1. Introduction
Sub-Saharan Africa remains home to a wide variety of pathogens transmissible to humans [1]; those transmitted from infected small mammal urine and feces are leptospirosis [2], intestinal helminths [3], arenaviruses [4] and hantavirus hemorrhagic fevers [5]. The arenaviruses and hantaviruses responsible for hemorrhagic syndromes are RNA viruses closely associated with infected small rodents that excrete the virus continuously in their excreta (urine, feces). This is the case with Lassa fever virus, for which Mastomys natalensis is the main reservoir host in Mali [6]. The geographic distribution of the viruses and their remarkabl biological adaptation in rodents suggest a co-evolution between the viruses and their murid hosts [7]. The feces of small rodents infected with Schistosoma mansoni, Hymenolepis diminuta and Hymenolepis nana that contaminate water are likely to cause intestinal schistosomiasis due to S. mansoni, helminthiasis due to H. diminuta or H. nana, or cause gastrointestinal infection induced by the presence of numerous helminths, in contact with humans [3].
Some small rodent pathogens are transmitted to humans via hematophagous ectoparasitic vectors, including fleas that transmit the plague bacillus Yersina pestis [8], whose reservoirs are Rattus norvegicus, Rattus rattus and the house mouse Mus musculus domesticus, but also to a lesser extent commensal species such as Arvicanthis niloticus, Mastomys erythroleucus and Crycetomys gambianus. Cutaneous leishmaniasis (CL) due to Leishmania major, which is more widespread in West Africa, is transmitted to humans by sandflies [9] that live in the burrows of Gerbilliscus gambianus, M. erythroleucus and A. niloticus, small rodents that serve as reservoirs. Recent epidemics of cutaneous leishmaniasis with L. major described in urban areas in Burkina Faso [10], Ghana [11] and in rural areas in Mali [12] illustrate a possible risk of emergence of these zoonotic diseases transmissible to humans. Schistosoma mansoni schistosomiasis remains a public health problem in Mali; despite the implementation of control strategies, the animal reservoir has been invoked as a possible factor linked to the persistence of the disease, and small mammals could play a role [13]. Tick-borne borreliosis, widely distributed in West and North Africa, is caused by Borrelia spp. which are transmitted to humans by ticks of the genus Ornithodoros living in the burrows of small rodents that are the primary animal reservoir for Borrelia infections [10,11,12,13,14]. The risk of vector-borne or direct transmission of bacterial diseases from small rodents to humans is high in Mali, with notably a 35% seroprevalence of borreliosis due to Borrelia crocidurae identified in small rodents in Bandiagara [15]. Most of these small mammal species sampled in our study represent a source of contamination of infectious diseases such as salmonellosis, leptospirosis, tick-borne relapsing fever borreliosis, murine typhus, Lassa fever, Rift Valley fever, Crimean–Congo hemorrhagic fever, viral meningitis, toxoplasmosis and coxiellosis, through ingestion of contaminated food, water or through the bites of infected arthropod vectors (ticks, fleas, mosquitoes) [1,6,7,8,14]. The emergence of bacteria transmitted by ticks is a threat to livestock keepers in Mali, where 15.8% to 58.3% of ticks carry bacteria such as Rickettsia spp., Coxiella burnetii, Borrelia spp. and Anaplasmataceae such as Wholbachia spp. and Ehrlichia ruminantium [16]. The Ebola epidemic in West Africa has made it urgent to investigate potential reservoirs of emerging pathogens circulating around and in humans dwelling in Mali. We used the data collected from the small mammal population from two sites Faladjè and Bougouni with different eco-climatic characteristics to test the hypothesis that small mammal distribution in different eco-climatic settings could explain the diversity and frequency of pathogens carried by the small mammals [16].
The security crisis in Mali has led to the displacement of populations, the abandonment of health structures and the disorganization of the communicable disease surveillance and prevention system. This situation is a factor favoring the unpredictable emergence and spread of transmissible pathogens. Few surveys of the population, distribution and abundance of small rodents and insectivores are available in Mali. Better implementation of small mammal control strategies at the national level to prevent the transmission of pathogens from small rodents to humans requires knowledge of their distribution. The purpose of this study is to identify commensal small mammal species circulating in the Faladjè and Bougouni areas that may represent a risk for the emergence of potentially epidemic diseases in Mali.
