Review Article Challenges and Economic Implications in...

Review ArticleChallenges and Economic Implications in the Control ofFoot and Mouth Disease in Sub-Saharan Africa Lessons fromthe Zambian Experience

Y Sinkala12 M Simuunza2 D U Pfeiffer3 H M Munangrsquoandu4 M Mulumba5

C J Kasanga6 J B Muma2 and A S Mweene2

1 Department of Veterinary Services Ministry of Agriculture and Livestock PO Box 50060 Lusaka Zambia2Department of Disease Control School of Veterinary Medicine University of Zambia Lusaka Zambia3 Royal Veterinary College London AL9 7TA UK4Norwegian School of Veterinary Sciences Ullevalsveien PO Box 8146 0033 Oslo Norway5Onderstepoort Veterinary Institute Agricultural Research Council Old Soutpan Road Onderstepoort Pretoria 0110 South Africa6 Sokoine University of Agriculture PO Box 3297 Chuo Kikuuu Morogoro Tanzania

Correspondence should be addressed to Y Sinkala yonasinkalasacidsorg

Received 4 February 2014 Revised 27 July 2014 Accepted 28 July 2014 Published 21 August 2014

Academic Editor Timm C Harder

Copyright copy 2014 Y Sinkala et alThis is an open access article distributed under theCreativeCommonsAttribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Foot andmouth disease is one of the worldrsquos most important livestock diseases for trade FMD infections are complex in nature andthere are many epidemiological factors needing clarification Key questions relate to the control challenges and economic impactof the disease for resource-poor FMD endemic countries like Zambia A review of the control challenges and economic impact ofFMD outbreaks in Zambia was made Information was collected from peer-reviewed journals articles conference proceedingsunpublished scientific reports and personal communication with scientists and personal field experiences The challenges ofcontrolling FMD using mainly vaccination and movement control are discussed Impacts include losses in income of over US$16 billion from exports of beef and sable antelopes and an annual cost of over US$ 27 million on preventive measures Furtherimpacts included unquantified losses in production and low investment in agriculture resulting in slow economic growth FMDpersistence may be a result of inadequate epidemiological understanding of the disease and ineffectiveness of the control measuresthat are being applied The identified gaps may be considered in the annual appraisal of the FMD national control strategy in orderto advance on the progressive control pathway

1 Introduction

Zambia is a sub-Saharan African country with potential toboost its economy through trade in livestock commodities[1 2] However this potential is hindered by the presenceof numerous disease challenges including foot and mouthdisease (FMD) FMD is an endemic disease in Zambia thathinders economic exploitation of the livestock resource in acountry where 80 of the population is dependent on agri-culture [1 3 4] The disease is described as an acute highlycontagious viral infection of wild cloven-hoofed animalsinvolving more than 70 wildlife species and domesticatedruminants including pigs [5] The disease is caused by FMD

virus (FMDV) which is a prototypic member of the genusAphthovirus There are seven FMDV serotypes A O C SAT1 SAT2 SAT 3 andAsia 1 [6] In southernAfrica two distinctmolecular epidemiological forms of the disease exist [7]which are the Southern African Territories (SAT) serotypesand the Eurasian or South American (A and O) serotypes

FMD has persisted in Zambia since the first recordedoutbreak in 1933 [8]The persistence may be a result of inade-quate epidemiological understanding and ineffective controlmeasures [9] Other reasons include the presence of thereservoir African wild buffalo (Syncerus caffer) [10] presenceof five serotypes O A SAT 1 2 and 3 the virusrsquo ability topersist in the environment without animal hosts and lack of

Hindawi Publishing CorporationVeterinary Medicine InternationalVolume 2014 Article ID 373921 12 pageshttpdxdoiorg1011552014373921

2 Veterinary Medicine International

Zambia

NamibiaZimbabwe

Botswana

Mozambique

Angola

D RCongo

Tanzania

Lusaka

Mbala

Mongu

Sesheke

Chobe0 260

520130

GMANational parks

District boundaryInternational boundary Wetlands

0 130 260390

390520

65(km)

(km)

35∘09984000998400998400E30

∘09984000998400998400E25

∘09984000998400998400E20

∘09984000998400998400E

N

35∘09984000998400998400E30

∘09984000998400998400E25

∘09984000998400998400E20

∘09984000998400998400E

10∘09984000998400998400S

15∘09984000998400998400S

10∘09984000998400998400S

15∘09984000998400998400S

FMD cases

Figure 1 Showing distribution of FMD cases in relation to wildlife protected areas and wetlands Map adapted from Sinkala et al 2014 [68]

a definitive domestic host for life cycle [11] The Food andAgriculture Organization (FAO) of the United Nations (UN)FMD progressive control pathway (PCP) classified Zambiaas being at level 2 [12] And as such identification of FMDcontrol challenges and economic impactsmay provide oppor-tunities for investment in advancing to the desired level 3classification of the (Organization of International Epizootics(OIE) progression criteria To attain this it is imperativethat we understand the limitations that have led Zambianot to progress into attaining the desired level 3 criteriaTherefore the objective of this review was to describe thecontrol challenges and economic impacts of FMD outbreaksin Zambia In doing so we reviewed published literature onFMD outbreaks control and impact The literature searchwas conducted on major electronic databases includingPubMed Science Direct Cabi direct and Springer usingspecified search terms The search terms included ldquoaphthousfever aphthae epizooticae hoof and mouth disease footand mouth disease and Zambiardquo The inclusion criteriawere studies published in English in peer-reviewed journalsand studies where full text was available Further greyliterature from government institutions was obtained Theseincluded annual reports from the Ministry of Agricultureand Livestock for the period 1933 to 1912 economic andpolicy documents from theMinistry of Finance and NationalPlanning as well as the Bank of Zambia between 2000 and2010 and Central Statistical Office population census reports2000 and 2010 Furthermore expert opinions on impacts

of FMD were obtained through focused discussions withfarmers scientists commodity associations and personalfield experiences We discuss the findings with the aimof bringing into perspective the challenges experienced bythe government in controlling FMD and the economicalimplication of the disease in Zambia that would serve asan example to other countries faced with similar challengesAnd we also highlight the possible solution that would helpovercome these predicaments

2 Challenges in the LivestockProduction System

Zambia is a landlocked country covering 752 610 km2between latitudes 8∘ and 18∘ south of the Equator and longi-tudes 22∘ and 34∘ east of the Greenwich Meridian (Figure 1)The country shares borders with eight Southern AfricaDevelopment Community (SADC) member countries [13]and is composed of 10 administrative areas called provincesZambia is regarded as one of the least urbanised countriesin Africa with an estimated total population of 134 millionpeople majority of whom (61) are concentrated mainly inthe rural areas [14] Agriculture contributes about 215 togross domestic product (GDP) out of which 28 is from thelivestock subsector [15 16] The national per capital incomeis one of the lowest in the world estimated at US$ 1700for 2012 [17] Of the total land 475 is agricultural land

Veterinary Medicine International 3

and 85 of this agriculture land is under pasture signifyingthe availability of more land for grazing than arable [2 18]The remaining 525 is forest national parks and gamemanagement areas [19] The livestock production system canbroadly be categorised into traditional and commerial sectors[20]

21 Traditional Livestock Production Systems Traditionalfarmers occupy the communal areas owning 84 of theestimated 34million cattle 68 of the 1000 sheep 97 of the1 million goats and 90 of the 15 million pigs [1 21] Cattleare raised on communal land under an extensive grazingsystem In the midlands and southern part of Zambia threelinked herding patterns exist village resident herds (alwaysin the villages) transhumant herds (move between villageand the floodplains) and interface herds (permanently stayon the floodplains) [22 23] In the rest of the country cattleare grazed in the communal areas as village resident herdsand the distances covered are dependent on season andavailability of pasture [20]The predominant cattle breeds areZebu and Sanga [20]

211 Communal Landuse Systems As pointed out above alarge proportion of livestock is owned by traditional farmerswho mainly occupy communal lands These farmers sharegrazing pasture and watering points This farming systemallows for cattle from different owners to share grazingpastures and water sources enabling disease transmissionbetween different herds During the dry season the watersources become scarce and grazing pastures shrink into a fewareas that are close to water sources and as such this tends toincrease the animal population density at the water sourcesand grazing pastures Generally it is known that transmissionof FMD is exacerbated by increase in population densityenhancing the transmission of the disease through contactbetween the infected and noninfected animals [24] Besidesgiven that cattle have been shown to carry their virus fromlast outbreaks for 2 to 35 years [25 26] environmental stressdue to decrease of grazing pastures and overcrowding atwatersources may cause recrudescence of the disease in the carrieranimals which could lead to occurrence of outbreaks Thisscenario is likely to be the cause of outbreaks in the Northernregion in between Mbala and Nakonde where there is notranshumance grazing system practiced and yet farmer sharegrazing pastures and water sources

