Animal trypanosomosis eliminated in a major livestock production region in Senegal following the eradication of a tsetse population.

African animal trypanosomosis (AAT) was one of the main disease-related constraints to the development of intensive livestock production systems in the Niayes region of Senegal, a 30 km wide strip of land along the coast between Dakar and Saint-Louis. To overcome this constraint, the Government of Senegal initiated an area-wide integrated pest management programme combining chemical control tactics with the sterile insect technique to eradicate a population of the tsetse fly Glossina palpalis gambiensis Vanderplank, 1949 (Diptera, Glossinidae) in this area. The project was implemented following a phased conditional approach, and the target area was divided into three blocks treated sequentially. This study aims to assess the temporal dynamics of the prevalence of Trypanosoma spp. during the implementation of this programme. Between 2009 and 2022, 4,359 blood samples were collected from cattle and screened for trypanosomes using both the buffy coat and ELISA techniques, and PCR tests since 2020. The seroprevalence decreased from 18.9% (95%CI: 11.2-26.5) in 2009 to 0% in 2017-2022 in block 1, and from 92.9% (95%CI: 88.2-97) in 2010 to 0% in 2021 in block 2. The parasitological and serological data confirm the entomological monitoring results, i.e., that there is a high probability that the population of G. p. gambiensis has been eradicated from the Niayes and that the transmission of AAT has been interrupted in the treated area. These results indicate the effectiveness of the adopted approach and show that AAT can be sustainably removed through the creation of a zone free of G. p. gambiensis.

Title: Trypanosomose animale éliminée dans une importante région de production d'élevage au Sénégal suite à l'éradication d'une population de glossines. Abstract: La trypanosomose animale africaine (TAA) était l'une des principales contraintes pathologiques au développement de systèmes de production animale intensifs dans les Niayes du Sénégal, une bande de terre large de 30 km longeant la côte entre Dakar et Saint-Louis. Pour surmonter cette contrainte, le Gouvernement du Sénégal a lancé un programme de lutte intégrée à l'échelle de la zone combinant lutte chimique et technique de l'insecte stérile pour éradiquer une population de Glossina palpalis gambiensis Vanderplank, 1949 (Diptera, Glossinidae). Le projet a été mis en œuvre selon une approche conditionnelle progressive, et la zone cible a été divisée en trois blocs, traités de manière séquentielle. L'objectif de cette étude était d'évaluer la dynamique temporelle de la prévalence de Trypanosoma spp. au cours de la mise en œuvre du programme. Entre 2009 et 2022, 4 359 échantillons de sang ont été prélevés sur des bovins et ont fait l'objet d'un dépistage des trypanosomes à l'aide des techniques du buffy-coat et ELISA, ainsi que de test PCR depuis 2020. Dans le bloc 1, la séroprévalence est passée de 18,9 % (IC 95 % : 11,2­26,5) en 2009 à 0 % entre 2017­2022 et de 92,9 % (IC 95 % : 88,2-97) en 2010 à 0 % en 2021 pour le block 2. Les données parasitologiques et sérologiques confirment les résultats du suivi entomologique selon lesquels il est très probable que la population de Glossina palpalis gambiensis soit éradiquée des Niayes, et que la transmission de la TAA a été interrompue dans la zone traitée. Elles indiquent l'efficacité de l'approche adoptée, et montrent que la TAA peut être durablement éliminée grâce à la création d'une zone exempte de G. p. gambiensis.

Environmental and economic determinants of temporal dynamics of the ruminant movement network of Senegal.

