Studies on the leishmaniases in the Sudan. 1. Epidemic of cutaneous leishmaniasis in Khartoum

44 TRANSACTIONSOF THE Rouar. Socren OF TROPICAL.MEDICINE AND HYGIENE (1991) 85, 44-47

Studies on the leishmaniases leishmaniasis in Khartoum

in the Sudan. 1. Epidemic

of cutaneous

S. H. El-Safi’ and W. Peters*’ ‘Institute for Tropical Medicine, P.O. Box 1304, Khartoum, Sudan; ‘0 artment of Medical Parasitology, London School of Hygiene and Tropical Medicine, Winches Farm La%ratories, 395 Hatfield Road, St Albans, Hertjkdshire, AL4 OXQ, UK Abstract A recent outbreak of cutaneous leishmaniasis (CL) in Khartoum province, the first ever reported, involved about 10 000 recorded cases. The peak incidence was in September 1986. It was widespread all over the province, but the most affected areaswere along the banks of the River Nile. People of both sexes, all age groups, different ethnic origins, and all socio-economic classeswere equally affected, suggesting that this epidemic was a new occurrence among a non-immune population. A leishmaniasis clinic was established and 736 caseswere treated and studied. The control measures, responsible parasite, possible animal reservoir, and vector are discussed. Possible contributory factors were mass population movement from known endemic areas of CL in Khartoum. expanding towns and new settlements in previously uninhabited areas, high population densities of sandflies, and an increase in the rodent population, including Arvicanthis species. Introduction The 3 forms of leishmaniasis, visceral, mucosal and cutaneous, are found in the Sudan with onlv the visceral d&ease posing a major health problem -up to the mid-1970s, since when several epidemics of cutaneous leishmaniasis (CL) have occurred (SATTI, 1987; YOUSIF, 1967). Cutaneous leishmaniasis was first reported m the Sudan by THOMSON81 BALFOUR (1910) in 2 Egyptians who had contracted the disease in their own country. ARCHIBALD(1911) then reported a nodular form of CL in a Sudanesemale adult from the Nuba mountains of Kordofan in western Sudan. Another case of ‘oriental sore’ was reported by CHRISTOPHERSON (1914) from Khartoum. KIRK & DREW (1938) reported other cases from Blue Nile province and Darfur; a single casewas recorded from Equatoria (KIRK, 1942), and a few cases were described from the Upper Nile province (CAHILL, 1964; HOOGSTRAAL

81 HEYNEMAN,

1969). ABDALLA

et al. (1973) studied 21 cases;the series included only

one patient from Omdurman in Khartoum province. Thus sporadic cases of CL have been reported throughout the Sudan, mainly from kala-azar endemic areas and, as a rule, from Darfur in the western Sudan as well as from the Nuba mountains in Kordofan. Since these verv sDoradic reoorts, there have been 3 outbreaks of dL in the Sudin; the first started in 1976-1977in the Shendi-Atbara area. about 170 km north of Khartoum (ABDALLA & .&ERIF, 1978), and a second, not reported before, occurred in *Author

for offprints.

early 1985 in El-Garrsa and nearby villages in the White Nile area. Dreviouslv believed not to be endemic for leishr;a&asis (Saiti & Abd El-Nur, 1987, personal communication). The present study describes the recent epidemic in Khartoum province. Materials and Methods Records of CL in the Commission of Health Affairs in Khartoum, Sudan, from September 1986 to October 1987, were examined; they had been received weekly from all the health c&t&s in the 4 areas of Khartoum Province (Omdurman, Khartoum, Khartoum North and East Nile). The records also included those received from the Host&l for TroDical Diseasesin Omdurman, Khartoh Skin Hos’pital, and the Dermatology Unit in Khartoum North Hospital. The records of leishmaniasis in the Sudan were obtained from the Statistics Department, Ministry of Health, Khartoum. Specialized CL clinics were held 3 days per week at the Omdurman Tropical Diseases Hospital, when patients were interviewed and examined by the senior author. The diagnosis was confirmed by direct smear examination and, in many cases, culture, further details of which will be presented elsewhere. Results 9657 caseswere reported between September 1986 and March 1987 from the 4 areas of Khartoum Province. The monthly records (Fig. 1) indicate that by September 1986 the diseasewas already at, or past, peak incidence. The number of casesdeclined and it dropped dramatically in March 1987. The distribution of cases between the clinics in the 4 areas is shown in Fig. 2. The results suggest that in Khartoum and East Nile areasthe pattern was very similar, the epidemic having passedits peak by October, while in Omdurman the peak was later, in November 1986. In Khartoum North there was a much lower prevalence of the diseaseduring the reporting period, but we were informed that the reporting system had been poor in this area. The aae distribution of the infection is shown in Fig. 3. In all age groups the number affected was high, although some increase was observed in the age group 20-24 years. In addition the data suggest that more males (61%) were affected than females (39%). People from all socio-economic classeswere affected. The infection was widespread in the whole Province, but the areasof greatest density were along the banks of the River Nile such as Kabbashi, Geili and Wad Ramli (Fig. 4) and Tuty, Ahnogran, Alfittaihab, Alshagara and Alkalakla in the Khartoum area itself. The numbers of casesof leishmaniasis in the Sudan between 1976and 1986are shown in Fig. 5. Although

