University ofKhartoum,POBox32, North, * Presentaddress:DepartmentofMicrobiology, FacultyofVeterinaryScience, Veterinary Science,UniversityofKhartoum, POBox32,KhartoumNorth,Sudan 2. DepartmentofPreventiveMedicine and VeterinaryPublicHealth,Facultyof 8067, Elamarat,Khartoum,Sudan 1. DepartmentofVirology,CentralVeterinary ResearchLaboratories,POBox disease. some epizootiologicalfeaturesofthispoorlystudiedcamel follow-up CCEoutbreaksinordertogainmoreinformationon epizootiology ofCCE.Thepresentworkhasbeenundertaken to Search oftheliteraturerevealsveryfewinformationon and years underthenames has beenrecentlyreportedandisbelievedtohaveexistedfor and Turkmenistan(3)Somalia(10).IntheSudandisease CCE hasbeenreportedinMongolia(4),Kenya(12),Kazakhstan both diseasesweresimilar(3). thought tobeaformofcamelpox(CP)sinceclinicalsymptoms (CCE), hasonlyrecentlybeenidentified(1).Formerlyitwas The parapoxvirus,responsibleforcamelcontagiousecthyma INTRODUCTION Sudan. Parapoxvirus -EpidemiologySeason Dromedary -Contagiousecthymavirus Key words Al kolate in theEasternregion(8). Abu Shalambo in theWesternregion(2) eating thorny seasonality associatedwithrainyseasonandcamelskinabrasioncausedby while themeanfatalitycaseratewas13%.Thediseasehadamarked mortality ratesincalveslessthanoneyearwere60.2and8.8%,respectively, were incamelcalveslessthanoneyearold.Themeanmorbidityand All CCEcasesoccurredinyoungcamelsupto3yearsoldand97.8%ofthem animals assmallpapulesandlaterdevelopedintoscabsfissuredcrusts. the disease.Clinicallypox-lesionsfirstappearedonlipsofaffected between 1992and1994.Thirty-eightherdswerefoundtobeaffectedwith were surveyedfortheoccurrenceofcamelcontagiousecthyma(CCE) Free-ranging camelsinButana,KassalaandtheBlueNileareasofSudan Summary in EasternSudan of camelcontagiousecthyma Epizootiology A.I. Khalafalla Retour aumenu Acacia

species: nilotica A. distribution intheSudanisshownfigure2. October) aroundKassalacityand inCentralButana.Inthedry Generally, theRashaidanomads spendtherainyseason(July- namely nomadism,semi-nomadism oragropastoralism. were keptunderdifferentmanagement andhusbandrysystems, (pack camels),AnnafiandBishari (ridingcamels)breeds.Herds Kawahla andArakiyin.Thecamels wereoftheArabiandDiaili Shukriya, Rashaida,Lahawiyin,Bawadra,Musallamiya,Ruffaa, The investigatedcamelherdsbelongedtomanytribesincluding Study animals in thestudyareaconsistedof Central Butanaduringtherainyseasons.Treescommonlyfound originating fromtheBlueNileareawereinvestigatedaswell at River werealsoincludedinthesurvey(figure1).Camelherds South andSouth-WestofKassalaaswellEasttheAtbara the BlueNileandAtbaraRiver(EasternpartofSudan).Areas It consistsoftheButanaplainswhichliebetweenmainNile, Study area MATERIALS ANDMETHODS trees. 1* A. laeta,albida M.E.M. Mohamed (1). Inaddition,theBlueNilehasfollowing and Acacia mellifera,A.nubica A. polyacantha 2 (6). Acacia

99

tree and PATHOLOGIE INFECTIEUSE communication Revue Élev. Méd. vét. Pays trop., 1997, 50 (2) : 99-103 Retour au menu

Epizootiology of came1 contagious ecthymain Sudan

u A. nilotica, A. albida

Figure 2: map of the Sudan showing the distribution of some Acacia spp. Source: modified from Elamin, Forest Research Figure 1: map of the Sudan showing the area of study. Institute, Bull. No. 2, 1976.