Our understanding of the drivers of the temporal dynamics of livestock mobility networks is currently limited, despite their significant implications for the surveillance and control of infectious diseases. We analyzed the effect of time-varying environmental and economic variables-biomass production, rainfall, livestock market prices, and religious calendar on long-distance movements of cattle and small ruminant herds in Senegal in the years 2014 and 2019. We used principal component analysis to explore the variation of the hypothesized explanatory variables in space and time and a generalized additive modelling approach to assess the effect of those variables on the likelihood of herd movement between pairs of administrative units. Contrary to environmental variables, the patterns of variation of market prices show significant differences across locations. The explanatory variables at origin had the highest contribution to the model deviance reduction. Biomass production and rainfall were found to affect the likelihood of herd movement for both species on at least 1 year. Market price at origin had a strong and consistent effect on the departure of small ruminant herds. Our study shows the potential benefits of regular monitoring of market prices for future efforts at forecasting livestock movements and associated sanitary risks.

Insight on Bluetongue virus transmission in small ruminants in Senegal.

Bluetongue (BT) is an infectious, arthropod-borne viral disease of domestic and wild ruminants. The disease causes animal mortality, production decrease and commercial limits for herds. Despite the active circulation of the disease in the world, few studies have been carried out in Senegal. The objective of this study was to assess the current prevalence of BT in small ruminants and the serotypes circulating in Senegal. A cross-sectional study was conducted in the fourteen regions of Senegal. After the sampling campaign, sera collected in sheep and goats herds were screened for the presence of Bluetongue virus (BTV) specific antibodies using c-Elisa. The whole blood of seropositive animals was further analyzed by RT-qPCR and positive samples were typed to identify BTV serotypes. Analysis of several risk factors such as age, sex and species of animals was performed using logistic regression. The overall seroprevalence of BTV in Senegal was 72.6% (95% CI: 70.3-74.9%) with 75.9% (95% CI: 72.2-79.5%) in goat and 70.6% (95% CI: 67.5-73.6%) in sheep. Female (prevalence=77.1%) and adult (prevalence=80%) animals showed the highest seropositivity to BTV compared respectively to male (55.7%, p=6.133e-09) and young (49.4%, p < 2.2e-16). The RT-qPCR results showed the presence of BT viral genome in 359 small ruminants. The results obtained from serological and genotyping studies showed an active spread of the Bluetongue virus in domestic ruminants and phylogenetic analysis showed that the BTV-2 is one of the circulating serotypes in Senegal. This study allows having baseline information for controlling Bluetongue in Senegal.

Effectiveness of a New Self-Marking Technique in Aedes aegypti under Laboratory Conditions.

In the implementation of mosquito control strategy programs using Sterile Insect Technique and other rear and release strategies, knowledge on the dispersion, competitiveness and survival of mosquitos is considered essential. To assess these parameters, marking techniques are generally used to differentiate colony mosquitoes from wild ones. Most of the existing mosquito marking methods require numerous manipulations that can impact their quality. In this study, we have developed a self-marking technique that can reduce the damage associated with mosquito handling. The marking technique consisted of adding fluorescent powder (DayGlo: A-17-N Saturn yellow) directly to the surface water of the receptacle containing Aedes aegypti male pupae. Different quantities of powder were used, and marking efficacy, powder persistence and mosquito survival were assessed. The results show a mean marking rate of 98 ± 1.61%, and the probability of marking increased significantly (p < 0.001) with increasing concentrations of fluorescent powder. Fluorescent powder persisted up to 20 days and did not induce a negative effect on mosquito survival (χ2 = 5.3, df = 7, p = 0.63). In addition, powder transfer did not occur between marked and unmarked populations. This marking method significantly reduces human intervention and mosquito handling during the marking process, improving the quality of marked mosquitoes used to assess SIT programs.

Identification of drivers of Rift Valley fever after the 2013-14 outbreak in Senegal using serological data in small ruminants.