2. Materials and Methods
2.1. Study Sites
Small Mammal Sampling Was Conducted in Two Areas: Bougouni and Faladjè
The rural village of Faladjè (Kati District/Koulikoro Region) and its rural surroundings (13°00′ N/8°20′ W and 13°08′ N/8°20′ W) is located 80 km northwest of Bamako. The village has a Catholic mission health center that serves 23,000 inhabitants living in the village and surrounding areas.
The semi-urban locality of Bougouni is located in the Sikasso Region (11°25′ N/7°29′ W and 11°25′ N/7°28′ W), 160 km from Bamako.
Faladjè and Bougouni are two sites with different bioclimatic patterns located northwest and southeast of Bamako, respectively (Figure 1). The village of Faladjè and the town of Bougouni are located in the Sudano-Saharan and Sudano-Sahelian zones, respectively, 77 km and 160 km from Bamako (Figure 1), and are research sites of the Malaria Research Training Center (MRTC) program. Housing is essentially traditional and rural in Faladjè, composed of mud-made houses with a few modern houses. In contrast, in the town of Bougouni, there are two contrasting types of housing: modern semi-urban and traditional rural. The populations of these two sites, who are mainly of Bambara ethnicity, practice rain-fed agriculture, family livestock raising, and market gardening in the dry season.
In Faladjè, the average temperatures in the dry season (December–April) and in the rainy season (May–August) are 41 °C and 32 °C, respectively, and the average rainfall in the dry season (December–April) is 8 mm compared to 134 mm in the rainy season (May–August). In Bougouni, the average temperature in the coldest month (December) is 26.0 °C, and in the hottest month (April) it is 32.5°C. During the least rainy months (December, January, February), the rainfall recorded was 1 mm, and in the wettest month (August) it reached 280 mm.
This study was implemented to investigate reservoirs of emerging pathogens in Mali; Faladjè and Bougouni were selected to initiate the survey because the two areas have been reported to be potential endemic areas of re-emerging viruses’ diseases. The Lassa virus is endemic in the southern area of Mali, with higher LASV IgG seroprevalence ranging from 14.5% to 44% per village in the Bougouni District, Sikasso region [17]. Faladjè is located in the Kita District, Koulikoro region. Both Koulikoro and Sikasso regions have recently reported cases of yellow fever.
2.2. Sampling and Dissection of Small Mammals Captured
In Faladjè, sampling sessions were conducted in a lowland rice field and cassava and/or market gardens outside, then inside village homes and in the Catholic parish garden. In Bougouni, the trapping series were carried out in maize and millet fields in Hérémakono North, in a lowland cultivation area in Dougounina and a cultivation area near a tributary of the Niger River in Niébala and then in the respective dwellings of Tourakabougou and Dougounina. In all of the capture sites, the traps were set in the evening and at night. They were then collected the next morning and a number was assigned chronologically to each small mammal captured, and the location of the various specimens was georeferenced. Captures of small rodents and insectivores were conducted from 11 to 14 and 15 to 18 December 2016 in the village of Faladjè and in Bougouni, respectively. Trapping was carried out using “Besançon tous services” (BTS) wire mesh traps baited with peanut paste and/or onion. Two trapping devices were used depending on the type of environment. In natural environments and crops, the method adopted was that of line trapping with an inter-trap distance of about 10 m. In homes, 1 to 4 traps were placed in attics, stores, and sleeping rooms, depending on the size of the room and the presence of small mammals. The type of trap and bait such as onions and peanuts were used because BTS has been successful in trapping small rodents with such bait in previous studies [18,19,20].
The small mammals were euthanized with chloroform, and each small mammal was attributed a unique ID number, identified morphologically, weighed and measured before necropsy, and the reproduction parameters were recorded. These parameters can be used to determine the risk of an outbreak. Rodent and insectivore organs such as spleen, liver, pancreas and blood from heart were taken for pathogen detection. The remaining small mammal body was kept in formol diluted at 10% for future use.
2.3. Molecular Detection of Microorganisms
DNA was extracted individually from small cuts of spleen of rodents and insectivores. Samples were incubated individually at 56 °C overnight in 1.5 mL tubes containing 180 µL G2 lysis buffer and 20 µL proteinase K (Qiangen, Hilden, Germany). After centrifugation at 1000 rpm for 30 s, 200 µL of supernatant was used to extract the DNA using the EZ1 DNA Tissue Kit (Qiagen) according to the manufacturer’s recommendations. DNA from each sample was eluted with 100 µL of Tris-EDTA buffer (Qiagen) and was either immediately tested or stored at −20 °C for further use. Quantitative PCRs were performed on CFX96 Real-Time System (Biod-Rad Marnes-la Coquette, France) and LigthCycler® 480 Probes Master mix (Indianaplis, IN, USA) to detect Leishmania spp., Borrelia spp., Leptospira spp., Bartonnella spp., Coxiella burnetii; Bartonnella spp. and Anaplasmataceae.