season(November-June), some of them move southwardup to sex of the affected animalswere collected.Herders’ accounts of Dokaarea, 350 km Southof ,few migratenorthward up to the diseasehistory and progressof symptomswere alsoobtained. GashDelta and others crossover to the Red Seatoast around Skin biopsiesor scabswere collectedfrom affected animalsfor Sawakin and Toker (400 km North East of Kassala)to take laboratoryconfirmation of preliminarytentative diagnosis. advantageof range developingas a resultof the winter rains (1). The Shukriya, Lahawiyin, Bawadra and Mussalamiya stay in Luboratory investigation in the rainy seasonand move during the dry season towardsthe River basin.A significantproportion of these Ten percent suspensionswere preparedfrom skin biopsiesor tribesas well as someof Rashaidacoordinate their movementsto scabsin phosphatebuffered saline (PBS). After light centrifugation coincidewith the harvest season(January-March) thus usingthe one dropof eachsample was placed onto a separatecarbon-coated trop residuesin the rain-fed agriculturalschemes of Gedarefarea grid. After stainingwith 2% phosphotungesticacid the grids were (1). Ruffaa, Kawahlaand Arakiyin tribes of the Blue area dried andexamined by electronmicroscopy. spendthe dry seasonat rain-fed agriculturalschemes in the area and move to the North towardsButana plains in the rainy season to usefree range pasture. WRESULTS The came1population in the study area has been estimatedat 750,000,which represents20% of a11Sudan camels (13). CCE clinical features Fifteen came1herds were visited monthly betweenMarch 1992 Initially small nodulesappeared on the lips of affected animals and June 1993 in connectionwith the French-SudaneseCame1 followed in most caseswith swellingof the,face and sometimes ResearchProject. The aimof thisproject was to studythe husbandry the neck (figure 3). Affected animalswere ataxic and off-food. and productionparameters of camelsin Butanaarea (1). During Papules and vesicles appeared later and within a few days eachvisit to the study areaadditional 15 to 20 herds,which were developedinto thick scabsand fissuredtrusts (figure 4). Lesions not coveredby the abovementioned project, were alsoinvestigated. occurred sometimeson the face, eyes and nares and in severe BetweenJuly 1993and December 1994 the studyarea was visited casesin the gingiva, dentalpad and tongue.‘Deathwas probably eight times in responseto reports of pox or pox-like disease due to starvationcaused by the inability of affected animalsto outbreaks.During the whole period of the study approximately grazeor suckletheir dams.Healing occurred within 20-30 daysin 20,740camels in 305 herdswere surveyed. mostcases, but sometimesthe courseof the diseaseextended up to threemonths. Epizootiological investigation Disease incidence During each field visit the investigatedherds were located and data on CCE occurrence were ‘collected. Sick animals were A numberof 305 came1herds were surveyed for CCE occurrence. carefully examinedfor clinical symptoms,site and type of lesions This numberrepresented approximately 3% of the whole came1 and generalanimal health. Additional dataconcerning the ageand herds in the study area. Thirty-eight herds were found tolbe 100 Retour au menu

Epizootiologie de l’ecthyma contagien du dromadaire au Soudan

Figure 4: came/ contagious ecthyma: a close-up view of the af- fected came1 face show@ scabby lesions around the lips, nos- trils and eyes. Note the lower lip is pendulous.