Rift Valley fever (RVF) is a mosquito-borne disease mostly affecting wild and domestic ruminants. It is widespread in Africa, with spillovers in the Arab Peninsula and the southwestern Indian Ocean. Although RVF has been circulating in West Africa for more than 30 years, its epidemiology is still not clearly understood. In 2013, an RVF outbreak hit Senegal in new areas that weren't ever affected before. To assess the extent of the spread of RVF virus, a national serological survey was implemented in young small ruminants (6-18 months old), between November 2014 and January 2015 (after the rainy season) in 139 villages. Additionally, the drivers of this spread were identified. For this purpose, we used a beta-binomial ([Formula: see text]) logistic regression model. An Integrated Nested Laplace Approximation (INLA) approach was used to fit the spatial model. Lower cumulative rainfall, and higher accessibility were both associated with a higher RVFV seroprevalence. The spatial patterns of fitted RVFV seroprevalence pointed densely populated areas of western Senegal as being at higher risk of RVFV infection in small ruminants than rural or southeastern areas. Thus, because slaughtering infected animals and processing their fresh meat is an important RVFV transmission route for humans, more human populations might have been exposed to RVFV during the 2013-2014 outbreak than in previous outbreaks in Senegal.

Improving the efficiency of the BG sentinel 2 trap to assess the activity of Aedes (Stegomyia) aegypti [Linnaeus, 1762] in Senegal.

The use of efficient mosquito sampling methods in vector surveillance programs is crucial to inform control actions and prevent outbreaks. amongst existing trapping methods, the BG sentinel trap is widely used for collecting mosquitoes from the subgenus Stegomyia. However, studies state that the BG-sentinel trap underestimates the relative abundance of mosquito vectors. In this study, we used mice to enhance the effectiveness of the BG-sentinel trap to collect Aedes aegypti (Linnaeus) and follow the species' daily abundance under local conditions. The Latin square method was used to compare different combinations in three different seasons. Of the 35,107 mosquitoes collected, Ae. aegypti (53.82%) and Culex quinquefasciatus (46.07%) were dominant. The combination of BG-Lure + 3 mice captured more Ae. aegypti individuals (apparent density per trap/day (ADT = 187.65 ± 133.53; p < 0.001) followed by the 3 mice-baited BG-sentinel trap (ADT = 163.47 ± 117.32), the BG-sentinel trap without attractant (ADT = 74.15 ± 117.07) and the BG-sentinel trap + BG-Lure (ADT = 47.1 ± 115.91). Aedes aegypti showed two peaks of activity in the day, one following the sunrise and one before the sunset, influenced by temperature and relative humidity. Our study suggests the use of mice to enhance the efficiency of the BG-Sentinel trap to catch Ae. aegypti. However, its application in large scale entomological monitoring programs should be difficult because of ethical and operational constraints.

Assessing the Risk of Occurrence of Bluetongue in Senegal.

Bluetongue is a non-contagious viral disease affecting small ruminants and cattle that can cause severe economic losses in the livestock sector. The virus is transmitted by certain species of the genus Culicoides and consequently, understanding their distribution is essential to enable the identification of high-risk transmission areas. In this work we use bioclimatic and environmental variables to predict vector abundance, and estimate spatial variations in the basic reproductive ratio  R0. The resulting estimates were combined with livestock mobility and serological data to assess the risk of Bluetongue outbreaks in Senegal. The results show an increasing abundance of C. imicola, C. oxystoma, C. enderleini, and C. miombo from north to south. R0 < 1 for most areas of Senegal, whilst southern (Casamance) and southeastern (Kedougou and part of Tambacounda) agro-pastoral areas have the highest risk of outbreak (R0 = 2.7 and 2.9, respectively). The next higher risk areas are in the Senegal River Valley (R0 = 1.07), and the Atlantic coast zones. Seroprevalence rates, shown by cELISA, weren't positively correlated with outbreak probability. Future works should include follow-up studies of competent vector abundancies and serological surveys based on the results of the risk analysis conducted here to optimize the national epidemiological surveillance system.

Ecological niche modelling to estimate the distribution of Culicoides, potential vectors of bluetongue virus in Senegal.

