ORIGINAL ARTICLES IMAJ • VOL 12 • noveMber 2010 Geographic and Epidemiologic Analysis of the Cutaneous Leishmaniasis Outbreak in Northern Israel, 2000–2003 Olga Vinitsky MD1, Liora Ore MD1,3, Hamza Habiballa MD2 and Michal Cohen-Dar MD1,3 1Ministry of Health – Northern District, and 2Ministry of Environmental Protection – Northern District, Nazareth Illit, Israel 3School for Public Health, Faculty of Social Welfare and Health Sciences, Haifa University, Haifa, Israel areas in Israel, with accumulating evidence supporting the ABSTRACT: Background: The incidence of cutaneous leishmaniasis in nor- notion that hyraxes in these areas are the reservoir host of thern Israel began to rise in 2000, peaking at 41.0 per 100,000 Leishmania tropica [5,10-13]. Sand flies (the disease vector) in the Kinneret subdistrict during the first half of2003 . transfer the Leishmania from the infected reservoir host to Objectives: To examine the morbidity rates of CL in northern humans. The lesions that develop in the bite area, mainly the Israel during the period 1999–2003, which would indicate face and limbs, are cosmetically damaging, may be prolonged whether new endemic areas were emerging in this district, [6,9,14,15] and may result in atrophic scars [9]. and to identify suspicious hosts. L. tropica, as compared to L. major, is characterized by Methods: The demographic and epidemiologic data for the higher severity, longer course (up to a year and a half), reported cases (n=93) were analyzed using the GIS and SPSS resistance to routine therapies, and a chronic or relapsing software, including mapping habitats of suspicious hosts and localizing sites of infected sand flies. clinical presentation [5,6,10,16]. Some cases need intra- Results: The maximal incidence rate in the district was venous sodium stibogluconate therapy, often resulting in found in the city Tiberias in 2003: 62.5/100,000 compared serious adverse effects requiring hospitalization [6,16,17]. In to 0–1.5/100,000 in other towns. The cases in Tiberias were endemic CL areas L. tropica may cause visceral leishmaniasis concentrated on the peripheral line of two neighborhoods, [5], a highly fatal disease particularly in children and immu- close to the habitats of the rock hyraxes. Sand flies infected nocompromised patients [19]. with Leishmania tropica were captured around the residence CL in Israel is an endemic disease and only a few patients of those affected. Results of polymerase chain reaction were contract the disease abroad. The incidence of CL during positive for Leishmania tropica in 14 of 15 tested patients. the period 1961–2000 was 0.13–7.0/100,000 [4]. During Conclusions: A new endemic CL area has emerged in the period 1995–1998 endemic areas of CL were identified Tiberias. The most suspicious reservoir of the disease is the in northern Israel near the Sea of Galilee (Kinneret) [5]. In rock hyrax. 2000 the incidence of the disease in the Kinneret subdistrict IMAJ 2010; 12: 652–656 began to rise, reaching the highest level in the country – KEY WORDS: cutaneous leishmaniasis, outbreak, epidemiology, Israel, 41.0/100,000 – in the first half of 2003 [20]. hyrax, sand flies In 2003 we carried out an epidemiologic survey to define the demographic characteristics of the affected CL patients and identify the possible animal reservoir. Results of this sur- vey were then translated into an intervention program aimed at reducing the disease burden. The Northern District data utaneous leishmaniasis, caused by Leishmania parasites, of the CL database show that during the years that followed, C is an endemic worldwide disease with about 1.5 million CL incidence rates in Tiberias fluctuated, with an overall cases occurring each year [1]. During the period 1993–2000 decreasing trend: 20.0–39.9/100,000 during 2004–2006 and the global incidence rate increased by 500% [2]. Urbanization 15.1–22.6/100,000 during 2007–2008. More details pertain- and the development of new neighborhoods close to nature ing to the association between the intervention program and areas contributed to this rise in morbidity [3-7]. The disease the disease reduction will be described in a separate article. is usually zoonotic with a variety of rodents and other mam- mals serving as the disease reservoir [2,8,9]. The rock hyrax, a small thickset herbivorous mammal, is MATERIALS AND METHODS the suspected disease reservoir in Kenya, Namibia and some The study was conducted in northern Israel, a region com- prising five subdistricts with a population of about 1,100,000. CL = cutaneous leishmaniasis Eligible for this study were all CL cases diagnosed in northern 652 IMAJ • VOL 12 • noveMber 2010 ORIGINAL ARTICLES district residents who had been reported to the Ministry of Incidence rates were calculated by