Figure 3: came/ contagious ecthyma: acutely affected Young Although no mention was madeof the morbidity and mortality came/ showing swelling of the head and Upper part of the neck. ratesin mostprevious reports on CCE, Munz et al. (12) reported no deathsdue to the disease,Dashtseren et al. (4) reported a mortality of O.l-0.6% calculatedfrom the total numberof Young andadults. affected with the disease(herd incidence rate in the sample: Khalafalla et al. (8) reported a total mortality rate of 17.5% 12.5%). The diseasewas recordedin 35 of theseherds (92.1%) (34.4% in calves lessthan one year old) in a CCE outbreak in during the rainy season(July-October) and only 3 affected herds Butana area of Eastern Sudan in 1991. They attributed the (7.9%) were recordedin the winter season(November-March), relatively higher mortality rate to the addedeffects of starvation while no diseaseoutbreak was seen in the sumrnerseason (April- andlack of food in the seasonpreceding the time of that outbreak. June). Dashtserenet al. (4) attributeddeaths caused by CCEin Mongolia to fatigueand exhaustion of affectedanimals. Table 1 showsthe morbidity and mortality rates and the fatality caserate of camelsaffected with CCE in Central Butana and Most camelsin the studyarea fed during the dry seasonon harvest Kassala,Southern Butana and the River Atbara, and the remains(Sorghum stalks) of the rain-fed agricultural schemes. areas.The meanmorbidity ratein came1calves less than oneyear Duringthe rainy seasonanimals fed mainly on free rangepasttire old in the three geographicalareas was 60.2% and the mean in Butanaplains. However, early in the rainy season(June-July) mortalityrate was 8.8%, while the meanfatality caserate was 13%. and due to the spoilingeffect of the rains on the Sorghumstalks camelswere obligedto leave theseschemes and browseAcacia Age and sex distribution treesin the areauntil adequategreen grasses developed in Butana plains.At that time of the year CCE outbreaksoccurred. A factor The age distributionof 280 CCE caseswith 34 deathsis shownin responsiblefor this seasonalitycould be lip skin abrasionresulting table II. Al1 casesoccurred in Young animalsup to 3 years old. from eatingthorny Acacia trees at this time of the year whenno Most of the affectedanimals (70.7%) were in the agegroup 7-12 other sourceof food wasavailable. BuEhnev et ul. (3) were of the 1’ monthsand 27.2%of casesoccurred in animalsagcd O-6 months. sameopinion when they arguedthat the thorny plantsdamaged the Four animals(1.4%) aged l-2 years and 2 animals(0.7%) aged lips allowingtransmission of the parapoxvirus. TO gain moredata 2-3 years accountedfor 2% only of the affected animals.The on the pattern of CCE outbreaksthe study area was revisited fatality caserate was higher in the age group O-6 months(21%) during the rainy seasonsof the years 1993and 1994.The disease than in that 7-12months (9%). pattemwas similarto that observedin 1992. It seemsthat CCE Sex distributionof CCE 274 casesrevealed a malelfemaleratio of constantly appearsevery year during the rainy seasonaffecting 111.2. Young came1calves in their first autumn seasonof grazing and alsoolder animals which escapedprevious exposure to the virus. n DISCUSSION The occurrenceof the diseasewas lower (24%) in the age group O-6 monthsthan in that of 7-12months (62.8%). This may be due to the passivetransfer of immunity which seemsto disappearafter The CCE outbreaksreported in the present study occurred in 6 months. severalcame1 herds belongingto different tribes and involving 1: differentbreeds of camels.The observedclinical symptomsof the In the presentstudy CCE incidenceand severityvaried depending diseasecompared well with thosedescribed previously (3, 5, 8, on the location. The morbidity and mortality rateswere relatively 11).The total morbidityrate wasfound to be 10% while the mean high in camelsfrom the Blue Nile areacompared to thosefrom morbidity and mortality ratesin the susceptibleage group (came1 Central and Southern Butana, Kassala or the Atbara River calvesless than one year old) were 60.2% and 8.8%, respectively. (table1). Thereis no clear explanationto thesevariations except

101 (Assumption: herdstructureissimilarinthethreeareas)

Animal prevalenceofCCEsignificantdependingontheage(lessthanoneyear)andstratifiedthreelocations.MantelHa Animal prevalenceofCCEsignificantdependingontheage(lessthanoneyear); 102 Revue Élev. Méd. vét. Pays trop., 1997, 50 (2) : 99-103 PATHOLOGIE INFECTIEUSE communication Epizootiology ofcamelcontagiousecthymainSudan even foryearsawayfromthehost (7). virus ofsheepandgoatscansurvive indryscabsformonthsand extremely resistanttoenvironmental factors.Similarlytheorf affected animals.AccordingtoBuchnev probably persistintheenvironment incrustmaterialsshedby grazing betweenJuneandSeptember.Thecausativeviruscould affect everyyearyoungcamelcalvesintheirfirstautumn of Many herdersinthestudyareaconsideredthatCCEappears to Butana plainscrossedoverintheearlyrainyseason. exhaustion causedbythelongdistancebetweenBlueNileand CCE infection.Anotherpossiblereasoncouldbestressand tree browsingseemedtorepresentthemajorpredisposingfactor to the BlueNileareawhere Kassala areasareknowntocontainfew in theannualrainfallsince,forexample,CentralButanaand Herd prevalenceofCCEsignificantdependingonthelocation; that theycouldbeduetovegetationdifferencesrelatedchanges - er 07)00 0 12.2% 0 9% 21% 34 0 2(0.7%) 18 16 4(1.4%) Total 280 2-3 years 198(70.7%) 76(27.2%) 1-2 years Num. 7-12 months 0-6 months Case Age aaiycs ae01%2.%14.6% 40 22.1% 274 (8.8%) 23 17% (60%) 455 (16%) 38 104 280 2896 0 17 (10%) (72.2%) 305 144 (9.6%) 100 105 10 842 (56.5%) (12.5%) 0 35 177 (0) (52.2%) (9.2%) 70 102 1103 15 125 134 (7.7%) 951 Fatality caserate 73 13 under 1yearold(mortalityrate) 145 Num. ofdeadcamelcalves with CCE(morbidityrate) under 1yearoldaffected Total num.ofcamelcalves under 1yearold Total num.ofcamelcalves with CCE(morbidityrate) Total num.ofanimalsaffected examined inaffectedherds Total num.ofanimals Num. ofherdsaffected investigated Total num.ofherds Age distributionofcasesanddeathsduetocamel Morbidity andmortalityratesincamelsaffectedwithcamelcontagiousecthymaEasternSudan contagious ecthymainEasternSudan fcsso etsfatality ofdeaths of cases Table II Acacia tree forestsareabundant. et al. Acacia (3) theCCEvirusis 2 with 2degreesoffreedom;p=0.006 trees comparedto χ eta uaa otenBtn Bu ieTotal BlueNile SouthernButana Central Butana Retour aumenu rate asl &RiverAtbara & Kassala Table I Acacia 2 χ Yates correctedwithtwodegreesoffreedom;p<0,0001