BACKGROUND: Vector-borne diseases are among the leading causes of morbidity and mortality in humans and animals. In the Afrotropical region, some are transmitted by Culicoides, such as Akabane, bluetongue, epizootic haemorrhagic fever and African horse sickness viruses. Bluetongue virus infection has an enormous impact on ruminant production, due to its high morbidity and mortality rates. METHODS: A nationwide Culicoides trapping campaign was organized at the end of the 2012 rainy season in Senegal. A Maximum Entropy approach (MaxEnt), Boosted Regression Tree (BRT) method and Ecological Niche Factor Analysis (ENFA) were used to develop a predictive spatial model for the distribution of Culicoides, using bio-climatic variables, livestock densities and altitude. RESULTS: The altitude, maximum temperature of the warmest month, precipitation of the warmest quarter, mean temperature of the wettest quarter, temperature seasonality, precipitation of the wettest quarter and livestock density were among the most important factors to predict suitable habitats of Culicoides. Culicoides occurrences were, in most of the cases, positively correlated to precipitation variables and livestock densities; and negatively correlated to the altitude and temperature indices. The Niayes area and the Groundnut basin were the most suitable habitats predicted. CONCLUSION: We present ecological niche models for different Culicoides species, namely C. imicola, C. oxystoma, C. enderleini and C. miombo, potential vectors of bluetongue virus, on a nationwide scale in Senegal. Through our modelling approach, we were able to determine the effect of bioclimatic variables on Culicoides habitats and were able to generate maps for the occurrence of Culicoides species. This information will be helpful in developing risk maps for disease outbreaks.

Host-feeding patterns of Aedes (Aedimorphus) vexans arabiensis, a Rift Valley Fever virus vector in the Ferlo pastoral ecosystem of Senegal.

BACKGROUND: Host-vector contact is a key factor in vectorial capacity assessment and thus the transmission of mosquito-borne viruses such as Rift Valley Fever (RVF), an emerging zoonotic disease of interest in West Africa. The knowledge of the host-feeding patterns of vector species constitutes a key element in the assessment of their epidemiological importance in a given environment. The aim of this work was to identify the blood meal origins of the mosquito Aedes vexans arabiensis, the main vector of RVF virus in the Ferlo pastoral ecosystem of Senegal. METHODOLOGY/PRINCIPAL FINDINGS: Engorged female mosquitoes were collected in Younouféré in the pastoral ecosystem in the Ferlo region during the 2014 rainy season. CO2-baited CDC light traps were set at six points for two consecutive nights every month from July to November. Domestic animals present around traps were identified and counted for each trapping session. Blood meal sources of engorged mosquitoes were identified using a vertebrate-specific multiplexed primer set based on cytochrome b. Blood meal sources were successfully identified for 319 out of 416 blood-fed females (76.68%), of which 163 (51.1%) were single meals, 146 (45.77%) mixed meals from two different hosts and 10 (3.13%) mixed meals from three different hosts. Aedes vexans arabiensis fed preferentially on mammals especially on horse compared to other hosts (FR = 46.83). Proportions of single and mixed meals showed significant temporal and spatial variations according to the availability of the hosts. CONCLUSION: Aedes vexans arabiensis shows an opportunistic feeding behavior depending on the host availability. This species fed preferentially on mammals especially on horses (primary hosts) and ruminants (secondary hosts).

PPR Control in a Sahelian Setting: What Vaccination Strategy for Mauritania?

Peste des Petits Ruminants (PPR) is a viral disease affecting domestic and small wild ruminants. Endemic in large parts of the world, PPR causes severe damages to animal production and household economies. In 2015, FAO and OIE launched a global eradication program (GCSE) based on vaccination campaigns. The success of GCSE shall depend on the implementation of vaccination campaigns, accounting for husbandry practices, mobility and the periodicity of small ruminants' population renewal. In Mauritania, PPR outbreaks occur annually despite ongoing annual vaccination campaigns since 2008. Here, we developed a mathematical model to assess the impact of four vaccination strategies (including the GSCE one), the importance of their timing of implementation and the usefulness of individual animal identification on the reduction of PPR burden. The model was calibrated on data collected through ad-hoc surveys about demographic dynamics, disease impact, and national seroprevalence using Monte Carlo Markov Chain procedure. Numerical simulations were used to estimate the number of averted deaths over the next 12 years. The model results showed that the GSCE strategy prevented the largest number of deaths (9.2 million vs. 6.2 for random strategy) and provided one of the highest economic returns among all strategies (Benefit-Cost Ratio around 16 vs. 7 for random strategy). According to its current cost, identification would be a viable investment that could reduce the number of vaccine doses to distribute by 20-60%. Whilst the implementation of the identification system is crucial for PPR control, its success depends also on a coordinated approach at the regional level.