212 Transhumance Grazing Systems The midlands andsouthern part of Zambia practice a transhumance grazingsystem This poses a significant challenge because of thelarge population densities of cattle that share grazing pasturesduring the dry season in the Kafue basin and on the wetlandareas of the Zambezi River in the areas between Kazungulaand Sesheke districts These areas tend to have the highestrecurrence of outbreaks and in most cases outbreaks occurduring the period of increased population densities of cattlein the dry seasonThemajor challengewith the transhumancegrazing system in the Kafue Flats being the most widelyaffected area is that cattle come from the upland areas into

the wetland areas for grazing The area has been estimatedto account for gt500000 cattle herds that graze in the wetlandareas [9]This allows for increased contact thereby increasingthe possibility of transmission from infected to noninfectedanimals At the end of the dry season animals aremoved backfrom thewetlands to the upland areas during which time theyspread the outbreak further [9 27] Generally this areamakesit difficult to implement movement restriction and the cattleherds at risk are usually many and as such ring vaccinationis difficult to implement Put together several factors makethis area highly vulnerable to FMDoutbreaks and at the sametime difficult to put timely control measures in place

22 Commercial Farming Systems Commercial farms keep-ing mostly exotic breeds of beef and dairy cattle are run asprivate business enterprise characterised by high productionefficiency and high offtake rates to the market Commercialfarms are concentrated along the line of rail within themidlands and southern parts of the country and are thelargest supplier of milk and beef to the urban population[28] Occassionally disease outbreaks from the traditionalsector might spill into these farms Outbreaks of FMD in thesector causes huge losses in productivity and income frommovement bans which in turn affects the national economythrough drop in supply and general rise in prices of beef andother competing commodities [29]

23 Beef and Dairy Products Market Forces One of thegreatest challenges faced by the Zambian government in thecontrol of FMD is that the market forces for beef and dairyproducts are placed in Lusaka and the Copperbelt provinceswere the human population density is high and yet thelargest producing areas of beef are in the communal landsand transhumance grazing areas of the central southernand western provinces of the country where the recurrenceof FMD outbreaks is high And as such during outbreaksthere is a tendency to move animals illegally to abattoirs andslaughter slab in the urban areas These illegal movementsexacerbate the transmission of FMD Enforcing movementrestrictions is often a challenge and disease easily moves tonew areas rapidly before it can be put under control

24 Transboundary Transmission Transborder transmissionof FMDbetween cattle is amajor problem in SouthernAfricaFor example the Northern Region of Zambia covering thearea between Mbala and Nakonde bordering the Rukwa andMbeya regions of Southern Tanzania tends to share the sameserotypes of FMD and outbreaks in this area tend to occurat the same time suggesting the likelihood of transmission ofthe disease between the two countries [30ndash32] Similarly out-breaks of FMD between Zambia Zimbabwe Botswana andNamibia in the south tend to follow transborder transmissionacross the Zambezi River Similarly FMD outbreaks havebeen reported across the border between Zambia andMalawiin the east [33] The major challenge with transboundarytransmission of FMD is that surveillance systems are notsynchronized between countries and during outbreaks con-trol strategies are not carried out simultaneously Hence


this raises the risk of back-and-forth transmission of FMDacross borders given the lack of synchronized control andsurveillance strategies

3 Challenges in the WildlifeProduction Systems

The Zambia Wildlife Authority (ZAWA) is a governmentinstitution responsible for the management of wildlifethrough protected areas and game ranches [34]

31 Game Management Areas The protected areas comprise19 national parks (NPs) and 35 game managements areas(GMAs) The GMAs act as buffer zones between NPs andhuman settlement areas (Figure 1)This buffer zone otherwiseknown as humanlivestockwildife interface is defined asa mosaic of human settlement livestock grazing wildlifeconservation and cultivation [35] Legal hunting is permittedin the GMAs while NPs are reserved for conservation andeducation purposes Several studies have shown how coex-istence of wildlife with livestock in the GMAs affects trans-mission of different wildlife diseases between livestock andwildlife [27 36ndash39] Hence it is likely that GMAs which aremost located in the wetlands such as the Kafue basin wheretranshumant and floodplain herds share grazing pastureswith wildlife serve as interface area for disease transmissionbetween wildlife and livestock [9 24 27] Hence this wouldacount for reasons why FMD outbreaks are the highest in theKafue flats where cattle and buffalo share common grazingpastures

32 FMD Wildlife Reservoir The African wild buffalopresent in most NPs is a major tourist attractions contribut-ing over 124 of the total hunting revenue through safarihunting for game trophies ecotourism and photographictourism [37] The NPs and GMAs are not fenced and humanencroachment into wildlife areas in search of pasture andwater is common Unfortunately the African buffalo asdescribed earlier is known to be a reservoir for FMDVand its interaction with domestic animals at the interfaceareas or GMAs poses a significant danger on resurgenceof FMDV outbreaks The African buffalo is an attractivecollection for game ranchers This would account for thereason why the African buffalo is not commonly reared ongame ranches because FMD has proved to be constraintin rearing the African buffalo [34 37 40 41] Generally itis becoming common practice that all ungulates capturedfrom national parks and GMAs known to be endemic withFMD are screened of FMD to ensure they do not carrythe disease to game ranches which are located in areasclose to livestock production areas Consequently this makesFMD a constraint to the expansion of the game ranchingindustry because of the prohibitive capture operation andFMD screening costs [34 37 41]

33 Expansion of the Game Ranching Industry Game rancheshave emerged since 1978 as an alternative conservationstrategy to conserve the depleting wildlife resources [42]Game ranching is considered environmentally sustainable

and economically viable industry because of its ability tointegrate ecotourism and wildlife utilization with livestockkeeping [37] while in those few game ranches with buffalopopulations the FMD status remains unknown [43]

4 FMD in Zambian Livestock and Wildlife

The SAT FMD is known to bemaintained by the wild buffalowhich is the stable biological reservoir of the FMDV [44]However transmission frombuffalo to cattle is not adequatelyunderstood because of little published research on the subject[45 46] Elsewhere transmission of FMD from buffalo tocattle has been demonstrated under both experimental andnatural conditions although it still remains a rare event [47ndash50] In addition other wildlife species have been describedto play an intermediary role in different ecological systems[49 51 52] Attempts to transmit FMDV from persistentlyinfected cattle under controlled field conditions have notyielded success except the one recorded in Zimbabwe [47]

The role of small stock (goat and sheep) in the transmis-sion of FMD is regularly debated but according to Hunter[53] evidence exists to indicate that small stock plays no roleas carrier animals As a result FMD had been controlledin several countries without vaccinating small stock [53]In Zambia few reports of FMDV cases in small stock existpartly because of subclinical manifestation of the diseasein these species low numbers of goats and sheep and lackof surveillance efforts targeting small livestock [54 55]However recent outbreaks of FMDV in Botswana involvingsmall livestock indicate that the disease in this host speciesstill remains significant [56]

5 Challenges of Controlling FMD in Zambia

Methods of control used in Zambia from 1933 to 1980shave been summarized [55] The methods of FMD controlthat are being implemented include surveillance quarantinemovement control and biannual vaccination of cattle in thehigh risk areas

51 Aphthization This practice was used from the 1940s until1973 when it was abolished [57] Aphthization involved delib-erate infection of cattle with infectious materials obtainedfrom neighbouring infected farms [58] The method wasintroduced as a means to speed up infection in cattlepopulation by burning out the disease Once all animals wereexposed it was assumed that they would develop immuneprotection from natural exposure

The limitations of aphthization have been described [55]It is probable that aphthization intensified the virulence ofthe FMDV and created a reservoir of infection in wildlife andother livestock for retransmission to cattle as their immunitywanes [55 59] Verification of this theory has not beenpossible because the central role of wildlife mainly buffalo inFMD transmission was only identified in the 1960s as a resultof operation Noah [60] However given growing evidencethat cattle exposed to FMD can serve as short term reservoirswith virus lasting up to 35 years in the oral-pharyngeal areasuggests that aphthizationwould cause a danger of increase in


the number of carriers in populations exposed to FMD andas such this strategy of FMD control was abandoned

