constrained by cation of PPR (FAO/OIE, 2015). The strategy outlines inadequate physical infrastructure, insufficient financial the four stages of PPR eradication in which stage 1 is resources and weak public sector-based veterinary ser- assessment stage, which includes different activities vice. This is further compounded by the fact that aiming to better understand the epidemiological situ- Somalia has a large small ruminant population associ- ation of PPR, followed by stage 2 of country-wide ated with high reproductive rate, high population turn- vaccination for control of PPR virus circulation. Stage over rate and massive cross-border movements between 3 mainly builds on stages 1 and 2 and aims at pro- Somalia/Ethiopia and Kenya. These factors are a major gressive control to a point of eradication by focussing hindrance to the implementation of a coordinated PPR on PPR vaccination backed by disease surveillance disease eradication programme. Past attempts by private and reporting in epidemiologically important areas. In sector actors to control PRR have not been very effect- stage 4, final eradication is considered. Somalia imple- ive. Unpublished reports by FAO (2001) point out ad mented a country-wide PPR vaccination campaign hoc vaccinations characterised by low vaccination cover- between 2012 which places the country at stage 2 of age and poor coordination among the stake holders. the eradication strategy. Figure 1 Map of Somalia showing the different zones Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 3 of 11 This paper seeks to contribute to the pool of know- number of vulnerable livestock-keeping households ledge on control of PPR in countries undergoing pro- and available budget. The numbers at the zonal level longed conflicts and also those with limited public were determined by the small ruminants’ population veterinary structures, considering that there is limited density, geographic distribution and frequency of re- published information available. The paper describes the ported PPR cases. All the sheep and goats belonging to mass PPR vaccination campaigns within a livelihood vulnerable livestock-keeping households were purpos- support programme framework, the suitability of vac- ivelytargetedapart from thosethatweresick, below cination as a tool for control of PPR virus circulation, three months of age or had been vaccinated previously. and also discusses the practical implications of such a Theage of theanimals wasdeterminedthrough inter- strategy in conflict-affected and fragile countries. views with targeted livestock owners and was further corroborated by use of dental formula. The vaccination Study area history was provided by the livestock owners. The study covered entire Somalia which was clustered into five zones of Banadir, central, north-eastern, north- Procurement of goods and services western and southern Somalia. The selection was based There was procurement of cold chain equipment and on sheep and goat population density, prevalence of PPR vaccines as well as constitution of vaccination Transboundary Animal Diseases (TADs) and mapping of teams prior to vaccination campaigns. The cold chain FAO-led livestock interventions. equipment consisted of large-sized and medium-sized deep freezers, cool boxes and vaccine carriers. The Methods freezers were solar powered and had provision for Selection of areas to target for PPR vaccination temperature regulation. The temperatures could be The PPR vaccination campaigns were conducted in adjusted for storage of vaccine and serum sample as well the five zones of Somalia namely Banadir, central, as making ice blocks that were used for the cool boxes. north-eastern, north-western and southern as shown In addition, approximately 20 million doses of freeze- in Figure 1. The entire country was chosen because dried live attenuated PPR vaccine strain Nigeria 75/1 first, there were many isolated PPR disease outbreaks strain were competitively procured from a Jordan Bio- reported throughout the country (Wamwayi et al. 1995). Industries Center(JOVAC®) with support of FAO. This Second, sheep and goats are kept under agro-pastoral and vaccine is certified by the African Union’s Pan African pastoral systems where they move freely within the coun- Veterinary Vaccine Centre (AU/PANVAC), the only or- try and across borders, thus increasing the likelihood of ganisation mandated to provide international independ- PPR spread in times of outbreaks. Third, PPR is endemic ent quality control of veterinary vaccines used in African in neighbouring Kenya and Ethiopia which puts all the countries. The vaccines were delivered directly in Somalia animals in Somalia at risk. after which they were inspected, before distribution for storage in the cold chain hubs. The vaccines were stored Selection of targeted population and transported at between + 2 and + 8 °C, from the hubs Approximately 20 million sheep and goats constitut- to the vaccination sites in cool boxes and vaccine carriers. ing 60% of the estimated Somalia national small ru- The cool boxes and vaccine carriers were replenished with minant population were targeted for vaccination in ice blocks every two to three days. The Livestock Profes- entire Somalia in 2012. Table 1 shows the distribution sional Associations (LPAs), namely South West Livestock of sheep and goats targeted for PPR vaccination by Professional Association (SOWELPA, Central Region Live- geographic zones. stock Professional Association (CERELPA), Banadir Region The number of small ruminants targeted for PPR Livestock Professional Association (BENALPA) and Minis- vaccination at the national level was based on the tries responsible for livestock in north-eastern and north- western zones, were also identified and contracted to con- Table 1 Number of sheep and goats targeted during PPR duct PPR vaccination campaigns based on technical ex- vaccination campaign in Somalia 2012 pertise, past records of successful implementation of Zones Total animal targeted vaccination campaigns and operational presence. Banadir 150,000 Central Somalia 6,000,000 Organisation of PPR vaccination campaigns The vaccination team leaders were taken through a one- Southern Somalia 6,000,000 day refresher training on planning and management of North-eastern Somalia 4,000,000 PPR vaccination campaigns. The record keepers were North-western Somalia 4,000,000 trained on vaccination field data capture using Form Total 20,150,000 Monitoring Tool (FMT) software for a period of 60 Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 4 of 11 working days. Further, the team members were also vaccination, as well as collection of serum samples taken through a refresher training on procedures of from sheep and goats. serum sample collection and proper sample labelling. The field activities were monitored by officers of the During this training, emphasis was put on the import- Ministries responsible for livestock in the five targeted ance of cold chain management. These trainings were zones. The process entailed visiting vaccination sites conducted by FAO technical staff in Garowe for north- and enquiring from community leaders and targeted eastern zone and Hargeisa for north-western zone. For households about the vaccination campaign and sero- the Banadir, central and southern zones, the trainings logical survey. Likewise, FAO technical staff and field were conducted in Nairobi, Kenya. monitors carried out independent monitoring through The vaccination teams were equipped with cold field visits, collection of data using pre-designed ques- chain equipment, vaccines, veterinary supplies and tionnaires and call centre surveys. This was in addition equipment, and facilitated with transport. They were to progress reports and photographic evidence on the also provided with pre-designed data entry sheets and implementation of the activities submitted by the laptops for the management of surveillance and vac- vaccination teams. cination data. Each team prepared a detailed work plan covering the entire vaccination period. The plans were shared with clan leaders, village elders and local Serological surveys authorities during community awareness creation and Two serological surveys were conducted. The first one sensitization. The awareness creation fora provided an was conducted in March 2012 and the second in opportunity to emphasise the importance of the September 2012. The sample size was calculated based vaccination campaign and collect important village on the percentage of the total number of animals tar- contact details. geted for vaccination. A two-stage cluster sampling methodology was used whereby a total of 18,377 sera samples were randomly collected from small ruminants, Implementation of PPR vaccination campaign representing 0.1% of the total number of the animals tar- The vaccination teams were deployed in the field from geted for vaccination. Table 2 illustrates the number of March to May 2012 for a period of 60 working days. serum samples taken during the serological surveys. Each team was required to vaccinate a minimum of Bloodwas drawnfromthejugular veininplain 2,500 sheep and goats daily apart from Banadir region 10-ml vacutainer tubes, kept in a cool place for up which had lower daily targets of 500 animals. Banadir to 24 h to allow for clotting. Then, sera were dec- was exceptional because it is peri-urban, and there anted into two aliquots which were then transferred was a challenge of gathering animals together for into 5-ml pre-labelled cryovials. The cryovials were vaccination. properly labelled to ensure quick identification of Full consent of the Somali veterinary authorities the sample by region, district, team and chrono- was sought before carrying out the PPR vaccination logical numbering of every sample. Every sample campaign, collection of disease surveillance data and collected was recorded in pre-designed recording the serological surveys. The authorities granted per- sheets. Sera were then stored in ice-filled cool boxes mission to collect and test field laboratory samples. for a period of two to three days until their transfer High levels of quality and integrity were observed to deep freezers where they were stored at − 20 °C. during the fieldwork. The livestock keepers were also The sera were subsequently airlifted from Somalia to sensitised prior to the field interventions after which