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Resurgence of Cutaneous Leishmaniasis in Israel, 2001–2012 Dan Gandacu,1 Yael Glazer,1 Emilia Anis, Isabella Karakis, Bruce Warshavsky, Paul Slater, and Itamar Grotto

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Resurgence of Cutaneous Leishmaniasis in Israel, 2001–2012 Dan Gandacu,1 Yael Glazer,1 Emilia Anis, Isabella Karakis, Bruce Warshavsky, Paul Slater, and Itamar Grotto Resurgence of Cutaneous Leishmaniasis in Israel, 2001–2012 Dan Gandacu,1 Yael Glazer,1 Emilia Anis, Isabella Karakis, Bruce Warshavsky, Paul Slater, and Itamar Grotto Cutaneous leishmaniasis has long been endemic in Is- been widely distributed in the Negev region in the Southern rael. After a 15-year period of moderate illness rates, report- health district, the arid and semi-arid area of southern Israel ed incidence increased from 0.4 cases per 100,000 popula- that that is sparsely populated and accounts for ≈60% of the tion in 2001 to 4.4 cases per 100,000 population in 2012, country’s land. More recently, illness caused by L. tropica and the disease emerged in areas where its presence had parasites has been reported in several semi-arid hilly areas previously been minimal. We analyzed all cases reported in Israel’s more densely populated, and less dispersed, cen- to the national surveillance system and found that outbreak patterns revealed an expansion of Leishmania major infec- tral and northern population centers (9,10). tions over large areas in the southern part of the country The recognized vector of CL in Israel is the female and the occurrence of spatially focused L. tropica outbreaks phlebotomine sand fly. The species predominantly respon- in the northern part of the country. Outbreaks often followed sible for CL cases in Israel have been Phlebotomus papa- new construction in populated areas. Further study of fac- tasi for L. major infections and Ph. sergenti for L. tropica tors affecting the transmission of cutaneous leishmaniasis infections. The reservoir of L. major parasites consists of is needed in Israel, as well as the development of effective rodents (e.g., Psamomys obeesus, Meriones crassus, Micro- methods to control the disease, an increase in awareness tus guentheri, Meriones tristrami, Gerbillus spp.), whereas among health care professionals, and intensive public edu- the main reservoir of L. tropica parasites is the rock hyrax cation regarding control measures in areas of known leish- (Procavia capensis). L. tropica infection tends regionally maniasis foci. to be an urban, anthroponotic phenomenon, but in Israel it is zoonotic in nature and has an incubation period that is eishmaniasis is a disease caused by parasites of the longer than that for L. major infection and is more resistant Lgenus Leishmania (Trypanosomatidae: Kinetplastida); to treatment. L. tropica infection also results in multiple le- global incidence approaches 2 million cases annually (1,2). sions and, when it results in leishmaniasis recidivans, has a Cutaneous leishmaniasis (CL), the most common form of lower tendency to heal spontaneously (11,12). the disease (3), is endemic in most Mediterranean countries Before 2001, a total of 3,352 cases of CL had been (4). Humans become hosts of the disease when the parasitic reported in Israel, and annual incidence ranged from 0.1 to infection develops in the immune system and causes skin 7.3/100,000 population. Two periods of particularly high lesions. The lesions tend to heal spontaneously after 3–18 illness rates occurred during this time, in 1967–1969 and in months (5) but often result in disfiguring scars (6,7). Func- 1980–1982 (13). The first peak, in the late 1960s, appeared tional complications are rare (8). after the June 1967 War, after the exposure of naive popu- CL has long been endemic in Israel, and the disease is lations to the parasite in disease-endemic areas. The sec- known colloquially in the region as the “Rose of Jericho.” ond peak, in the early 1980s, was assumed to have resulted Historically, the main source of the disease in Israel has been primarily from the continuing increase in the number of L. major parasites; cases resulting from this species have new settlements westward from the Jordan Valley toward Jerusalem (13). A decade and a half of relatively moderate Author affiliations: Israel Ministry of Health, Jerusalem, Israel incidence followed, and at the end of 2000, reported na- (D. Gandacu, Y. Glazer, E. Anis, I. Karakis, B. Warshavsky, tional incidence stood at 0.3/100,000 population. However, P. Slater, I. Grotto); Hebrew University and Hadassah–Braun by 2012, reported incidence had increased to 4.4/100,000 School of Public Health, Jerusalem (E. Anis); and Ben-Gurion population and CL had emerged in areas where its presence University of the Negev Department of Public Health, Be’er Sheva, had previously been minimal. We describe these changes Israel (Y. Glazer, I. Karakis, I. Grotto) from an epidemiologic point of view and discuss factors DOI: http://dx.doi.org/10.3201/eid2010.140182 1These authors contributed equally to this article. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 20, No. 10, October 20142014 1605 SYNOPSIS that might explain the increase in CL rates and distribution using Microsoft Excel 2010 (Microsoft, Redmond, WA, from 2001 to 2012. USA) and SPSS version 19.0 (SPSS IBM, Armonk, NY, USA). We considered p<0.05 as statistically significant. Methods The Israeli Ministry of Health has conducted routine Results national surveillance of CL since 1949, when the disease Overall, 2,061 cases of CL that occurred in Israel were became reportable. Cases are reported through a computer- reported during January 1, 2001–December 31, 2012. Of ized notification system network from each of 15 regional the case-patients, 58% were men, and 93.8% were Jew- health districts in the country. The ministry’s Division ish. The mean age at disease onset was 31.1 + 22.1 (range of Epidemiology (DOE) monitors and processes the case 0–90, median 28) years. More than 42% of reported cases report data on a national basis. Although the surveillance occurred during 2010–2012, and 40% of case-patients were method is passive and is assumed to underestimate the ac- residents of the Southern health district/Negev region. tual number of CL cases, no changes in reporting methods From 2001 to 2012, the CL incidence rate in Israel in- and no official efforts to increase the frequency of notifica- creased tenfold, from 0.4 to 4.4/100,000 population (Figure tion have been implemented. Therefore, we assumed in our 1). Over this period, mean annual incidence increased by research that the reported incidence data are a good indica- 0.36/100,000 population. These increases reflect, in part, tion of actual epidemiologic trends in the population. the spread of CL to central and northern areas of the coun- Two caveats should be noted regarding any CL in- try, where reports of the disease had previously been mini- cidence data. Underreporting of CL is widely acknowl- mal. Those increases were highlighted by several outbreaks edged to be a problem for a variety of clinical, logistic, and incidence peaks. An outbreak occurred in the Kinneret cultural, and other reasons (14); we discuss some of the subdistrict near Lake Tiberias in northern Israel in 2003; underlying causes for underreporting later in this article. several dozen cases were reported, sometimes >1 per fam- However, during major outbreaks or when infection oc- ily, in 2 new periphery neighborhoods at the edge of the curs in previously non–CL-endemic areas, heightened city of Tiberias. During 2004–2005, an outbreak of >100 awareness may increase the proportion of CL cases that cases occurred in 2 new neighborhoods near the ravines are officially reported. of a suburb, Ma’ale Adumim, in the Jerusalem health dis- Laboratory confirmation of suspected CL cases is cur- trict. A peak in national incidence occurred in 2007–2008, rently not required, and therefore, laboratory tests are not a result of an increase in CL cases in the Southern health routinely performed on samples from all reported case- district, where L. major parasites are endemic, and an patients. Consequently, both probable and confirmed CL outbreak of L. tropica infections in the northern district. cases are reported to the DOE, and distinctions cannot be Whereas cases from the southern region were sporadically made in the national incidence data between L. major and distributed, in the northern region, cases were restricted to L. tropica infections. Because the laboratory results that are peripheral houses near the borders of 1 rural settlement in available provide an indication of the Leishmania species, the Yizre’el subdistrict, where few cases had been reported these results can be used to make reasonable species-re- in the past. The main sources of a subsequent peak in 2012 lated assumptions regarding specific outbreaks and regard- were the occurrence of 37 cases in Ofakim, a small town ing other reported cases in nearby geographic areas where in the Southern health district, and 44 cases that occurred another species has not been detected. However, for those with the continuation of the outbreak in Ma’ale Adumim areas in which >1 species of Leishmania is found, such as- (24.2% and 64.7% of the district totals, respectively). To- sumptions cannot be made (15). ward the end of 2012, a new outbreak began in Carmiel, in We analyzed all CL cases that were reported to the the Akko subdistrict. CL illness rates also increased within Israel national surveillance system for which onset oc- the Southern health district in several localities, including curred during January 1, 2001–December 31, 2012. For Be’er Sheva, Eilat, Yeruham, and Arad, and expanded else- methodologic reasons, all cases reported here are from where to other, much smaller, rural villages (Figure 2). the civilian population; the Israeli military uses active Among age groups, increases in incidence were high- surveillance for CL and commonly includes only cases est during most years among infants. Nevertheless, the with a clinical diagnosis. 15–44-year-old age group comprised the greatest portion The denominators used for calculations of crude and of case-patients each year compared with the other age specific incidence rates per 100,000 persons according to groups; these differences were significant in 2006 (p = age, sex, population group, and health district were derived 0.03), 2007 (p = 0.016), 2009 (p = 0.025), 2010 (p<0.001), from annual population estimates from the Central Bureau and 2012 (p<0.001) (Table).
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