research article a qualitative assessment of the risk of...

Research ArticleA Qualitative Assessment of the Risk of Introducing Pestedes Petits Ruminants into Northern Zambia from Tanzania

R Chazya12 J B Muma2 K K Mwacalimba3 E Karimuribo4

E Mkandawire2 and M Simuunza2

1 Department of Veterinary Services Ministry of Agriculture and Livestock PO Box 830011 Mumbwa Zambia2Department of Disease Control School of Veterinary Medicine University of Zambia PO Box 32379 Lusaka Zambia3 Independent Policy Researcher 4639 D Santa Cruz Drive Indianapolis IN 46268 USA4Department of Veterinary Medicine and Public Health Sokoine University of Agriculture PO Box 3021 Morogoro Tanzania

Correspondence should be addressed to J B Muma jmumaunzazm

Received 6 August 2013 Accepted 18 October 2013 Published 12 January 2014

Academic Editor Timm C Harder

Copyright copy 2014 R Chazya et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

A qualitative risk assessment was performed to evaluate the risk of introducing Peste des petits ruminants virus into northernZambia from Tanzania via live goat trade Data was collected during a mission to Tanzania and northern Zambia and also fromliterature and interviewswith expertsThe risk of PPRV introductionwas evaluated as a function of the probability of hazard (PPRV)release exposure of susceptible hosts and the consequences of spread using the following parameters prevalence of infectionvolume of trade C-ELISA and quarantine screening missing an infected animal PPRV viability (remaining infective) in transitand the virus potential for infection The magnitude of the consequences was derived from the probability of transmission andspread and the impact of PPRV introduction and establishment Accordingly the probability of occurrence of PPRV in northernZambia from Tanzania was rated as ldquohighrdquo and the economic consequences were also rated as ldquohighrdquo Finally the overall risk ofintroducing PPRV into northern Zambia from Tanzania at the time of the assessment was rated ldquohighrdquo It was concluded thatimport of goats and sheep be prohibited until efficient and adequate measures to reduce the risk have been put in place

1 Introduction

Peste des petits ruminants (PPR) is a viral disease of smallruminants that threatens the national food security of affectedcountriesThe disease has high morbidity andmortality ratesand greatly impacts the economies of affected countries oftenas a consequence of trade loss due to sanitary embargoes [1]In the Southern African Development Community (SADC)region the disease was officially reported in northern Tan-zania in 2008 [2] and later spread to the south in 2010[3] The Democratic Republic of Congo (DRC) reportedoutbreaks of PPR that caused death of almost 120000 smallruminants valued at US$53 million from 2010 to June 2012[4] This did not take into account the socioeconomic andother benefits of goats and sheep to smallholder farmers [5]In October 2012 Angola reported an outbreak of PPR inCabinda Province due to illegal movement of a herd of 55sheep and goats brought from DRC [6] Therefore PPR is

a disease of increasing importance in Africa particularly inareas where small ruminants form an important componentof agricultural food production Livestock production is animportant agricultural activity in most of the countries inSouthern Africa [7] and goats play an important socioeco-nomic role in rural areas especially for women who areamong the most vulnerable farmers in AfricaThis is becausegoats and sheep are prolific and require low capital inputs fora moderate level of production reaching maturity early andare profitable to keep [8] Until recently PPR was consideredabsent in the SADC region and as such most countrieshave not developed strategies on how to stem the spread ofthe disease in the event of an incursion [9] It is thereforeassumed that if the disease were allowed to spread from theDRC and Tanzania into the whole of the 15-nation SADCregion it could potentially devastate the livelihoods and foodsecurity of millions of vulnerable smallholder farmers andagropastoralists [9] In Zambia PPR is a notifiable disease

Hindawi Publishing CorporationVeterinary Medicine InternationalVolume 2014 Article ID 202618 10 pageshttpdxdoiorg1011552014202618

2 Veterinary Medicine International

Isoka

Chinsali

Mpika

Kasama

Chilubi

Luwingu

Mporokoso

KaputaMpulungu

Mbala

MungwiNakonde

Tanzania

Malawi

DRCMozambique

Figure 1 Location ofMpulunguMbala andNakonde in relation to other districts ofNorthernZambia andTanzania onNorthWest Tanzaniais located in the north

which has not been reported despite its sharing borders withthe affected countries [5]

PPR is caused by the PPR virus (PPRV) which belongsto the genus morbillivirus under the family Paramyxoviridae[1] PPRV is an RNA virus which is closely related to themeasles rinderpest and distemper viruses [10] There isonly one serotype of PPRV but there are at least 4 lineageswhich are distinguishable by nucleic acid sequencing Thevirus is not very resistant and is rapidly inactivated at envi-ronmental temperatures by solar radiation and desiccation[10] Transmission of PPR between infected and susceptiblehosts is achieved by direct contact close contact or throughrespiratory and oral routes [11] PPRV targets epithelial cellsand pneumocytes leading to respiratory lesions includinginterstitial pneumonia and bacterial bronchopneumonia [12]as well as bronchointerstitial pneumonia [13] The lymphnodes are characterized by oedema [13] PPR is characterizedby high fever erosive stomatitis mucopurulent nasal andocular discharge pneumonia necrosis and ulceration ofmucous membranes and inflammation of gastrointestinaltract leading to severe diarrhoea [14] The PPRV is bio-logically and antigenically related to rinderpest virus andclinically the diseasemimics rinderpest in goats [15] Clinicaldisease is seen in sheep and goats and has been describedin zoological garden collections of wild small ruminantsincluding Laristan sheep (Ovis gmelini laristanica) Dorcas-type gazelles (Gazella granti) gemsbok (Oryx gazelle) andthe Nubian ibex (Capra ibex nubiana) Cattle buffaloescamels and pigs can become infected but there is little orno evidence of disease associated with their infection [16ndash18] PPRV antigen has been detected in an outbreak ofrespiratory disease in camel and sick domestic buffaloes [19ndash21] The tenacity of PPRV is considered to be low as thevirus does not usually remain infective outside the body forlonger than four days given the usual climatic conditionsfor Southern Africa The virus is inactivated by UV lightand most lipid-solvent based detergents and is both thermo-