52 Vaccination From the 1960 onwards vaccination wasintroduced using an attenuated SAT 2 vaccine in villagessurrounding an outbreak area while for infected villagesaphthization was used until its later was abolishment [57]In 1973 an inactivated adjuvant vaccine replaced the liveattenuated vaccine [57] Vaccination has traditionally beendone in cattle except once in 1979 in Livingstone whenother species like goats pigs and sheep were vaccinated withT155 bivalent SAT1 and SAT 2 vaccine supplied by Well-come (Kenya) limited [61] The source of vaccines remainedWellcome laboratories of Kenya until early 1990s when thecontract was awarded to Botswana Vaccine Institute

521 Private Sector Involvement In the late 1990s and early2000s vaccinations were done through contracts to privateveterinarian [33] These initiatives were targeted to supportthe privatization of veterinary services and improve servicedelivery However vaccination coverage during these con-tracts was generally unsatisfactory due to the many problemsassociated with awarding of these contracts to the privatesector (Peter Sinyangwe personal communication)

522 Vaccines in Use The vaccines currently in use consistof complete chemically inactivated 146S virion particlescombined with saponin-alhydrogel adjuvant [25] The vac-cines are multivalent that provide protection against multipleserotypes and a potency of at least 3 PD

50per dose [3] but

this is still a challenge for Zambia with five serotypes andmultiple topotypes that have to be incorporated into a singlevaccine The vaccination does not induce sterile immunityand animals may still be able to infect nonvaccinated animalsand may also become persistently infected [25 26] Assuch the urgent need for new SAT vaccine strains withgood immunogenicity for use in Africa was highlighted atthe recent Global FMD Research Alliance (GFRA) congress[62]

523 Vaccination Strategy The inactivated vaccines in useinduce short-lived immunity and require a booster dose every4ndash6months [53] However some areas are inaccessible due toannual flooding in some of the FMD high risk areas Furtherthe lack of reliable census figures in the traditional sectormakes verification of the required 80 vaccine coverageproblematic [25] Whilst vaccination of cattle with virusesthat are antigenically closely related to those carried by buf-falo form an integral part of FMD control in Southern Africa[53 63] it has not been a common practice in Zambia [64]This is because collecting samples from buffalo and havingthem tested at reference laboratories is expensive Usuallyduring vaccinations following an outbreak no distinctionis made between infected and susceptible animals Strainsused for routine vaccinations are presumed effective duringvaccination response to outbreaks However there is noempirical data that show the efficacy of these vaccines in thevarious situations they have been applied

524 Inadequate Vaccine Storage Facilities Inadequate cold-chain facilities have been a major challenge in handling the

vaccine in the field This is particularly the case during thesecond round of vaccination around October to Novem-ber when temperatures sometimes exceed 35∘C Frequentbreakdowns of the cold chain have to be suspected leadingto degradation of the vaccine antigen (146S particles) into12S particles which elicit almost no antibodies Howeverup to now there are no laboratory data to confirm thishypothesis [65] Given the status quo Zambia would benefitfrom vaccines with improved stability which are less relianton a cold chain

53 Movement Control

531 Livestock Movement Control Challenges exist in con-trolling movement in the traditional sector due to communalgrazing transhumance use of oxen for transport hiring ofbulls for mating and other vices like shifting from village tovillage mafisa and lobola [66] The immunological diversityin prevalent serotypes and topotypes that exist in Zambiamay render FMDdifficult to control in present circumstances[67 68]

Movement restrictions since the first outbreak in 1933have generally not been satisfactory in Zambia [55] After theoutbreaks recorded in 1934 1953 1973 1980 2004 and 2007geographical spread to other areaswas recorded For exampleduring the 2007 Sesheke outbreak the disease spread east-wards to Kazungula northwest to Senanga Mongu Kalaboand Shangombo near the border with Angola It is suspectedthat following the closure of the local abattoirs imposed bythe veterinary officials in enforcing the total movement banfarmers opted to search for market elsewhere spreading thedisease in the process The situation was exacerbated by thefact that oxen are a commonmeans of transport in the Barotsesands (an extension of the Kalahari sands) where motorvehicle transport is not often used because of poor tractionafforded by the sandy terrain

532 Fencing Separating Wildlife from Livestock Separationof wildlife from livestock using game fences is not currentlypracticed in Zambia because of the prohibitive costs Thisis despite movement of wildlife and livestock within andbetween ecosystems including transborder movement beingrife Previously game fences were erected in 1950s to controlmovement of tsetse flies from wildlife to cattle around theKafue national park until the 1980s when they collapsedbecause they could not be maintained [66] The effectivenessof these fences in controlling FMD is questionable giventhat outbreaks were recorded during the period Since the1990s movement of livestock and wildlife (ungulates) fromhigh risk areas is not permitted without prior screening forFMD The screening is through serology and virus isolationusing probing samples collected from the oral pharyngealarea while serology is by nonstructural protein (NSP) ELISAand liquid phase blocking ELISA (LPBE)

54 FMDDiagnostic Capacity Diagnosis of FMD is based onclinical suspicion followed by serology and virus isolation

541 Serology Serology using NSP and LPB ELISA is under-taken locally at Central Veterinary Research Institute (CVRI)


The world reference laboratory protocol for LPBE has beenadopted at CVRI with technical support from the regionalreference laboratories of Onderstepoort Veterinary Institute(OVI) of South Africa and Botswana Vaccine Institute (BVI)inBotswana [69] through the initiatives of the laboratory sub-committee of the Livestock Technical Committee of SADCBriefly the NSP detects antibodies to the polyproteins 3ABCof FMDV as an indicator of past or present infection for anyof the five serotypes of the virus existing in Zambia whetheror not the animal has been vaccinated [70] The LPBE onthe other hand detects antibodies to viral structural proteinsis more serotype specific and highly sensitive and detectsantibodies elicited by both vaccination and infection TheLPBE is a prescribed test for trade because it is appropriate forconfirming previous or on-going infection in nonvaccinatedanimals as well as for monitoring the immunity conferred byvaccination in the field if purified vaccines have been used[71 72]

The NSP and LPB ELISAs being used at CVRI requireto be optimised for the FMDV serotypes circulating inZambia The serology could be improved by validating theNSP assays that are being used to develop confidence in theresults In order to deal with ambiguity the LPBE test resultsrequire investment in virus neutralisation test (VNT) TheVNT could be used as confirmatory test in the detectionof FMDV-specific antibody in animals previously exposedto the virus [73 74] The VNT requires technical skill tobe performed accurately and is dependent on cell culturefacilities [6] which may not be conducive for laboratories inendemic regions The vaccines currently in use in Zambiaare not purified and the repeated vaccinations that existmay lead to NSP being produced that may be confusedwith NSP from natural infection This is a challenge in theinterpretation of NSP test results and impacts on the ability toexport from FMD-controlled regions Currently it is difficultto differentiate between vaccinated and previously infectedanimals in Zambia where nonpurified vaccines are used[75]

542 Virus Isolation Samples for virus isolation and charac-terisation are routinely sent to regional reference laboratoriesof OVI BVI and World Reference Laboratory (WRL) in theUnited Kingdom because Zambia lacks biosecurity level 3(BSL3) facilities However this involves the transportationof samples containing infectious FMDV which representsa significant biosecurity hazard and also incurs significantcosts The success of virus isolation is dependent on thesample quality and requires special transport conditionsfrom the sampling point to the laboratory [75] this presentschallenges for Zambia with poor laboratory infrastructureand trained manpower

Samples sent to reference laboratories are for virusisolation antigen ELISA and sequencing and phylogeneticanalysis [75] Such samples may include vesicular tissuesand fluids from outbreaks and oropharyngeal scrapping forsurveillance of carriers because more than 50 of infectedanimals may become carriers [26 76] but the duration ofpersistence and proportion that become carriers in Zambiaare not known It is not clear whether these carriers transmit

infection to susceptible cattle [75] Sequencing of the VP1gene or the full genome provides forensic evidence for thesource of the FMDV in outbreak situation as well as intracking the movement of buffalo strains [77]

543 Field Diagnostic Tests Themain challenge facing FMDdiagnostic capacity in Zambia is unavailability of real timeon the spot field diagnostic tests that could be used duringoutbreaks to identify circulating FMDV serotypes and topo-types for quick vaccinematching To overcome this challengeseveral tests have been developed