AU-PANVAC laboratories in Ethiopia in August they voluntarily presented and participated in the 2014 for serological analysis. Table 2 Number of serum samples taken before and after PPR vaccination campaigns in Somalia, 2012 Zones Number of animals vaccinated Number of pre-vaccination Number of post-vaccination Total number of sera samples sera samples collected sera samples collected Banadir 148,100 88 168 256 Central Somalia 5,824,724 2,294 3,750 6,044 Southern Somalia 5,953,821 2,996 4,711 7,707 North-eastern Somalia 3,750,466 1,056 1,408 2,464 North-western Somalia 3,989,736 1,300 606 1,906 Total 19,666,847 7,734 10,643 18,377 Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 5 of 11 The Competitive Enzyme-Linked Immunosorbent vaccines, cold chain equipment, vaccination supplies and Assay (c-ELISA), the test recommended by OIE equipment. Other requirements that were costed in- (2004), was used for PPR diagnoses. Serum samples cluded transport for the vaccination teams, time dedi- were tested for IgG PPR antibodies using monoclonal cated to vaccination campaigns by the vaccination antibody-based c-ELISA directed against nucleopro- teams, capture of field data, analyses of serum samples, tein (N protein) as described by Libeau et al. (1995). monitoring the vaccination campaigns and cold chain Any serum samples with a percentage inhibition value maintenance. equal to or greater than 50% were considered positive Hence: for PPR. The laboratory test results were released in January 2015. Total cost of the vaccinationðÞ TCV ¼ðÞ Cost of establishing and maintaining cold chain Data analysis þðÞ Cost of procuring PPR vaccines The vaccination data was analysed using Form Moni- toring Tool (FMT) software and thereafter exported to þðÞ Cost of procuring vaccination supplies and equipment Microsoft® Excel 2013 (Microsoft Inc. USA) for the þðÞ Cost of services for vaccine delivery computation of summary statistics which were presented in form of tables. The Ascent™ Software from Thermo The unit cost of vaccination was calculated as follows: Scientific™ was used to generate sero-prevalence results from the ELISA reader. Data were then exported to Microsoft® Excel 2013 (Microsoft Inc. USA), to enable Total cost of vaccinationðÞ TCV =number of animals vaccinated: generation of preliminary sero-prevalence frequency tables. The sero-prevalence estimates were derived using the formula: Results P ¼ðÞ y=n  100 Positioning of vaccination teams, cold chain equipment and PPR vaccines where y denoted the total number of samples testing A total of 140 teams from livestock professional positive for PPRV antibodies and n was the sample size associations and Ministries responsible for livestock (Thrusfield 2005). were deployed in the five zones to conduct the vaccin- This formula was applied in calculating zone-specific ation campaign. Each team was comprised of five as well as country-wide sero-prevalence values. Subse- members that included four livestock professionals quent analyses for homogeneity between pre- and post who were either veterinarians or veterinary parapro- PPR vaccination sero-prevalence values was done using fessionals and a record keeper. The team leaders were Mantel Hensel test in Stata® Statistical Software, Release veterinarians. The Federal Government of Somalia, 13 (StataCorp 2013). The Mantel-Haenszel chi-square represented by the Ministry of Livestock, Forestry and value tests the null hypothesis that the individual Range (MoLFR), supervised and monitored the stratum odds ratios are all equal to one versus the alter- vaccination campaign implemented by SOWELPA, native hypothesis that at least one odds ratio is different CERELPA and BENALPA. The cold chain equipment from unity. was distributed in pre-determined strategic locations closer to vaccination sites prior to commencement of Estimation of the PPR vaccination costs vaccination. The distribution of the teams, the PPR The estimation of PPR vaccination cost was based on vaccine doses and the cold chain equipment is shown the requirements that included purchase of PPR in Tables 3 and 4. Table 3 The distribution of PPR vaccine doses in the five zones according to the implementing organisations and public institutions, 2012 Zones Implementing organisations/institutions Number of vaccination teams PPR vaccine doses distributed Banadir Banadir Livestock Professional Association (BENELPA) 10 150,000 Central Somalia Central Livestock Professional Association (CERELPA) 45 6,000,000 North-eastern Somalia Ministry of Livestock and Animal Husbandry (MoLAH) 20 4,000,000 North-western Somalia Ministry of Livestock (MoL) 20 4,000,000 Southern Somalia South West Livestock Professional Association (SOWELPA) 45 6,000,000 Total 140 20, 150,000 Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 6 of 11 Table 4 Distribution of cold chain equipment in the five zones of Somalia, 2012 Zone Location of cold Large-sized deep Medium-sized deep Cool Vaccine chain hub freezers (336 l) freezers (280 l) boxes (22 l) carriers (1.6 l) Banadir Mogadishu 6 5 0 7 Central Somalia Belet Weyne 6 6 15 5 North-eastern Somalia Garowe 8 8 4 0 North-western Somalia Hargeisa 8 8 4 6 Southern Somalia Baidoa 7 8 15 8 Total 35 35 38 26 PPR vaccination coverage Pr > chi = 0.0000. The vaccination campaign implemented in the five zones of Somalia achieved an overall vaccination coverage of Since the confidence intervals did not include 1, it 97.6% (19,666,847 out of 20,150,000) goats and sheep. implied that the differences in antibody levels pre- The highest vaccination coverage was 99.7% in north- and post PPR vaccination could not have been by western Somalia whereas the lowest was 95.4% in central chance. There was significant difference in sero- Somalia zone. The high vaccination coverage was as a prevalence values pre- and post PPR vaccination at result of limited vaccine losses during the vaccination 95% confidence level. campaigns. This was achieved through sensitisation of livestock-keeping communities to present target animals Costs of PPR vaccination in pre-identified vaccination sites and pre-positioning of The overall cost of vaccination entailed the cost of con- cold chains in strategic field location for vaccine storage tract time by the vaccination teams, vaccines, transport, during the vaccination campaigns. The vaccination sites cold chain, field equipment, vaccination equipment and were mainly watering points and grazing sites. Table 5 other supportive services such as monitoring, data and provides a summary of vaccination coverage for each of serum collection. This was costed per animal vaccinated the five zones. as tabulated in Table 7. The cost of contract service during vaccination was Analyses of serology results USD 2,770,160 which constituted nearly 50% of the total There was an increase in sero-prevalence after PPR vaccination costs. Based on the number of sheep and vaccination campaign. The serology results revealed an goats targeted for vaccination against PPR which was overall sero-prevalence of 62% (4,792/7,734) before 20,150,000, the unit cost of service delivery of the vaccination and 76% (8,089/10,643) after vaccination vaccine per animal was USD 0.14 per animal whereas at (p <005) (Table 6). The pre-vaccination sero-prevalence the estimated cost of a dose of PPR vaccine was USD was highest in north-eastern zone (74%) and lowest 0.12. The overall PPR vaccination cost per animal was in Banadir (39%), whereas the post-vaccination sero- estimated as 0.28 USD. prevalence was highest in central Somalia zone (87%) and lowest in Banadir (58%). The results of Mantel Hensel test of homogeneity at Discussion 95% confidence interval were as follows: The cold chain was an important requirement from the point of manufacture, during the transportation and Test of homogeneity Mantel-Haenszel Chi2 (1) = 753.57 storage to the point of vaccine use. The cold chain equipment was appropriately positioned in the field Table 5 Analyses of PPR vaccination coverage in sheep and prior to the vaccination campaign to ensure the storage goats in the five zones of Somalia, 2012 temperatures of between + 2 and + 8 °C were main- Zones Total animal Total animal % coverage of tained. Where cold chain equipment was insufficient, targeted vaccinated the targets prior arrangements were made to use the cold chain Banadir 150,000 148,100 98.7 facilities from organisations providing health services in Central Somalia 6,000,000 5,824,724 95.4 Somalia. To overcome challenges of electric power supply, solar-powered freezers were supplied in the five Southern Somalia 6,000,000 5,953,821 99.2 zones. Solar-powered refrigeration has been used for North-eastern Somalia 4,000,000 3,750,466 96.2 vaccine storage by United Nations Children Fund North-western Somalia 4,000,000 3,989,736 99.7 (UNICEF) mainly in Africa where other sources of reliable Total 20,150,000 19,666,847 97.6 electricity are inadequate or costly (McCarney et al. 2013). Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 7 of 11 Table 6 Analyses of PPR serum samples collected from small ruminants before and after PPR vaccination in the five zones in Somalia, 2012 Zones Pre-vaccination Post-vaccination No. of samples tested % PPR sero-prevalence No. of samples tested % PPR sero-prevalence Banadir 88 39 168 58 Central Somalia 2,294 73 3,750 87 Southern Somalia 2,996 56 4,711 82 North-eastern Somalia 1,056 74 1,408 79 North-western Somalia 1,300 66 606 73 Total 7,734 62 10,643 76 The PPR disease control strategy in Somalia was ini- following up on young animals between four months and tially though country-wide vaccination campaigns, the one year in age (FAO/OIE 2015). Considering the pre- method prescribed for the control of PPR in endemic dominant extensive and mobile livestock production sys- countries (Diallo 2004). Vaccinating a large number of tems in Somalia, vaccination is still an effective control animals minimises the spread of the PPR by decreasing measure of PPR despite the inherent challenges of the effective contact rate. Despite the immense socio- large sheep and goat populations, high reproductive rates political challenges existing currently in Somalia, nearly exemplified by short gestation period and high twinning 20 million small ruminants distributed across the coun- percentage as well as high turnover. The PPR vaccinations try were immunised achieving an overall vaccination conducted in Somalia has reduced the disease incidence coverage of 97.6%, placing Somalia among the first coun- to a level where relatively small-scale targeted vaccination tries in the Horn of Africa to implement a country-wide can be carried out in line with the time-bound PPR PPR vaccination campaign of such magnitude. This level disease control strategy for Somalia (FAO 2011a, b, c). of coverage is much higher than the average annual vac- The large-scale vaccination has reduced the effective con- cination coverage of 15% reported to World Animal tact rate, thus curbing the spread of PPR among the small Health Organisation (OIE) by PPR-infected countries, ac- stock. Moreover, such vaccination campaigns have been cording to a study by Jones et al. (2016). In the Greater reported to reduce the socio-economic impact of PPR Horn of Africa region, Kenya vaccinated an estimated two (Jones et al. 2016). million goats and sheep against PPR in 2006 in Turkana The serology survey results from the analyses of 7,734 County (Kihu et al. 2015a, b). According to studies by serum samples collected from sheep and goats before Singh (2011), 85.4% vaccination coverage is necessary for the PPR vaccination revealed an overall individual ani- control of PPR infection in sheep population. mal sero-prevalence of 62% with a low of 39% and a high Vaccination has been described as the preferred tool for of 74% in Banadir zone and north-eastern zone respect- controlling and eradicating PPR, especially in countries ively. These values are high compared to those recorded where it is difficult to control animal movement (Jones et in a baseline PPR sero-survey conducted by Somali al. 2016). Ideally, the PPR vaccination should be time- Animal Health Services Project (SAHSP) in Somalia be- limited with high coverage to achieve the necessary herd tween 2001 and 2007 which gave a low of 6.5% in north- immunity in high-risk areas. The PPR Global Eradication western zone and a high of 37.6% in southern Program recommends two-year vaccination campaigns Somalia (SAHSP 2006a, b, 2009). The overall indi- vidual animal pre-vaccination sero-prevalence was also relatively higher compared to 35.5% reported in Table 7 Analyses of estimated cost of PPR vaccination studies by Chavan et al. (2009) in India and 46.5% campaigns and serological Survey in Somalia, 2012 Ekue et al. (1992) in Cameroon. In Ethiopia, an Description of activity Amount USD overall individual animal sero-prevalence of 30.9% Procurement of PPR vaccine 2,414,040 was reported in a study by Megersaa et al., 2011.Other Contract service fee for vaccine delivery 2,770,160 studies conducted in the Somali region of Ethiopia, an area Procurement and maintenance of cold chain 392,933 under pastoral management system, gave a sero-prevalence of 21.3% at 95% confidence level (Waret-Szkuta et al. 2008). Serum sampling and testing 70,522 The high pre-vaccination sero-prevalence of PPR in Total 5,647,655 Somalia can be attributed to increased PPR virus circula- No. of animals targeted against PPR 20,150,000 tion as illustrated by the confirmed PPR outbreaks by Cost of vaccinating one animal 0.28 SAHSP between 2005 and 2009 (SAHSP 2009), taking Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 8 of 11 into consideration that the past vaccination attempts by Faris et al. (2012) in a cross-sectional epidemiological have been on a small scale and largely uncoordinated study conducted in selected districts in Ethiopia. A simi- (FAO 2001). This corroborates work by Waret-Szkuta et lar vaccine made from the same Nigeria 75/1 strain from al. (2008) who in their study concluded that high anti- National Veterinary Institute in Debre-Zeit, Ethiopia, body levels in small ruminant population with minimal gave a relatively lower post vaccination seroconversion vaccination coverage is due to a circulating PPR virus. of 61%, which was attributed to the poor handling of the Considering the high reproductive rate, uncontrolled cold chain Faris et al. (2012). movements and high turnover of small stock in Somalia, The overall unit cost of PPR vaccination in Somalia, an antibody prevalence of 62% is unlikely to offer pro- 2012, was estimated as USD 0.28 per animal. This is tection and prevent further epidemics. much less than the overall individual animal vaccination The results of 10,643 serum samples collected after cost for Rinderpest from a study by (Tambi et al. 1999) the PPR vaccination campaign showed an increase in which estimated the individual animal vaccination cost herd immunity from 62 to 76% at (p < 005). There is an as ECU 0.42 equivalent of USD 0.51 based on average argument by Inter Government Authority for Develop- ECU value between 1989 and 1996. In the same study, ment (IGAD) that due to the high annual turnover of unit cost of Rinderpest vaccination in Ethiopia was esti- the small ruminants, the herd immunity threshold is un- mated as ECU 0.27 (USD 0.33) and this relatively low likely to increase by using repeated annual vaccination, unit cost was attributed to economies of scale. The esti- and instead, large numbers of vaccinations should be mated cost of a dose of PPR vaccine in Somalia was delivered in a short time period under targeted vaccin- USD 0.12 which compares favourably with the USD 0.10 ation programmes (IGAD-2014). A sero-epidemiological reported by Jones et al. (2016) in other parts of Africa. survey in Turkana, Kenya, by Kihu et al. (2015a, b) con- However, the unit cost of service delivery of the PPR firms that high demographic changes reduce the PPR vaccine per animal was different. In Somalia, it was USD herd immunity of small ruminants with introduction of 0.14 per animal which was much lower than USD 0.3 naïve and vulnerable weaned kids and lambs that have estimated by Jones et al. (2016). This could have been decreasing maternal immunity into the already immu- due to the economy of scale, considering that nearly 20 nised herd. Studies by Ata et al. (1989) and Bidjeh et al. million sheep and goats were vaccinated against PPR (n.d.) have shown that maternal antibodies in young ani- disease. The differences could have also arisen due to mals are detectable up to six months of age and fall different ways of costing the service delivery. In the below the protection threshold level at 3.5 and 4. Somalia study, the cost of service delivery was calculated 5 months in lambs and kids, respectively. Therefore, an- based on the cost of personnel time and the transport nual PPR vaccination campaigns targeting middle age costs during data and serum collection. The procure- group can improve the herd immunity to levels that can ment of vaccine increased the total cost of vaccination. contain spread of the PPR disease (Kihu et al. 2015a, b). In this study, it constituted 50% of the total vaccination Outcomes of two studies by Singh (2011) and Balamurugan cost. One way of reducing this cost is vaccinating against et al. (2014) elucidate that PPR mass vaccination campaigns more than one disease that is prevalent in the area. The that achieve 70 to 80% levels of herd immunity threshold control of sheep and goat pox and contagious caprine break the effective transmission of the virus irrespective of pleuropneumonia diseases could be done alongside PPR the population dynamics, disparities in husbandry practices disease (Kumar et al. 2014; FAO/OIE 2015). and the agro-climatic conditions affecting the pattern of disease. In essence within this herd immunity threshold range, there is sufficient proportion of immune small Conclusions and recommendations ruminant population for PPR virus to become stable as all This paper has provided a detailed account of a success- the vaccinated, infected and recovered animals are pro- ful mass PPR vaccination in Somalia. It has brought out tected (Balamurugan et al. 2014). The herd immunity practical implications of PPR control in a conflict- threshold for Rinderpest, which is closely related to PPR, affected and fragile country that can be adopted by other was estimated as 75 to 80% (Rossiter and James 1989). countries. PPR vaccination campaigns in such countries There was significant difference in sero-prevalence characterised by limited public veterinary personnel can values pre- and post PPR vaccination at 95% confidence be implemented through involvement of private live- level which gave a Mantel-Haenszel chi2 (1) of 753.57 stock professional organisations which have operational Pr > chi = 0.0000. All the zones had antibodies greater presence and technical capabilities. In Somalia, the than 76% except Banadir and north-western zones that Livestock Professional Associations in Banadir, central had sero-prevalence values of 58 and 73% respectively. and southern Somalia and the Ministries responsible for The overall post vaccination serum antibody level ob- livestock in the north-eastern and north-western Somalia served in Somalia was much higher than that observed were contracted to carry out the mass vaccination Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 9 of 11 campaigns, which built confidence and improved goodwill understanding of the role of wild and other domestic with pastoral communities. ruminants in the maintenance of peste des petits rumi- Mass vaccination against PPRV in countries endemic nants virus (PPRV). with PPR controls the virus circulation in the small Abbreviations ruminant population to a level where targeted vaccin- AU-PANVAC: African Union’s Pan African Veterinary Vaccine Centre; ation can be considered. Vaccinations carried out before BENALPA: Banadir Livestock Professional Association; c-ELISA: Competitive the expected seasonal movements enhance vaccination Enzyme-Linked Immunosorbent Assay; CERELPA: Central Region Livestock Professional Association; ELISA: Enzyme-Linked Immunosorbent Assay; coverage. Although funding sources for a PPR disease FAO: Food and Agriculture Organisation of the United Nations; FMT: Form control programmes are limited in most developing Monitoring Tool; IGAD: Inter Governmental Authority for Development; countries, Somalia successfully vaccinated nearly 20 mil- JOVAC: Jordan-based Vaccine Production Company; MoLAH: Ministry of Livestock and Animal Husbandry; MoLFR: Ministry of Livestock, Forestry and lion sheep and goats against PPRV within a livelihood Range; OIE: World Animal Health Organisation; PPR: Peste de Petits