(gt70∘C) and pH-labile (inactivated at pH lt 56 and gt96)[18] It is not well understood how the virus is maintainedbetween outbreaks [18] PPR outbreaks have been associatedwith seasonal variations that is more frequent outbreaksoccur during the rainy season or the dry cold season PPR isalso associated with seasonal periods of increased local tradein goats [17]

The ruminant livestock subsector in Zambia contributesabout 35 to the national agricultural output The countryhas a livestock population estimated at 36 million cattle06 million sheep 18 million goats 33 million poultry and11 million pigs [22] The Zambian livestock sector plays animportant role in socioeconomic development householdfood and nutritional security and poverty alleviation Itaccounts for about 364 of total agricultural productionAbout 23of the per capita supply of protein comes fromani-mal products [22] Trade in livestock and livestock productsexist between Tanzania and Zambia Despite the imminentrisk of PPR spreading from Tanzania into northern Zambiathere has been no objective risk assessment conducted todetermine the risk of pathogen introduction into the countrythrough importation of livestock commodities fromTanzaniainto Zambia This paper therefore reports the results of aqualitative assessment of the risk of introducing PPR virusfrom Tanzania into northern Zambia based on the datacollected in 2012

2 Materials and Methods

21 Study Areas The study was conducted in 3 districts ofnorthern Zambia namely Mbala Mpulungu and Nakondein 2012 (Figure 1) The districts were purposively selectedbased on their relative proximity to Tanzania and humanand animal traffic between Zambia and Tanzania The geo-graphical position of Mbala is latitude 8∘5041441015840 Southand longitude 31∘2195221015840 East that of Mpulungu is latitude8∘4600021015840 South and longitude 31∘799981015840 East while that of

Veterinary Medicine International 3

Nakonde is latitude 9∘2052781015840 South and longitude 32∘4471015840EastThe total goat and sheep population in the three districtsis estimated at 36662 and 1148 respectively [23]

22 Data Collection and Tools Data used to estimate themodel input parameters was collected during a study visitto Tanzania from 17 to 24 October 2012 where discussionswere held with officials from the National EpidemiologicalUnit in the Ministry of Livestock and Fisheries Development(MLFD) relevant documents were obtained and linkages toother officers involved in PPR control were made Data wascollected on disease prevalence disease distribution controlmeasures livestock movement patterns between Zambiaand Tanzania PPR vaccination coverage and other relevantepidemiological and surveillance data

Further data was collected through a questionnairesurvey conducted along the border areas of Zambia andTanzania from 10 to 24 October 2012 The areas includedSumbawanga and Tunduma districts in Tanzania and MbalaMpulungu and Nakonde districts of Zambia Livestockfarmers veterinary staff border staff and other stakeholderswere interviewed A structured questionnaire with differentsections for farmerstraders veterinary staff and border staffwas used Purposive sampling was employed to select initialrespondents and snowball sampling was used to identifysubsequent interviewees with the help of area veterinaryassistants Questionnaires were administered on one-on-onebasis with the interviewer sitting down with the respondentsOne hundred and thirty-eight farmers twelve veterinarystaff working in border areas and three border staff wereinterviewed using local languages (Mambwe Namwangaand Bemba) or English where appropriate In-depth oralinterviews were also conducted with district veterinary offi-cers (DVOs) for Nakonde Mbala and Mpulungu with afocus on gathering data on livestock populations commondiseases in goats and sheep husbandry practices by farmersmovement patterns of livestock between the two countriessurveillance methods used knowledge on PPR and capacityof the veterinary department to conduct surveillance

Data from the questionnaire was coded and entered intoa spreadsheet usingMicrosoft Excel Data obtained from oralinterviews was transcribed and transferred into MicrosoftWord for further analysis GIS coordinates were entered intoa spreadsheet using Microsoft Excel Other sources of infor-mation were from published literature grey literature on-line publications through internet searches (key terms PPRrisklowast PPR surveillancelowast PPR prevalencelowast PPR controllowast PPRpolicylowast Peste des petits ruminantslowast and specific databasessuch as pubmed and Google scholar) and expert opinions

23 Qualitative Assessment The methods used to conductthis risk assessment were based on the World Organisationfor Animal Health (OIE) Terrestrial Animal Health Code2001 framework and the work of Zepeda [24] Evaluation ofthe following factors both in the country of origin (Tanzania)and destination (Zambia) was also conducted organisa-tion of the veterinary structure presence and capability ofdiagnostic facilities epidemiological surveillance systems

disease status in Northern Province animal population andmovements and the legal framework

231 OIE Risk Assessment Framework For import of animalsand their products the technical steps in a risk analysisas per [25] guidelines were done as follows (a) frame thequestion (b) identify the hazards (c) model the pathway(outline the conceptual model and develop the risk scenariotrees) (d) collect information (quantify inputs and impactsprobability combinations) (e) assess the risk (release assess-ment exposure assessment consequence assessment and riskassessment) and (f) describe uncertainties in the qualitativemodel

232The Risk Question The question we were attempting toanswer is ldquowhat is the annual risk of introducing PPR virusinto northern Zambia through importation of live goats fromTanzaniardquo

233 Hazard Identification The hazard identified is themorbillivirus causing Peste des petits ruminants (PPR) ingoats and sheep

234 Risk Scenario Trees The scenario trees for release ofPPR intoNorthern Province of Zambia exposure assessmentand consequence assessment are shown in Figures 2 3 and 4

