Leishmania (Leishmania) donovani (Laveran et Mesnil, 1903), 1908

Rioux, Jean-Antoine, Gramiccia, Marina, Léger, Nicole, Desjeux, Philippe & Depaquit, Jérôme, 2020, Leishmaniasis and phlebotomine sand flies in Oman Sultanate, Parasite (Paris, France) 27 (68), pp. 1-13 : 10

Leishmania (Leishmania) donovani (Laveran et Mesnil, 1903)

The record of L. donovani ZMON- 31 in Oman leads us to briefly discuss the taxonomic status and the geographical distribution of this zymodeme and closely related zymodemes.

Starting in the 1980s, enzymatic taxonomy studies led to consider the linnean taxa L. donovani and L. infantum as two distinct phenetic groups. Cladistic analysis confirmed these results by showing their monophyly [ 37, 48, 60]. In fact, these phylogenetic groups (or complex) possessed a series of synapomorphic states, such as G6 PD 100, G6 PD 102 G6 PD 105, GPI 86, GPI 100, GOT1 100, GOT2 100, GOT 113, and GOT2 113. Some of these states were common to both branches, others only present in one of them. This was the case of PGM 100, present in the donovani-infantum set (complex synapomorphies), GOT1 100 and GOT2 100 present in the single subset L. infantum, and GOT1 113 and GOT2 113 present in the single subset L. donovani (specific synapomorphies). The taxonomic status of the donovani-infantum group changed at the end of the 1980s. Enzymatic analysis of human Leishmania strains isolated in Sudan [ 49, 60] and the vector Ph. orientalis [ 11] showed an original zymodeme (MON-82, L. archibaldi) characterised by a heterozygous structure for GOT1 (100/113) and GOT2 (100/113), and highlighted the complexity of the systematics of L. donovani s. l. [ 54]. Moreover, hybrids could develop differently in sandfly vectors [ 66].

L. donovani ZMON-31, isolated from CL in Oman, was already known from Saudi Arabia [ 51] and Yemen [ 56] as responsible for VL. Moreover, this zymodeme is phylogenetically closely related to L. donovani ZMON-83 ( Ethiopia), ZMON-3 ( Iraq), ZMON-37 ( Kenya), and ZMON-2 ( India), all responsible for VL. Finally, a new zymodeme, L. donovani MON-191, close to ZMON-31, was isolated from a French tourist traveling to Yemen contracting a CL [ 52]. Multilocus microsatellite typing ( MLMT) revealed genetically isolated populations in the main endemic VL regions [ 35]. Leishmania donovani ZMON31 was identified within the predominantly anthroponotic L. donovani cluster of Sudan / Ethiopia.

Regarding the clinical aspect, even though L. donovani s.st. is poorly studied for tissue tropism, the complex L. donovani–L. infantum appears to cause both CL and VL.

Therefore, we consider L. donovani s.st. as the most probable agents of VL in Oman. However, L. infantum s. st. would be in second place, if its presence should be confirmed, as it is in Yemen (Taëz), a country where L. donovani, L. infantum and L. tropica are sympatric [ 57]. In Oman, the scarcity of dogs, domestic or feral, in relation to the significant number of reported human cases seems more in agreement with the circulation of L. donovani than that of L. infantum. On the basis of the sandflies collected, the proven or candidate vectors of L. donovani were not recorded: Ph. (Eup.) argentipes [ 34], Ph. (Lar.) orientalis, Ph. (Syn.) celiae, Ph. (Syn.) martini, or Ph. (Ana.) rodhaini [ 3]. Consequently, the vector candidates for L. donovani transmission in the Sharqiyah region still remain unknown. For us, the only candidate could be Ph. alexandri, a species suspected in China [ 27] or in Cyprus [ 9, 38], but the low densities of this species observed in Oman do not argue in favour of any role.

The low positivity rate of the skin test (8%) reported in children of Ibra province suggests a weak interaction between the young population and the Leishmania parasite, confirming a low density of sandfly vectors or their weak anthropophilia.

Consequently, in order to better understand the epidemiology of the leishmaniases in Oman, we encourage the isolation and typing of Leishmania strains in the future, because each Leishmania complex often corresponds to a specific vector and to a particular parasitic cycle (anthroponosis/zoonosis). This was the problem previously raised when L. infantum was suspected to be the causative agent of VL in Oman [ 30], whereas L. donovani s.l. was later incriminated as the agent of VL [ 63].