2.4. Statistical Analysis
Data were entered into SPSS (version 16.0, 2007) and analyzed to assess the relative abundance, diversity and difference in species composition of the stand between the two locations. The variation in relative abundance of the small mammal population was evaluated, using the binomial test, to compare catch rates in Faladjè and Bougouni. The variation in relative abundance was considered significant when p ˂ 0.05. The indices used to examine the community of small rodents and insectivores were the Shannon index (H′), which expresses the specific diversity of a stand, and the equi-partition index (E).
H’= -∑ Pi.log2 (pi)
i = 1
-
pi = the proportional abundance or percent abundance of a species present (pi = ni/N);
-
ni = the number of individuals counted for a species present;
-
N = the total number of individuals counted from all species combined;
-
S = the total or cardinal number of the list of species present.
If the stand is homogeneous, consisting of one and the same species, then the index H′ = 0. The more different species are present in a stand, the higher its value becomes and it is common to see H′ values between 1 and 5 to account for species diversity. The value Hmax = log2(S) corresponds to a heterogeneous stand for which all individuals of all species are equally distributed. To better discuss the Shannon index, it must be accompanied by the equi-partition index whose formula corresponds to the ratio between H′ and H max. E = H′/H max and varies between 0 and 1. If E tends towards 1, then the species present in the stand have identical abundances, while if E tends towards 0, then there is the presence of an imbalance where a single species dominates the entire stand.
3. Results
3.1. Size of Small Mammals Captured
A total of 123 small rodents and insectivores were captured inside homes and outdoors in Faladjè and Bougouni over 674 trap-nights, for a total capture efficiency of 18.25% including 75 animals captured in Faladjè over 318 trap-nights (23.58%) and 48 individuals captured in Bougouni over 356 trap-nights (3.48%) (Table 1). Six species of small rodents and insectivores were identified in each of the two study areas (Table 2). In Faladjè, there were almost as many males as females, but in Bougouni the predominance of males was greater (Table 3).
3.2. Specific Diversity and Relative Abundance of the Sampled Species
Shannon index (H) calculation (Table 2) showed low species diversity of small rodents and insectivores in both study areas. The equi-partition index (E) indicated that there is an imbalance in the population of small rodents and insectivores in Faladjè where M. erythroleucus was the dominant species. This imbalance was also noted in Bougouni where R. rattus was the dominant species in the entire stand. The relative abundance of small rodents and insectivores was 60.97% (CI 95%: 51.8–69.6) in Faladjè and 39.02% (CI 95%: 30.3–48.2) in Bougouni. The variation in relative abundance between the small mammal species in Faladjè and Bougouni was significant (binomial test, p = 0.018).
3.2.1. Small Rodents Caught
All captured animals were morphologically identified, as previously described [21]. All the animals captured belong to the Muridae family. The subdivision by subfamily and species is shown in Table 2. Four species (P. daltoni, G. gambianus, T. gracilis, M. erythroleucus) were captured outdoors and two other species (M. natalensis, R. rattus) were trapped inside houses. Mastomys natalensis and R. rattus are strictly commensal species due to their frequentation inside houses, but M. erythroleucus was the only ubiquitous species captured (Table 2) in both areas.
3.2.2. Insectivores Caught
As well as small rodents, insectivore species were captured both indoors and outdoors. Atelerix cf albiventris of the family Erinaceidae was trapped outdoors, while Crocidura cf olivieri and Crocidura spp. of the family Soricidae were trapped inside houses (Table 2).