In this study the probability of occurrence of the risk(PPR virus infection and the consequences of the outbreaks)was equated to the probability of entry of the hazard (fromTanzania to northern Zambia) combinedwith the probabilityof exposure of susceptible animals to PPR virus Each param-eter in the assessment was evaluated based on the availableinformation [24] The descriptive scale developed by Zepeda[24]was used to evaluate the probability of occurrence of eachevent (Table 1) Combination of probabilities at each stage ofthe pathway that is release exposure and consequence wasdone using a combination matrix (Table 2)

3 Results

31 Probability of Release The four parameters examined inorder to determine the probability of release of the PPRV intonorthern Zambia from Tanzania were as follows probabilityof PPR virus infection of a goat selected for export volumeof trade probability of C-ELISA and quarantine screeningmissing an infected goat probability of pathogen viability(remaining infective) during transit

311 Probability of Infection The probability of infection ofa goat selected for export is a function of the probabilityof occurrence of the hazard It was dependent on thefollowing factors prevalence of PPRV from the area of originorganisation and efficacy of the veterinary epidemiologicalsurveillance system diagnostic facilities and PPR vaccina-tion coverage

A serosurvey carried out in northern Tanzania (Ngoron-goro Monduli Longido Karatu Mbulu Siha and Simanjiro)indicated an overall seroprevalence of PPRV infection in


Goat on afarm in

Tanzaniaselected for

export

Yes

Yes

YesIs a goat on farminfected with PPR

No

No

No

Is an infected goatdetected on

preexport test

P1a

P1b

P1c

Does the PPR virussurvive in transit

PPR infectedgoat releasedinto Zambia

No risk

No risk

No risk

Figure 2 Scenario tree for PPR exposure to goats in Northern Zambia

Does the infected goatcome in contact with

the susceptible

Is an infected goatquarantined

Is an importedgoatsheep

infected with PPRGoat importedin the country

No risk

No risk

No risk

P2c

P2b

P2a

Yes

No

Yes

No

No

Yes

Figure 3 Scenario tree for PPR consequence of release exposure and infection

Table 1 Practical interpretation of qualitative probability ratings [24]

Term Meaning for probability of event occurrence Meaning for consequence Meaning for risk estimated

Negligible Probability of occurrence of the event ispossible only in exceptional circumstances Low or no impact Allow import without restrictions

Low Occurrence of an event is a possibility insome cases Minor impact Authorise with specific measures to reduce

the risks

Moderate Occurrence of the event is a possibility Average impact Provide assessment of mitigation optionsbefore authorising

High Occurrence of the event is clearly apossibility Serious impact

Prohibited until measures to reduce the riskhave proven their efficiency (implement andaudit)


PPR infected goatsheep on index village

Yes

No

Consequences at district and national level

Consequences restricted to index case

Yes

No

Does PPR spread beyond index village

Consequences restricted to

village

Yes

No

Does PPR spread beyond district


district

Are the in-contactanimals susceptible

P3a

P3b

Figure 4 Scenario tree for consequence assessment

Table 2 Matrix showing probabilities when two parameters are combined [24]

Results of the assessment of Parameter 1 Results of the assessment of Parameter 2Negligible Low Moderate High

Negligible Negligible Low Low ModerateLow Low Low Moderate ModerateModerate Low Moderate Moderate HighHigh Moderate Moderate High High

small ruminants of 458 Highest seroprevalence (426ndash8802) was observed inMbulu Siha Longido and Ngoron-goro districts [26] Laboratory findings confirmed presenceof PPRV in southern Tanzania by RT-PCR and serologicalanalysis revealed that seroprevalence was 31 [27] Theofficial veterinary network in both countries that is Tanzaniaand Zambia is well structured and covers the whole countryin terms of territory In Zambia districts are divided intoveterinary camps run by veterinary assistants (VArsquos) whoin turn report to district veterinary officers (DVOs) InTanzania the equivalent of a veterinary camp is a ward whichis subdivided into villages Wards are run by livestock fieldofficers (LFOs) who in turn report to DVOs DVOs rundistricts and are in charge of all disease control activities intheir territories However in Tanzania district vets are underthe local government hence at times it is difficult for theDepartment of Veterinary Services (DVS) to get informationfrom them For example in 2009 during the PPRV outbreakit took almost 1 year from suspicion to disease confirmation[28] This clearly presents challenges in disease surveillance

In Zambia there are VAs on the ground but not allveterinary camps are manned A number of districts face thischallenge which impacts negatively on disease surveillanceand control activities Moreover compared to agriculturalcamps veterinary camps are too large for oneVA to effectivelymanage For example in the study area Mpulungu Districtonly had one veterinary camp against 14 agricultural campsfor the same territory One VA inMpulungu covered a radiusof more than 75Km the furthest distance being 204Kmwithin the district The staffing situation of VAs in veterinarycamps was severely inadequate

The MLFD in Tanzania had seven zonal laboratories andone central laboratory Capacity of the laboratory staff todiagnose PPR was good as most laboratory staff were trainedThree regional laboratories and one central laboratory wereable to diagnose PPR using ELISA Recently the central lab-oratory had acquired capacity to conductmolecular diagnosisof PPRV The antibody-based C-ELISA kits the commontest that was used were acquired from the United Kingdomthough at times they faced some problems acquiring them

Zambia has five regional laboratories namely ChipataMazabuka Ndola Mongu and Isoka and one central veteri-nary laboratory The regional laboratory in northern Zambia(Isoka) was nonfunctional Out of all these laboratoriesonly the Central Veterinary Research Institute (CVRI) hadcapacity to diagnose PPR CVRI had 4 members of staff whohad been trained in PPR diagnosis using C-ELISA The C-ELISA is used to detect presence of antibodies to PPRV inthe serumbyquantifying the amount ofmonoclonal antibody(MAb) [29] Most commonly used ELISA kits for PPR-specific diagnosis show that sometimes it does not detectPPR virus antigens from some clinical samples and B95a cellderived virus Sandwich ELISA has been developed whichis able to detect PPRV antigens from clinical samples [29]The test has undergone extensive field evaluation and hasbeen found to be suitable for the diagnosis of acute PPR virusinfection [29] However this test is not available in Tanzania