(1) Lateral Flow Devices Lateral flow devices (LFDs) havebeen developed and evaluated which are either serotypespecific [78] or can detect all seven FMDV serotypes [7980] LFDs are immunochromatographic tests that allow thediagnosis of FMDV at the site of a suspected outbreakThe LFD can utilise vesicular fluid or vesicular epithelialsuspensions but not nasal swabs or sera [78] The methodmakes use of capture and detection of monoclonal antibodiesor specific polyclonal antisera on a strip test and studies donethis far have shown the test to be as sensitive and specific asthe antigen ELISA however the sensitivity of the strip testmay differ for the various FMDV strains [81]

(2) Portable Real-Time PCR Platforms Portable real-timePCR platforms offer many advantages in endemic countrieslike Zambia [82] An example of is the Enigma FL fieldlaboratory platform (Enigma diagnostics) capable of nucleicacid extraction PCR thermocycling and analysis of datawithout the requirement for user intervention and has beentested for FMD diagnosis [82] These platforms require to beevaluated whether field-based assays can detect new virusesas they continue to evolve in sub-Saharan Africa Theseplatforms can be utilized by nonspecialists and are designedto perform all the steps of a RT-PCR test such as nucleicacid extraction and performing RT-PCRwhich is valuable forevaluating carriers

(3) Loop-Mediated Isothermal Amplification The loop-mediated isothermal amplification (LAMP) assay is an alter-native molecular detection technique with similar perfor-mance to real-time reverse transcriptase polymerase chainreaction (rt RT-PCR) that has been used widely for thedetection of RNA and DNA viruses that infect livestock [83]LAMP has the capacity to identify on the spot serotypes andcarriers in the field Yamazaki et al [84] developed amultiplexRT-LAMP approach to accommodate the high sequencevariability encountered in RNA virus genomes particularlyfor SAT strains and found the analytical sensitivity to becomparable to the singleplex RT-LAMP assays [83]

(4) Novel Diagnostic Assays Additional novel diagnosticassays such as biosensors [85] microarrays [86] goldnanoparticle (GNP) improved immuno-PCR (GNP-IPCR)[87] and nucleic acid sequence based amplification (NASBA)[88] have shown promising ability for rapid and reliable diag-nosis surveillance screening and strain typing for FMDVfor sub-Saharan Africa Some of the limitations of these


assays are that they are yet to beoptimised for the FMDVSAT serotypes with a high degree of sequence variability likeZambia The costs involved per test will also determine howwidely these assays will be used especially for developingcountries like Zambia The field-based novel assays willrequire training of personnel and some laboratory-based testsrequire specialised equipment which is not readily availabletogether with personnel capable of correctly interpreting andanalysing the datasets produced

55 Emergency Preparedness FMDdisease outbreaks requireimmediate and defined response in case of an incursionEmergency response plans exist in document form butrequire translation into action such as simulation exercisesAlthough an emergency disease control fund has been cre-ated funding is usually inadequate and contingency vaccinebanks have not been established and as such there is a longtime lag between disease identification and institution ofcontrol measures [1 43] This status quo usually exacerbatesthe spread of the disease resulting in increased cost of control[4]

56 Sociological Aspects Understanding smallholder farmersknowledge attitudes and perception and how they adapt toFMDoutbreaks is inadequate [29]During the 2004Namwalaoutbreak farmers abandoned their usualLutanga (local namefor transhumant village) located in the epicentre of theoutbreak For fear of the disease they opted for new grazingareas further away from the epicentre and consequentlyspreading the disease along the way

57 Delivery of Veterinary Services Zambia has experienceda decline in delivery of veterinary services since privatizationof veterinary services in the early 1990s and the introductionof the structural adjustment programmes [66]Thismay havenegatively affected the surveillance required for early warningsystem disease reporting and confirmation as required forthe FMD progressive control pathway [89 90]

6 Impact of FMD on the Zambian Economy

Impacts of FMD in sub-Saharan Africa have been describedin several studies but none for Zambia [29 91] Experiencein developed countries has shown that it is impossible toeconomically do livestock farming in the presence of FMD[92] The impacts reported here were based on Knight-Jonesand Rushton [93] framework

61 Direct Visible Losses Direct losses limit livestock produc-tivity creating food insecurity and contributing to malnutri-tionDuring the 2004Kafue flatsNamwala outbreak the calv-ing rate reduced during the calving season as most cows didnot conceive (Musso Munyeme personal communication)Herdsrsquo men had earlier observed that the bulls were failingto mount the cows during heat periods because of sores onthe feet On average around 300000 calves are born everyyear in this region [94] During the 2008 outbreak of FMDat a commercial farm in Mazabuka district milk productionwas reported to have dropped from 255 to 05 litres per

cow per day (Martin Ndhlovu personal communication) InZambia traditional farming using draught power accountsfor the largest production of crops [95] Elsewhere oxen havebeen observed to stay off plough for the whole season whenoutbreaks occur in a cropping season with drop in draughtpower of 60ndash70 after one month following infection [25]

62 Direct Invisible Losses Low conception rates of 52 to69 calving rates averaging 40 to 58 and long calvingto conception intervals of 18 to 20 months characterize thereproductive efficiency in Zambia [43] This may be a resultof endemic FMD infections [29] Fertility reduces because ofincrease in abortion rates of up to 10 [25] and prolongedintercalving interval by 12months due to delays in conception[96]

63 Indirect Impacts It is estimated that the Zambian-Government spends overUS$ 27million yearly on procuringvaccines and conducting and monitoring vaccination cam-paigns [97] Biannual vaccination campaigns conducted eachyear consume the productive time of both the farmer and thefield extensive officers to invest in other productive activitiesThis is difficult to quantify but in part offers a probableexplanation to the slow growth in the livestock sector [29]With respect to government cost of control it is estimatedthat the cost of erecting and maintaining one checkpointduring the 2004 Namwala outbreak was US$ 10000 for twoweeks [43] This figure may rise if the period is longer andsometimes three or more checkpoints were required Thecost of surveillance extension and farmer training in diseaseidentification and awareness adds to expenditure

64 InternalMarket Constraints In Zambia demand for beefis the highest in Lusaka with a human population of 2196996and the Copperbelt with 1958623 [14] During diseaseoutbreaks movement restrictions imposed on livestock fromaffected regions create a deficit that leads to upswing of pricesof beef and competing goods [29] Zambia currently importsbeef to satisfy local market demand and any drop in the localsourceworsens the situation Another consequence of being acountrywith endemic FMD is that Zambia cannot participatein international livestock trade For example as a result of the2010 Mbala serotype O outbreak Botswana imposed a totalban on import of maize bran from Zambia Zambia exportsin excess of 30000 metric tons of maize bran annually toBotswana [98] It is further estimated that over US$ 3Millionwas lost in revenue during the ban (George Phiri GrainTraders Association personal communication) In 2008 over500 sable antelopes (Hippotragus niger) could not be exportedto South Africa because of trade politics related to FMDLosses in income from exports of these prime sable antelopeshave been estimated at US$ 35 million annually [99]The lossin income from potential exports of beef and dairy productsif a disease free zone existed has been estimated to be overUS$ 16 billion per annum [2]

65 Effect on the Internal Economic Growth The periodbetween 2000 and 2010 was characterised by increase inthe numbers of FMD outbreaks in comparison to previousdecades During the same period the Zambian human


population was increasing at an average of 28 per annum[14] The cattle decline experienced in the early 2000s wasprobably due to droughts and eventual FMD outbreaks onthe Kafue flats The reduction in calving and conceptionrates alluded to earlier may have contributed Even thoughthe country recorded an upswing in cattle numbers from2381421 in 2005 to 2559 953 in 2010 [100] the growthwas not commensurate with the human population growthProbably the extension of the 2004 Namwala outbreak to2005 and 2006 as well as the 2007 to 2009 Mwandi outbreakin the middle Zambezi basin may have contributed Zambiaalso experienced positive economic growth in real GDP from2000 to 2010 [15] but the economic growth was slow tosupport the population growth This was mainly because thegrowth was driven by improved performance in mining andconstruction sectors while agriculture uponwhich 80 of thepopulation depends did not performwell recording relativelylow average growth rates inadequate infrastructure and poormarket access [1 101]

