Epidemiology of cutaneous leishmaniasis in Kabul, Afghanistan

Bull. Org. mond. Santa 1974, 31, 45-49 Bull. Wld Hlth Org. 1 Epidemiology of cutaneous leishmaniasis in Kabul, Afghanistan A. NADIM 1 & Gh. S. ROSTAMI 2 Severe outbreaks of cutaneous leishmaniasis in Kabul led to complaints from the public. It was felt that a study of the epidemiology of the disease in this city would help not only in organizing better control measures in Kabul, but also in dealing with similar conditions that might arise elsewhere because of urbanization and migration from rural to urban areas. A housing project in north-west Kabul was studied through house-to-house visits of selected households. The prevalence of active sores was 11.6% and that of scars 4.3 %, indicating both the recentness and the severity of the outbreak. All ages and both sexes were involved. The finding of infected dogs suggests that these animals may be reservoirs of infection. A survey ofsandflies in the Kabul area showed the presence of 7 species ofPhlebotomus, 4 of which are potential vectors, and 4 species of Sergentomyia. Although cutaneous leishmaniasis has been known in some parts ofAfghanistan since ancient times, no systematic study of the disease was undertake until 1962. In that year, Eliseev and Kellina (1) carried out an epidemiological study of the disease in various parts of the country and reported the presence of zoonotic cutaneous leishmaniasis in the northern parts, where they found infections in Rhombomys opimus in 22 localities. They mentioned the presence of urban cutaneous leishmaniasis in the cities of Herat and Kandahar; however, in eastern Afghanistan (Kabul, Gazni, Saroobi, Jalalabad) they found no cases of cutaneous leishmaniasis. They reported that several people with scars whom they met in Kabul had caught the disease in northern Afghanistan, Kandahar, or Herat. Omar et al. (2-3) studied cutaneous leishmaniasis in Kabul city in 1967. They pointed out that autoch- thonous cases of this infection had been reported from Kabul city since 1947. The number of cases recorded in the city had been very low between 1947 and 1963, but from 1964 to 1967 had increased to a very significant level (334 in 1967). They noted that the majority of people who had scars dating from before 1965 had been infected in other provinces of the country. However, they found almost 1 000 recent 1 Professor of Epidemiology, School of Public Health, Teheran, Iran; WHO consultant to Afghanistan at the time of this study. ' Entomologist, Institute of Public Health, Kabul, Afgha- nistan. acute cases and scars that occurred in the city of Kabul, mostly in newly constructed sectors, either on the outskirts or at the foot of the two hills in the middle of the city. In early 1972, severe outbreaks in various parts of the city resulted in complaints from the inhabitants. In March 1972 a special team, organized to determine which localities ought to be put under a control programme, reported the existence of outbreaks in 12 different and separate localities in the city of Kabul and on its outskirts. Most cases were found in the area of the Khair Khana housing project to the north-west of the city. The present report contains the results ofepidemio- logical studies of cutaneous leishmaniasis at Khair Khana carried out from 12 June to 20 July 1972. METHODS The Khair Khana housing project, begun 3-4 years earlier, was designed to include about 5 000 houses; however, only 2 000 had been built at the time of the study and the rest were under construction. Not all the completed houses were built by the project authorities because, as soon as work began, people came from the city to build their own houses (mostly of very low standard) near the project. At the time of the study, houses were scattered over all parts of the project area, with many empty spaces between them. Three sections in this area were selected to study human infection and other epidemiological aspects. 