Eco-epidemiology of visceral leishmaniasis in Ethiopia

Visceral leishmaniasis (VL or kala-azar) is a (re)emerging 1] neglected tropical disease, endemic in over 79 countries 2], 3]. Diagnosis and treatment of VL is difficult and without appropriate treatment an
estimated 95 % of VL patients will die. The disease may kill between 20,000 and 40,000
people per year globally. Of those infected, a large majority remain asymptomatic.
The subclinical to clinical case ratio ranges from 1:1.2 to 1:9 depending on the eco-epidemiological
situation 4]–6]. Over 90 % of the annual incidence, 0.2 to 0.4 million new cases per year, occur
in Bangladesh, India, Nepal, Sudan, South Sudan, Ethiopia and Brazil. Eastern Africa,
the second largest VL focus after the Indian subcontinent, contributes to the global
burden with 30,000–40,000 new cases per year, of which Ethiopia, South Sudan and Sudan
contributing the largest proportion of the cases 2]. In Ethiopia an estimated 2500 to 4000 new cases occur per year and over 3.2 million
people are at risk of infection 7], 8].

The recorded history of VL in Ethiopia dates back to the 1940s with reports of VL
cases among members of the East African British Army deployed along the Ethiopian-Kenyan
border during the Second World War 9]. In their report on the outbreak of kala-azar in the battalion of the King’s African
Rifles, Cole et al. 10] documented that among confirmed cases of leishmaniasis, half (10/22) probably contracted
the disease in the low lying Omo River area, in the south-western corner of Ethiopia.
Subsequent field and longitudinal studies confirmed the endemicity of VL in Ethiopia
11]–14]. The vernacular name in Konso language, ‘golloba’, referred to in the retrospective
study by Lindtjorn (1970–1981) indicates that the disease was already well known in
the communities of the Segen and Woyto valley before World War Two 12].

The VL foci from which clinical cases are reported differ in their eco-epidemiology
and the sandfly vectors involved. Currently, VL transmission is known to occur in
three different ecological settings, spanning from lower Kola to the Woina Dega ecological
zones (Fig. 1). However, VL seems not to have been established despite the presence of the appropriate
vectors and high reported leishmanin skin test positivity and/or sero-prevalence along
the course of the Awash valley 15]–17] and in the Gambella region 18].

Fig. 1. Endemic foci of visceral leishmaniasis (VL) in Ethiopia. VL occurs mainly in the Kola
agro-ecological zones with recent spread to the Woina degas of Libo Kemkem and Fogera.
The circles summarize endemic foci so far described: confirmed human cases from autochthonous
transmission (blue circles); doubtful: no evidence of VL cases from autochthonous
transmission (circles with central black triangle); or seroprevalence only with no
human clinical VL (half black circles)

Importantly affected by altitude, Ethiopia’s climate is mainly of the tropical monsoon
type with wide topography-induced variation. Classified by topography and thermal
and moisture regimes (from over 20 year (1974 to 1993) ground data on major rain-fed
agricultural crops), Ethiopia has six agro-ecological zones: Unsuitable Wurch, Wurch,
Dega, Woina Dega, Upper Kola and Lower Kola 19]. In terms of geographical extent, 0.14 % (1187.34 km
²
), 0.33 % (2870.83km
²
), and 5.09 % (43,943.81km
²
) of the total landmass belongs to the Unsuitable Wurch, the Wurch and the Dega agro-ecological
zones, whilst the major portion of the country, 31.04 % (267,847.95 km
²
), 46.02 % (397,115.47 km
²
), and 17.38 % (149,945.56 km
²
) is covered by the Woina Dega, Upper Kola and Lower Kola zones respectively. Overlaying
20 consecutive years of Ethiopian National Meteorology Agency data (1989 to 2009),
the average mean surface temperature for Lower Kola, Upper Kola and Woina Dega is
26.35 °C, 22.05 °C and 17.81 °C, and the average annual rainfall is 490.48 mm, 871.84
mm and 1162.80 mm respectively. When the FAO (2000) soil map is clipped to the country’s
boundary and overlaid on the agro-ecologic zones, the five major soil types in a decreasing
order are Leptosols, Nitosols, Vertisols, Cambisols and Calsisols in all agro-ecological
zones. The major agricultural activities and production of the country occur in the
Woina Dega ecological zone whereas large scale private, government and resettlements
for both irrigated and rain-fed agriculture are currently being implemented or planned
in the upper and lower Kola agro-ecological zones.