Although farmers in northern Tanzania were aware ofefforts being made to control the disease only 32 had theiranimals vaccinated against PPR [26] The low vaccinationcoverage suggests continued presence of PPR in the studyarea It was concluded that there was limited capacity with


respect to veterinary disease surveillance reporting and con-trol of transboundary and emerging diseases which neededto be addressed in the country [26]

Based on the preceding information that is seropreva-lence of the disease in Tanzania of 458 [26] and 31[29] a low vaccination coverage in high-risk areas [28]reasonable but inadequate diagnostic capability from thestate laboratories and well-organized veterinary structurecovering the whole country the probability that any oneanimal selected for export would be infected with PPR viruswas determined to be high

312 Volume of Trade The questionnaire survey conductedalong the border areas between Zambia and Tanzania indi-cated the following

(1) on average each farmer purchased and brought (fromdifferent sources) into the flock 2 (95 CI 1ndash3) goatsin a year

(2) forty-eight farmers bought at least one goat in the last1 year (215 goats in total)

(3) goat sources 956 (CI 922ndash990) bought within thevillage 22 (0ndash46) bought within district and 14(0ndash35) bought within the province

(4) twenty-two goats were purchased from Tanzania by17 farmers among those interviewed on average eachfarmer bought 1 goat in a year

(5) an interview of the 11 veterinary staff working onthe border areas estimated that 4612 goats (95 CI2296ndash11520) were imported into the country in thelast 1 year

Based on the above considerations the probability ofentry as determined by trade volume was rated low

313 Probability of C-ELISA and Quarantine Screening Miss-ing an Infected Goat C-ELISA has a relative specificity of984 and a relative sensitivity of 924 [30] Sensitivity ofC-ELISA for PPR serosurveillance could further be increasedto 954 if the target population is nonvaccinated [30]There were 19 quarantine facilities for farm animals and 28wildlife quarantine facilities under supervision of VeterinaryServices in Tanzania (Zoosanitary inspectorate ServicesMLFD) Field staff in Tanzania was able to diagnose clinicalcases of PPR [28] This implied that an infected animalwhich manifested clinical signs of PPR during quarantinecould be diagnosed and removed from the consignmentand destroyed Choi et al [31] reported a relative specificityand sensitivity of the rapid C-ELISA of 985 and 934respectively Therefore the probability that both C-ELISAand quarantine screening will miss an infected goat on pre-export screening was determined to be negligible Howevertrade in livestock between the two countries was primarilyinformal hence most animals were not likely to go throughquarantine and screening and hence this assessment mayunderestimate the risk for such type of movements

314 Viability of the Pathogen (Remaining Infective) duringTransit Tears nasal discharges coughed secretions andall other secretions and excretions of incubating and sickanimals are all sources of the virus [32] Due to an incubationperiod of 4-5 days and considering the travel period betweenTanzania and Zambia (1-2 days) an infected goat will be ableto carry the virus over long distances and be able to shedit to in-contact susceptible animals Based on the evidencethat suggests viability of the pathogen in live goats andconsidering the short distance travelled across the borderfrom Tanzania the probability that the virus would remainviable during transit was high

315 Assessment Using the matrix (Table 2) the probabilityof release is a function of the combination of risks relatingto probability of infection (high) volume of trade (low)C-ELISA and postexport quarantine screening missing apositive animal (negligible) and viability of pathogen (high)thus the probability of release is rated ldquomoderaterdquo (Figure 1)

32 Probability of Exposure The parameters used to deter-mine the probability of exposure were as follows the prob-ability of an imported goatsheep being quarantined (post-transit) probability of a positive animal having contact withsusceptible goats or sheep on index village proportion of sus-ceptible contact goats and sheep probability of transmissionof PPR virus to susceptible goats

321 Probability of the Posttransit Quarantine Missing aPositive Animal An in-depth interview with the DVOs forMbala Mpulungu and Nakonde revealed that there wereno quarantine facilities in the 3 districts instead on-farmquarantine was employed when need arose The herdflockor individual animals were placed under observation for aperiod of not less than 21 days The animals were monitoredby a VA for development of clinical signsdisease under thesupervision of the DVO who authorized the end of the quar-antine after certifying for disease absenceThe challenge withthis type of quarantine was that properly fenced quarantinefacilities that can adequately restrict animal movement werenonexistent Monitoring was also infrequent The VeterinaryDepartment did not always provide resources at camp levelto do this effectively including surveillance Hence the campofficers relied on farmer compliance There was a clearpossibility that mixing with local animals could still occureven when animals were under quarantine

An interview with the officer responsible for ZoosanitaryInspectorate unit of the Ministry of Livestock and Fisheries(MLFD) in Tanzania revealed that there was little formaltradeexport of live animals from Tanzania into ZambiaThismeant that much trade relating to livestock between thetwo countries was informal or illegal This situation made itdifficult to carry out quarantine and inspection of importedgoatssheep into Zambia fromTanzania On-farm quarantineunder supervision of veterinary services for formal move-ments remained the only option while informal movementrsquoswas a challenge This quarantine was only employed insituations where the Veterinary Department had information


of illegal movement of livestock Based on the evidencethat suggested lack of quarantine facilities illegal animalmovements and on-farm quarantine that was unsecure (nofences) and poorly monitored the probability of post-transitquarantine screening missing an infected animal was high