3.2.3. Molecular Detection of Pathogens
Molecular detection of pathogens such as Rickettsia spp., Borrelia spp., Bartonella spp., Anaplasmataceae, Coxiella burnetii, Leishmania spp. and Leptospira spp. was performed on cuts of spleen and in ectoparasites collected from small mammals in Faladjè and Bougouni. The qPCR method was used, and findings have been detailed in a previous publication [16]. The distribution and prevalence of pathogens detected in small mammals was quite different between the two sites. The overall prevalence of Bartonella DNA in small mammals was 23/130 (17.7%): 7/44 M. erythroleucus (16%), 5/14 M. natalensis (35.7%), 1/8 P. daltoni (12.5%) and 1/20 C. olivieri (20%) were infected by Bartonnella spp. in Faladjè, but M. erythroleucus was commonly infected by Bartonnella spp. in Bougouni (5/14) (35.7%) compared to Faladjè (4/44) (16%); similarly, M. natalensis was more frequently infected by Bartonnella spp. (35.7%) in Faladjè than M. erythroleucus (1/12) (8%) in Bougouni. R. rattus captured in Bougouni were not infected any pathogens compared to R. norvegicus, which were more frequently infected with Bartonnella spp. (3/6) (30%) in Bamako. Coxiella burnetii was detected only in Faladjè, where M. erythroleucus (2/44) (4.5%) and P. daltoni (1/8) (12.5%) were infected. These two species were trapped around human dwellings in Faladjè. All small mammal spleen cuts tested for Leishmania spp., Leptospira spp. and Borrelia spp. DNA were negative.
4. Discussion
The sampling sessions performed during our study revealed the presence of several small mammal species circulating in the Faladjè and/or Bougouni areas, including M. erythroleucus, M. natalensis, R. rattus, P. daltoni, G. gambianus, T. gracilis, Crocidura cf olivieri, Atelerix cf albiventris and Crocidua spp. Among them, three species were found in both areas (M. erythroleucus, M. natalensis, P. daltoni) and five other species (R. rattus, G. gambianus, T. gracilis, C. cf olivieri, A. cf abiventris) associated with the genus Crocidura spp. were captured either in Faladjè or in Bougouni. The variation in relative abundance between the Faladjè and Bougouni stands of small mammals was significant. Mastomys erythroleucus was the most dominant (57.33%, 43/75) in the Faladjè stand and R. rattus dominated (37.5%, 18/48) in that of Bougouni. These differences in variation in relative abundance between the two sites could be explained by the sites’ eco-climatic characteristics; Faladjè is a rural village and Bougouni is a semi-urban setting. Other factors such as anthropogenic pressure, small mammal control measures and the number of cats may have an impact on the composition and the number of circulating rodents and insectivores in endemic areas; we did not investigate these factors during the survey. A classical pressure in rural areas is children’s practice of hunting small mammals.
In Benin, 20.8% of gray rats were found to be infected with Bartonella spp., and none of the black rats analyzed were positive [22]. Bartonnella spp. was reported to infect rodents, cats and dogs in South Africa, with a high prevalence of infection in HIV-positive patients [23]. The seroprevalence of bartonnellosis in the general population of the Democratic Republic of Congo was 4.5% in 2011 [21]. These data show that the transmission of Bartonella spp. to humans occurs and immunocompromised patients may be at a higher risk of contamination.
In Tanzania, a total of 12 (3.1%) of 382 (95% CI: 1.6–5.4) small mammal spleens were positive for C. burnetii DNA. Coxiella burnetii DNA was detected in R. rattus, M. musculus, A. wilson, P. flavovottis and A. albiventris. Among those, eleven of twelve (91.7%, 95% CI: 61.5–99.8) C. burnetii DNA-positive small mammals were trapped within Moshi Urban District [24]. In Mali, PCR revealed a low prevalence of Coxiella burnetii carriage in febrile patients who tested negative using malaria Paracheck® rapid diagnostic tests (RDTs) [25]. These findings highlight a possible risk of transmission of these emerging pathogens to humans in rural areas in Mali and urban areas in Tanzania.
Differences in the pathogen species and distribution between the Bougouni and Faladjè could be explained by factors such as eco-climatic characteristics. The eco-climatic parameters may also play a role on emerging pathogen species carriage of small mammals; in Mali, R. rattus in rural areas was not infected by Bartonella spp. and Coxiella burnetii, while R. norvegicus was infected by Bartonella spp. in urban areas [16].