The southern lowland foci

The southern foci are the south-western savannah and the south-eastern semi-arid lowlands
which account for approximately 20 % of the total VL burden in Ethiopia 11]. The Omo and Aba-Roba plains and the Woyto and Segen River valleys in the Southern
Nations, Nationalities and Peoples’ Regional State (SNNPR) are the oldest known VL
foci in Ethiopia 13], 14]. These foci are characterized by lower to upper Kola agro-ecology with an altitude
that ranges from 500–1500 m above sea level (masl). The area is inhabited by nomadic
or semi-nomadic pastoralist communities. Several studies have described the foci.
Leishmanin skin test surveys in the 1970s showed different levels of VL endemicity
among the communities in the lower Omo (400–600 masl), upper Omo (1400 masl) and Hamar
(~1000 masl) areas with 65 %, 6.4 % and 21.2 % positivity rates respectively 13], 14]. A survey conducted in the 1880s identified the Genale river basin and the western
part of Moyale town as endemic areas 11]. A prospective study conducted from 1997 to 2000 in Aba-Roba further established
it as the focus with the highest VL endemicity of the south-west 20], and confirmed earlier reports of the spatio-temporal and age differences in the
prevalence and incidence of VL in the region 4]. Further eastward, in the Oromia regional state, sporadic VL cases have been reported
from Lake Abaya, Moyale area and the Dawa and Genale River valleys 11], 21]. Down in the south-eastern semi-arid lowlands, there is a recent report of VL transmission
in the Afder and Liben areas in the Somali regional state 22].

Northern lowland foci

The Metema and Humera plains in the Tigray and Amhara regional states, bordering Sudan
and Eritrea, constitute the main VL endemic area in the country, contributing over
60 % to the burden. These foci are also in the lower and upper Kola agro-ecological
zones, with wide, open plains covered in bush scrubs and Acacia woodland. The woodland
cover is in process of being replaced by extensive commercial agriculture that produces
sesame as the main cash crop. Leishmanin skin test surveys on 1057 participants in
Humera in the 1970s among predominantly new settlers (4.4 years average stay) documented
a marked difference of prevalence in the farming (45.6 %) and non-farming (8.3 %)
communities and showed that overall skin test positivity increased with the duration
of stay in the area 23]. A sharp rise in the number of VL cases was attributed to the influx of seasonal
temporary workers for the large-scale agricultural schemes and forced resettlements
of populations from the neighboring highlands 23]–25]. A high HIV prevalence among seasonal workers has contributed to the rise in VL prevalence
in this group 26]–28]. The highest HIV/VL co-infection rate world-wide (~38 %) was reported in this region.
A Médecins Sans Frontières (MSF) treatment centre treated 2000 to 5000 VL cases per
year in this area at one point in time 28]. Recently, VL has spread beyond the Metema and Humera plains to Tahtay Adiabo, Welkaite,
and Mierab Armacheho in the Tigray and Amhara regional states 7], 29].

The highland foci

The claim that VL also exists in Ethiopia’s highlands dates back to the 1970s with
the narrative of two cases reported in Belessa without a travel history 30]. Yet, the confirmation of autochthonous transmission remains doubtful. Belessa is
a highland area (1800 to 2500 masl) with broad plateau expanses of black soil, steep
mountain sides, flat topped promontories and deep cuts of river valleys and galleys.
Its ecology is distinctly different than the lowland foci. In 2005–07 the adjacent
highland (1800 masl) districts Libo Kemkem and Fogera experienced a large-scale outbreak
of VL which affected thousands of people 31], 32]. Initially, VL was misdiagnosed as drug resistant malaria since the disease was not
supposed to occur at this altitude. The apparently continued low transmission after
the outbreak in Libo Kemkem 33] indicates the potential dispersal and establishment of VL transmission in highlands
adjacent to the lowland foci; a growing concern for the upper Kola to Woina Dega ecological
zones.