322 Probability of Contact with GoatsSheep in IndexVillage PPRV is considered to be highly infectious oftenspreading rapidly between groups of susceptible animals[18] Infection may be associated with the introductionof animals from another area the general movement ofanimals contact with livestock returning unsold from mar-ket contact with traded livestock or nomadic animals (egshared grazing land water housing) and husbandry changes[18]

The questionnaire survey with farmers and traders innorthern Zambia revealed the following as sources of goats956 (95 CI 922minus990) bought goats within the village22 (95 CI 0minus46) within the district and 14 (95CI 0 to 35) within the province As to whether theimported goats were mixed with local goats 618 (95 CI513 to 725) of 84 respondents indicated that the goatsbought from Tanzania did not mix with the local goatswhile 381 (95 CI 275 to 487) indicated knowledge ofmixing Separate interviews with 11 veterinary staff workingon the border areas estimated that 4612 goats (95 CI2296 to 11520) were imported into the country in the last1 year However most of these goats were imported intoNakonde and were slaughtered in restaurants For instanceone restaurant owner indicated slaughtering 8 goats per dayThis significantly contributed to reducing the risk of contactwith susceptible goats Thus the risk of PPRV transmissionfrom imported goats to susceptible animals in northernZambia was considered to be low

323 Proportion of Susceptible Contact GoatsSheep Therehave never been reported outbreaks of PPR in goats andsheep in Northern Province of Zambia Therefore smallruminant populations will be expected to be naıve to PPRvirus infection In Northern Province of Zambia goats werekept under free range and chances of exposure to the virusfrom infected goats and sheep were likely to be high insuch type of husbandry practice Moreover vaccination ofsmall ruminants against the disease was not practiced hencethe animals had no immunity to the PPRV We thereforedetermined that the proportion of susceptible goats in therecipient flock was high

324 Probability of Transmission of PPR Virus to SusceptibleGoatsSheep PPR is a severe and fast-spreading highlycontagious and infectious viral disease of domestic andwild small ruminants [17] Transmission of PPR is achievedby direct contact from infected to susceptible animals byclose contact or through respiratory and oral routes [11]Up to 100 of the animals in a flock may be affected in aPPR outbreak with between 20 and 90 mortality [17] Wetherefore determined the probability of transmission to behigh

325 Assessment Using the matrix (Table 2) the probabil-ity of exposure is a function of the combination of risksrelating to probability of the post transit quarantine miss-ing an infected animal (high) probability of contact withgoatssheep in index village (low) proportion of susceptiblecontact goats (high) and probability of transmission of PPRvirus to susceptible goats (high) thus the probability ofexposure was rated ldquoHighrdquo (Figure 1)

33 Magnitude of the Consequences In the border districtsof Northern Province goats are mainly kept by traditionalfarmers on a very small scale Local breeds of cattle withno genetic improvement are thus kept However morbidityand mortality rates in susceptible naıve populations are highMorbidity of up to 100 and mortality rates between 20 and90 are common except in endemic areas or when milddisease occurs [10 33]

While the direct consequences may be marginal indirectones are likely to have far reaching effects Presence of PPRVin the area may not only affect trade in small ruminantsfrom these areas but also the cattle and the pig industriesin the area are likely to suffer from trade restrictions incase of an outbreak There is significant livestock trade inNorthern Province to warrant concern over PPR incursionsOnce the disease is in northern Zambia the rest of the countycould easily get infected considering the limited diseasesurveillance efforts in place and inadequate veterinary servicedelivery Such an outbreak may be challenging to controlconsidering there are no emergency preparedness plans inplace to combat such an outbreak in the country althoughat regional level SADC could be expected to render someassistanceTherefore the whole of Zambia could easily sufferfrom a ban on export of live animals or animal productsIn this context the possible impacts of PPRV outbreak wereconsidered ldquoHighrdquo

34 Probability of Occurrence Probability of occurrence is aproduct of two probabilities the probability of releaseentry(P1) which was rated moderate and the probability of expo-sure (P2) which was rated high Based on the combinationmatrix of probabilities employed in this study (Table 2) theprobability of occurrence was thus high (Figure 5)

35 The Assessed Risk of PPRV Introduction into NorthernZambia The assessed risk is a combination of the probabilityof occurrence (high) and the magnitude of the consequencesof occurrence (high) and is thus rated ldquohighrdquo

From the interpretation of the probability scale providedby Zepeda Sein (Table 1) high implies prohibiting importuntil measures to reduce the risk have proven their efficiencyand adequate verification procedures are available to ensuresafe implementation All uncertainties in the qualitativemodel were described (Table 3)

4 Discussion

In this paper we report the results of a qualitative assess-ment of the risk of introducing PPR virus from Tanzania


Table 3 Description of model uncertainties

Assessment component Uncertainty description Direction of error Magnitude

Release

Probability of C-ELISA andquarantine missing an infected goat

There have been no formal movement ofgoatssheep from Tanzania into Zambia hencemost goats will not undergo testing andquarantine

Underestimated risk High

Volume of trade Most movements are illegal due to the porousborder resulting in many trade routes Underestimated risk Moderate

Exposure The probability of the quarantinemissing a positive animal

There are no known quarantine stations inNorthern Zambia On-farm quarantine is difficultto enforce in cases where illegal animalmovements are not detected


(A) Probability of release

Probability of infection ldquohighrdquoVolume of trade ldquolowrdquo

Test series missing infection ldquonegligiblerdquo

Pathogen viability ldquohighrdquo

(B) Probability of exposure

Probability of quarantine missing ldquohighrdquoProbability of contact ldquolowrdquo

Proportion of susceptible ldquohighrdquoProbability of transmission ldquohighrdquo