Environmental impact of tsetse eradication in Senegal.

The sterile insect technique is an environment friendly control tactic and is very species specific. It is not a stand-alone technique and has been used mostly in combination with other control tactics within an area-wide integrated pest management strategy. For a period of eight years, the direct impact of a campaign to eradicate a population of the tsetse fly Glossina palpalis gambiensis in Senegal was monitored using a set of fruit-feeding insect species (Cetoniinae and Nymphalidae) that served as ecological indicators of the health of the ecosystem. Here we show that the eradication campaign had very limited impacts on the apparent densities of the most frequent species as well as three diversity indexes during the reduction phase involving insecticides but reverted to pre-intervention levels as soon as the release of the sterile male insects started. These results greatly expand our understanding of the impact of vector eradication campaigns on non-target species.

DNA barcoding and molecular identification of field-collected Culicoides larvae in the Niayes area of Senegal.

BACKGROUND: Biting midge species of the genus Culicoides Latreille (Diptera: Ceratopogonidae) comprise more than 1300 species distributed worldwide. Several species of Culicoides are vectors of various viruses that can affect animals, like the African horse sickness virus (AHSV), known to be endemic in sub-Saharan Africa. The ecological and veterinary interest of Culicoides emphasizes the need for rapid and reliable identification of vector species. However, morphology-based identification has limitations and warrants integration of molecular data. DNA barcoding based on the mitochondrial gene cytochrome c oxidase subunit 1 (cox1) is used as a rapid and authentic tool for species identification in a wide variety of animal taxa across the globe. In this study, our objectives were as follows: (i) establish a reference DNA barcode for Afrotropical Culicoides species; (ii) assess the accuracy of cox1 in identifying Afrotropical Culicoides species; and (iii) test the applicability of DNA barcoding for species identification on a large number of samples of Culicoides larvae from the Niayes area of Senegal, West Africa. RESULTS: A database of 230 cox1 sequences belonging to 42 Afrotropical Culicoides species was found to be reliable for species-level assignments, which enabled us to identify cox1 sequences of Culicoides larvae from the Niayes area of Senegal. Of the 933 cox1 sequences of Culicoides larvae analyzed, 906 were correctly identified by their barcode sequences corresponding to eight species of Culicoides. A total of 1131 cox1 sequences of adult and larval Culicoides were analyzed, and a hierarchical increase in mean divergence was observed according to two taxonomic levels: within species (mean = 1.92%, SE = 0.00), and within genus (mean = 17.82%, SE = 0.00). CONCLUSIONS: Our study proves the efficiency of DNA barcoding for studying Culicoides larval diversity in field samples. Such a diagnostic tool offers great opportunities for investigating Culicoides immature stages ecology and biology, a prerequisite for the implementation of eco-epidemiological studies to better control AHSV in the Niayes region of Senegal, and more generally in sub-Saharan Africa.

Ecological distribution and population dynamics of Rift Valley fever virus mosquito vectors (Diptera, Culicidae) in Senegal.