Vectors

Sandflies are limited with respect to the Leishmania species they are able to transmit 34]. Of the 42 sandfly species implicated in the Old World, only six transmit L. donovani35]. Of these, only Phlebotomus orientalis (P. orientalis), P. celiae36] and P. martini36] are incriminated as vectors for L. donovani in Ethiopia. The transmission is generally assumed to be anthroponotic, yet no evidence
exists to refute the early assumption of zoonoses with occasional spill-over to humans
11], 37]. Recent detection of DNA typed as L. donovani from wild rodents 38], epidemiological 39], 40] and parasite genetics data 41] actually seem to strengthen the zoonotic claim. However, the reservoir host(s) and
vector(s) supporting zoonotic L. donovani transmission in Ethiopia remain to be determined. The lack of information on a zoonotic
cycle could possibly be due to inadequate range of trapping methods 42] and screening surveys in animal hosts. Documented studies so far showed that the
geographic extent of P. orientalis and P. martini is wider than the known endemic foci of VL (Fig. 2). Thus delineating areas with vector presence from zones endemic for VL is a priority
to plan for containment of transmission. The flight range of most sandfly species
is typically short (~300 m), while the breeding sites are assumed to be in the vicinity
of areas where males with unrotated external genitalia and females with blood meal
and egg stages exist 34], 35]. Thus systematic representation of ecological zones with appropriate trapping techniques
complemented by GIS based modelling could give adequate information on their habitat
preference and/or geographic extent. Overlaying the sandfly vector geographic extent
information on the autochthonous VL transmission zone would enable the delineation
of areas that are potentially at high risk of introduction of VL.

Fig. 2. Geographic spread of sandfly vectors in Ethiopia. Current data show that the geographic
distribution of the sandfly vector for L. donovani seems to extend from the lower Kola to the Weina Dega ecological zones. Circles summarize
approximate (data compiled from description of trapping/study site or place/village
names or village/community level) coordinates of trapping sites or exact coordinates
of the trapping point

Phlebotomus (Larroussius) orientalis (Parrot)

P. orientalis, one of the principal vectors of L. donovani in East Africa, was first described in the Dire-Dawa area of the Oromia regional
state of Ethiopia (an area from where no clinical cases of VL have so far been reported).
P. orientalis has also been reported in Chad, Egypt, Kenya, Niger, Rwanda, Saudi Arabia, South
Yemen, Sudan, South Sudan and Uganda 43]. In Ethiopia, P. orientalis has been observed in a 600m to 1930m altitudinal range 44]. It seems that its distribution is positively influenced by the presence of Acacia–Balanites
vegetation and cracks in black cotton clay soil 23], 45], as observed in the Metema-Humera foci. In the Omo 14] and Awash 17] river valleys, and in the highlands of Belessa 30] and Libo Kemkem 46], black cotton soil was also claimed to form the habitat for P. orientalis.

Despite the ecological changes in the Metema and Humera foci, with Acacia–Balanites
vegetation being substituted for crop agricultural schemes, P. orientalis is still the major vector of L. donovani47]. Observation of male sandflies with unrotated genitalia suggests that deeply cracked
black cotton soil is likely to be the most productive breeding habitat. Emergence
from gaps in a stone wall in peri-domestic habitats 48] implicate that house wall material could serve the same function. This observation
is further strengthened by the evidence from blood meal analysis: high numbers of
blood fed, gravid and semi-gravid female P. orientalis were collected near villages despite the known high population density of sandflies
in tickets of Acacia trees or farmland 49]. In the highlands of Belessa, no significant variation in populations size was noted
between rainy and dry seasons 30], yet in the extra-domestic agricultural fields and thickets of A. seyal forests in
Kafta-Humera, peak population was reached in March and April (dry season) 47].

While ecological differences have resulted in seasonality of the P. orientalis population size, geographical and ecological variation did not result in a difference
in vector competence. Despite the distinct requirements for larval food and humidity
during pupation, two colonies of P. orientalis; from a VL focus (1800–2000 m) and a non-endemic area (800 m), showed similar vector
competence 50]. Furthermore, the colonies showed high similarity in morphology, transcriptomes,
proteomes or enzymatic properties of the salivary components and mitochondrial genes.
They interbred and the F1/F2 generations were shown to be even more fit in terms of
reproductive capacity 50], 51].

Only few studies have described the natural feeding behaviour, peak of biting activity
and blood meal preference of P. orientalis in Ethiopia. Ashford noted that except freshly blood-fed females, all stages of P. orientalis were observed to feed on plants with noxious sap. In terms of blood feeding, P. orientalis seem to be exophagic and catholic; in Metema-Humera up to 92 % (250/273) fed from
cattle 49], 52], in Awash valley 54 % (51/94) fed from camels and 2 % (2/94) from squirrel and in
Belessa 2 sandflies fed from porcupines 30]. According to the description of Ashford in his Belessa study, P. orientalis bit humans voraciously and was the most common species. Of 1018 dissected sandflies,
1006 were P. orientalis and most (900) were from human landing catch. Thus the lesser proportion of human
blood meals in the other studies might indicate a zooprophylactic effect due to their
sheer number. A study on peak human biting time of P. orientalis near Arbaya, Belessa district, documented that the peak was reached shortly after
dark: between 28 °C and 19 °C and approximately 2:15 h after sunset 44]. Moreover, they were seen to come to bite man in large numbers in a gulley 30]. Also, it was indicated that mating occurs at dusk and wind considerably affects
both the swarm size and mating behaviour of P. orientalis. The ubiquitousness of P. orientalis, its catholic feeding behaviour and phenotypic plasticity with no loss of vectorial
competence may have resulted in its importance as a vector for L. donovani in Ethiopia.