result ofcalfmortality. economic impactonthegrowth rateandmilkproductionasa due toitshighcontagiousness,significant mortalityrateandother endemic problemintheSudan needs tobelookedintoseriously In conclusion,thispoorlystudied diseasewhichrepresentsan provision ofsoftfoodtoyoungcamelswhenpossible. camel herders.Careshouldbetakentoavoidskinabrasions by of camelmovements,aswellprovisionextensionservices to disposal ofcarcassesandallcontaminatedmaterials,management measures mustincludequarantineofinfectedareas,proper area. IntheabsenceofaneffectivevaccineagainstCCEcontrol to controlthisdiseaseintheSudanparticularlyBlueNile Special attentionshouldbedirectedtowardsintroducingmeasures and theirassociationwiththorny are: seasonoftheyear,camelage,movementsandlocation factors associatedwithincreasedlikelihoodofCCEoccurrence From thefindingsofpresentstudyitappearsthatmajor in ordertocompletethepicture. involving historicalanalysisattheanimallevelaremuchneeded myxomatosis virus(15).Moredetailedepizootiologicalstudies (16), sheeppox(9),fowl(14),swinevirusand members ofthePoxviridaesuchaslumpyskindiseasevirus suspected orreportedtoberesponsiblefortransmissionofother excluded. Thisisnotunexpectedsinceinsectshavebeen the possibleinvolvementofinsecttransmissioncannotbe mind themeteorologicaldataondirectionofseasonalwinds movements ofcamelstowardsButanaplains.However,bearingin infection extendednorthwardcoincidingwiththeannual (June) intheBlueNileandSouthernButanaareas the diseasetendedtofirstappearatstartofrainyseason of CCEinthestudyarea.Theauthorsobservedthatoutbreaks Seasonal movementsofcamelshadasignificantroleinthespread

enszel Summary

Acacia 2 ; p<0.0001 χ trees. Retour au menu

Epizootiologie de l’ecthyma contagieux du dromadaire au Soudan

Acknowledgements 8. KHALAFALLA A.I., AGAB H., ABBAS B., 1994. An outbreak of contagious ecthyma in camels (Camelus dromedarius) in Eastern Sudan. The facilities provided by the French-Sudanese Camel Research Trop. Anim. Health Prod., 26: 253-254. Project of Butana were highly appreciated. The authors are 9. KITCHING R.P., MELLOR P.S., 1988. Insect transmission of grateful to Drs. H. Agab, X.R. Pacholek and H. Jaafer for their capripoxvirus. Res. vet. Sci., 40: 255-258. interest and cooperation. Part of this work was funded by the International Foundation for Science (IFS), Stockholm, Sweden. 10. MOALLIN A.S.M., ZESSIN K.H., 1988. Outbreak of camel contagious ecthyma in Central Somalia. Trop. Anim. Health Prod., 20: 185-186.

