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Leishmaniasisinthe Sudan: aliteraturereview withemphasisonclinicalaspects
Omran F.Osman
1
,Piet A.Kager
2
and Linda Oskam
3
1
DepartmentofZoology,FacultyofScience,UniversityofKhartoum,Sudan
2
DepartmentofInfectiousDiseases,TropicalMedicineandAIDS,AcademicMedicalCenter,UniversityofAmsterdam,TheNetherlands
3
DepartmentofBiomedicalResearch,RoyalTropicalInstitute,Amsterdam,TheNetherlands
Summary
The literature on the leishmaniases in the Sudan is reviewedwith an emphasis on clinical aspects and on lit-erature related to the recentoutbreaks in the south and eastof the country.The numbers ofcases of subclinicalinfection and post-kala azardermal leishmaniasis in the recentoutbreaks are remarkable. Newdiagnostictechniques have been introduced and evaluated, notably the direct agglutination test and polymerase chainreaction technology.The latter gives very promising results and further research into application of the tech-nique is warranted.Treatment with pentavalent antimony is still satisfactory.The reservoir host has notbeenidentified definitely.
keywords
Sudan, leishmaniasis, kala-azar, PKDL, clinical features, diagnosis, treatment, entomology
correspondence
Dr Linda Oskam, Departmentof Biomedical Research, Royal Tropical Institute (KIT),Meibergdreef 39, 1105 AZ Amsterdam,The Netherlands.
Introduction
Theleishmaniasesareagroup ofdiseaseswithabroadrange of clinical manifestations caused by several species of parasitesbelonging to the genus
Leishmania
(Family:Trypanosomati-dae).The
Leishmania
parasite, a haemo-flagellate protozoanorganism, is exclusively transmitted by the bite of a femalesandfly of the genus
Phlebotomus
or
Lutzomyia
.There arethree clinical forms of leishmaniasis: visceral leishmaniasis(VL) including post-kala azardermal leishmaniasis (PKDL),cutaneous leishmaniasis (CL) and cutaneous leishmaniasiswith involvementof the mucous membranes, also called mu-cocutaneous leishmaniasis (MCL).In Sudan,VL and CL are endemic in several areas (Figure 1).PKDL,acomplication ofVL of unknown cause,nowoccursinup to 50% ofcases (Zijlstra
et al 
.1995), much more frequentlythan in the past (Kirk & Sati1940b). Aparticular form of `mu-cosal leishmaniasis', different from MCL ^ which is found inCentral and Latin America ^ occurs in Sudan. It is called Su-danese mucosal leishmaniasis (SML).VL is one of the most important endemic diseases in thecountryand Sudan is considered to be one of the main foci of VL in the world. Occasionally, severe epidemics have claimedthelives of thousands of people. In recent years the disease hasspread outside established endemic areas, and a resurgence of cases has become apparent in regions with a previouslylow in-cidence (Siddig
et al 
.1990).VL spreads overawide belt fromthe Atbara river in the north-east along the Sudanese^Ethio-pian border to south of the Sobat riverand Nassirand Malakaland extending west across theWhite Nile. Other foci are theKapoeta area, the Nuba Mountains and scattered areas in theDarfur region.