Phlebotomus martini (Parrot) and Phlebotomus celiae (Minter)

Phlebotomus martini (P. martini) was first described from Dire Dawa, Ethiopia; it has also been reported from Kenya,
Somalia, Sudan, Uganda, and recently from Tanzania 53], 54]. It is incriminated as a vector of L. donovani in Sudan, Ethiopia, Kenya and Uganda 55]. The closely related Phlebotomus celiae (P. celiae) was described in ventilation shafts of termite hills of Kitui, Kenya, occurring in
close association with P. martini56]. Subsequently in 1984, P. celiae was reported in the Aba-Roba VL focus of Ethiopia, in a similar habitat 57]. P. martini has also been caught biting humans in the highlands of Belessa 30]. Additionally, P. martini has been caught in small numbers from the northern lowland foci 47] and the Rift valley 58]. It has so far been reported to exist at altitudes ranging from 637 to 1750 masl
36], 44], 47]. P. martini and P. celiae occur sympatrically in the south and southwest of Ethiopia. They are judged from
abundance and infection rate data to be the primary and secondary agents of anthroponotic
VL transmission respectively at an altitude of 1200 masl in this area 37]. From a study in Aba-Roba, it was documented that both species are nocturnal and
exophagous. Their peak biting activity, as determined from human landing catches,
was between 20:00 and 22:00 h both at termite hills and in dwelling compounds 36]. In terms of population dynamics in this focus, P. martini was abundant with no seasonal pattern while P. celiae populations reached their peak during the wet seasons (February to May and October
to September), and were minimal during the dry season ( November to December and June
to August) 36].

Though it is inferred that termite hills (Macrotermes termites) are the natural breeding and resting habitat for P. martini and P. celiae, no study has so far confirmed this in Ethiopia. Moreover, a survey in south-west
Ethiopia, in the Omo and Akobo river basins and the drainage basin from Chow Bahar
at an altitudinal range of 375 to 2000 masl (largely between 375 and 1000 masl), documented
no association between leishmanin skin test positivity and the presence of both chimney
and pipe organ type termite hills 14]. The study involved ecotypes occupied by different tribes: the Dassanetch; Nyangatom;
Hamar; Suri; Bale; Anuak; Kerre; Shako; Ulam; Tishena, Bodi; Magugi; Bachada and Banna
tribe, with little or no inter-tribal and/or external migration. Thus the existing
data set underlines the possible existence of alternative resting and breeding sites
that need to be explored. In addition, the blood meal source preference, vectorial
competence and behaviour of both species in different ecological settings in Ethiopia
(other than the Aba-Roba focus) is unknown.