(C) Probability of occurrence of hazard

Probability of release (A) ldquomoderaterdquo

Probability of exposure (B) ldquohighrdquo

(D) Magnitude of consequences

The probability of PPR spread within index village ldquohighrdquo

The probability of PPR spread beyond district ldquohighrdquo

Consequences of PPR Introduction and establishment ldquohighrdquo

(E) Risk estimation

Probability of occurrence ldquohighrdquo

Magnitude of the consequence ldquohighrdquo

Moderate

Moderate

Moderate

Moderate

High

High

High

High

High

High

Figure 5 The risk estimation process

into northern Zambia based on the data collected in 2012Our design was based on evaluating the risk of PPR virusintroduction through formal trade in goats However thestudy revealed that most movements of goats were informaland we thus redesigned the investigation plan to take theseinto account in assessing the risk Under informal trade littleinformation is captured by government officers and thereforethe information provided by the veterinary and border staffwas likely to underestimate the actual trade volumes andother investigated parameters It is therefore acknowledged

that there are uncertainties surrounding the probability esti-mates in our study especially data from government officials

The probability of occurrence of PPR virus in NorthernProvince of Zambia was determined to be high The magni-tude of the consequences of occurrence of PPRV was alsodetermined to be highThe assessed riskwas a combination ofthe probability of occurrence (high) and themagnitude of theconsequences of occurrence (high) and was thus rated ldquohighrdquoFrom the interpretation of the probability scale providedby Zepeda et al [24] high implies prohibit import untilmeasures to reduce the risk have proven their efficiency andadequate verification procedures are available to ensure safeimplementation Although prohibition of import could berecommended its implementation would be difficult sincemuch trade in goats and sheep between Zambia and Tanzaniawas informal

Therefore risk management measures could include for-malising trade in small ruminants between the two countriesand strengthening veterinary services and capacity to con-duct epidemiological surveillance Since most of the crossborder movements of goats and sheep were informal thereis need for the Department of Veterinary Services along theborder on both sides to create awareness among the farmersof the need for government to regulate trade in livestockand also intensify surveillance monitoring and livestockmovement controls A joint surveillance system by bothTanzanian and Zambian Veterinary authorities could be putin placeThis could help prevent the spread of transboundarydiseases between the two countries including PPRV

Another important measure of mitigating the risk is tocreate a vaccination bufferzone of 50 km from the borderinto the high-risk areas to avert a possible incursion ofPPR [5] PPR vaccine has been proved to be protectiveto small ruminants for a period of at least 3 years [17]hence most animals will only need vaccination twice intheir lifetime Subsequent vaccinations should target naıvenewly born kidslambs At least 85 of the small ruminantpopulation should be vaccinated in the high-risk zone thisincludes Mbala Nakonde Mpulungu and possibly Isoka Ifthe strategy of vaccinations is taken up there will be needto build laboratory capacity to carry out the differentiationof infection from vaccinated (DIVA) animals In the absenceof this proper animal identification will be required forexample ear tagging or branding of all vaccinated animals


5 Conclusion

Considering that northern Zambia has a small populationof goats and sheep the actual consequences resulting fromlosses in terms of mortality and morbidity are likely to beminimal However the indirect losses far outweigh the directlosses and these should prompt the veterinary Department toimplement measures to prevent any such incursions

Conflict of Interests

The authors of this paper declare that none of them havefinancial or personal relationships with individuals or organi-sations that would unacceptably bias the content of this paperand therefore declare that there is no conflict of interests

Acknowledgments

The authors convey sincere thanks to the veterinary officialsin Tanzania and the three districts visited in Zambia namelyMbala Mpulungu and NakondeThe authors would also liketo thank SACIDS for sponsoring this research work

References

[1] P N Wambura ldquoSerological evidence of the absence of pestedes petits ruminants in Tanzaniardquo Veterinary Record vol 146no 16 pp 473ndash474 2000

[2] E S Swai A Kapaga F Kivaria D Tinuga G Joshua and PSanka ldquoPrevalence and distribution of Peste des petits rumi-nants virus antibodies in various districts of Tanzaniardquo Veteri-nary ResearchCommunications vol 33 no 8 pp 927ndash936 2009

[3] J Decapua ldquoPeste des petits ruminants in Southern Tanzaniardquo2010 httpcoalgeologycomdeadly-animal-virus-peste-des-petits-ruminantsthreatenstospread-to-southernAfrica8302

[4] FAO Livestock Epidemic Causing Havoc in Democratic Republicof the Congo vol 1 FAO Rome Italy 2013

[5] SADC SADC Control Strategy for Pest de Pestes Rumi-nants SouthernAfricanDevelopmenetCommunity GaboroneBotswana 2012

[6] OIE ldquoPeste des petits Ruminants [PPR]rdquo Weekly DiseaseInformation vol 25 no 41OIEWAHID (WorldAnimalHealthInformation Database) Paris France 2012

[7] M J Mamabolo and E C Webb Goat Production Survey-Fundamental Aspects to Model Goat Production Systems inSouthern Africa-Case Study Agricultural Commission 2005

[8] C Devendra and M Burns Goat Production in the TropicsCommon wealth agricultural bureaux Farnham royal bucksUK 1970

[9] SADC SADC Pestes des Petits Ruminants (PPR) Control andEradication Working Group SADC Gaborone Botswana 2012

[10] S Geerts ldquoGoat Plaque or Peste des Petits Ruminantsrdquo EAZWVTransmissible Disease Fact Sheet 25 Institute of TropicalMedicine Antwerp Belgium 2009

[11] H C Chauhan B S Chandel H N Kher et al ldquoPeste des petitsruminants virus infection in animalsrdquo Veterinary World vol 2no 4 pp 150ndash155 2009

[12] A W Aruni P S Lalitha A C Mohan P Chitravelu and SP Anbumani ldquoHistopathological study of a natural outbreak

of Peste des petits ruminants in goats of Tamilnadurdquo SmallRuminant Research vol 28 no 3 pp 233ndash240 1998