7 Discussion and Recommendations

The challenges of controlling FMD and economic impactsof its occurrence have been highlighted Zambia has devel-oped a risk based national FMD control strategy but theimplementation process needs to be scaled up In order tomaintain Zambiarsquos level 2 PCP status more work is neededto improve the organisation of infrastructure including thediagnostic capacity the epidemiology capacity to provideevidence on the absence of disease and if present the mag-nitude and mitigation measures being implemented Zambiamust undertake an annual assessment of evidence based onFMD related activities being undertaken to understand theepidemiology and control the disease [75] Understandingthe local epidemiology of FMD and the active monitoringof the virus circulating are the foundations of the PCP-FMD and activities to meet the requirements [75] Furtherdetermination of the factors influencing themaintenance andspread of the disease as well as knowledge of circulatingsubtypes of FMDV is essential for effective control of thedisease At present knowledge gaps exist in determinants ofdisease occurrence mechanisms of virus maintenance andtransmission

Control measures appear to be ineffective to stop thereoccurrence of disease [11] FMD control requires hugefinancial investments in infrastructure and research as thereare many epidemiological factors needing clarification [102]There is little research done on FMD in Zambia in compari-son to other southern African countries

Therefore FMD control in Zambia currently must focuson risk reduction measures for specified commodities ratherthan country or at least zonal freedom [103] One alternativefor sustainable FMD control under the existing endemic situ-ation could be Article 8525 of the Terrestrial Animal HealthCode [104] adopted by the Southern African DevelopmentCommunity Livestock Technical Group [105] Commoditybased trade (CBT) standard [104] offers a cost effectivealternative in deriving benefits from livestock and wildlifeconservation in endemic settings in comparison to zoning

The CBT may be utilized in the short to medium term toaccrue benefits whilst implementing the PCP in the longterm Care must be made to assess the risks of other diseasessuch as tuberculosis and brucellosis among others [106] CBTand the PCP need to complement each other for Zambiato accrue the benefits from livestock and wildlife trade Theadoption of CBT is envisaged to boost intraregional tradethat may accelerate sub-Saharan Africarsquos economic growthTherefore guidelines to operationalize CBT standards whenavailable may offer countries like Zambia an alternative forFMD control in view of the TFCA that have been created

FMD is essentially a disease of poverty in Zambia becauseof the negative effects on livestock production and produc-tivity competitiveness and access to lucrative internationalmarkets The disease is a drain on the national treasuryin a country where resources are scarce and FMD controlcompetes with other priority sectors like health and educa-tion Even within agriculture priority is given to maize andfertilizer support programs the commodity being a staplefood and preference is understandably for economic andpolitical reasons

Clearly FMD impacts negatively on the Zambian econ-omy and may be responsible for the low economic growth[29] Zambiarsquos FMD endemic situation inhibits delivery ofeconomic benefits through animal exports with 80 of itspopulation being dependent on agriculture [1] The FMDendemicity may be the reason for poor investment in live-stock as noted from the stagnant cattle numbers in relationto the upswing in human population For example whilst thehuman population has been increasing annually at 28 thecattle numbers have relatively remained stagnant [14 21]

In order to ensure effective disease surveillance andmonitoring there is need to invest in a low containmentbiosecurity level 2 laboratories for the country to engagein monitoring of FMDV strains circulating in livestock andwildlife Investment in diagnostic tests may need scalingup to monitor field performance of vaccines and determineserological levels needed for protection Included is themonitoring of the development of carriers an importantaspect for regulating movement control and creation ofdisease freedom Budget allocation for diagnostic kits and in-house reagents with proficiency testing with regional centersmust be scaled up Onsite tests that can identify incubatinganimals not fit for vaccination may need to be developed Wepropose an annual review of the vaccination programs usingempirical data from carrier development vaccine efficacyand coverage surveys The review may also include socialeconomic factors that relate to vaccination and uptakeThere-fore to understand the epidemiology of FMD endemicityin Zambia various research approaches may be requiredIncluded is the identification of risk determinants includingsociological epidemiological and ecological factors in orderto be able to advance on the FAOOIE progressive controlpathway for FMD

Conflict of Interests

The authors have no conflict of interests that could influenceor bias the content of this paper


Authorsrsquo Contribution

Y Sinkala conducted the review and prepared the paper MSimuunza J B Muma and H M Munangrsquoandu edited thepaper andM Mulumba C J Kasanga A S Mweene and DU Pfeiffer approved and proofread the work

Acknowledgments

The work is supported through a Grant WTO 87546MAfrom the Wellcome Trust to Southern Africa Centre forInfectious Disease Surveillance (SACIDS) The authors aregrateful to the Government of the Republic of Zambia for allthe documents referenced in this study

References

[1] Sixth National Development Plan for Zambia 2011 to 2015Republic of Zambia Ministry of Finance and National Plan-ning Lusaka Zambia 2011 httpwwwmofnpgovzm

[2] WorldBank What Would it Take for Zambiarsquos Beef and DairyIndustries to Achieve Their Potential 2011 httpsopenknowl-edgeworldbankorghandle109862771

[3] M Rweyemamu P Roeder D MacKay K Sumption J Brown-lie and Y Leforban ldquoPlanning for the progressive controlof foot-and-mouth disease worldwiderdquo Transboundary andEmerging Diseases vol 55 no 1 pp 73ndash87 2008

[4] G R Thomson ldquoCurrently important animal disease manage-ment issues in sub-Saharan Africardquo Onderstepoort Journal ofVeterinary Research vol 76 no 1 pp 129ndash134 2009

[5] ldquoFoot-and-mouth disease (FMD Aphthous fever)rdquo in Veteri-nary Medicine A Textbook of the Diseases of Cattle Sheep PigsGoats andHorses O Radostits D C Blood and C C Gay Edspp 965ndash974 WB Saunders Company London UK 1994

[6] OIE ldquoOIE Manual of Diagnostics for Foot and Mouth Diseasechapter 215rdquo 2012 httpwwwoieintfileadminHomeengHealth standardstahm20105 FMDpdf

[7] N Knowles ldquoFoot-and-Mouth Disease Virus Variation andMolecular Epidemiology in Africardquo in Global Foot and MouthDisease Research Alliance Workshop Arusha Tanzania 2013httpwwwarsusdagovGFRAevents201320GFRA20work-workshop20AGENDApdf

[8] J P A Morris Annual Report for the Department of VeterinaryServices for the Year 1933 Government of Northern RhodesiaPrinted by Government Printers Lusaka Zambia 1934

[9] P Chilonda J D Woodford B Ahmadu K L Samui MSyakalima and J E D Mlangwa ldquoFoot and mouth diseasein Zambia a review of the aetiology and epidemiology andrecommendations for possible controlrdquo Revue Scientifique etTechnique vol 18 no 3 pp 585ndash592 1999

[10] Annual Report for Zambia Wildlife Authority for the Year 2007Zambia Wildlife Authority Lusaka Zambia 2008

[11] G Thomson M-L Penrith and G Fosgate ldquoTechnical chal-lenges associated with the eradication of TADs in southernAfrica with special reference to FMDrdquo in Proceedings of theJoint SADCAHEAD Workshop Reconcilling Livestock Healthand Wildlife Conservation Goals in Southern Africa Strategiesfor Sustainable Economic Development Gaborone BotswanaNovember 2012

[12] OIE et al ldquoProgressing towards Foot and Mouth Disease(FMD) Control and OIE recognized status of SADC Member

Statesrdquo in FAOOIE Subregional SeminarmdashJoint meeting onthe Progressive Control Pathway for Foot and Mouth Diseaseand approaches to support its implementation GaboroneBotswana OIE and FAO 2011 httpwwwoieintdocgedD10576PDF

[13] SADC Southern African Development Community MemberStates 2014 httpwwwsadcintmember-states

[14] CSO 2010 Census of Population and Housing Lusaka 2010httpunstatsunorgunsddemographicsourcescensus2010phcZambiaPreliminaryReportpdf

[15] ldquoAnonymousrdquo Annual Report Bank of Zambia Lusaka Zam-bia 2010 httpwwwbozzmAnnualReportsBOZAnnualRe-port2010pdf

[16] J B Muma M Munyeme K L Samui et al ldquoMortality andcommercial off-take rates in adult traditional cattle of ZambiardquoTropical Animal Health and Production vol 41 no 5 pp 783ndash789 2009

[17] World Fact Book-Zambia 2013 httpswwwciagovlibrarylibrarypublicationsthe-world-factbookgeoszahtml

[18] FAO Livestock Sector Brief on Zambia 2005 httpwwwfaoorgagagainforesourcesenpublicationssector briefslsbZMBpdf