3236 -45- A. NADIM & GH. S. ROSTAMI Table 1. Prevalence of cutaneous leishmaniasis in the Khair Khana area, Kabul, by age and sex, June - July 1972 No. of peoplevisited No.withscar Prevalence of scars No. with active Prevalence of activeNo. of pe plevis ted o. th s (%) lesions lesions (%) M F total M F total M F total M F total M F total <1 21 21 42 - - - - - - - - - - - - 1-4 148 150 298 7 3 10 4.8 2.0 3.3 22 1 1 33 14.8 7.3 11.0 5-9 164 161 325 9 10 19 5.4 6.2 5.8 29 31 60 17.6 19.2 18.4 10-19 208 177 385 12 6 18 5.1 3.4 4.9 30 22 52 14.5 12.4 13.7 ,20 438 382 820 24 11 35 5.4 2.8 4.2 35 38 73 7.9 10.0 8.9 all ages 979 891 1 870 52 30 82 5.3 3.3 4.3 116 102 218 11.7 11.4 11.6 One was in the centre and one in the north-west part of the housing project; the third was a village (Qalae Najjarha) on the eastern side of the area which, because of the extension of the housing project, had become joined to it. All houses within the selected sections were visited and special forms were filled out for each household showing the age and sex of the inhabitants, the presence or absence of sores or scars and their number and sites if present, the place of residence of each infected individual during the summer before the lesion started, and the presence or absence of dogs in the house. Sticky traps were used to collect sandflies. The traps consisted of pieces of paper measuring about 10x 17 cm covered with castor oil and supported by a wooden stick about 30 cm long. They were placed before dusk in rooms and near animal burrows, rock crevices, and other likely places. Some 3-5 ml of oil was enough for each trap. Sandflies collected on the traps were removed early in the morning. Some bloodfed and gravid individuals were dissected, but all others were washed in acetone and preserved in 50% ethanol for subsequent microscopic identifi- cation. RESULTS AND DISCUSSION Characteristics ofhuman infection Table 1 shows the prevalence of infection by age and sex in the Khair Khana area. It can be seen that the prevalence of active oriental sores was 11.6 %, a very high figure compared with foci of urban cuta- neous leishmaniasis in other parts of the world, which testifies to the intensity of the outbreak. On the other hand, the prevalence of scars was very low in the surveyed area (4.3 Y.), indicating the recent arrival of the infection among the inhabitants. If the disease had been endemic for a long time, the prevalence of scars would have been much higher. All ages showed the infection (it was absent from the <1-year age group because most of the children in this group had been born after the transmission season of the previous year). Many patients between the ages of 1 and 2 years were seen. On the other hand, many cases were observed in people aged more than 50 years. The highest prevalence was in the 5-9-year age group, but the figures for other age groups were not much lower. There was little difference between the sexes. The ages of patients were recorded for the 218 acute cases seen in this survey and also for 1 734 acute cases registered at a clinic in the housing project. It can be seen (Table 2) that referrals to the clinic did not have the same age distribution as patients seen in the house-to- house visits. Although 33.5% of the patients were aged over 20 years in the house-to-house visits, only Table 2. Age distribution of 1 734 cases registered at a clinic and 218 acute cases seen in a house-to-house survey in the same area, July 1972 Registered at clinic Seen in survey Age group No. of cases % No. of cases % <1 5 0.3 0 0 1-4 322 18.3 33 15.1 5-9 516 29.9 60 27.7 10-19 520 30.0 52 23.8 >20 371 21.5 73 33.5 all ages 1 734 100.0 218 100.0 46 CUTANEOUS LEISHMANIASIS IN KABUL 21.5% of the patients registered at the clinic were in this group. This is because the inhabitants are more concerned about the disease in their children and young people. The number of sores in the two groups of cases is shown in Table 3. The figures, which do not differ greatly, show that about 41 % of the patients had one sore, 23% two sores, and the rest 3 sores or more. Patients were seen with 15-20 sores, mostly on the face and hands. Not all of the patients with scars had been infected in Kabul; many had been infected in other parts of the country. Table 3. Number of sores in 1 397 cases registered at a clinic and 218 cases seen in a house-to-house survey No. of Seen in survey Registered at clinic lesions/case No. of cass % No. of cases % 