Epidemiology in historical perspective 
Neave was the first to describeVL in Sudan in1904 (El-Hassan
et al 
.1995a), although the disease was alreadyknown there inthe19th century (Henderson1937). At the turn of the 20thcentury, VL was recognized as a serious health problem in theSudan.This realization led to the establishmentof the SudanKala Azar Commission, which operated from1909 to1913(Zeese & Frank1987). In the 3rd and 4thWellcome ResearchLaboratory Reports published in1908 and1911, respectively,chapters are devoted to kala azar with notes on epidemiology,clinical and diagnostic aspects, trials at treatment, case de-scriptions and post mortem reports (Balfour1908, 1911).Ar-chibald and Mansour (1937) identified the main endemic areaas the Kassala and Fung districts bordering the Abyssinianfrontierand the Kapoeta district in the south. Sporadic caseswere found in the Nuba Mountains and in the western districtof Darfur. At that time no epidemics had been described.The first epidemic was reported in the Upper Nile Province
ß 2000 Blackwell Science Ltd
553
Tropical Medicine and International Health
volume 5 no 8 pp 553^562 august 2000
 
in1936^38: at least 300 cases occurredwith a recorded deathrate of 80% (Stephenson1940).The second epidemic in thesouthern Fung area of Blue Nile Province in1956^60 killedthousands of people (Sati1958) and led to the establishmentof aresearchteamthatbetween1960and1964providedcleardataon medical and zoological aspects of the vectorand reservoirhosts (Hoogstraal & Heyneman1969). In1979^81there was anincreased number ofcases in Melut (Zeese & Frank1987), anarea described as a new focus in1962 byVan Peenen & Reid.Around1985 the average number of patients requiring treat-ment was1300 per year, 75% of whomwere treated in Gedaref and Hawata (Zeese & Frank1987).In the last decade, several new outbreaks of VL occurred: amajor epidemic in the south of the country (Perea
et al 
.1991;Ashford
et al 
.1992;El-Hassan
et al 
.1993b;Seaman
et al 
.1993)came to lightonlyafterVL had been found in the Khartoumarea in1988 among displaced people fromWestern Upper NileProvince who had fled the civilwar in the south (De Beer
et al 
.1991). Subsequent studies confirmed this (Zijlstra
et al 
.1991b;El-Hassan
et al 
.1993b), and itbecame clear that a devastatingoutbreak had been going on in southern Sudan since1984(Perea
et al 
.1991),whichaffectedallage groupsand by the endof1988 had alreadykilled 20^30 000 people (Seaman
et al 
.1992). During the period1986^95 an estimated100 000 from apopulation of about 280 000 people died of the disease inWestern Upper Nile Province. Population movement, civilwarand poor nutritional status mayhave contributed to this highdeath rate (Seaman
et al 
.1996).The Masariya, a nomadic tribe from southern Kordofan inwestern Sudan, traditionally move theircattle to the northern
LibyaEgyptSudanChadCentral AfricanRepublicUgandaEthiopiaKenya
Abri 
27
°
30 E
'   
30
°
00 E
'   
R   e  d    S   e  a  
Congo
A   t    b   a   r   a   
DarfurNubaMountains
   W   h   i   t  e   N   i   l  e
S o b at 
   B   l   u   e    N   i   l   e
   R   i  v  e  r   N   i   l  e
Khartoum
24
°
N22
°
N20
°
N18
°
N16
°
N14
°
N12
°
N10
°
N8
°
N6
°
N4
°
N400 km0Cutaneous LeishmaniasisVisceral Leishmaniasis
Figure 1
Endemic and epidemic areas of visceral and cutaneous leishmaniasis in theSudan (adapted from Osman1998).
554
ß 2000 Blackwell Science Ltd
Tropical Medicine and International Health
volume 5 no 8 pp 553^562 august 2000
O. F. Osman
etal.
Leishmaniasisinthe Sudan
 
partof the epidemic area inWestern Upper Nile Province insearch of pasture. During this trek theybecame infected andthus brought VL to their home area (Hashim
et al 
.1994). In1994 another outbreakwas reported in Nasir Districtof East-ern Upper Nile Province whichwas probably related to peopletravelling to a food distribution centre located in the southernpartof theVL-endemic zone in eastern Sudan (Mercer
et al 
.1995). Until recently, at least1000 cases of VL occurred eachyear in Gedaref State, eastern Sudan (Zeese & Frank1987; El-Hassan
et al 
.1995b; Osman
et al 
.1998b); the incidence of thedisease was estimated to be stable at 4% (Zijlstra
et al 
.1994).However, by the end of1997, a sharp increase in the numberof VLcaseswasreported from thisareaand also fromEritreaandthe north-west Ethiopian focus (McGregor1998).This hascontinued through1998 and1999 (unpublished data).The first case of possible PKDL was described by Christo-pherson (1921).The first definite cases were reported by Kirkand Drew (1938).The number ofcases might have been muchgreater than supposed until recently, or mayhave increasedover time (Zijlstra
et al 
.1995). PKDL patients may serve as areservoir for transmission of the parasite (El-Hassan
et al 
.1992).The firstcases of CL in Sudan described at the beginning of the 20th centuryhad contracted the disease in Egypt (KirkandDrew1938).The first reported autochthonous CL case wasfromtheNubamountains(Archibald1911).CLpatientsmainlycome from Darfurand the central beltof Sudan (Abdalla
et al 
.1973; Abdalla & Sherif1978). So far, three outbreaks of CLhavebeen reported:the firststarted in1976^77in the region of Shendi-Atbara north of Khartoum, the second in1985 in andaround El-Gerrsa in theWhite Nile area, and the last majorepidemic took place in Khartoum Province with about10 000recorded cases in1985^87. Heavy rainfall after severalyears of drought, the discontinuation of insecticide spraying for ma-laria control and rodentoutbreaks have all been implicated asfactors in the outbreaks (El-Safi & Peters1991).SML is uncommon: only 78 cases have been reported sincethe disease was first described by Christopherson in1914 (El-Hassan
et al 
.1995a).SMLisseen inadultmalesinVL-endemicareas: eastern Sudan, Darfurand Kordofan. Cases are sporadicand isolated: SML has never occurred in epidemic form.