Of these infectious diseases cited above, it is particularly important to note that all of the small mammal species captured have been previously found to be naturally infected with Borrelia crocidurae, the pathogen of tick-borne relapsing fever borreliosis that us endemic in West African countries (Senegal, Mali, Mauritania and the Gambia). Borreliosis is also common in North Africa (Morocco, Algeria and Tunisia), with a high prevalence of Borrelia infections in small rodents and insectivores and Ornithodoros tick vectors [26]. Mastopmys natalensis, frequently captured in both sites, seems to be the principal reservoir of the Lassa virus in West Africa [27]. Other small rodents like P. daltoni and M. erythrolocus, identified as carriers of LASV IgG in Guinea, are involved in the transmission of the Lassa virus (LASV) to humans [27]. Rattus rattus and Crocidura spp. were found to be positive for LASV IgG in Nigeria [4]. Human illness due to LASV is currently reported in Guinea, Sierra Leone, Liberia and the Central African Republic. However, in Mali, a death due to LASV was reported in 2010 [28]. There are many asymptomatic forms and only 1% of cases are reported to be fatal. In Senegal, positive serologies have been found in M. erythroleucus, but no human cases are known [29]. The emergence of hantavirus hemorrhagic fevers in West Africa has been caused by the threat of Crocidura theresae (C. obscurior) which was found to be infected by Tanganya virus (TGNV), the only shrew-associated hantavirus reported to date from sub-Saharan Africa [30]. Numerous positive serologies have also been reported throughout Senegal in domestic animals [31]. In Mauritania, cases of human Crimean–Congo hemorrhagic fever virus (CCHF) infection have been observed [32]. CCHV has already been isolated from bats in the Central African Republic [33]. Small rodents may participate in the epizooty of CCHF [34].
Evidence of the passage of antiviral antibodies to this virus has been identified in rodents in Nigeria, Senegal, Ethiopia, Namibia, Madagascar and Egypt, and R. rattus could be involved in the amplification of the virus. In addition, M. natalensis, R. rattus and C. olivieri, abundant in both sites, were reported elsewhere with a potential role in the dissemination of Leptospira [35]. In Senegal, many species such as R. rattus, Mastomys huberti, A. niloticus and M. erthroleucus, identified as carriers of anti-Rift Valley fever (RVF) antibody, play a potential role as reservoirs of RVF virus. The role of rodents as a potential host within the natural cycle of RVF virus in the enzootic zone of Senegal is discussed; however, the highest antibody prevalence was recorded at Richard Toll (9.6%), within the enzootic area of the Senegal River delta [36].
The trapping yield was higher in Faladjè (23.58%) than in Bougouni (13.48%), while the capture effort was greater and comparable to that obtained in three villages in Mali [36]. M. erythroleucus and M. natalensis were the most frequently captured species at both study sites, but the predominance of M. erythrolocus observed in this sampling has also been reported in other localities in Senegal where it is endemic [9]. A study on Lassa fever in Mali [28] showed that the predominance of the genus Mastomys spp. was 79.6%. Arvicanthis ansorgei was not collected at either site, although this species had been reported in Mali [37]. The absence of Arvicanthis niloticus and/or A. ansorgei in our sample could be explained by the fact that the sampling was performed at night while this species has diurnal activity. Rattus rattus was more abundant in Bougouni; Rattus norvegicus was also found to be the predominant species in Algeria [38]. Bougouni is a inland city, which explains why Rattus norvegicus, often co-endemic with R. rattus in African port cities, is absent there. The study of small mammalian species’ reservoirs, geographic distribution and habitat associations help define potential disease endemic areas and more precisely identify the spatial variation in relative risk to humans.
5. Conclusions
Sampling of small rodents and insectivores revealed a variation in the relative abundance of small mammals between Faladjè and Bougouni. The specimens of small rodents and insectivores captured suggest that relative abundance was greater in the Faladjè area than in Bougouni with low species diversity. The commensal species R. rattus was more common in Bougouni but appeared to be rare in Faladjè, while M. natalensis was relatively more frequent in Faladjè than in Bougiouni. M. erythroleucus and R. rattus, the two dominant species in Faladjè and Bougouni, are known reservoirs of bacteria and viruses potentially transmissible to humans. Thus, taking appropriate measures to ensure epidemiological surveillance of these small mammal populations is an important health requirement. Future investigation should be conducted in Mali to determine the role of small mammals in the dissemination of salmonellosis, leptospirosis, tick-borne relapsing fever borreliosis, murine typhus, Lassa fever, Rift Valley fever, Crimean–Congo hemorrhagic fever, viral meningitis and toxoplasmosis and identify any correlations between the local abundance and species composition of small mammals with prevalence of these infections.
Conceptualization, O.K.D., M.A.T., A.D. and I.S.; Methodology, A.K.K., D.S.N., G.D., S.A.A., A.Z.D. and M.C.; Sample collection, A.K.K., G.D. and D.S.N.; Data curation, A.K.K. and G.D.; Writing—original draft preparation, A.K.K. and G.D.; Writing—review and editing, A.K.K., G.D. and M.A.T.; Visualization and supervision, M.A.T. All authors have read and agreed to the published version of the manuscript.
The study protocol was submitted to the ethics committee of USTTB/FMPOS and approved under the number #2016/113/CE/FMOS. The small mammals were collected under the framework of a survey of the prevalence, surveillance and investigation of emerging and re-emerging viruses and causes of fevers in Mali.