[19] FAO Country Statistics on Zambia 2014 httpwwwfaoorgcountryprofilesindexeniso3=ZMB

[20] B D Perry B Mwanaumo H F Schels E Eicher and MR Zaman ldquoA study of health and productivity of traditionallymanaged cattle in Zambiardquo Preventive Veterinary Medicine vol2 no 5 pp 633ndash653 1984

[21] Annual Report for the Department of Veterinary Services for2010 Government of Zambia Ministry of Livestock and Fish-eries Development Lusaka Zambia 2011

[22] J B Muma K L Samui V M Siamudaala et al ldquoPrevalence ofantibodies to Brucella spp and individual risk factors of infec-tion in traditional cattle goats and sheep reared in livestock-wildlife interface areas of Zambiardquo Tropical Animal Health andProduction vol 38 no 3 pp 195ndash206 2006

[23] M Munyeme J B Muma K L Samui et al ldquoPrevalence ofbovine tuberculosis and animal level risk factors for indigenouscattle under different grazing strategies in the livestockwildlifeinterface areas of Zambiardquo Tropical Animal Health and Produc-tion vol 41 no 3 pp 345ndash352 2009

[24] J L Siembieda R A Kock T A McCracken and S H New-man ldquoThe role of wildlife in transboundary animal diseasesrdquoAnimal Health Research Reviews vol 12 no 1 pp 95ndash111 2011

[25] T R Doel ldquoFMD vaccinesrdquo Virus Research vol 91 no 1 pp81ndash99 2003

[26] J S Salt ldquoThe carrier state in foot and mouth diseasemdashanimmunological reviewrdquo British Veterinary Journal vol 149 no3 pp 207ndash223 1993

[27] J B Muma K L Samui V M Siamudaala et al ldquoPrevalenceof antibodies to Brucella spp and individual risk factorsof infection in traditional cattle goats and sheep reared inlivestock-wildlife interface areas of Zambiardquo Tropical AnimalHealth and Production vol 38 no 3 pp 195ndash206 2006

[28] J B Muma Epidemiology of Brucella Infections in LivestockmdashWildlife Interface Areas in Zambia Department of Food Safetyand Infection Biology Norwegian School of Veterinary ScienceOslo Norway 2006

[29] BD Perry andKM Rich ldquoPoverty impacts of foot-and-mouthdisease and the poverty reduction implications of its controlrdquoVeterinary Record vol 160 no 7 pp 238ndash241 2007


[30] F Banda C J Kasanga R Sallu et al ldquoInvestigation of foot-and-mouth disease outbreaks in the Mbala and Kazungula districtsof Zambiardquo Onderstepoort Journal of Veterinary Research vol81 no 2 6 pages 2014

[31] C J Kasanga J Wadsworth C A Mpelumbe-Ngeleja et alldquoMolecular characterization of foot-and-mouth disease virusescollected in Tanzania between 1967 and 2009rdquo Transboundaryand Emerging Diseases 2014

[32] FAO-WRLFMD ldquoOIEFAO Reference Laboratory ContractReport JanuaryndashMarch 2012rdquo December 2013 httpwwwwrlfmdorgref labsref lab reportsOIE-FAO20FMD20Ref20Lab20Report20Jan-Mar202012pdf

[33] Anonymous Annual Report for the Department of VeterinaryServices for the Year 2001 Ministry of Ministry of AgricultureFood and Fisheries Lusaka Lusaka Zambia 2002

[34] P A Lindsey J Barnes V Nyirenda et al ldquoThe zambian wildliferanching industry scale associated benefits and limitationsaffecting its developmentrdquo PLoS ONE vol 8 no 12 Article IDe81761 2013

[35] P Chaminuka R A Groeneveld and E C van IerlandldquoReconciling interests concerning wildlife and livestock nearconservation areas a model for analysing alternative land usesrdquoEcological Economics vol 98 pp 29ndash38 2013

[36] J B Muma A Lund V M Siamudaala et al ldquoSerosurveyof Brucella spp infection in the Kafue lechwe (Kobus lechekafuensis) of the Kafue flats in Zambiardquo Journal of WildlifeDiseases vol 46 no 4 pp 1063ndash1069 2010

[37] H M Munangrsquoandu V M Siamudaala A Nambota et alldquoDisease constraints for utilization of the African buffalo(Syncerus caffer) on game ranches in Zambiardquo Japanese Journalof Veterinary Research vol 54 no 1 pp 3ndash13 2006

[38] M Munyeme J B Muma E Skjerve et al ldquoRisk factorsassociated with bovine tuberculosis in traditional cattle of thelivestockwildlife interface areas in the Kafue basin of ZambiardquoPreventive Veterinary Medicine vol 85 no 3-4 pp 317ndash3282008

[39] K K Mwacalimba C Mumba andMMunyeme ldquoCost benefitanalysis of tuberculosis control in wildlife-livestock interfaceareas of Southern Zambiardquo Preventive Veterinary Medicine vol110 no 2 pp 274ndash279 2013

[40] C Chomba C Obias and V Nyirenda ldquoGame ranchinga sustainable land use option and economic incentive forbiodiversity conservation in Zambiardquo Open Journal of Ecologyvol 4 no 9 pp 571ndash581 2014

[41] R Bengis R A Kock G R Thomson and R D BigalkeldquoInfectious diseases of animals in sub-Saharan Africa thewildlifelivestock interfacerdquo in Infectious Diseases of Livestockpp 225ndash238 2004

[42] D A McGranahan ldquoManaging private commercial rangelandsfor agricultural production and wildlife diversity in Namibiaand Zambiardquo Biodiversity and Conservation vol 17 no 8 pp1965ndash1977 2008

[43] Disease Free Zone Concept Paper Ministry of Agricultureand Cooperatives Department of Veterinary and LivestockDevelopment Lusaka Zambia 2009

[44] M D Hall N J Knowles J Wadsworth A Rambaut andM E J Woolhouse ldquoReconstructing geographical movementsand host species transitions of foot-and-mouth disease virusserotype SAT 2rdquoMBio vol 4 no 5 Article ID e00591-13 2013

[45] R S Hedger ldquoFoot-and-mouth disease and the African buffalo(Syncerus caffer)rdquo Journal of Comparative Pathology vol 82 no1 pp 19ndash28 1972

[46] W Vosloo L de Klerk C I Boshoff et al ldquoCharacterisation ofa SAT-1 outbreak of foot-and-mouth disease in captive Africanbuffalo (Syncerus caffer) clinical symptoms genetic charac-terisation and phylogenetic comparison of outbreak isolatesrdquoVeterinary Microbiology vol 120 no 3-4 pp 226ndash240 2007

[47] P S Dawe F O Flanagan R L Madekurozwa et al ldquoNaturaltransmission of foot-and-mouth disease virus from Africanbuffalo (Syncerus caffer) to cattle in a wildlife area of Zim-babwerdquo Veterinary Record vol 134 no 10 pp 230ndash232 1994

[48] M D Gainaru G R Thomson R G Bengis J J Ester-huysen W Bruce and A Pini ldquoFoot-and-mouth disease andthe African buffalo (Syncerus caffer) II Virus excretion andtransmission during acute infectionrdquoTheOnderstepoort Journalof Veterinary Research vol 53 no 2 pp 75ndash85 1986

[49] S K Hargreaves C M Foggin E C Anderson et al ldquoAninvestigation into the source and spread of foot and mouthdisease virus from a wildlife conservancy in Zimbabwerdquo OIERevue Scientifique et Technique vol 23 no 3 pp 783ndash790 2004

[50] M Rweyemamu P Roeder D MacKay et al ldquoEpidemiologicalpatterns of foot-and-mouth disease worldwiderdquoTransboundaryand Emerging Diseases vol 55 no 1 pp 57ndash72 2008

[51] E C Anderson C Foggin M Atkinson K J Sorensen R LMadekurozva and J Nqindi ldquoThe role of wild animals otherthan buffalo in the current epidemiology of foot-and-mouthdisease in Zimbabwerdquo Epidemiology and Infection vol 111 no3 pp 559ndash563 1993

[52] A D S Bastos C I Boshoff D F Keet R G Bengis and GR Thomson ldquoNatural transmission of foot-and-mouth diseasevirus between African buffalo (Syncerus caffer) ans impala(Aepyceros melampus) in the Kruger National Park SouthAfricardquo Epidemiology and Infection vol 124 no 3 pp 591ndash5982000