Nod 3ooo

C&e8

1

2500 2000 ,600

l Wad Ramli eWawissi

1000 500

l Geili

.,

n

@

10 1, 1986

I

12,

1

2

3

I

4

8 5 1007

7

6

9

OSagqai

10,

Date

l Kabbashi @Khogalab

Fig. 1. Numbers of cases of cutaneous leishmaniasis in Khartoum province monthly from September 1986 to October 1987.

eKadaro Hittanad/

Naof Cases

1400

eSha(pmHbaa:ayat e’ M”‘uk eHag Yosuf

9

1200

oGerif sharg

1000

dgbbal

800 600 400 200 0

i KHARTOUM

OMDURMAN

N.KHARTOUM

EAST

NILE

Fig. 2. Numbers of cases of cutaneous leishmaniasis in the four areas of Khartoum province monthly from September 1986 to January 1987.

Fig. 4. Distribution of cases of cutaneous leishmaniasis in Khartoum province from September to October 1986.

Age Wears)

No.of

o-4 s-9 to-14 IS-19 20-24 26-29 30-34 35-39 40-44 45-49 50-54 55-50

cases

(Thousands)

‘::--I

60. 0

50

100 150 200 250 No. and Proportion by Age

300

350

Fig. 3. The numbers of cases of cutaneous leishmaniasis and proportion in different age groups in Khartoum province in September 1986.

the records obtained did not differentiate between the different types of the disease, there were 2 peaks in 1979 and 1986 which almost coincided with the 2 epidemics of CL in the Sudan. Discussion This is the third recorded epidemic of CL in Sudan, and the first ever reported from Khartoum province.

Year Fig. 5. Total numbers of outpatient (heavy line) and inpatient (thin line) cases of leishmaniasis (cutaneous and visceral) reported to the Ministry of Health of the Sudan between 1976 and 1986.

It was a most severeoutbreak in ternis of the number of cases and severity of the lesions. Suddenly, in October 1985, cases of CL started to appear from Tuty (Fig. 4), an island of about 20 000 inhabitants at the junction of the Blue and White Niles in the midst of the 3 towns of Khartoum, Khartoum North and Omdurman. Subsequently there was a gradual in-

creasein the number of casesreaching the dermatology clinics in Khartoum, indicating the commencement of an epidemic (Drs Abdel Rahim, Wasfi, & Lavla. 1987. oersonal communication). A few months later, ‘the nymber of cases declined’and then cases ceasedto appear until August, but this time patients were from different Darts of Khartoum nrovince. Bv September the same year there was- a dramatic increase in the number of cases; the infection was transmitted throughout the 3 towns in the province and caused great-panic. From September -1986 to March 1987 almost 10 000 caseswere renorted from Khartoum province. Obviously this was an underestimate of the actual number of cases,as reporting was not mandatory until the epidemic was at or past its peak. Many people with minor lesions did not seek medical treatment, others went to private clinics, and some acquired drugs directly from private pharmacies or friends suffering from the disease. From March 1987 the number of casescontinued to decline steadily and, by June the samevear, it was hard to fmd a new case. In September isolatedcases started to appear again in the Hosnital for Tronical Diseasesin Omdurman. and the number increased slightly in October to reach 12 cases per week in November, when another outbreak was at its height in the Blue Nile province. Thus it may appear reasonable to suggest that the oeak seasonalincidence of the diseasecoincided with ihe months August to December; ARCHIBALD & HASSEEB(1937)-suggested a seasonal incidence of kala-axar durink Tulv and October. It is verv difficult to estimate the-incubation period as the disease has been present around Khartoum for a considerable time. However, surveys carried out by EL-AMIN (1986) indicated that Phlebotomus pupatusi, yet to be proved to be the vector, was abundant between March and Iulv. Hence it is reasonable to assume that the incubation period lies between one and 3 months. The nrevalence data from Seotember 1986 (Fie. 3) showed that all age groups were affected,‘ which indicated that this epidemic was a new occurrence among a non-immune nonulation. A similar finding was &ported by ABD~L~A & SHERIF (1987), wh6 described the first enidemic of CL in the Sudan. Both sexes, people of all ethnic origins and all socioeconomic classeswere equally affected. The disease was prevalent in all the 4 areasof Khartoum province. However, the lower prevalence in Khartoum North (Fig. 2) was probably due to the reporting system not being strictlv adhered to in that area. This view is subsiantiate~ by the fact that almost 300 caseswere seen during Sentember in Khartoum North Skin Department (T~HA, 1986). The fact that the most affected areas in Khartoum province were along the River Nile’s banks may have been associatedwith the optimum geographical and ecological conditions for the breeding of sandllies and Nile rats. ABDALLA & SHERIF(1978) also found that CL was common in villages along the banks of the Nile between Shendi and Atbara. The clinical features of the diseaseobserved in the present study (to be reported in the second paper of this series) are consistent. with those of classical Old World CL due to L. major (GRIFFITHS, 1987). Treatment of CL during the epidemic posed a problem. Doctors were faced with large numbers of