Ruminants; support programme framework. The capacity of public PPRV: Peste de Petits Ruminants Virus; SAHSP: Somalia Animal Health Project; and private veterinary services in Somalia was enhanced SOWELPA: South West Livestock Professional Association; TCV: Total cost of the vaccination; UNICEF: United Nations Children Fund through country-wide provision of cold chain facilities and vaccination equipment, which is anticipated to fur- Acknowledgements ther reduce the cost of vaccination delivery in the future. The support of the Ministries responsible for livestock in Somalia to allow the Furthermore, where there was insufficient cold chain, ar- work to be carried out in Somalia and the paper to be published is highly rangements were put in place to share cold chain facil- acknowledged. The authors give thanks to Somalia livestock owners for their cooperation during serum sample collection. The authors give many thanks ities between human and animal vaccines under the to the veterinarians and animal health auxiliaries in Somalia for their support “One Health” programme which reduced the frequency during the field work. The authors give gratitude to Mr. Daniela Donati, FAO of replenishing the ice-packs to two to three days. Des- Somalia representative (acting) in Somalia, and Mr. Rudi VanAaken, FAO Somalia Head of Programme, for their support to have the paper published. pite Somalia not having the capacity to produce PPR The technical support of Dr. Bouna Diop from FAO/OIE PPR Global vaccine, it was still possible to source a good quality vac- Secretariat and Dr. Massimo Castiello for the technical input during drafting cine certified by AU-PANVAC from external sources at of the paper is gratefully acknowledged. Many thanks to Charles Bodjo of AU-PANVAC in Addis Ababa, Ethiopia, for a competitive cost of USD 0.12. It was possible to deter- his support in analysing the serum samples. The support of Ms. Baru Adan mine the effectiveness of the mass vaccination through and Ms. Jeniffer Kariuki of FAO Somalia for their input in analysing the data two serological surveys. The cost of the pre-vaccination and producing the map is acknowledged. survey was significantly reduced by using the PPR vaccination teams to collect the sero-surveillance serum Funding This paper is based on FAO work funded by various government institutions samples prior to vaccination. The analyses of the serum and funding agencies that include Belgium, Switzerland, Australia, Spain, UK, samples were carried out at the AU-PANVAC labora- World Bank, and UN-OCHA. The findings, conclusions and recommendations tory. Somalia attained a herd immunity threshold of 76% contained are exclusively from the authors and do not in any way reflect positions or policies of FAO and the above-mentioned government through the country-wide mass PPR vaccination institutions and funding agencies. The funds were used to purchase the PPR programme of nearly 60% of the national small ruminant vaccines, supplies and equipment, contract out vaccination services and population. This was shown to stabilise the virus within supplement salaries or honoraria of the authors. There was no additional external funding received for this work. The authors are employees of FAO the target population as there were no reported clinical and were involved in the design of the vaccination campaign, data analysis, cases of the disease. decision to publish and preparation of the manuscript. The focus should therefore be to increase the herd immunity threshold to 80% as a way of reducing virus Authors’ contributions circulation, considering the high turnover, uncontrolled SN, KS, JM and CB designed the study. SN, KS and JM undertook the fieldwork. SN, SM JM and KT analysed the data and drafted the original movements and the new annual introduction of naïve manuscript with further input from KS and CB. All authors read and population. This should be achieved through annual tar- approved the final manuscript. geted vaccination based on extensive epidemiological surveillance. It will be worthwhile to target only sheep Authors’ information and goat above three months with no history of PPR SN is a veterinary epidemiologist and economist, and a postdoctoral researcher working on animal disease surveillance systems and vaccination. Further investment should be made on solar transboundary animal disease control at the Food and Agriculture of the powered cold chain facilities to increase penetration of United Nations (FAO) in Somalia. KS is a veterinarian and researcher working the vaccines to the remote rural vaccination sites. This as the livestock sector emergency and programme coordinator at the FAO in Somalia. SM is a veterinarian and postdoctoral researcher working at FAO at will not only reduce the transport cost of replenishing the time of the study and now a livestock consultant. JM is animal health the ice packs but shall also improve the seroconversion officer at FAO in Somalia and is working on tropical animal health research rates due to better cold chain maintenance. Somalia at the Institute of Tropical Medicine, Antwerp, Belgium. CB is a veterinarian and a livestock specialist working as the livestock sector coordinator at FAO should invest in laboratory facilities for confirming in Somalia at the time of the study and now working at FAO office for disease cases and monitoring PPR herd immunity levels. Central Africa. KT is an economist currently working as information and Further studies should be conducted to improve the knowledge management officer at the FAO in Somalia. Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 10 of 11 Ethics approval and consent to participate from Awash Fentale District, Afar, Ethiopia. Preventive Veterinary Medicine 103 Written approval for undertaking PPR vaccination, serum sample collection and (PubMed): 157–162. shipping of samples to PANVAC was granted by respective Ministries Gargadennac, L., and A. Lalanne. 1942. La peste des petit ruminantis. Bulletin des responsible for livestock in different regions of Somalia in 2012. The livestock Service Zootechniques et des Epizooties de l’Afrique Occidentale Francaise 5: 16–21. owners were sensitised on the importance of vaccination and serological IGAD 2014: The IGAD Regional peste des petits ruminants (PPR) progressive survey after which they gave their verbal consent for the activities to be control and eradication strategy. https://icpald.org/wp-content/uploads/ undertaken. The livestock owners were required to append their thumb print 2016/01/Progressive-Control-and-Eradication-Strategy-1.pdf. on the vaccination form as a proof of consent as most of them were illiterate. Jones B.A., Rich K.M., Mariner J.C., Anderson, J., Jeggo, M., Thevasagayam S., Cai Y., Peters, A.R., and Roeder, P. 2016. The economic impact of eradicating peste Competing interests des petits ruminants: A benefit-cost analysis. PLoS One 11 (2):e0149982. The authors declare that they have no competing interests. https://doi.org/10.1371/journal.pone.0149982. Karimuribo, E.D., Loomu, P. M., Mellau, L.S.B. and Swai, E.S. 2008. Retrospective study on sero-epidemiology of peste des petits ruminants before its official Publisher’sNote confirmation in northern Tanzania in 2008. Department of Veterinary Springer Nature remains neutral with regard to jurisdictional claims in Medicine and Public Health, Sokoine University of Agriculture, Morogoro published maps and institutional affiliations. Tanzania; Veterinary Investigation Centre (VIC), Arusha, Tanzania. http://agris.fao. org/agris-search/search.do?recordID=DJ2012071861. Accessed 14 Dec 2016. Author details Kaukarbayevich, K.Z. 2009. Epizootological analysis of PPR spread on African Food and Agriculture Organisation of the United Nations (FAO), Somalia continent and in Asian countries. African Journal of Agricultural Research 4 (9): Country Office, P.O Box 30470-00100, Nairobi, Kenya. P.O Box 4810-00506, 787–790. Available online at https://www.researchgate.net/publication/ Nairobi, Kenya. 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Peste des Petits Ruminants (PPR) in Ethiopia: Analysis of a national serological survey. BMC Veterinary Research 4: 34. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Pastoralism Springer Journals

Sero-prevalence study to determine the effectiveness of Peste de Petits Ruminants vaccination in Somalia

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Abstract

Peste de Petits Ruminants (PPR) is an acute or sub-acute highly contagious viral disease of small ruminants caused by morbillivirus and associated with high mortality and morbidity rates in naïve populations, colossal economic losses, reduced production and productivity as well as high control costs. Sero-surveys conducted in Somalia between 2006 and 2009 revealed sero-prevalence of 6.5% in north-western Somalia, 28.7% in north-eastern Somalia, 32.6% in central Somalia and 37.6% in southern Somalia. Somalia, like other countries in conflict, has limited capacity to control PPR. In this regard, Food and Agriculture Organisation of the United Nations (FAO) conducted country-wide PPR vaccination campaigns covering the five zones of Somalia, namely, Banadir, central, north-eastern, north-western and southern using a public-private partnership approach. Approximately 20 million sheep and goats constituting 60% of the estimated Somalia national small ruminant population were targeted for vaccination in entire Somalia in 2012. Data on vaccination was captured using FAO’s Form Monitoring Tool (FMT) software. The overall unit cost of PPR vaccination was estimated to be USD 0.28 per animal. Two serological surveys were conducted before and after the vaccination campaigns where a two-stage cluster sampling methodology was used to collect sera samples for analysis. The results showed an overall increase in individual animal sero-prevalence from 62 to 76% after PPR vaccination campaign. This paper primarily focuses on practicality of PPR control in Somalia, a conflict-affected and fragile zone, which can be adopted by other countries. Keywords: Somalia, PPR, Vaccination, Sero-prevalence, Cost of disease control Introduction increased vulnerability to shocks as reported during the Peste de Petits Ruminants (PPR) is an acute or sub-acute PPR outbreak in Kenya (FAO 2009a, b). In addition, the highly contagious viral disease of small