[13] N A Osman A S Ali M E Rahman and M A FadolldquoAntibody seroprevalences against Peste des Petits Ruminants(PPR) virus in sheep and goats in Sudanrdquo Tropical AnimalHealth and Production vol 41 no 7 pp 1449ndash1453 2009

[14] S C Sarker and H Islam ldquoPrevalence and risk factor assess-ment of Peste des petits ruminants in goats in RajshahiBangladeshrdquoVeterinaryWorld vol 4 no 12 pp 546ndash549 2001

[15] DD Kulkarni AU BhikaneM S Shaila P VaralakshmiM PApte and B W Narladkar ldquoPeste des petits ruminants in goatsin Indiardquo Veterinary Record vol 138 no 8 pp 187ndash188 1996

[16] F M Hamdy A H Dardiri and O Nduaka ldquoEtiology of thestomatitis pneumoenteritis complex in Nigerian dwarf goatsrdquoCanadian Journal of Comparative Medicine vol 40 no 3 pp276ndash284 1976

[17] P L Roeder and T U Obi ldquoRecognising peste de petitsruminants a field manualrdquo FAOAnimal HealthManual 5 FAOAnimal Health Rome Italy 1999

[18] OIE Peste des Petits Ruminants Disease Factsheets 2012[19] W P Taylor S Al Busaidy and T Barrett ldquoThe epidemiology of

peste des petits ruminants in the Sultanate of OmanrdquoVeterinaryMicrobiology vol 22 no 4 pp 341ndash352 1990

[20] G R Scot ldquoRinderpest and peste des petits ruminantsrdquo VirusDiseases of Food Animals vol 2 pp 401ndash425 1981

[21] G Abraham A Sintayehu G Libeau et al ldquoAntibody sero-prevalences against peste des petits ruminants (PPR) virusin camels cattle goats and sheep in Ethiopiardquo PreventiveVeterinary Medicine vol 70 no 1-2 pp 51ndash57 2005

[22] NALEIC Annual Report vol 52 Ministry of agriculture andlivestock Lusaka Zambia 2012

[23] NALEIC Peste des Petits Ruminants (PPR) Surveillance inChama Isoka Lundazi Mbala Mpulungu and Nakonde Dis-tricts of Zambia Department of Veterinary Services Ministryof Agriculture and Livestock Lusaka Zambia 2010

[24] C Zepeda ldquoWorld Organisation for Animal Health Seminar onSafeguarding Animal Health in Trade in the Caribbeanrdquo Port ofSpain Trinidad and Tobago 1998

[25] OIEManual of the Diagnostic Tests and Vaccines for TerrestrialAnimals vol 1 Office International Des Epizooties ParisFrance 5th edition 2010

[26] EDKarimuribo PM Loomu L S BMellau et al ldquoRetrospec-tive study on sero-epidemiology of peste des petits ruminantsbefore its official confirmation in northern Tanzania in 2008rdquoResearch Opinions in Animal and Veterinary Sciences vol 1 no3 pp 184ndash187 2011

[27] E A Muse E D Karimuribo G C Gitao et al ldquoEpidemiologi-cal investigation into the introduction and factors for spread ofPeste des Petits Ruminants Southern Tanzaniardquo OnderstepoortJournal of Veterinary Research vol 79 no 2 pp E1ndashE6 2012

[28] Ministry of Livestock and Fisheries Development ldquoTrade inLivestock between Zambia and Tanzaniardquo Tech Rep Ministryof Livestock and Fisheries Development Dar es Salaam Tanza-nia Data Collection Phase of the Research Project 2012

[29] E A Muse R B Matondo E D Karimuribo et al ldquoClinico-pathological findings of the 2011 outbreak of Peste des PetitsRuminants (PPR) in Tandahimba district Southern TanzaniardquoResearch Opinions in Animal and Veterinary Sciences vol 2 no4 pp 256ndash262 2012

[30] R P Singh B P Sreenivasa P Dhar and S K Bandy-opadhyay ldquoA sandwich-ELISA for the diagnosis of Peste des


petits ruminants (PPR) infection in small ruminants usinganti-nucleocapsid protein monoclonal antibodyrdquo Archives ofVirology vol 149 no 11 pp 2155ndash2170 2004

[31] K-S Choi J-J Nah Y-J Ko et al ldquoRapid competitive enzyme-linked immunosorbent assay for detection of antibodies to pestedes petits ruminants virusrdquo Clinical and Diagnostic LaboratoryImmunology vol 12 no 4 pp 542ndash547 2005

[32] OIE Peste des Petits Ruminants Technical Disease Card Scien-tific and Technical Department Paris France 2009

[33] O M Radostits C C Gay D C Blood et al VeterinaryMedicine WB Saunders London UK 10th edition 2007

Submit your manuscripts athttpwwwhindawicom

Veterinary MedicineJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Veterinary Medicine International



International Journal of

Microbiology


AnimalsJournal of

EcologyInternational Journal of


PsycheHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evolutionary BiologyInternational Journal of


Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Biotechnology Research International


Agronomy




Journal of Parasitology Research

Hindawi Publishing Corporation httpwwwhindawicom


Volume 2014

Zoology

GenomicsInternational Journal of


InsectsJournal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


VirusesJournal of

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Cell BiologyInternational Journal of



Case Reports in Veterinary Medicine


Isoka

Chinsali

Mpika

Kasama

Chilubi

Luwingu

Mporokoso

KaputaMpulungu

Mbala

MungwiNakonde

Tanzania

Malawi

DRCMozambique

Figure 1 Location ofMpulunguMbala andNakonde in relation to other districts ofNorthernZambia andTanzania onNorthWest Tanzaniais located in the north

which has not been reported despite its sharing borders withthe affected countries [5]