patients, most of the medical wards were full with severe cases that needed parenteral therapy with sodium stibogluconate (Pentostam@), and most of these patients had to wait for a considerable time for treatment. (Further details of treatment will be given in our next paper.) Biochemical characterization of the isoenxvmes of a number of isolates proved that L. major zymodeme LON-1 was resnonsible for this enidemic (to be reported in the next paper). Natural infection was demonstrated by smearsfrom 13 Atzicanthis niloticus and one Genetta genetta caught in Khartoum Province (Badi, 1988, personal communication). P. paputasi has been considered to be the vector on epidemiological grounds (EL&UN, 1986); it was the dominant species, forming about 52% of the total catch (ElAmin, 1988, personal communication). However, natural infection could not be demonstrated in the thousands of sandflies dissected. Several factors may have been involved in the causation of this massive epidemic. During the last 6 years the population of Khartoum province has increased due to immigration from the west of Sudan. The infection may have been brought by these immigrants; their home areas are known to be endemic for CL, but the vectors must already have been present in the reception area. The massive population movement in 1956, after the opening of the ‘closed area’ of southern Sudan, carried kala-azar from the endemic areasin northern Fung and resulted in an epidemic in southern Fung (SATTI, 1958,1962). The recent expansion of small towns and villages, the construction of new houses, establishment of new settlements, and development of previously uninhabited areas constitute other factors. Similar factors have contributed to outbreaks of zoonotic CL in Libya (ASHFORDet al., 1977), Saudi Arabia (PETERS, 1988). and Tordan (OUMEISH& SALIBA. 1987). 1n”Khartoum province rainfall was v&v low for more than 5 years before the heavy rains in 1985 and 1986. Thus the cracked. drv soils became waterloaged, to create ideal breeding conditions for the sandfly. A similar situation was reported by SATTI (1958, 1962) in southern Fung; he stated that ‘the year of the epidemic the rainfall had been exceptionally heavy’. Similar events occurred in the epidemics of Paloich and Melut in southern Sudan (HOOGSTRAAL & HEYNEMAN,1969). An increase in the population of sandllies may also have resulted from the discontinuation of insecticide spraying for malaria control. It had always previously been the practice to spray the 3 towns twice a year, before and after the rainy season (Dr Osman, 1987, personal communication). A similar situation was reported from Iran (SEYEDI-RASHTI & NADIM, 1975) and from India (VIOUKOV, 1987). Moreover, deterioration of public health services resulted in favourable conditions for the sandflies. STEPHENSON (1940) considered that a poor general standard of living was one of the predisposing factors of the Melut epidemic. The environmental and ecological changes that favoured an increasein the vector population may also have led to the rodent population increasing and coming into the city. Reports that Nile rats w&e on the increase in Khartoum province began in 1985 (Dr Mahir, 1987, personal communication). By 1986 the rat population was estimated to be about 150ikm2,

47

well above the epidemic rate of 4/km*. Many rodents were found in ‘houses, factories and offices. The recent rat outbreak (1986-1987) involved manv areas in the Sudan, and was the most intensive recorded ( SULIEMAN,1987). A. niloticus was seenin all parts of the countrv. Another severerodent outbreak occurred in Sudan in 1976-1977 (SULIEMAN,1987), coinciding with the first outbreak of CL. The nossibihtv that man may act as a reservoir of L. majh, or even that direct transmission may occur, may also be suggested by the recent massive epidemic in Khartoum. This was previously postulated in relation to the transmission of kala-azar bv HEYNEMAN(1961). However. it is generally accepted that man is‘unlikely to act ‘as a reservoir of L. major (ASHFORD& BETTINI, 1987). Vector control measureswere started bv the Ministry of Health in Khartoum province (Ministry of Health. 1987. unnublished renort). A nationwide rodent control programme was commenced in Khartoum province in June 1987 by the Ministry of Agriculture (1987, unpublished report); the campaign was launched by the Plant Protection Department as the rodents had damaged more than half of the agricultural production that year (Dr Mahir, 1987, personal communication). It- is hoped that -such a camoaian will influence the incidence of the diseaseas spe&cmeasures against rodents have resulted in the successful control of zoonotic CL in other countries (VIOUKOV, 1987; ASHFORD, 1988). Acknowledgements

We recordour gratitude to the late Dr AhmedM. Arabi,

former Director General of the Commission of Health

Affairs in Khartoum, for giving us accessto the Commis-

sion’s reports. We are also grateful to Mr Osman Ali Abu Bakr, Deputy Director, Environmental Health Department at the SudaneseMinistry of Health, for helpful discussion, and to Dr Mohamad A/Aziz Mohamad? Plant Protection specialist, and Dr Abdel Gawi Mahir, Chief Entomologist in the Ministry of Agriculture, for valuable information. The senior author was the recipient of a training grant and other financial support from the UNDPAVorld Bank/WHO Special Programme for Research and Training in Tropical Diseases.

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