[53] PHunter ldquoVaccination as ameans of control of foot-and-mouthdisease in sub-saharan AfricardquoVaccine vol 16 no 2-3 pp 261ndash264 1998

[54] G Akafekwa ldquoThe sanitary position and methods of controlused in Zambiamdash1979rdquo Bulletin de lrsquoOffice International desEpizooties vol 92 no 7-8 pp 647ndash653 1980

[55] BD Perry andR SHedger ldquoHistory and epidemiology of foot-and-mouth disease in zambia a reviewrdquo Tropical Animal Healthand Production vol 16 no 2 pp 107ndash114 1984

[56] OIE Disease status report on Foot and mouth disease inBotswana information received on 31102012 from DrLetlhogile Modisa Director Veterinary Services Ministry ofAgriculture Gaborone Botswana 2013 httpwwwoieintwahis 2publicwahidphpReviewreportReviewreportid=12450

[57] Annual Report of the Department of Veterinary and TsetseControl Services for the Year 1973 Republic of Zambia Ministryof Rural Development Lusaka Zambia 1976

[58] P Sutmoller and S J Barteling ldquoThe history of foot-and-mouthdisease vaccine development a personal perspectiverdquo in Foot-and-Mouth Disease Control Strategies pp 259ndash272 2003

[59] P Sutmoller S S Barteling R COlascoaga andK J SumptionldquoControl and eradication of foot-and-mouth diseaserdquo VirusResearch vol 91 no 1 pp 101ndash144 2003

[60] Anonymous Operation Noah a Zambia Safari Rescue Story2013 httpoperationnoahblogspotcom

[61] AnonymousAnnual Report of theDepartment of Veterinary andTsetse Control Services for the Year 1979 Ministry of Agricultureand Water Development Lusaka Zambia 1985


[62] GFRA Global Foot and Mouth Disease Research AllianceWorkshop Resolutions in 2013 GFRA Scientific Workshop Epi-demiology Surveillance Transmission and Control of Foot-and-Mouth Disease in Endemic Settings of Africa Hosted bySokoine University of Agriculture and Southern Africa Centrefor Infectious Disease Surveillance 8 to 10 October 2013 GFRAArusha Tanzania 2013 httpwwwarsusdagovGFRAevents201320GFRA20workshop20AGENDApdf

[63] A D S Bastos D T Haydon O Sangare C I Boshoff J LEdrich and G RThomson ldquoThe implications of virus diversitywithin the SAT2 serotype for control of foot-and-mouth diseasein sub-Saharan Africardquo Journal of General Virology vol 84 no6 pp 1595ndash1606 2003

[64] FAO-WRLFMD ldquoMolecular Epidemiology Reports on Foot-and-Mouth Disease in Zambia by the FAO World ReferenceLaboratory for Foot-and Mouth Disease for 2011rdquo 2013

[65] A J M Garland ldquoVital elements for the successful control offoot-and-mouth disease by vaccinationrdquo Vaccine vol 17 no 13-14 pp 1760ndash1766 1999

[66] G Muuka N Songolo S Kabilika B M Hangrsquoombe KS Nalubamba and J B Muma ldquoChallenges of controllingcontagious bovine pleuropneumonia in sub-Saharan Africa aZambian perspectiverdquo Tropical Animal Health and Productionvol 45 no 1 pp 9ndash15 2012

[67] W Vosloo A D S Bastos O Sangare S K Hargreaves andG R Thomson ldquoReview of the status and control of foot andmouth disease in sub-Saharan Africardquo OIE Revue Scientifiqueet Technique vol 21 no 3 pp 437ndash449 2002

[68] Y Sinkala M Simuunza J B Muma D U Pfeiffer C JKasanga and A Mweene ldquoFoot and mouth disease in Zambiaspatial and temporal distributions of outbreaks assessment ofclusters and implications for controlrdquo Onderstepoort Journal ofVeterinary Research vol 81 no 2 6 pages 2014

[69] ldquoSADC Harmonised SOP for the detection of foot and mouthdisease virus (FMDV) antibodies using liquid phase block-ing ELISArdquo in Annonymous G Thobokwe and R DwarkaEds Southern Africa Development Community GaboroneBotswana 2010

[70] D K J Mackay M A Forsyth P R Davies et al ldquoDifferentiat-ing infection from vaccination in foot-and-mouth disease usinga panel of recombinant non-structural proteins in ELISArdquoVaccine vol 16 no 5 pp 446ndash459 1998

[71] C Hamblin I T R Barnett and R S Hedger ldquoA new enzyme-linked immunosorbent assay (ELISA) for the detection of anti-bodies against foot-and-mouth disease virus I Developmentand method of ELISArdquo Journal of Immunological Methods vol93 no 1 pp 115ndash121 1986

[72] B M D C Bronsvoort S Parida I Handel et al ldquoSerologicalsurvey for foot-and-mouth disease virus in wildlife in easternAfrica and estimation of test parameters of a nonstructural pro-tein enzyme-linked immunosorbent assay for Buffalordquo Clinicaland Vaccine Immunology vol 15 no 6 pp 1003ndash1011 2008

[73] E Brocchi I E Bergmann A Dekker et al ldquoComparativeevaluation of six ELISAs for the detection of antibodies tothe non-structural proteins of foot-and-mouth disease virusrdquoVaccine vol 24 no 47-48 pp 6966ndash6979 2006

[74] D J Paton K de Clercq M Greiner et al ldquoApplication ofnon-structural protein antibody tests in substantiating freedomfrom foot-and-mouth disease virus infection after emergencyvaccination of cattlerdquoVaccine vol 24 no 42-43 pp 6503ndash65122006

[75] S M Jamal and G J Belsham ldquoFoot-and-mouth disease pastpresent and futurerdquo Veterinary Research vol 44 p 116 2013

[76] P Sutmoller and A Gaggero ldquoFoot-and mouth diseases carri-ersrdquoThe Veterinary Record vol 77 no 33 pp 968ndash969 1965

[77] W Vosloo R M Dwarka A D S Bastos et al ldquoMolecularepidemiological studies of foot-and-mouth disease virus insub-Saharan Africa indicate the presence of large numbers oftopotypes implications for local and international controlrdquo inProceedings of the Open Session of the EU-FMD Research Grouppp 149ndash158 FAO Crete Greece 2004 httpwwwfaoorgagagainfocommissionsdocsgreece04App22pdf

[78] M Yang M Goolia W Xu H Bittner and A ClavijoldquoDevelopment of a quick and simple detectionmethodology forfoot-and-mouth disease virus serotypes O A and Asia 1 usinga generic RapidAssay Devicerdquo Virology Journal vol 10 article125 2013

[79] S M Reid N P Ferris A Bruning G H Hutchings ZKowalska and L Akerblom ldquoDevelopment of a rapid chro-matographic strip test for the pen-side detection of foot-and-mouth disease virus antigenrdquo Journal of Virological Methodsvol 96 no 2 pp 189ndash202 2001

[80] N P Ferris A Nordengrahn G H Hutchings et al ldquoDevelop-ment and laboratory validation of a lateral flow device for thedetection of serotype SAT 2 foot-and-mouth disease viruses inclinical samplesrdquo Journal of Virological Methods vol 163 no 2pp 474ndash476 2010

[81] KO JaeN P Ferris K Lee Y Joo BHyun and J Park ldquoSimpleand rapid lateral-flow assay for the detection of foot-and-mouthdisease virusrdquo Clinical and Vaccine Immunology vol 16 no 11pp 1660ndash1664 2009

[82] D P King J P Dukes S M Reid et al ldquoProspects for rapiddiagnosis of foot-and-mouth disease in the field using reversetranscriptase-PCRrdquo Veterinary Record vol 162 no 10 pp 315ndash316 2008

[83] J P Dukes D P King and S Alexandersen ldquoNovel reversetranscription loop-mediated isothermal amplification for rapiddetection of foot-and-mouth disease virusrdquoArchives of Virologyvol 151 no 6 pp 1093ndash1106 2006

[84] W Yamazaki V Mioulet L Murray et al ldquoDevelopmentand evaluation of multiplex RT-LAMP assays for rapid andsensitive detection of foot-and-mouth disease virusrdquo Journal ofVirological Methods vol 192 no 1-2 pp 18ndash24 2013

[85] M T Sanchez-Aparicio M F Rosas R M Ferraz et alldquoDiscriminating foot-and-mouth disease virus-infected andvaccinated animals by use of 120573-galactosidase allosteric biosen-sorsrdquo Clinical and Vaccine Immunology vol 16 no 8 pp 1228ndash1235 2009