Aetiology of visceral leishmaniasis in Ethiopia

Deoxyribonucleic acid based typing of 63 new parasite isolates from VL cases from
different parts of the country indisputably established that L. donovani is the causative agent of VL in Ethiopia 41], 59]. However, using 14 microsatellite markers, Gelanew et al. 41] differentiated between strains circulating in the north and south and subsequently,
Zackay et al. 59] reached similar conclusions using HASPB (k26) PCR and sequencing. The aforementioned
studies distinguished the circulating L. donovani in East Africa into two populations: the northern Ethiopia and the Sudan strain,
and the southern Ethiopia and Kenya/Uganda strain. The difference between the two
populations is congruent with a difference in sandfly vector (P. orientalis vs P. martini/celiae) 60]. The inheritance of genes responsible for virulence/drug-resistance depends on the
extent of genetic recombination in the parasite. The intra-specific genetic exchange
in natural Ethiopian L. donovani populations 61] and the co-existence of clonally and sexually reproducing strains in the southern
foci 41] has recently been documented, indicating the existence of an enabling environment
for genetic exchange. It was proposed that existing differences in clinical response
to treatment may be due to parasite and/or host genetics. Yet, data from clinical
trials in East Africa did not reflect a high genetic exchange potential and/or a difference
in parasite genetics. A multicentre, open-label, randomized, controlled clinical trial
compared three treatment regimens for VL with paromomycin (PM) monotherapy 62]. PM elicited the poorest treatment response at the Sudanese sites with final cure
rates of 14.3 and 46.7 % at Um el Kher and Kassab respectively. The results in north
Ethiopia (Gondar) were comparable to those in Kenya; the efficacy of PM was between
75 and 80 % respectively in both sites. In south Ethiopia (Arba Minch), PM showed
a final cure rate of 96.6 %. However, in another trial comparing single dose AmBisome
(liposomal amphotericin B) with multiple dose AmBisome (7 doses of 3 mg/kg) 63], the final cure rate in Sudan (Kassab) was 76 and 39 % for multiple and single (10
mg/kg) doses respectively, and similarly, in Ethiopia (Gondar) it was 71 % for multiple
and 33 % for single (10mg/kg) doses, while in south Ethiopia (Arba Minch) the final
cure rates were 100 % for multiple and single (10 mg/kg) doses. The presence of a
large number of ethnic groups in south Ethiopia living in similar environmental and
ecological conditions with no/little mixing and a more homogenous population in north
Ethiopia implies that host and/or parasite genetics may not play an important role
in the observed differences in treatment response. Intraregional differences in treatment
response between East African sites can’t be fully explained by L. donovani variability. Thus, other than parasite and host genetics, socio-cultural conditions
should be considered in planning VL control/elimination efforts with existing and
future drugs in East Africa.

Risk factors associated with VL disease or Leishmania infection in VL foci in Ethiopia

Many studies in Ethiopia, using either clinical VL or Leishmania infection as an end point, have implicated exogenic transmission as major source
of infection both in the northern and southern foci. Early studies in the epidemiology
of VL, using leishmanin skin test positivity as a read-out, documented a strong association
of VL with age (increasing age), occupation (herding/night grading of cattle), and
sex (more in male than females) 14], 23], 64], 65]. Entomological and epidemiological studies also support outdoor biting and sylvatic
transmission as major source of infection 66]. Yet a recent study of clinical VL in children in north-west Ethiopia reported 23 %
(28/122) of cases to be of the under five age group. Although it is impossible to
rule out the possibility of outdoor biting, this might indicate the increasing risk
of domestication of VL transmission in this focus 67]. In addition to the soil (black cotton soil) 14], 47], vegetation type (Acacia-Balanites vegetation) 39], 68], presence of termite hills 36], 37] and mass movement of people 22], 23], 32], 69], different behavioural, household and environmental factors have been implicated
as risk factors for either asymptomatic Leishmania infection or clinical VL. Studies done in the Libo Kemkem and Fogera areas documented
increasing age (per year), being male, sleeping outside at any time of the year, past
history of VL in the family, living in a straw roofed house and whether the family
owned sheep as risks for Leishmania infection 70]. The factors associated with clinical VL were dog ownership, sleeping under Acacia
trees during the day, and habitually sleeping outside at night 39]. A similar study among residents of Kafta Humera incriminated family size (increased),
living in a house with cracked walls, ownership of a goat and number of days spent
in the farming fields as factors increasing the odds of having clinical VL 71]. In a similar area, another study comparing residents and migrant labourers concluded
that sleeping under Acacia trees at night and lower educational status were associated
with an increased risk of clinical VL in both populations. Living in a house with
thatched walls and sleeping on the ground were associated with high risk of clinical
VL for residents; among migrants those sleeping near dogs were most likely to have
clinical VL 68]. A case–control study to understand the link between clinical VL and domestic animals
screened dogs, cats, cattle, donkeys, sheep and goats. The outcome showed that dogs
owned by people with a history of VL have a high risk of infection (OR:8.9, P:0.016)
compared to cattle though the overall infection prevalence reported was a similar
42 % (18/43) and 40 % (36/90) in cattle and dogs respectively 40]. From studies so far, implicated domestic animals in VL transmission yet their role
as risk and/or protective factors in specific eco-epidemiologic setting need to be
ascertained.

Studies with respect to knowledge, attitude and practice and community acceptability
of existing control measures are rare. A study in the rural communities of Libo Kemkem
indicated that although the knowledge regarding signs, symptoms, and causes of VL
was very low at the beginning of a longitudinal study, it improved substantially over
a 3 year period, and the community had a positive attitude towards prevention 72]. A similar study in Addis Zemen town showed that in general good practice was low
despite the good awareness and favourable attitude towards measures to prevent and
control VL 73]. Overall, the studies implied a need to better understand the specific reasons for
failure of effective community interventions and social mobilization.