geographic area. Associations Health during 1999–2003. between age and gender and the place where the patient con- tracted the disease were examined using the chi-square test. DATA COLLECTION AND VARIABLES DEFINITIONS Student's t-test was used for comparing groups regarding con- Several data sources were used: tinuous variables, and the one-way ANOVA test was used for • Individual notification forms completed by the diagnosing comparing differences among more than two groups. physicians and including the patient’s demographic data, A GIS layer was created for all study cases based on the address, diagnosis and laboratory test results following data: residence and site of disease contraction as • Epidemiologic investigation questionnaires, routinely well as the year the first signs appeared. Regarding Tiberias, filled in by the subdistrict's health department team and an additional two GIS layers were created for mapping out the including additional data on the clinical manifestations, habitats of rock hyraxes and sand-fly traps. All three layers date of disease onset, places visited during the year prior were then matched to examine the degree of their overlap. to disease onset, and information on mosquito bites and the presence of animals around the patient’s residence • Data collected from the Ministry of Environmental RESULTS Protection on the location of traps used to collect sand The district incidence rate of CL was more than four times flies infected by Leishmania higher in 2003 than in 1999 [Figure 1A]. The rate in the • Information from the National Parks Protection Authority Kinneret subdistrict increased from 6.1 per 100,000 to 26.0 and the municipality veterinarian regarding the location of the rock hyrax habitats in Tiberias Figure 1. [A] Incidence rate (per 100,000) of cutaneous leishmaniasis in northern Isra- • The Central Bureau of Statistics denominator data used el by subdistrict, 1999–2003. [B] Distribution (%) of CL cases: Tiberias vs. other locations, by month of disease onset during 1999–2003 (N=93). for the calculation of CL incidence rates • The patients' polymerase chain reaction results, which were 30 obtained from the Leishmaniasis Reference Laboratory A § Northem district 26.0 25 (Kuvin Center for the Study of Infectious and Tropical ‡ Other subdistrict Diseases, IMRIC, Hebrew University-Hadassah Medical † Safed 20 ¶ Kinneret School, Jerusalem) that carried out PCR diagnosis and Leishmania species typing. 15 13.9 9.1 Incidence rate Incidence 10 8 In order to monitor the CL morbidity and enable integra- 6.1 5 tion of data received from the above sources into one data- 3.3 3.5 2.7 3.2 1.7 5 1.6 0.8 9 0.2 1.5 1 0.8 base, computerized software, based on SQL SERVER, was 0 0 0 developed. The following definitions were used: 1999 2000 2001 2002 2003 • The place where the disease was contracted was deter- mined by the district’s epidemiologist, taking into account B the information about visiting endemic areas, as in the 30 Tiberias N=52 ** 25.0 questionnaire received from the relevant subdistrict’s epi- 25 demiologic team. For those not visiting any endemic area Other N=41 †† the place where the disease was contracted was assumed 20 19.5 17.1 to be the city or township of the patient’s residence. 15.4 15 14.6 • The time of disease onset was defined as the date of appearance of the first signs (i.e., nodules or macula) re- 10 9.6 9.6 9.6 9.6 9.6 9.8 7.3 7.3 ported by the patient in the epidemiologic questionnaire. 5.8 5.8 5 4.9 4.9 4.9 4.9 This information was later used for calculation of the CL 1.9 2.4 1.9 2.4 1.9 incidence rates, rather than the date of reporting to the 0 Ministry of Health. Dec Nov Oct Sep Aug July June May April Mar Feb Jan ¶ Population of the Kinneret subdistrict during 1999–2003: 97,720–102,326. STATISTICAL PROCESSING AND GEOGRAPHIC ANALYSIS † Population of the Safed subdistrict during 1999–2003: 118,215–124,938. The demographic and epidemiologic data of the study population ‡ Population in the remaining subdistricts during 1999–2003: 97,720–102,326. was exported from the CL database into GIS and SPSS software. § District population during 1999–2003: 1,058,736–1,142,546 ¶¶ Disease contracted in Tiberias IMRIC = Institute for Medical Research Israel-Canada †† Disease contracted in other places PCR = polymerase chain reaction 653 ORIGINAL ARTICLES IMAJ • VOL 12 • noveMber 2010 per 100,000; in the Safed subdistrict it increased from 1.7 to Map 1. Geographic distribution of the CL cases in the northern district according to place of residence and place of disease contraction, 2000–2003 3.2/100,000 and in the rest of the region it remained low. In the Kinneret subdistrict, the highest incidence rate was in Tiberias, reaching 62.5/100,000 in 2003 compared to 10.0/100,000 in 2002.