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

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.

Epidemiological Aspects of Zoonotic Cutaneous Leishmaniasis (ZCL) in Iran, the Middle East, and Worldwide: A Comprehensive Systematic Review

“…This geographical spread shows that ZCL is not only a problem in Iran but also poses a challenge across countries. This underscores the need for a coordinated international effort in research and control measures to address this issue effectively (16–17,22–25,34–35,88–89,90,97,4,13,20,38,54,57,59,66,64,69).…”

“…In Tunisia, children under 10 years of age and those aged 10-20 years were more affected (34). The increase in P. papatasi sand fly densities is linked to the burrows of P. obesus or M. shawi rodents in ecotone areas (25). Increased P. papatasi populations were also observed in farmers involved in irrigation activities (57) due- to factors like increased rainfall, humidity (16), rodent density, average temperature, cumulative rainfall, and average relative humidity (69,59,54).…”

“…In our view, joint programs that take a holistic approach have a better chance of reducing the burden of ZCL in North Africa and the Middle East. This approach should include management of reservoir hosts and sandflies as well as consideration of human behavior and environmental needs as part of the One Health approach (22)(23)(24)(25). Over the past 10 years, approximately 1.5 million new cases of zoonotic cutaneous leishmaniasis (ZCL) have been reported each year.…”

Seasonal Patterns of Zoonotic Cutaneous Leishmaniasis Caused by L. major and Transmitted by Phlebotomus papatasi in the North Africa Region, a Systematic Review and a Meta-Analysis

“…One or more lesions appear after the bite by an infected sand fly, and the inflammation causes scarring if not treated, which leads to traumatic psychological impacts. Shaw's jird (Meriones shawi) and the fat sand rat (Psammomys obesus) are the identified reservoirs, while P. papatasi is the proven vector of L. major [6,7]. This disease affects regions with semi-arid and arid climates in North African countries, especially in the poorest provinces.…”