Retrospective Analysis of Leishmaniasis in Central Tunisia: An Update on Emerging Epidemiological Trends (Tropical Diseases Due to Protozoa and Helminths) Part 1

Introduction

This study aimed at describing the spatio-temporal distribution of leishmaniasis in patients who have sought diagnosis in the laboratory of Parasitology of Farhat Hached hospital, Sousse, Tunisia, across the 1986-2010 period in order to: i) highlight important features and trends of leishmaniasis and its epidemiology; ii) and to assess whether the activity of the unit reflects the situation of the disease at the national level and whether it could constitute an indicator of public health relevance.

Current situation of leishmaniasis in Tunisia

Tunisia is located in Northern Africa, bordering the Mediterranean sea between Algeria and Libya. Its climate is of the hot temperate Mediterranean type. Bioclimatic zones range from humid in the north to saharian in the extreme south (Figure 1).

The country is divided into 24 governorates, each composed of a variable number of "delegations"; and each delegation is subdivided into localities also named "imadas" (Figure 2). Four forms of leishmaniasis are known to occur in Tunisia: i) the sporadic cutaneous leishmaniasis (SCL); ii) the chronic cutaneous leishmaniasis (CCL); iii) the zoonotic cutaneous leishmaniasis (ZCL); iv) the visceral leishmaniasis (VL).

The sporadic cutaneous leishmaniasis (SCL)

This form is caused by dermotropic zymodemes of Leishmania infantum, mainly the zymodeme MON 24 and to a lesser extent MON 1 (Aoun et al., 2000, 2008; Ben Ismail et al, 1986, 1992; Gramiccia et al., 1991; Haouas et al., 2007; Kallel et al., 2005, 2008b). The dog is supposed to be the reservoir as it is the case for the viscerotropic zymodemes and Phlebotomus perfiliewi as the phletotomine vector. But other vectors can not be excluded; following an outbreak of SCL in the locality of Oued Souani, le Kef governorate, P. langeroni was found infected by L. infantum (Guerbouj et al., 2007).

Fig. 1. Map of Tunisia showing the distribution of bioclimatic zones.

SCL was first described in 1917 in a patient from Sakiet Sidi Youssef (Le Kef governorate) located next to the Algerian frontier (Nicolle & Blanc, 1917), and again in 1945 (Chadli et al., 1968; Vermeil, 1956). Since 1945, the disease has sporadically been reported with, however, an incidence that gradually increased from a median of one case / year between 1945 and 1955 to 22 cases /year in the 1990s and 59 cases/year in the 2000s (Table 1; Anonymous ; Ben Abda et al., 2009; Ben Said et al., 2006; Ben Ismail & Ben Rachid, 1989; Ben Rachid et al., 1983, 1992; Chadli et al., 1968 ; Chaffai et al., 1988; Ladjimi & Lakhoua, 1955 ; Vermeil, 1956). SCL has long been supposed to be confined to the humid and subhumid bioclimatic areas north to the "dorsale" or "tunisian Ridge" (the eastern extension of the Atlas mountains), in rural areas where its distribution overlaps with that of VL (Ben Ismail et al., 1989; Ben Rachid et al., 1983; Ben Rachid & Ben Ismail, 1989; Chadli et al., 1986 ; Vermeil, 1956). However, over the last three decades, many cases originating from central Tunisia governorates (Monastir, Sousse, Mahdia and Kairouan) and referred to our laboratory were found to be very suggestive of SCL on the basis of epidemiological, clinical and parasitological criteria. Typed strains obtained from some of these patients proved indeed to be L. infantum (Ben Said et al., 2006). These data were very indicative of SCL spread towards the south of the country. These findings were further confirmed by additional reports (Aoun et al, 2000, 2008; Ben Abda et al., 2009; Kallel et al., 2008a, 2008b). The revised SCL distribution is shown in figure 3. SCL usually occurs sporadically within no particular season. However, over the last few years, local outbreaks were reported like that of Sidi Bourouis in Siliana governorate, which involved more than 30 patients over a short period (Bel Hadj et al., 2003).

Fig. 2. Map of Tunisia showing its subdivision into 24 governorates (Grand Tunis is composed of 4 governorates).

Table 1. Number of recorded sporadic cutaneous leishmaniasis cases since 1945.

Clinically, SCL is characterized in more than 90 % of patients by a small single ulcerated or lupoid lesion of the face that often lasts longer than one year and up to three years (Bel Hadj et al., 1996; Ben Ismail & Ben Rachid, 1989; Chaffai et al, 1988; Masmoudi et al., 2007). On a parasitological level, amastigotes of L. infantum are smaller than those of L. major, usually less than 3μ , and promastigotes are difficult to maintain on NNN medium (Aoun et al., 2000, 2003).

: corresponds to the classical distribution of the cases;: illustrates the emerging distribution of cases.

Fig. 3. Updated distribution of sporadic cutaneous leishmaniasis in Tunisia.

The chronic cutaneous leishmaniasis (CCL)

Formerly known as anthroponotic CL, CCL sporadically occurs in micro-foci located in the south-eastern presaharian and saharian areas of Tunisia. Its distribution is rural, sub-urban and urban; and cases are reported from houses, farms, and even from troglodytes of Tataouine (Tataouine governorate) and Matmata (Gabès governorate), with a median annual incidence of 10 cases / year (Figure 4; Ben Ismail & Ben Rachid, 1989; Ben Rachid et al., 1983, 1992; Chadli et al., 1968). CCL was first reported in 1957 and nearly nothing was known about the disease before this date. In 1979, an outbreak involving 47 individuals arose in Tataouine; and the epidemiological investigation, which included the isoenzymatic typing of strains isolated from the patients, led to the identification of the parasite as the MON 8 zymodeme of L. tropica, named L. killicki, a species previously described in Kenya, Namibia, Yemen and, more recently in Algeria and Libya (Harrat et al., 2009; Rioux et al., 1986; Sang et al., 1994).

Fig. 4. Actual distribution of chronic cutaneous leishmaniasis.

Surprisingly, over the last decade, cases of CCL were reported in patients originating from areas where this form has never been previously reported, the first case being in a child from Meknassy in Sidi Bouzid governorate (Haouas et al., 2005). Later, additional cases were reported from Kairouan, Gafsa and Siliana governorates, very far from the classical foci of Tataouine (Aoun et al., 2008; Ben Abda et al., 2009; Bouratbine et al., 2005).

Hence the actual distribution and incidence of CCL need further investigations and obviously should be revised.

L. killicki is transmitted by Phlebotomus sergenti, but the reservoir is still debated. Median age of patients suffering of CCL is 21 years (Ben Abda et al., 2009; Ben Ismail & Ben Rachid, 1989). Clinically, CCL most often presents as single or very few lesions on the face or limbs, that are dry, extensive, and chronic, lasting for up to six years (Ben Abda et al., 2009; Ben Ismail & Ben Rachid., 1989; Chaffai et al., 1988; Masmoudi et al., 2007).