11. MUNZ E., 1992. Pox and pox-like diseases of camels. In: Allen REFERENCES W.R., Higgins A.J., Mayhew I.G., Snow D.H., Wade J.F. eds, Proc. first int. camel conf., Dubai, UAE, February 2-6, 1992. London, United Kingdom, R & W Publications, p. 43-46. 1. AGAB H., 1993. Epidemiology of camel diseases in Eastern Sudan with emphasis on brucellosis. M.V. Sc. thesis, University of Khartoum, 12. MUNZ E., SCHILLINGER D., REIMANN M., MAHNEL H., 1986. Khartoum, Sudan. Electron microscopical diagnosis of Ecthyma contagiosum in camels (Camelus dromedarius). First report of the disease in Kenya. J. vet. Med. 2. ALI O.A., KHEIR S.A.M., ABU DAMIR H., BARRI M.E.S., 1991. Camel B, 33: 73-77. (Camelus dromedarius) contagious ecthyma in the Sudan. A case report. Revue Elev. Méd. vét. Pays trop., 44: 143-145. 13. MUSA B.E., CHABEUF N., ABBAS B., BONNET P., PLANCHENAULT D., 1989. Survey of camel raising in the Butana 3. BUCHNEV K.N., TULEPBAEV S.Z., SANSYZBAEV A.R., 1987. region of the Sudan (North East). In: Int. symp. on the development of Infectious diseases of camels in the USSR. Revue sci. tech. Off. int. animal resources in the Sudan, Khartoum, Sudan, January 3-7, 1989, Epizoot., 6: 487-495. p. 13-27. 4. DASHTSEREN Ts., SOLOVYEV B.V., VAREJKA F., KHOKHOO A., 1984. Camel contagious ecthyma (Pustular dermatitis). Acta Virol., 28: 14. TRIPATHY D.W., CUNNINGHAM C.H. 1980. Avian Pox. In: 122-127. Hofstad M.S., Barnes H.J., Calnek B.W., Reid W.M. Yoder, H.W. eds., Diseases of poultry. Ames, Iowa, USA, Iowa State University press, p. 5. DIOLI M., STIMMELMAYR R., 1992. Camel contagious ecthyma. In: 525-534. Schwartz H.J., Dioli M. eds, The one humped camel in Eastern Africa. A pictorial guide to diseases, health care and management. Berlin, 15. TRIPATHY D.W., HANSON L.E., CRANDEL R.A., 1981. Poxviruses Germany, Verlag Joseph Margraf Scientific Books, p. 155-164. of veterinary importance. In: Kurstad E., Kurstad C. eds., Comparative diagnosis of virus diseases, vol. 3. London, United Kingdom, Academic 6. ELAMIN H.M., 1976. Geographical distribution of the Sudan Acacias. Press, p. 265-346. Khartoum, Sudan, Forest Research Institute, p. 2-3. (Bulletin No. 2) 16. WOODS J.A., 1988. Lumpy skin disease: a review. Trop. Anim. 7. HUNTER A., 1994. Orf. In: Animal health, vol. 2: Specific diseases. Health Prod., 20: 11-17. London, United Kingdom, Macmilian, p. 18-20. (The tropical agriculturalist series) Reçu le 9.5.96, accepté le 15.9.97

Résumé Resumen

Khalafalla A.I., Mohamed M.E.M. Epizootiologie de l’ecthyma Khalafalla A.I., Mohamed M.E.M. Epidemiología del ectima contagieux du dromadaire à l’Est du Soudan contagioso del dromedario al Este de Sudán

Une enquête sur des dromadaires élevés en liberté dans les Se llevó a cabo una encuesta sobre los dromedarios criados régions de Butana, Kassala et Blue Nile au Soudan a été en libertad en las regiones de Butana, Kassala y el Nilo Azul, effectuée entre 1992 et 1994 pour évaluer l’incidence de en Sudán, entre 1992 y 1994, con el fin de evaluar la l’ecthyma contagieux du dromadaire (ECD). Trente-huit incidencia del ectima contagioso del dromedario (ECD). Se troupeaux étaient atteints de la maladie. D’un point de vue encontraron treinta y ocho hatos afectados con la clinique, des lésions sont d’abord apparues sur les lèvres des enfermedad. Desde un punto de vista clínico, las lesiones animaux atteints sous forme de croûtes ou de croûtes aparecieron primero sobre los labios de los animales fissurées. Tous les cas d’ECD concernaient les jeunes afectados, bajo forma de costras o de costras fisuradas. Todos dromadaires jusqu’à 3 ans d’âge et, pour 97,8 p. 100 d’entre los casos de ECD concernieron dromedarios jóvenes, hasta la eux, ceux de moins d’un an. Les taux de morbidité et de edad de 3 años, con 97,8% de ellos de menos de un año. Las mortalité moyens chez des jeunes de moins d’un an étaient tasas de morbilidad y de mortalidad medias en los jóvenes de respectivement de 60,2 et 8,8 p. 100 alors que la létalité menos de un año fueron respectivamente de 60,2 y de 8,8%, moyenne était de 13 p. 100. Cette maladie variait selon la mientras que la letalidad media fue de 13%. La enfermedad saison, étant associée à la saison des pluies et à la varió segun la estación y estuvo asociada con la estación consommation d'acacias épineux causant l’abrasion de la lluviosa y la alimentación con acacias espinozas, causando peau. lesiones de la piel.

Mots-clés : Dromadaire - Virus echtyma contagieux - Palabras clave: Dromedario - Virus ectima contagioso - Parapoxvirus - Epidémiologie - Saison - Soudan. Parapoxvirus - Epidemiología - Estación del año - Sudán. Revue Élev. Méd. vét. Pays trop., 1997, 50 (2) : 99-103 103