Concomitant morbidities, especially HIV/VL co-infection have a strong impact on VL
control. In 1995 only 7 HIV/VL co- infected cases were reported 74]. Subsequent hospital based studies in the northern foci, mainly serving migrant labourers,
documented an alarming increase of HIV/VL co-infection: 29 % (167/375) 75], 41 % (87/212) 76], 38 % (92/241) 27] and 46.4 % (13/30) 77] in 2006, 2007 and 2010 respectively. More recently this trend is decreasing Mengesha
et al. reported a lower prevalence of 10.4 % in 2014 78]. Malnutrition is another important co-morbidity; a high prevalence of malnutrition
(up to 95 %) was reported in VL patients 67], 78]. Intestinal parasitosis was also noted to be common in VL cases 67], 78]. Thus, in planning control efforts in the Ethiopian context, there is a need to consider
HIV/VL co-infection, as well as parasitosis and/or malnutrition in VL patients as
priorities.

Risk mapping

Despite the long-standing presence and focalized distribution of VL in Ethiopia, little
work has been done to determine its association with environmental factors. Understanding
spatio-temporal diffusion patterns and the mapping of existing hotspots will have
paramount importance for more focused interventions and control of the spread of VL.
The use of techniques such as GIS and remote sensing (RS) will enable the analysis
of complex information as well as geographically targeted control programmes. Good
models, based on high quality predictor data of epidemiological and biological relevance,
have reasonable accuracy in explaining the actual situation and are independently
verifiable. A VL risk model for Ethiopia based on soil type, altitude, mean annual
rainfall, surface temperature and slope vis-à-vis GPS data on clinical VL presence
and absence predicted that 33 % of the total land mass is at high and very high risk
of VL endemicity 8]. According to this model, over 3.2 million people live in areas at risk (Fig. 3), yet considering the large scale immigration of temporary labourers and settlers
to these areas this might be an underestimation. Among the studied environmental factors,
mean annual surface temperature (26–31 °C) and soil type (presence of vertisol) were
the best predictors of VL transmission. The validation of the model through verification
of the presence/absence of VL cases (random selection) showed an accuracy of 86 %.
This modelling exercise provided important background information for a further study,
which considered temporal information and additional environmental and climatic variables
and focused on the Kafta Humera foci. Taking mean monthly rainfall and temperature,
seasonal normalized difference vegetation index, soil type, altitude and slope, and
comparing these to 15 years (1998 to 2012) of monthly VL data from the Kahsay Abera
hospital, concluded that VL incidence and presence of transmission were directly related
to temperature and presence of vertisol. The relation with altitude, rainfall, slope
and the mean seasonal normalized difference vegetation index was inverse 79]. In terms of risk, the villages Bereket, Rawoyan, Baeker, Adebay, May Kadra and Humera
town all were high risk areas for VL.

Fig. 3. Visceral leishmaniasis risk areas in Ethiopia. The risk areas extend from the Kola
to the Weina Dega agro-ecological zones; yet the major part of the high risk and very
high risk areas are within the Kola (Lower and Upper) agro-ecological zone

Regarding sandfly vectors, Gebre-Michael et al. 80] used environmental variables and historical sandfly data to make GIS based predictive
maps of P. orientalis and P. martini. Their findings showed that while average altitude (12–1900 m), average annual mean
temperature (15–30 °C), annual rainfall (274–1212 mm), average annual potential evapotranspiration
(1264–1938 mm) and readily available soil moisture (62–113 mm) were found to be the
best fitting ecological variables for P. martini presence; for P. orientalis, average altitude (200–2200 m), annual rainfall (180–1050 mm), annual mean temperature
(16–36 °C) and readily available soil moisture (67–108 mm) were the major ecological
determinants. On the other hand, mid-day land surface temperature (LST), dry season
composite of the satellite data, average altitude, mean annual temperature and readily
available soil moisture were the best ecological determinants for P. martini. For P. orientalis, LST annual composite was the only important ecological determinant. According to
this model the ecological extent of both vectors correspond with the climatic conditions
currently prevailing and the lack of association with soil type might be due to ecological
changes, for the sandfly data used were very old. Thus updating sandfly collection,
soil, other environmental and remote sensing data to remodel the P. martini and P. orientalis distribution could help to better understand the (re)emergence of VL in Ethiopia.