Clinicalfeaturesof VL
Skin manifestations
After the infectious bite of the sandflya`leishmanioma'mayappear.We do not knowhowoften this happens as it is infre-quentlyreported and generallyseems to go unnoticed. A leish-manioma is a nonitching papule that may ulcerate and then re-sembleCL(Kirk1938),but in general itevolves gradually intoatuberculoid lesion (Manson-Bahr1959). Histologically it con-sists oflymphocytes,macrophages and plasma cells (ElHassan& Modabber1999).The leishmanioma may precedeVL or bepresent whenVL becomes manifest.Two offourleishmaniomapatients studied in Upper Nile Province developed VL (Adler
et al 
.1966). In another study, one offive leishmanioma casesnot treated and followed up 6 months laterdeveloped VL, an-otherdeveloped PKDL without apparent VL and the remain-ing three were without symptoms (Zijlstra
et al 
.1994). Skinpigmentation did notchange (Siddig
et al 
.1990), in contrasttothe situation in India, where the dark skin associatedwithVLgave the disease its Hindi name kala azar (`black sickness').
Other clinical manifestations
The clinical features of SudaneseVL have been described byanumber of authors (Henderson1937;Van Peenen & Reid1962;Ahmed
et al 
.1988; El-Hassan
et al 
.1990a; Siddig
et al 
.1990;El-Safi
et al 
.1991b; Zijlstra
et al 
.1991a, b; Hashim & El-Has-san1994; Hashim
et al 
.1994, 1995).The disease is character-ized by the developmentof fever, splenomegaly, varying de-grees of hepatomegaly, weight loss in combinationwith ahealthyappetite, and pancytopenia. Splenomegaly maybe ab-sent: in 4% ofcases Zijlstra
et al 
. (1991b) did notobserve anenlarged spleen.The number of patients with lymphadenopa-thy ranges from 36% (Hashim
et al 
.1994) to more than 80%(Zijlstra
et al 
.1991a).
Complications
Complications such as epistaxis (El-Hassan
et al 
.1990a; Sid-dig
et al 
.1990), severe tineaversicolordue to depressed cell-mediated immunity (Hashim & El-Hassan1994) and neurolo-gical changes such as deafness, foot drop and a sensation of burning feet (Hashim
et al 
.1995) have been reported.
Congenital and placental leishmaniasis
Acase ofcongenital leishmaniasis was reported, together witha patient who a fewdays after the startof treatmentof VLaborted a 5-month-old foetus.The placenta contained manyparasites, the foetus did not (Eltoum
et al 
.1992).
Subclinical infection
In Sudan subclinical infectionwas defined as serological con-version and/orconversion in the leishmanin skin test (LST) inthe absence ofclinical symptoms. Using this definition, the ra-tio ofclinical to subclinical cases was1.6:1and 2.4:1in twosuccessive years in a longitudinal study in eastern Sudan (Zijl-stra
et al 
.1994).This ratio is higher than those in Italy (1:4),Kenya(1:5)(Ho
et al 
.1982)andBrazil(1:18.5for`astudyareaatlarge'and1:6.5 for the`areawith the highest prevalence of dis-
ß 2000 Blackwell Science Ltd
555
Tropical Medicine and International Health
volume 5 no 8 pp 553^562 august 2000
O. F. Osman
etal.
Leishmaniasisinthe Sudan
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