1 91 41.7 585 41.1 2 50 22.9 329 23.5 3 24 11 192 13.7 > 4 53 24.4 291 21.7 4 25 11.4 5 9 4.1 6 9 4.1 7 2 1 8 1 5 >9 7 3.3 all cases 218 100.0 1 397 100.0 Reservoir of the disease There are several villages around Khair Khana that have been in existence for years. A visit to these villages showed that, although the present population had been living there all their lives, none of them had developed cutaneous leishmaniasis. A study of hu- man infection in the village of Qalae Najjarha showed that all the inhabitants had been free of infection up to 1971. At that time, the housing project reached the village and, although living conditions did not change, within a very short period about 60% of the population became infected. This observation rules out the possibility of the natural nidality of the disease in the area and suggests that some factor associated with the housing project and urbanization has brought the disease to these people. Efforts were made to find rodent colonies in and around infected areas. In Khair Khana, only the house mouse Mus musculus was collected. There were no gerbil colonies within 500m of built-up areas. One colony of Meriones was found in the Tarakhil graveyard, 3 km north of Kabul Airport, but this place is some distance from any inhabited locality. Moreover, there were no cases of leishmaniasis in the nearest village and sandflies were almost absent in the colony (from 100 sticky traps, only two specimens of Sergentomyia greckovi were collected, and no Phlebo- tomus). It was concluded that rodents have no role as a reservoir of the disease in the Kabul area and that the epidemics are of the urban type with man and probably dogs as reservoirs. In the course of a house-to-house visit of 300 houses, 21 house dogs were found, 6 of them (28.5 %) showing sores clinically diagnosed as cutaneous leish- maniasis. Microscopic examination of smears re- vealed the presence of parasites in two dogs, large numbers of Leishman-Donovan bodies being found in each field. Although a few weeks before the study, in early May 1972, more than 150 stray dogs had been poisoned and destroyed in this area, a drive through the streets of Khair Khana showed that many remained. Inspection from a distance of 2-3 m showed that 2 out of 7 examined had clinical cutaneous leishmaniasis. The question arises whether these dogs are only victims of human infection or reservoirs of the disease as well. It appears that they should be regarded as important reservoirs. When a sandfly bites a human being, the available body surface is extensive and even if the person has the disease, the probability of the sandfly becoming infected is very low (no evidence has been reported that the insects show a preference for biting on or close to a sore). On the other hand, when a sandfly tries to bite a dog, it can do so only on parts of the body not covered with hair. The surface available for biting is thus very small: the tip of the nose, the corners of the mouth, and the inner corners of the eyes. The probability of a sandfly becoming infected from an infected dog is therefore very high. Possible vectors: Phlebotomid sandflies of the Kabul area Seven species of Phlebotomus (P. papatasi, P. ser- genti, P. caucasicus, P. mongolensis, P. keshishiani, P. chinensis, and P. alexandri) and 4 species of Sergentomyia (S. dentata, S. pawlowskyi, S. greckovi, 47 A. NADIM & GH. S. ROSTAMI and S. bailyi) were found in the Kabul area. Table 4 shows the characteristics of the collection sites and Table 5 the number of each species collected from each site. Common endophilic sandflies included P. papatasi, P. sergenti and P. caucasicus. Most other species were also caught in houses in small numbers. During this survey, S. pawlowskyi was collected only from under rocks in the mountains. P. chinensis was also very abundant in mountainous areas, while P. papatasi, P. caucasicus and P. mongolensis were found only in the plains, where the soil is mostly of the clay type. The collecting sites that yielded most sandflies were lizard burrows and bird holes, as well as some rooms in old houses. Altogether, 90 bloodfed and gravid females were dissected (31 P. sergenti, 58 P. papatasi and one