[86] M K Baxi S Baxi A Clavijo K M Burton and D DeregtldquoMicroarray-based detection and typing of foot-and-mouthdisease virusrdquo Veterinary Journal vol 172 no 3 pp 473ndash4812006

[87] Y Z Ding Y Liu J Zhou et al ldquoA highly sensitive detection forfoot-and-mouth disease virus by gold nanopariticle improvedimmuno-PCRrdquo Virology Journal vol 8 article 148 2011

[88] R A Collins L Ko K Y Fung L Lau J Xing and A C H YuldquoAmethod to detect major serotypes of foot-and-mouth diseasevirusrdquo Biochemical and Biophysical Research Communicationsvol 297 no 2 pp 267ndash274 2002

[89] K Sumption M Rweyemamu and W Wint ldquoIncidence anddistribution of foot-and-mouth disease in Asia Africa andSouth America combining expert opinion official disease


information and livestock populations to assist risk assessmentrdquoTransboundary and Emerging Diseases vol 55 no 1 pp 5ndash132008

[90] OIE and FAO ldquoEuFMD-ECTAD-OIE-BVI joint meeting onthe progressive control pathway for foot andmouth disease andapproaches to support its implementationrdquo in Proceedings ofthe FAOOIE Sub-Regional Seminar OIE Gaborone BotswanaMarch 2011 httpwwwrr-africaoieintdocspdfen2011PCPFMD Reportpdf

[91] T F Randolph J A Morrison and C Poulton ldquoEvaluatingequity impacts of animal disease control the case of foot andmouth disease in Zimbabwerdquo Review of Agricultural Economicsvol 27 no 3 pp 465ndash472 2005

[92] G R Thomson ldquoOverview of foot and mouth disease insouthern Africardquo Revue Scientifique et Technique vol 14 no 3pp 503ndash520 1995

[93] T J D Knight-Jones and J Rushton ldquoThe economic impactsof foot and mouth disease what are they how big are they andwhere do they occurrdquo Preventive Veterinary Medicine vol 112no 3-4 pp 161ndash173 2013

[94] CSO Post Harvest Survey for the period 2010mdash2011 Ministryof Finance and National Planning Central Statistical OfficeLusaka Zambia 2011

[95] J B Muma M Munyeme K K Simuunza et al ldquoContributionof ox draught power towards crop production a case study ofsouthern provincerdquo UNZA Journal of Science and Technologyvol 15 no 2 pp 29ndash35 2011

[96] B Bayissa G AyeletM Kyule Y Jibril and EGelaye ldquoStudy onseroprevalence risk factors and economic impact of foot-and-mouth disease in Borena pastoral and agro-pastoral systemsouthern Ethiopiardquo Tropical Animal Health and Production vol43 no 4 pp 759ndash766 2011

[97] Estimates of Revenue and Expenditure (Activity Based Budget)for the Year 1st January 2012 to 31st December 2012 Governmentof the Republic of Zambia Ministry of Finance and NationalPlanning Lusaka Zambia 2012 Printed by Government Print-ers

[98] CSO International Trade Statistics Ministry of Finance andNational Planning Central Statistics Office Lusaka Zambia2013

[99] Anonymous Wildlife Auctions 2010 httpwwwwildlifeauc-tionscozagamephp

[100] Annual Report for the Year 2010 Ministry of Agricultureand Cooperatives Department of Veterinary and LivestockDevelopment Lusaka Zambia 2011

[101] ldquoFifth National Development Plan for 2006 to 2010rdquo Ministryof Finance and National Planning Lusaka Zambia 2006

[102] W Vosloo ldquoFoot and mouth disease situation and controlstrategies in sub-Saharan Africamdashthe current situationrdquo inProceedings of the OIEFAO Global Conference on Foot andMouth Disease The Way Towards Global Control AsuncionParaguay June 2009 httpwwwoieintfileadminHomeengConferences EventssitesA FMD 2009presentations-FMDhtml

[103] G R Thomson M L Penrith M W Atkinson S J AtkinsonD Cassidy and S A Osofsky ldquoBalancing livestock productionand wildlife conservation in and around southern Africarsquostransfrontier conservation areasrdquo Transboundary and EmergingDiseases vol 60 no 6 pp 492ndash506 2013

[104] OIETerrestrial AnimalHealth Code on Foot andMouthDiseaseArticle 861 2012 httpwwwoieintindexphpid=169ampL=0amphtmfile=chapitre 186htm

[105] ldquoResolution by the Southern AfricanDevelopment Community(SADC) calling for adoption of commodity-based trade andother non-geographic approaches for foot and mouth diseasemanagement as additional regional standards for trade inanimal productsrdquo in Proceedings of the Joint SADCAHEADWorkshop Reconcilling Livestock Health and Wildlife Con-servation goals in Southern Africa Strategies for SustainableEconomic Development Gaborone Botswana November 2012httpwwwwcs-aheadorgphakalane declarationhtml

[106] P Sutmoller ldquoThe fencing issue relative to the control offoot-and-mouth diseaserdquo Annals of the New York Academy ofSciences vol 969 pp 191ndash200 2002

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D RCongo

Tanzania

Lusaka

Mbala

Mongu

Sesheke

Chobe0 260

520130

GMANational parks

District boundaryInternational boundary Wetlands

0 130 260390

390520

65(km)

(km)

35∘09984000998400998400E30

∘09984000998400998400E25

∘09984000998400998400E20

∘09984000998400998400E

N

35∘09984000998400998400E30

∘09984000998400998400E25

∘09984000998400998400E20

∘09984000998400998400E

10∘09984000998400998400S

15∘09984000998400998400S

10∘09984000998400998400S

15∘09984000998400998400S

FMD cases

Figure 1 Showing distribution of FMD cases in relation to wildlife protected areas and wetlands Map adapted from Sinkala et al 2014 [68]

a definitive domestic host for life cycle [11] The Food andAgriculture Organization (FAO) of the United Nations (UN)FMD progressive control pathway (PCP) classified Zambiaas being at level 2 [12] And as such identification of FMDcontrol challenges and economic impactsmay provide oppor-tunities for investment in advancing to the desired level 3classification of the (Organization of International Epizootics(OIE) progression criteria To attain this it is imperativethat we understand the limitations that have led Zambianot to progress into attaining the desired level 3 criteriaTherefore the objective of this review was to describe thecontrol challenges and economic impacts of FMD outbreaksin Zambia In doing so we reviewed published literature onFMD outbreaks control and impact The literature searchwas conducted on major electronic databases includingPubMed Science Direct Cabi direct and Springer usingspecified search terms The search terms included ldquoaphthousfever aphthae epizooticae hoof and mouth disease footand mouth disease and Zambiardquo The inclusion criteriawere studies published in English in peer-reviewed journalsand studies where full text was available Further greyliterature from government institutions was obtained Theseincluded annual reports from the Ministry of Agricultureand Livestock for the period 1933 to 1912 economic andpolicy documents from theMinistry of Finance and NationalPlanning as well as the Bank of Zambia between 2000 and2010 and Central Statistical Office population census reports2000 and 2010 Furthermore expert opinions on impacts

of FMD were obtained through focused discussions withfarmers scientists commodity associations and personalfield experiences We discuss the findings with the aimof bringing into perspective the challenges experienced bythe government in controlling FMD and the economicalimplication of the disease in Zambia that would serve asan example to other countries faced with similar challengesAnd we also highlight the possible solution that would helpovercome these predicaments

2 Challenges in the LivestockProduction System

Zambia is a landlocked country covering 752 610 km2between latitudes 8∘ and 18∘ south of the Equator and longi-tudes 22∘ and 34∘ east of the Greenwich Meridian (Figure 1)The country shares borders with eight Southern AfricaDevelopment Community (SADC) member countries [13]and is composed of 10 administrative areas called provincesZambia is regarded as one of the least urbanised countriesin Africa with an estimated total population of 134 millionpeople majority of whom (61) are concentrated mainly inthe rural areas [14] Agriculture contributes about 215 togross domestic product (GDP) out of which 28 is from thelivestock subsector [15 16] The national per capital incomeis one of the lowest in the world estimated at US$ 1700for 2012 [17] Of the total land 475 is agricultural land






























50per dose [3] but





53 Movement Control













































Acknowledgments


References























































































































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of



































50per dose [3] but





53 Movement Control













































Acknowledgments


References























































































































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of













































Acknowledgments


References























































































































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of






























































































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of






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