ruminants disease is a major impediment to attaining a major glo- caused by morbillivirus. The disease affects both goats bal development objective to eradicate extreme poverty and sheep; however, goats are considered more suscep- and hunger. tible than sheep (Gargadennac and Lalanne 1942). The PPR was first recorded by Gargadennac and Lalanne disease is associated with high mortality and morbidity (1942) in Cote d’Ivoire, West Africa, and has since rates in naïve populations (Kaukarbayevich 2009), colos- widely spread in other parts of Africa and Asia (Taylor sal economic losses (Couacy-Hymann et al. 1995), et al. 1990; Banyard et al. 2010; Munir et al. 2013). In reduced production, productivity as well as high control the Greater Horn of Africa region, PPR outbreaks were costs (FAO 2010). PPR negatively affects livelihoods reported in Sudan, Ethiopia, Somalia and Kenya (Diallo through diminished and complete loss of incomes and 1988; Roeder et al. 1994; Karimuribo et al. 2008 and Kihu et al. 2012). In Somalia, there were unconfirmed PPR outbreaks but sero-surveys conducted between 2006 * Correspondence: Sophycate.Njue@fao.org and 2009 (SAHSP 2006a, b, 2009) revealed sero-prevalence Food and Agriculture Organisation of the United Nations (FAO), Somalia Country Office, P.O Box 30470-00100, Nairobi, Kenya of 6.5% in north-western Somalia, 28.7% in north-eastern Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 2 of 11 Somalia, 32.6% in central Somalia and 37.6% in southern In response to the country’s needs and in line with Somalia. Although these results are inconclusive on the its mandate, FAO supported the Somalia Government frequency and distribution of PPR in Somalia, they are a in developing a 15-year phased strategy for control of good indicator of PPR virus circulation and hence PPR PPR with possible eradication (FAO 2011a, b, c) infection as reported by Waret-Szkuta et al. (2008)in under a livelihood support programme. The strategy other studies. is in line with the FAO/World Animal Health Organ- Somalia, like other countries in conflict, has limited isation (OIE) global strategy for the control and eradi- capacity to control PPR. The country is constrained by cation of PPR (FAO/OIE, 2015). The strategy outlines inadequate physical infrastructure, insufficient financial the four stages of PPR eradication in which stage 1 is resources and weak public sector-based veterinary ser- assessment stage, which includes different activities vice. This is further compounded by the fact that aiming to better understand the epidemiological situ- Somalia has a large small ruminant population associ- ation of PPR, followed by stage 2 of country-wide ated with high reproductive rate, high population turn- vaccination for control of PPR virus circulation. Stage over rate and massive cross-border movements between 3 mainly builds on stages 1 and 2 and aims at pro- Somalia/Ethiopia and Kenya. These factors are a major gressive control to a point of eradication by focussing hindrance to the implementation of a coordinated PPR on PPR vaccination backed by disease surveillance disease eradication programme. Past attempts by private and reporting in epidemiologically important areas. In sector actors to control PRR have not been very effect- stage 4, final eradication is considered. Somalia imple- ive. Unpublished reports by FAO (2001) point out ad mented a country-wide PPR vaccination campaign hoc vaccinations characterised by low vaccination cover- between 2012 which places the country at stage 2 of age and poor coordination among the stake holders. the eradication strategy. Figure 1 Map of Somalia showing the different zones Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 3 of 11 This paper seeks to contribute to the pool of know- number of vulnerable livestock-keeping households ledge on control of PPR in countries undergoing pro- and available budget. The numbers at the zonal level longed conflicts and also those with limited public were determined by the small ruminants’ population veterinary structures, considering that there is limited density, geographic distribution and frequency of re- published information available. The paper describes the ported PPR cases. All the sheep and goats belonging to mass PPR vaccination campaigns within a livelihood vulnerable livestock-keeping households were purpos- support programme framework, the suitability of vac- ivelytargetedapart from thosethatweresick, below cination as a tool for control of PPR virus circulation, three months of age or had been vaccinated previously. and also discusses the practical implications of such a Theage of theanimals wasdeterminedthrough inter- strategy in conflict-affected and fragile countries. views with targeted livestock owners and was further corroborated by use of dental formula. The vaccination Study area history was provided by the livestock owners. The study covered entire Somalia which was clustered into five zones of Banadir, central, north-eastern, north- Procurement of goods and services western and southern Somalia. The selection was based There was procurement of cold chain equipment and on sheep and goat population density, prevalence of PPR vaccines as well as constitution of vaccination Transboundary Animal Diseases (TADs) and mapping of teams prior to vaccination campaigns. The cold chain FAO-led livestock interventions. equipment consisted of large-sized and medium-sized deep freezers, cool boxes and vaccine carriers. The Methods freezers were solar powered and had provision for Selection of areas to target for PPR vaccination temperature regulation. The temperatures could be The PPR vaccination campaigns were conducted in adjusted for storage of vaccine and serum sample as well the five zones of Somalia namely Banadir, central, as making ice blocks that were used for the cool boxes. north-eastern, north-western and southern as shown In addition, approximately 20 million doses of freeze- in Figure 1. The entire country was chosen because dried live attenuated PPR vaccine strain Nigeria 75/1 first, there were many isolated PPR disease outbreaks strain were competitively procured from a Jordan Bio- reported throughout the country (Wamwayi et al. 1995). Industries Center(JOVAC®) with support of FAO. This Second, sheep and goats are kept under agro-pastoral and vaccine is certified by the African Union’s Pan African pastoral systems where they move freely within the coun- Veterinary Vaccine Centre (AU/PANVAC), the only or- try and across borders, thus increasing the likelihood of ganisation mandated to provide international independ- PPR spread in times of outbreaks. Third, PPR is endemic ent quality control of veterinary vaccines used in African in neighbouring Kenya and Ethiopia which puts all the countries. The vaccines were delivered directly in Somalia animals in Somalia at risk. after which they were inspected, before distribution for storage in the cold chain hubs. The vaccines were stored Selection of targeted population and transported at between + 2 and + 8 °C, from the hubs Approximately 20 million sheep and goats constitut- to the vaccination sites in cool boxes and vaccine carriers. ing 60% of the estimated Somalia national small ru- The cool boxes and vaccine carriers were replenished with minant population were targeted for vaccination in ice blocks every two to three days. The Livestock Profes- entire Somalia in 2012. Table 1 shows the distribution sional Associations (LPAs), namely South West Livestock of sheep and goats targeted for PPR vaccination by Professional Association (SOWELPA, Central Region Live- geographic zones. stock Professional Association (CERELPA), Banadir Region The number of small ruminants targeted for PPR Livestock Professional Association (BENALPA) and Minis- vaccination at the national level was based on the tries responsible for livestock in north-eastern and north- western zones, were also identified and contracted to con- Table 1 Number of sheep and goats targeted during PPR duct PPR vaccination campaigns based on technical ex- vaccination campaign in Somalia 2012 pertise, past records of successful implementation of Zones Total animal targeted vaccination campaigns and operational presence. Banadir 150,000 Central Somalia 6,000,000 Organisation of PPR vaccination campaigns The vaccination team leaders were taken through a one- Southern Somalia 6,000,000 day refresher training on planning and management of North-eastern Somalia 4,000,000 PPR vaccination campaigns. The record keepers were North-western Somalia 4,000,000 trained on vaccination field data capture using Form Total 20,150,000 Monitoring Tool (FMT) software for a period of 60 Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 4 of 11 working days. Further, the team members were also vaccination, as well as collection of serum samples taken through a refresher training on procedures of from sheep and goats. serum sample collection and proper sample labelling. The field activities were monitored by officers of the During this training, emphasis was put on the import- Ministries responsible for livestock in the five targeted ance of cold chain management. These trainings were zones. The process entailed visiting vaccination sites conducted by FAO technical staff in Garowe for north- and enquiring from community leaders and targeted eastern zone and Hargeisa for north-western zone. For households about the vaccination campaign and sero- the Banadir, central and southern zones, the trainings logical survey. Likewise, FAO technical staff and field were conducted in Nairobi, Kenya. monitors carried out independent monitoring through The vaccination teams were equipped with cold field visits, collection of data using pre-designed ques- chain equipment, vaccines, veterinary supplies and tionnaires and call centre surveys. This was in addition equipment, and facilitated with transport. They were to progress reports and photographic evidence on the also provided with pre-designed data entry sheets and implementation of the activities submitted by the laptops for the management of surveillance and vac- vaccination teams. cination data. Each team prepared a detailed work plan covering the entire vaccination period. The plans were shared with clan leaders, village elders and local Serological surveys authorities during community awareness creation and Two serological