P. caucasicus). None of them showed leptomonad infection, but nothing can be concluded from so few dissections. On the basis of epidemiological evidence, it seems most probable that the main vector is P. sergenti, but it should be noted that several other potential vectors exist in the area (P. papatasi, P. caucasicus, P. mongolensis), all of which are domestic or peridomestic sandflies. Table 4. Sandfly collection sites, Kabul area, June - July 1972 No. Locality 1 Qalae Najjarha (indoors) 2 Qalae Najjarha (outdoors) 3 Qalae Seyed Khan 4 Kariz Mir (Panjeh mountain) 5 Baghe Bala 6 Qalae Menar 7 Jalalabad road (17 km from Kabul) 8 Tangi-Mahipar 9 Karte-i-Seh 10 Kariz Mir (dry river-bed) 11 Tarakhil graveyard 1 2 Farzeh Collection site Sprayed rooms Rodent and lizard burrows Bird holes and lizard burrows on hill Mountain caves and stone heaps Ruined building in orchard Bird and lizard holes by dry river-bed Rodent and lizard burrows Crevices under rocks (mountain) Room and courtyard in house in city centre Bird and lizard holes Gerbil colony Crevices under rocks (mountain) Table 5. Phlebotomid sandflies collected in Kabul area, June - July 1972 Collection site a Species 1 2 3 4 5 6 7 8 9 10 11 12 total Phiebotomus papatasi 70 444 - - 4 - I - 35 1 - - 555 P. sorgenti 197 797 101 12 62 35 25 4 12 72 - - 1 317 P. caucasicus - 57 - - - - - - - - - - 57 P. mongolensis 1 2 - - - - 19 - - 34 - - 56 P. keshishiani 1 2 1 - 1 - - - - - - - 5 P. alexandri - 2 3 2 - - - - - - - - 7 P. chinensis 15 39 1 65 - 1 1 8 - 24 - - 154 Sergentomyia dentate 47 31 3 31 25 - - 1 - 4 - 7 149 S.pawlowskyi - - - - - - 4 - - - 1 7 S. greckovi - 11 13 104 30 2 2 - - 105 2 1 260 S. bailyi 22 4 - 2 30 - - - 2 29 - 5 94 all species 353 1 379 122 218 152 38 48 17 49 269 2 14 2 661 a The sites are identified in Table 4. 48 CUTANEOUS LEISHMANIASIS IN KABUL 49 RESUME EPIDEMIOLOGIE DE LA LEISHMANIOSE CUTANEE A KABOUL (AFGHANISTAN) La leishmaniose cutan6e est end6mique dans certaines r6gions de I'Afghanistan. A Kaboul, des cas ont ete signal6s en petit nombre depuis 1947, mais depuis 1964 leur frequence s'est notablement accrue pour atteindre 334 en 1967. En 1972, de graves 6pidemies ont ete obser- vees en divers endroits de Kaboul et de sa banlieue, le nouveau quartier de Khair Khana etant particuliere- ment touch6. Des enquetes epid6miologiques, men6es dans ce der- nier foyer en juin-juillet 1972, ont rev616 que 11,6% des habitants 6taient porteurs d'ulcares en activite et que 4,3% pr6sentaient des cicatrices, ce qui t6moigne a la fois de la gravit6 et du caractere recent de 1'6pidemie. Tous les Ages et les deux sexes 6taient 6galement atteints. Parmi les malades, 41% 6taient porteurs d'un ulcere, 23 % de deux, et les autres de trois uIceres ou plus. Dans certains cas, on comptait 15 A 20 ulcares, localises pour la plupart A la face et aux mains. Six chiens domes- tiques (sur 21 examin6s) et de nombreux chiens errants pr6sentaient des ulcares ayant I'aspect clinique de la leish- maniose cutan6e. L'examen microscopique de frottis de l6sions a montr6 chez deux chiens la pr6sence d'un grand nombre de parasites. L'enquete a fait ressortir que les rongeurs ne jouaient aucun r6le dans cette epidemie urbaine, I'homme et probablement le chien etant les reservoirs de l'infection. Sept especes de Phlebotomus (P. papatasi, P. sergenti, P. caucasicus, P. mongolensis, P. keshishiani, P. chinensis et P. alexandri) et 4 esp&es de Sergentomyia (S. dentata, S. pawlowskyi, S. greckovi et S. bailyi) ont ete recoltees en diff6rents points de la region de Kaboul, pour la plupart dans des terriers de lzards, des abris pour oiseaux et dans certaines habitations v6tustes. Les donn6es epide- miologiques indiquent que P. sergenti est probablement le vecteur principal, mais d'autres phl6botomes aux habitudes domestiques ou peridomestiques (P. papatasi, P. caucasicus, P. mongolensis) sont aussi des vecteurs potentiels. REFERENCES 1. ELiSEEV, L. N. & KELLINA, 0. I. Med. Parazit. (Mosk.), 32: 728-35 (1963). 2. OMAR, A. ET AL. Preliminary study on the foci of cutaneous leishmaniasis in Kabul City. Z. Tropenmed. Parasit., 20: 292-303 (1969). 3. OmAR, A. ET AL. Cutaneous leishmaniasis in Afghanistan. Afghan J. Pub. Hlth, 1(2): 1-6 (1968).