Informed consent was obtained from all household heads involved in the study. Before initiation of small mammal collection, communty permission to capture small mammals arround and in human dwellings was first obtained from community leaders.
Data is contained within the article.
We thank the community leaders, village chiefs, the heads household and the populations of Faladjè and Bougouni for their participation to the study.
The authors declare no conflicts of interest.
Footnotes
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Enlarge this image.Figure 1. Location of sampling sites of small rodents and insectivores captured in 2016 in Mali.
Number of captures and trap-nights per small mammal sampling site in Faladjè and Bougouni in Mali, December 2016.
| Sites/Place of Capture | Number of | Number of Animals Captured | Trapping Yield (%) |
|---|---|---|---|
| Faladjè | |||
| Dwellings | 166 | 25 | |
| Lowland rice cultivation | 15 | 1 | |
| Hedge 1 of a cultivated garden | 50 | 17 | |
| Hedge 2 of a cultivated garden | 63 | 29 | |
| Catholic parish garden | 24 | 3 | |
| Sub-total | 318 | 75 | 23.58% |
| Bougouni | |||
| Dwellings in Tourakabougou | 86 | 18 | |
| Dwellings in Dougounina | 62 | 15 | |
| Cultivated area in Dougounina | 30 | 1 | |
| Cultivated area in Niébala | 120 | 11 | |
| Natural habitat and cultivated area in Hérémakono North | 58 | 3 | |
| Sub-total | 356 | 48 | 13.48% |
| Total | 674 | 123 | 18.25% |
Small rodent and insectivore species caught in Faladjè and Bougouni in Mali, December 2016.
| Species Captured | Family | Subfamily | Number of Specimens Captured | Number of Specimens Captured in Bougouni | Total |
|---|---|---|---|---|---|
| Mastomys erythroleucus | Muridae | Murinae | 43 | 14 | 57 |
| Mastomys natalensis | Muridae | Murinae | 15 | 12 | 27 |
| Rattus rattus | Muridae | Murinae | 0 | 18 | 18 |
| Praomys daltoni | Muridae | Murinae | 8 | 2 | 10 |
| Gerbilliscus gambianus | Muridae | Gerbillinae | 3 | 0 | 3 |
| Taterillus gracilis | Muridae | Gerbillinae | 1 | 0 | 1 |
| Crocidura cf olivieri | Soricidae | Crocidurinae | 5 | 0 | 5 |
| Crocidura spp. | Soricidae | Crocidurinae | 0 | 1 | 1 |
| Atelerix cf albiventris | Erinaceidae | Erinaceinae | 0 | 1 | 1 |
| Total | 3 | 4 | 75/123 (60.97%) | 48/123 (39.02%) | 123 |
Sexes of small rodent and insectivore specimens autopsied in Faladjè and Bougouni in Mali, December 2016.
| Sex | Faladjè (n = 75) | Bougouni (n = 48) |
|---|---|---|
| Male (M) | 38 (50.7%) | 28 (58.3%) |
| Female (F) | 37 (49.3%) | 20 (41.7%) |
| Total | 75 (100) | 48 (100) |
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Details
; Diatta, Georges 2
; Doumbo Safiatou Niare 1 ; Solimane Ag Atteynine 3 ; Coulibaly, Maïmouna 1 ; Adama Zan Diarra 4 ; Sagara, Issaka 1
; Djimdé, Abdoulaye 1
; Doumbo, Ogobara K 1 ; Mahamadou Ali Thera 1
1 Malaria Research and Training Center (MRTC), IRL 3189 Environnement, Santé, Sociétés (USTTB/UCAD/UGB/CNRST/CNRS), Faculté de Médecine et d’Odonto-Stomatologie (FMOS), Université des Sciences, des Techniques et des Technologies de Bamako, Bamako 1805, Mali;
2 Institut de Recherche pour le Développement (IRD), UMR 279 IRD MINES, Campus International IRD-UCAD, Hann BP. 1386, Dakar 18524, Senegal;
3 Institut de Recherche pour le Développement (IRD), Bamako 2528, Mali;
4 Malaria Research and Training Center (MRTC), IRL 3189 Environnement, Santé, Sociétés (USTTB/UCAD/UGB/CNRST/CNRS), Faculté de Médecine et d’Odonto-Stomatologie (FMOS), Université des Sciences, des Techniques et des Technologies de Bamako, Bamako 1805, Mali;