surveys were conducted. The first one sensitization. The awareness creation fora provided an was conducted in March 2012 and the second in opportunity to emphasise the importance of the September 2012. The sample size was calculated based vaccination campaign and collect important village on the percentage of the total number of animals tar- contact details. geted for vaccination. A two-stage cluster sampling methodology was used whereby a total of 18,377 sera samples were randomly collected from small ruminants, Implementation of PPR vaccination campaign representing 0.1% of the total number of the animals tar- The vaccination teams were deployed in the field from geted for vaccination. Table 2 illustrates the number of March to May 2012 for a period of 60 working days. serum samples taken during the serological surveys. Each team was required to vaccinate a minimum of Bloodwas drawnfromthejugular veininplain 2,500 sheep and goats daily apart from Banadir region 10-ml vacutainer tubes, kept in a cool place for up which had lower daily targets of 500 animals. Banadir to 24 h to allow for clotting. Then, sera were dec- was exceptional because it is peri-urban, and there anted into two aliquots which were then transferred was a challenge of gathering animals together for into 5-ml pre-labelled cryovials. The cryovials were vaccination. properly labelled to ensure quick identification of Full consent of the Somali veterinary authorities the sample by region, district, team and chrono- was sought before carrying out the PPR vaccination logical numbering of every sample. Every sample campaign, collection of disease surveillance data and collected was recorded in pre-designed recording the serological surveys. The authorities granted per- sheets. Sera were then stored in ice-filled cool boxes mission to collect and test field laboratory samples. for a period of two to three days until their transfer High levels of quality and integrity were observed to deep freezers where they were stored at − 20 °C. during the fieldwork. The livestock keepers were also The sera were subsequently airlifted from Somalia to sensitised prior to the field interventions after which AU-PANVAC laboratories in Ethiopia in August they voluntarily presented and participated in the 2014 for serological analysis. Table 2 Number of serum samples taken before and after PPR vaccination campaigns in Somalia, 2012 Zones Number of animals vaccinated Number of pre-vaccination Number of post-vaccination Total number of sera samples sera samples collected sera samples collected Banadir 148,100 88 168 256 Central Somalia 5,824,724 2,294 3,750 6,044 Southern Somalia 5,953,821 2,996 4,711 7,707 North-eastern Somalia 3,750,466 1,056 1,408 2,464 North-western Somalia 3,989,736 1,300 606 1,906 Total 19,666,847 7,734 10,643 18,377 Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 5 of 11 The Competitive Enzyme-Linked Immunosorbent vaccines, cold chain equipment, vaccination supplies and Assay (c-ELISA), the test recommended by OIE equipment. Other requirements that were costed in- (2004), was used for PPR diagnoses. Serum samples cluded transport for the vaccination teams, time dedi- were tested for IgG PPR antibodies using monoclonal cated to vaccination campaigns by the vaccination antibody-based c-ELISA directed against nucleopro- teams, capture of field data, analyses of serum samples, tein (N protein) as described by Libeau et al. (1995). monitoring the vaccination campaigns and cold chain Any serum samples with a percentage inhibition value maintenance. equal to or greater than 50% were considered positive Hence: for PPR. The laboratory test results were released in January 2015. Total cost of the vaccinationðÞ TCV ¼ðÞ Cost of establishing and maintaining cold chain Data analysis þðÞ Cost of procuring PPR vaccines The vaccination data was analysed using Form Moni- toring Tool (FMT) software and thereafter exported to þðÞ Cost of procuring vaccination supplies and equipment Microsoft® Excel 2013 (Microsoft Inc. USA) for the þðÞ Cost of services for vaccine delivery computation of summary statistics which were presented in form of tables. The Ascent™ Software from Thermo The unit cost of vaccination was calculated as follows: Scientific™ was used to generate sero-prevalence results from the ELISA reader. Data were then exported to Microsoft® Excel 2013 (Microsoft Inc. USA), to enable Total cost of vaccinationðÞ TCV =number of animals vaccinated: generation of preliminary sero-prevalence frequency tables. The sero-prevalence estimates were derived using the formula: Results P ¼ðÞ y=n  100 Positioning of vaccination teams, cold chain equipment and PPR vaccines where y denoted the total number of samples testing A total of 140 teams from livestock professional positive for PPRV antibodies and n was the sample size associations and Ministries responsible for livestock (Thrusfield 2005). were deployed in the five zones to conduct the vaccin- This formula was applied in calculating zone-specific ation campaign. Each team was comprised of five as well as country-wide sero-prevalence values. Subse- members that included four livestock professionals quent analyses for homogeneity between pre- and post who were either veterinarians or veterinary parapro- PPR vaccination sero-prevalence values was done using fessionals and a record keeper. The team leaders were Mantel Hensel test in Stata® Statistical Software, Release veterinarians. The Federal Government of Somalia, 13 (StataCorp 2013). The Mantel-Haenszel chi-square represented by the Ministry of Livestock, Forestry and value tests the null hypothesis that the individual Range (MoLFR), supervised and monitored the stratum odds ratios are all equal to one versus the alter- vaccination campaign implemented by SOWELPA, native hypothesis that at least one odds ratio is different CERELPA and BENALPA. The cold chain equipment from unity. was distributed in pre-determined strategic locations closer to vaccination sites prior to commencement of Estimation of the PPR vaccination costs vaccination. The distribution of the teams, the PPR The estimation of PPR vaccination cost was based on vaccine doses and the cold chain equipment is shown the requirements that included purchase of PPR in Tables 3 and 4. Table 3 The distribution of PPR vaccine doses in the five zones according to the implementing organisations and public institutions, 2012 Zones Implementing organisations/institutions Number of vaccination teams PPR vaccine doses distributed Banadir Banadir Livestock Professional Association (BENELPA) 10 150,000 Central Somalia Central Livestock Professional Association (CERELPA) 45 6,000,000 North-eastern Somalia Ministry of Livestock and Animal Husbandry (MoLAH) 20 4,000,000 North-western Somalia Ministry of Livestock (MoL) 20 4,000,000 Southern Somalia South West Livestock Professional Association (SOWELPA) 45 6,000,000 Total 140 20, 150,000 Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 6 of 11 Table 4 Distribution of cold chain equipment in the five zones of Somalia, 2012 Zone Location of cold Large-sized deep Medium-sized deep Cool Vaccine chain hub freezers (336 l) freezers (280 l) boxes (22 l) carriers (1.6 l) Banadir Mogadishu 6 5 0 7 Central Somalia Belet Weyne 6 6 15 5 North-eastern Somalia Garowe 8 8 4 0 North-western Somalia Hargeisa 8 8 4 6 Southern Somalia Baidoa 7 8 15 8 Total 35 35 38 26 PPR vaccination coverage Pr > chi = 0.0000. The vaccination campaign implemented in the five zones of Somalia achieved an overall vaccination coverage of Since the confidence intervals did not include 1, it 97.6% (19,666,847 out of 20,150,000) goats and sheep. implied that the differences in antibody levels pre- The highest vaccination coverage was 99.7% in north- and post PPR vaccination could not have been by western Somalia whereas the lowest was 95.4% in central chance. There was significant difference in sero- Somalia zone. The high vaccination coverage was as a prevalence values pre- and post PPR vaccination at result of limited vaccine losses during the vaccination 95% confidence level. campaigns. This was achieved through sensitisation of livestock-keeping communities to present target animals Costs of PPR vaccination in pre-identified vaccination sites and pre-positioning of The overall cost of vaccination entailed the cost of con- cold chains in strategic field location for vaccine storage tract time by the vaccination teams, vaccines, transport, during the vaccination campaigns. The vaccination sites cold chain, field equipment, vaccination equipment and were mainly watering points and grazing sites. Table 5 other supportive services such as monitoring, data and provides a summary of vaccination coverage for each of serum collection. This was costed per animal vaccinated the five zones. as tabulated in Table 7. The cost of contract service during vaccination was Analyses of serology results USD 2,770,160 which constituted nearly 50% of the total There was an increase in sero-prevalence after PPR vaccination costs. Based on the number of sheep and vaccination campaign. The serology results revealed an goats targeted for vaccination against PPR which was overall sero-prevalence of 62% (4,792/7,734) before 20,150,000, the unit cost of service delivery of the vaccination and 76% (8,089/10,643) after vaccination vaccine per animal was USD 0.14 per animal whereas at (p <005) (Table 6). The pre-vaccination sero-prevalence the estimated cost of a dose of PPR vaccine was USD was highest in north-eastern zone (74%) and lowest 0.12. The overall PPR vaccination cost per animal was in Banadir (39%), whereas the post-vaccination sero- estimated as 0.28 USD. prevalence was highest in central Somalia zone (87%) and lowest in Banadir (58%). The results of Mantel Hensel test of homogeneity at Discussion 95% confidence interval were as follows: The cold chain was an important requirement from the point of manufacture, during the transportation and Test of homogeneity Mantel-Haenszel Chi2 (1) = 753.57 storage to the point of vaccine use. The cold chain equipment was appropriately positioned in the field Table 5 Analyses of PPR vaccination coverage in sheep and prior to the vaccination campaign to ensure the storage goats in the five zones of Somalia, 2012 temperatures of between + 2 and + 8 °C were main- Zones Total animal Total animal % coverage of tained. Where cold chain equipment was insufficient, targeted vaccinated the targets prior arrangements were made to use the cold chain Banadir 150,000 148,100 98.7 facilities from organisations providing health services in Central Somalia 6,000,000 5,824,724 95.4 Somalia. To overcome challenges of electric power supply, solar-powered freezers were supplied in the five Southern Somalia 6,000,000 5,953,821 99.2 zones. Solar-powered refrigeration has been used for North-eastern Somalia 4,000,000 3,750,466 96.2 vaccine storage by United Nations Children Fund North-western Somalia 4,000,000 3,989,736 99.7 (UNICEF) mainly in Africa where other sources of reliable Total 20,150,000 19,666,847 97.6 electricity are inadequate or costly (McCarney et al. 2013). Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 7 of 11 Table 6 Analyses of PPR serum samples collected from small ruminants before and after PPR vaccination in the five zones in Somalia, 2012 Zones Pre-vaccination Post-vaccination No. of samples tested % PPR sero-prevalence No. of samples tested % PPR sero-prevalence Banadir 88 39 168 58 Central Somalia 2,294 73 3,750 87 Southern Somalia 2,996 56 4,711 82 North-eastern Somalia 1,056 74 1,408 79 North-western Somalia 1,300 66 606 73 Total 7,734 62 10,643 76 The PPR disease control strategy in Somalia was ini- following up on young animals between four months and tially though country-wide vaccination campaigns, the one year in age (FAO/OIE 2015). Considering the pre- method prescribed for the control of PPR in endemic dominant extensive and mobile livestock production sys- countries (Diallo 2004). Vaccinating a large number of tems in Somalia, vaccination is still an effective control animals minimises the spread of the PPR by decreasing measure of PPR despite the inherent challenges of the effective contact rate. Despite the immense socio- large sheep and goat populations, high reproductive rates political challenges existing currently in Somalia, nearly exemplified by short gestation period and high twinning 20 million small ruminants distributed across the coun- percentage as well as high turnover. The PPR vaccinations try were immunised achieving an overall vaccination conducted in Somalia has reduced the disease incidence coverage of 97.6%, placing Somalia among the first coun- to a level where relatively small-scale targeted vaccination tries in the Horn of Africa to implement a country-wide can be carried out in line with the time-bound PPR PPR vaccination campaign of such magnitude. This level disease control strategy for Somalia (FAO 2011a, b, c). of coverage is much higher than the average annual vac- The large-scale vaccination has reduced the effective con- cination coverage of 15% reported to World Animal tact rate, thus curbing the spread of PPR among the small Health Organisation (OIE) by PPR-infected countries, ac- stock. Moreover, such vaccination campaigns have been cording to a study by Jones et al. (2016). In the Greater reported to reduce the socio-economic impact of PPR Horn of Africa region, Kenya vaccinated an estimated two (Jones et al. 2016). million goats and sheep against PPR in 2006 in Turkana The serology survey results from the analyses of 7,734 County (Kihu et al. 2015a, b). According to studies by serum samples collected from sheep and goats before Singh (2011), 85.4% vaccination coverage is necessary for the PPR vaccination revealed an overall individual ani- control of PPR infection in sheep population. mal sero-prevalence of 62% with a low of 39% and a high Vaccination has been described as the preferred tool for of 74% in Banadir zone and north-eastern zone respect- controlling and eradicating PPR, especially in countries ively. These values are high compared to those recorded where it is difficult to control animal movement (Jones et in a baseline PPR sero-survey conducted by Somali al. 2016). Ideally, the PPR vaccination should be time- Animal Health Services Project (SAHSP) in Somalia be- limited with high coverage to achieve the necessary herd tween 2001 and 2007 which gave a low of 6.5% in north- immunity in high-risk areas. The PPR Global Eradication western zone and a high of 37.6% in southern Program recommends two-year vaccination campaigns Somalia (SAHSP 2006a, b, 2009). The overall indi- vidual animal pre-vaccination sero-prevalence was also relatively higher compared to 35.5% reported in Table 7 Analyses of estimated cost of PPR vaccination studies by Chavan et al. (2009) in India and 46.5% campaigns and serological Survey in Somalia, 2012 Ekue et al. (1992) in Cameroon. In Ethiopia, an Description of activity Amount USD overall individual animal sero-prevalence of 30.9% Procurement of PPR vaccine 2,414,040 was reported in a study by Megersaa et al., 2011.Other Contract service fee for vaccine delivery 2,770,160 studies conducted in the Somali region of Ethiopia, an area Procurement and maintenance of cold chain 392,933 under pastoral management system, gave a sero-prevalence of 21.3% at 95% confidence level (Waret-Szkuta et al. 2008). Serum sampling and testing 70,522 The high pre-vaccination sero-prevalence of PPR in Total 5,647,655 Somalia can be attributed to increased PPR virus circula- No. of animals targeted against PPR 20,150,000 tion as illustrated by the confirmed PPR outbreaks by Cost of vaccinating one animal 0.28 SAHSP between 2005 and 2009 (SAHSP 2009), taking Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 8 of 11 into consideration that the past vaccination attempts by Faris et al. (2012) in a cross-sectional epidemiological have been on a small scale and largely uncoordinated study conducted in selected districts in Ethiopia. A simi- (FAO 2001). This corroborates work by Waret-Szkuta et lar vaccine made from the same Nigeria 75/1 strain from al. (2008) who in their study concluded that high anti- National Veterinary Institute in Debre-Zeit, Ethiopia, body levels in small ruminant population with minimal gave a relatively lower post vaccination seroconversion vaccination coverage is due to a circulating PPR virus. of 61%, which was attributed to the poor handling of the Considering the high reproductive rate, uncontrolled cold chain Faris et al. (2012). movements and high turnover of small stock in Somalia, The overall unit cost of PPR vaccination in Somalia, an antibody prevalence of 62% is unlikely to offer pro- 2012, was estimated as USD 0.28 per animal. This is tection and prevent further epidemics. much less than the overall individual animal vaccination The results of 10,643 serum samples collected after cost for Rinderpest from a study by (Tambi et al. 1999) the PPR vaccination campaign showed an increase in which estimated the individual animal vaccination cost herd immunity from 62 to 76% at (p < 005). There is an as ECU 0.42 equivalent of USD 0.51 based on average argument by Inter Government Authority for Develop- ECU value between 1989 and 1996. In the same study, ment (IGAD) that due to the high annual turnover of unit cost of Rinderpest vaccination in Ethiopia was esti- the small ruminants, the herd immunity threshold is un- mated as ECU 0.27 (USD 0.33) and this relatively low likely to increase by using repeated annual vaccination, unit cost was attributed to economies of scale. The esti- and instead, large numbers of vaccinations should be mated cost of a dose of PPR vaccine in Somalia was delivered in a short time period under targeted vaccin- USD 0.12 which compares favourably with the USD 0.10 ation programmes (IGAD-2014). A sero-epidemiological reported by Jones et al. (2016) in other parts of Africa. survey in Turkana, Kenya, by Kihu et al. (2015a, b) con- However, the unit cost of service delivery of the PPR firms that high demographic changes reduce the PPR vaccine per animal was different. In Somalia, it was USD herd immunity of small ruminants with introduction of 0.14 per animal which was much lower than USD 0.3 naïve and vulnerable weaned kids and lambs that have estimated by Jones et al. (2016). This could have been decreasing maternal immunity into the already immu- due to the economy of scale, considering that nearly 20 nised herd. Studies by Ata et al. (1989) and Bidjeh et al. million sheep and goats were vaccinated against PPR (n.d.) have shown that maternal antibodies in young ani- disease. The differences could have also arisen due to mals are detectable up to six months of age and fall different ways of costing the service delivery. In the below the protection threshold level at 3.5 and 4. Somalia study, the cost of service delivery was calculated 5 months in lambs and kids, respectively. Therefore, an- based on the cost of personnel time and the transport nual PPR vaccination campaigns targeting middle age costs during data and serum collection. The procure- group can improve the herd immunity to levels that can ment of vaccine increased the total cost of vaccination. contain spread of the PPR disease (Kihu et al. 2015a, b). In this study, it constituted 50% of the total vaccination Outcomes of two studies by Singh (2011) and Balamurugan cost. One way of reducing this cost is vaccinating against et al. (2014) elucidate that PPR mass vaccination campaigns more than one disease that is prevalent in the area. The that achieve 70 to 80% levels of herd immunity threshold control of sheep and goat pox and contagious caprine break the effective transmission of the virus irrespective of pleuropneumonia diseases could be done alongside PPR the population dynamics, disparities in husbandry practices disease (Kumar et al. 2014; FAO/OIE 2015). and the agro-climatic conditions affecting the pattern of disease. In essence within this herd immunity threshold range, there is sufficient proportion of immune small Conclusions and recommendations ruminant population for PPR virus to become stable as all This paper has provided a detailed account of a success- the vaccinated, infected and recovered animals are pro- ful mass PPR vaccination in Somalia. It has brought out tected (Balamurugan et al. 2014). The herd immunity practical implications of PPR control in a conflict- threshold for Rinderpest, which is closely related to PPR, affected and fragile country that can be adopted by other was estimated as 75 to 80% (Rossiter and James 1989). countries. PPR vaccination campaigns in such countries There was significant difference in sero-prevalence characterised