PPR is caused by the PPR virus (PPRV) which belongsto the genus morbillivirus under the family Paramyxoviridae[1] PPRV is an RNA virus which is closely related to themeasles rinderpest and distemper viruses [10] There isonly one serotype of PPRV but there are at least 4 lineageswhich are distinguishable by nucleic acid sequencing Thevirus is not very resistant and is rapidly inactivated at envi-ronmental temperatures by solar radiation and desiccation[10] Transmission of PPR between infected and susceptiblehosts is achieved by direct contact close contact or throughrespiratory and oral routes [11] PPRV targets epithelial cellsand pneumocytes leading to respiratory lesions includinginterstitial pneumonia and bacterial bronchopneumonia [12]as well as bronchointerstitial pneumonia [13] The lymphnodes are characterized by oedema [13] PPR is characterizedby high fever erosive stomatitis mucopurulent nasal andocular discharge pneumonia necrosis and ulceration ofmucous membranes and inflammation of gastrointestinaltract leading to severe diarrhoea [14] The PPRV is bio-logically and antigenically related to rinderpest virus andclinically the diseasemimics rinderpest in goats [15] Clinicaldisease is seen in sheep and goats and has been describedin zoological garden collections of wild small ruminantsincluding Laristan sheep (Ovis gmelini laristanica) Dorcas-type gazelles (Gazella granti) gemsbok (Oryx gazelle) andthe Nubian ibex (Capra ibex nubiana) Cattle buffaloescamels and pigs can become infected but there is little orno evidence of disease associated with their infection [16ndash18] PPRV antigen has been detected in an outbreak ofrespiratory disease in camel and sick domestic buffaloes [19ndash21] The tenacity of PPRV is considered to be low as thevirus does not usually remain infective outside the body forlonger than four days given the usual climatic conditionsfor Southern Africa The virus is inactivated by UV lightand most lipid-solvent based detergents and is both thermo-

(gt70∘C) and pH-labile (inactivated at pH lt 56 and gt96)[18] It is not well understood how the virus is maintainedbetween outbreaks [18] PPR outbreaks have been associatedwith seasonal variations that is more frequent outbreaksoccur during the rainy season or the dry cold season PPR isalso associated with seasonal periods of increased local tradein goats [17]

The ruminant livestock subsector in Zambia contributesabout 35 to the national agricultural output The countryhas a livestock population estimated at 36 million cattle06 million sheep 18 million goats 33 million poultry and11 million pigs [22] The Zambian livestock sector plays animportant role in socioeconomic development householdfood and nutritional security and poverty alleviation Itaccounts for about 364 of total agricultural productionAbout 23of the per capita supply of protein comes fromani-mal products [22] Trade in livestock and livestock productsexist between Tanzania and Zambia Despite the imminentrisk of PPR spreading from Tanzania into northern Zambiathere has been no objective risk assessment conducted todetermine the risk of pathogen introduction into the countrythrough importation of livestock commodities fromTanzaniainto Zambia This paper therefore reports the results of aqualitative assessment of the risk of introducing PPR virusfrom Tanzania into northern Zambia based on the datacollected in 2012

2 Materials and Methods

21 Study Areas The study was conducted in 3 districts ofnorthern Zambia namely Mbala Mpulungu and Nakondein 2012 (Figure 1) The districts were purposively selectedbased on their relative proximity to Tanzania and humanand animal traffic between Zambia and Tanzania The geo-graphical position of Mbala is latitude 8∘5041441015840 Southand longitude 31∘2195221015840 East that of Mpulungu is latitude8∘4600021015840 South and longitude 31∘799981015840 East while that of













3 Results





Goat on afarm in


export

Yes

Yes


No

No

No


preexport test

P1a

P1b

P1c



No risk

No risk

No risk



the susceptible




No risk

No risk

No risk

P2c

P2b

P2a

Yes

No

Yes

No

No

Yes






the risks






Yes

No



Yes

No



village

Yes

No



district


P3a

P3b






































4 Discussion





Release






















(E) Risk estimation



Moderate

Moderate

Moderate

Moderate

High

High

High

High

High

High








5 Conclusion




Acknowledgments


References












































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of


















3 Results





Goat on afarm in


export

Yes

Yes


No

No

No


preexport test

P1a

P1b

P1c



No risk

No risk

No risk



the susceptible




No risk

No risk

No risk

P2c

P2b

P2a

Yes

No

Yes

No

No

Yes






the risks






Yes

No



Yes

No



village

Yes

No



district


P3a

P3b






































4 Discussion





Release






















(E) Risk estimation



Moderate

Moderate

Moderate

Moderate

High

High

High

High

High

High








5 Conclusion




Acknowledgments


References












































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of







Goat on afarm in


export

Yes

Yes


No

No

No


preexport test

P1a

P1b

P1c



No risk

No risk

No risk



the susceptible




No risk

No risk

No risk

P2c

P2b

P2a

Yes

No

Yes

No

No

Yes






the risks






Yes

No



Yes

No



village

Yes

No



district


P3a

P3b






































4 Discussion





Release






















(E) Risk estimation



Moderate

Moderate

Moderate

Moderate

High

High

High

High

High

High








5 Conclusion




Acknowledgments


References












































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of








Yes

No



Yes

No



village

Yes

No



district


P3a

P3b






































4 Discussion





Release






















(E) Risk estimation



Moderate

Moderate

Moderate

Moderate

High

High

High

High

High

High








5 Conclusion




Acknowledgments


References












































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of


































4 Discussion





Release






















(E) Risk estimation



Moderate

Moderate

Moderate

Moderate

High

High

High

High

High

High








5 Conclusion




Acknowledgments


References












































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of









Release






















(E) Risk estimation



Moderate

Moderate

Moderate

Moderate

High

High

High

High

High

High








5 Conclusion




Acknowledgments


References












































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of







5 Conclusion




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






research article a qualitative assessment of the risk of...

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