Risk Assessment of the Role of the Ecotones in the Transmission of Zoonotic Cutaneous Leishmaniasis in Central Tunisia.

Walid Barhoumi,Mohamed Abbas,Wasfi Fares,Marcelo Ramalho-Ortigao,Ifhem Chelbi,Mohamed Derbali,Sami Zhioua,Elyes Zhioua

doi:10.3390/ijerph18179274

Abstract

Zoonotic cutaneous leishmaniasis (ZCL), endemic in Central and Southern Tunisia, is caused by Leishmania major (Kinetoplastida: Trypanosomatidae), which is transmitted by the sand fly Phlebotomus papatasi. In Tunisia, the fat sand rat Psammomys obesus and the desert jird Meriones shawi are the principal reservoir hosts of L. major. The presence of the P. papatasi vector of the L. major etiologic agent of ZCL was assessed in the vicinity of villages in endemic areas of Central Tunisia. The study was performed from September through October 2019, a period corresponding to the main peak of activity of P. papatasi. Sand flies were collected from rodent burrows located at the ecotone level, which is the transition zone between the natural environment and human settlement. Sand flies were identified to species level and tested for the presence of L. major by PCR. Our entomological survey showed that P. papatasi is the most abundant sand fly species associated with rodent burrows, and this abundance is even higher in ecotones primarily occupied by P. obesus in comparison to ecotones occupied by M. shawi. Infections with Leishmania major were detected only in P. papatasi, with an overall minimum infection rate (MIR) of 2.64%. No significant difference was observed between the MIRs in ecotones of P. obesus and of M. shawi. Incidence of ZCL in the studied areas ranged from 200 to 700 cases per 100,000 inhabitants, with a mean incidence of 385.41 per 100,000. Higher ZCL incidence was identified in ecotones of M. shawi compared to ecotones of P. obesus. ZCL cases are positively correlated with the MIRs. Considering the short flight range of P. papatasi, increases in its densities associated with burrows of P. obesus or M. shawi at the ecotone level expand the overlap of infected vectors with communities and subsequently increase ZCL incidence. Therefore, control measures should target P. papatasi populations at the ecotones.

Highlights

While several studies performed in Tunisia reported high infection rates of P. obesus and M. shawi with L. major varying from 40 to 70% [6,7], few studies were performed on L. major infection prevalence in P. papatasi associated with rodent burrows and its association with Zoonotic cutaneous leishmaniasis (ZCL)
We reported that P. papatasi is the most abundant sand fly species associated with rodent burrows in all investigated sites
Based on our entomological and epidemiological findings, we provided strong evidence that the two clearly distinct ecotones associated with the interaction of P. papatasi with P. obesus and M. shawi are intertwined and play critical roles regarding the origin of ZCL emergence in rural communities

Summary

Introduction

In North Africa, zoonotic cutaneous leishmaniasis (ZCL) is caused by the parasite. Leishmania major and is transmitted by infected bites of the sand fly species Phlebotomus papatasi [1,2]. In several ZCL endemic areas throughout North Africa, the fat sand rat Psammomys obesus and the desert jird Meriones shawi are the principal reservoir hosts of. L. major [3,4,5,6,7,8]. Thousands of ZCL cases are reported from Central and Southern. Tunisia [9,10], with the governorate of Sidi Bouzid alone having an estimated annual ZCL incidence rate of 669.7 per 100,000 inhabitants [11].

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