by limited public veterinary personnel can values pre- and post PPR vaccination at 95% confidence be implemented through involvement of private live- level which gave a Mantel-Haenszel chi2 (1) of 753.57 stock professional organisations which have operational Pr > chi = 0.0000. All the zones had antibodies greater presence and technical capabilities. In Somalia, the than 76% except Banadir and north-western zones that Livestock Professional Associations in Banadir, central had sero-prevalence values of 58 and 73% respectively. and southern Somalia and the Ministries responsible for The overall post vaccination serum antibody level ob- livestock in the north-eastern and north-western Somalia served in Somalia was much higher than that observed were contracted to carry out the mass vaccination Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 9 of 11 campaigns, which built confidence and improved goodwill understanding of the role of wild and other domestic with pastoral communities. ruminants in the maintenance of peste des petits rumi- Mass vaccination against PPRV in countries endemic nants virus (PPRV). with PPR controls the virus circulation in the small Abbreviations ruminant population to a level where targeted vaccin- AU-PANVAC: African Union’s Pan African Veterinary Vaccine Centre; ation can be considered. Vaccinations carried out before BENALPA: Banadir Livestock Professional Association; c-ELISA: Competitive the expected seasonal movements enhance vaccination Enzyme-Linked Immunosorbent Assay; CERELPA: Central Region Livestock Professional Association; ELISA: Enzyme-Linked Immunosorbent Assay; coverage. Although funding sources for a PPR disease FAO: Food and Agriculture Organisation of the United Nations; FMT: Form control programmes are limited in most developing Monitoring Tool; IGAD: Inter Governmental Authority for Development; countries, Somalia successfully vaccinated nearly 20 mil- JOVAC: Jordan-based Vaccine Production Company; MoLAH: Ministry of Livestock and Animal Husbandry; MoLFR: Ministry of Livestock, Forestry and lion sheep and goats against PPRV within a livelihood Range; OIE: World Animal Health Organisation; PPR: Peste de Petits Ruminants; support programme framework. The capacity of public PPRV: Peste de Petits Ruminants Virus; SAHSP: Somalia Animal Health Project; and private veterinary services in Somalia was enhanced SOWELPA: South West Livestock Professional Association; TCV: Total cost of the vaccination; UNICEF: United Nations Children Fund through country-wide provision of cold chain facilities and vaccination equipment, which is anticipated to fur- Acknowledgements ther reduce the cost of vaccination delivery in the future. The support of the Ministries responsible for livestock in Somalia to allow the Furthermore, where there was insufficient cold chain, ar- work to be carried out in Somalia and the paper to be published is highly rangements were put in place to share cold chain facil- acknowledged. The authors give thanks to Somalia livestock owners for their cooperation during serum sample collection. The authors give many thanks ities between human and animal vaccines under the to the veterinarians and animal health auxiliaries in Somalia for their support “One Health” programme which reduced the frequency during the field work. The authors give gratitude to Mr. Daniela Donati, FAO of replenishing the ice-packs to two to three days. Des- Somalia representative (acting) in Somalia, and Mr. Rudi VanAaken, FAO Somalia Head of Programme, for their support to have the paper published. pite Somalia not having the capacity to produce PPR The technical support of Dr. Bouna Diop from FAO/OIE PPR Global vaccine, it was still possible to source a good quality vac- Secretariat and Dr. Massimo Castiello for the technical input during drafting cine certified by AU-PANVAC from external sources at of the paper is gratefully acknowledged. Many thanks to Charles Bodjo of AU-PANVAC in Addis Ababa, Ethiopia, for a competitive cost of USD 0.12. It was possible to deter- his support in analysing the serum samples. The support of Ms. Baru Adan mine the effectiveness of the mass vaccination through and Ms. Jeniffer Kariuki of FAO Somalia for their input in analysing the data two serological surveys. The cost of the pre-vaccination and producing the map is acknowledged. survey was significantly reduced by using the PPR vaccination teams to collect the sero-surveillance serum Funding This paper is based on FAO work funded by various government institutions samples prior to vaccination. The analyses of the serum and funding agencies that include Belgium, Switzerland, Australia, Spain, UK, samples were carried out at the AU-PANVAC labora- World Bank, and UN-OCHA. The findings, conclusions and recommendations tory. Somalia attained a herd immunity threshold of 76% contained are exclusively from the authors and do not in any way reflect positions or policies of FAO and the above-mentioned government through the country-wide mass PPR vaccination institutions and funding agencies. The funds were used to purchase the PPR programme of nearly 60% of the national small ruminant vaccines, supplies and equipment, contract out vaccination services and population. This was shown to stabilise the virus within supplement salaries or honoraria of the authors. There was no additional external funding received for this work. The authors are employees of FAO the target population as there were no reported clinical and were involved in the design of the vaccination campaign, data analysis, cases of the disease. decision to publish and preparation of the manuscript. The focus should therefore be to increase the herd immunity threshold to 80% as a way of reducing virus Authors’ contributions circulation, considering the high turnover, uncontrolled SN, KS, JM and CB designed the study. SN, KS and JM undertook the fieldwork. SN, SM JM and KT analysed the data and drafted the original movements and the new annual introduction of naïve manuscript with further input from KS and CB. All authors read and population. This should be achieved through annual tar- approved the final manuscript. geted vaccination based on extensive epidemiological surveillance. It will be worthwhile to target only sheep Authors’ information and goat above three months with no history of PPR SN is a veterinary epidemiologist and economist, and a postdoctoral researcher working on animal disease surveillance systems and vaccination. Further investment should be made on solar transboundary animal disease control at the Food and Agriculture of the powered cold chain facilities to increase penetration of United Nations (FAO) in Somalia. KS is a veterinarian and researcher working the vaccines to the remote rural vaccination sites. This as the livestock sector emergency and programme coordinator at the FAO in Somalia. SM is a veterinarian and postdoctoral researcher working at FAO at will not only reduce the transport cost of replenishing the time of the study and now a livestock consultant. JM is animal health the ice packs but shall also improve the seroconversion officer at FAO in Somalia and is working on tropical animal health research rates due to better cold chain maintenance. Somalia at the Institute of Tropical Medicine, Antwerp, Belgium. CB is a veterinarian and a livestock specialist working as the livestock sector coordinator at FAO should invest in laboratory facilities for confirming in Somalia at the time of the study and now working at FAO office for disease cases and monitoring PPR herd immunity levels. Central Africa. KT is an economist currently working as information and Further studies should be conducted to improve the knowledge management officer at the FAO in Somalia. Njue et al. Pastoralism: Research, Policy and Practice (2018) 8:17 Page 10 of 11 Ethics approval and consent to participate from Awash Fentale District, Afar, Ethiopia. Preventive Veterinary Medicine 103 Written approval for undertaking PPR vaccination, serum sample collection and (PubMed): 157–162. shipping of samples to PANVAC was granted by respective Ministries Gargadennac, L., and A. Lalanne. 1942. La peste des petit ruminantis. Bulletin des responsible for livestock in different regions of Somalia in 2012. The livestock Service Zootechniques et des Epizooties de l’Afrique Occidentale Francaise 5: 16–21. owners were sensitised on the importance of vaccination and serological IGAD 2014: The IGAD Regional peste des petits ruminants (PPR) progressive survey after which they gave their verbal consent for the activities to be control and eradication strategy. https://icpald.org/wp-content/uploads/ undertaken. The livestock owners were required to append their thumb print 2016/01/Progressive-Control-and-Eradication-Strategy-1.pdf. on the vaccination form as a proof of consent as most of them were illiterate. Jones B.A., Rich K.M., Mariner J.C., Anderson, J., Jeggo, M., Thevasagayam S., Cai Y., Peters, A.R., and Roeder, P. 2016. The economic impact of eradicating peste Competing interests des petits ruminants: A benefit-cost analysis. PLoS One 11 (2):e0149982. The authors declare that they have no competing interests. https://doi.org/10.1371/journal.pone.0149982. Karimuribo, E.D., Loomu, P. M., Mellau, L.S.B. and Swai, E.S. 2008. Retrospective study on sero-epidemiology of peste des petits ruminants before its official Publisher’sNote confirmation in northern Tanzania in 2008. Department of Veterinary Springer Nature remains neutral with regard to jurisdictional claims in Medicine and Public Health, Sokoine University of Agriculture, Morogoro published maps and institutional affiliations. Tanzania; Veterinary Investigation Centre (VIC), Arusha, Tanzania. http://agris.fao. org/agris-search/search.do?recordID=DJ2012071861. Accessed 14 Dec 2016. Author details Kaukarbayevich, K.Z. 2009. Epizootological analysis of PPR spread on African Food and Agriculture Organisation of the United Nations (FAO), Somalia continent and in Asian countries. African Journal of Agricultural Research 4 (9): Country Office, P.O Box 30470-00100, Nairobi, Kenya. P.O Box 4810-00506, 787–790. Available online at https://www.researchgate.net/publication/ Nairobi, Kenya. 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PastoralismSpringer Journals

Published: May 30, 2018

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