BACKGROUND: Many zoonotic infectious diseases have emerged and re-emerged over the last two decades. There has been a significant increase in vector-borne diseases due to climate variations that lead to environmental changes favoring the development and adaptation of vectors. This study was carried out to improve knowledge of the ecology of mosquito vectors involved in the transmission of Rift Valley fever virus (RVFV) in Senegal. METHODS: An entomological survey was conducted in three Senegalese agro-systems, Senegal River Delta (SRD), Senegal River Valley (SRV) and Ferlo, during the rainy season (July to November) of 2014 and 2015. Mosquitoes were trapped using CDC light traps set at ten sites for two consecutive nights during each month of the rainy season, for a total of 200 night-traps. Ecological indices were calculated to characterize the different populations of RVFV mosquito vectors. Generalized linear models with mixed effects were used to assess the influence of climatic conditions on the abundance of RVFV mosquito vectors. RESULTS: A total of 355,408 mosquitoes belonging to 7 genera and 35 species were captured in 200 night-traps. RVFV vectors represented 89.02% of the total, broken down as follows: Ae. vexans arabiensis (31.29%), Cx. poicilipes (0.6%), Cx. tritaeniorhynchus (33.09%) and Ma. uniformis (24.04%). Comparison of meteorological indices (rainfall, temperature, relative humidity), abundances and species diversity indicated that there were no significant differences between SRD and SRV (P = 0.36) while Ferlo showed significant differences with both (P < 0.001). Mosquito collection increased significantly with temperature for Ae. vexans arabiensis (P < 0.001), Cx. tritaeniorhynchus (P = 0.04) and Ma. uniformis (P = 0.01), while Cx. poicilipes decreased (P = 0.003). Relative humidity was positively and significantly associated with the abundances of Ae. vexans arabiensis (P < 0.001), Cx. poicilipes (P = 0.01) and Cx. tritaeniorhynchus (P = 0.007). Rainfall had a positive and significant effect on the abundances of Ae. vexans arabiensis (P = 0.005). The type of biotope (temporary ponds, river or lake) around the trap points had a significant effect on the mosquito abundances (P < 0.001). CONCLUSIONS: In terms of species diversity, the SRD and SRV ecosystems are similar to each other and different from that of Ferlo. Meteorological indices and the type of biotope (river, lake or temporary pond) have significant effects on the abundance of RVFV mosquito vectors.

Response of insect relative growth rate to temperature and host-plant phenology: estimation and validation from field data.

Between 1975 to 2011, aphid Relative Growth Rates (RGR) were modelled as a function of mean outdoor temperature and host plant phenology. The model was applied to the grain aphid Sitobion avenae using data on aphid counts in winter wheat at two different climate regions in France (oceanic climate, Rennes (western France); continental climate, Paris). Mean observed aphid RGR was higher in Paris compared to the Rennes region. RGR increased with mean temperature, which is explained by aphid reproduction, growth and development being dependent on ambient temperature. From the stem extension to the heading stage in wheat, there was either a plateau in RGR values (Rennes) or an increase with a maximum at heading (Paris) due to high intrinsic rates of increase in aphids and also to aphid immigration. From the wheat flowering to the ripening stage, RGR decreased in both regions due to the low intrinsic rate of increase in aphids and high emigration rate linked to reduced nutrient quality in maturing wheat. The model validation process showed that the fitted models have more predictive power in the Paris region than in the Rennes region.

A spatiotemporal model for predicting grain aphid population dynamics and optimizing insecticide sprays at the scale of continental France.

We expose here a detailed spatially explicit model of aphid population dynamics at the scale of a whole country (Metropolitan France). It is based on convection-diffusion-reaction equations, driven by abiotic and biotic factors. The target species is the grain aphid, Sitobion avenae F., considering both its winged and apterous morphs. In this preliminary work, simulations for year 2004 (an outbreak case) produced realistic aphid densities, and showed that both spatial and temporal S. avenae population dynamics can be represented as an irregular wave of population peak densities from southwest to northeast of the country, driven by gradients or differences in temperature, wheat phenology, and wheat surfaces. This wave pattern fits well to our knowledge of S. avenae phenology. The effects of three insecticide spray regimes were simulated in five different sites and showed that insecticide sprays were ineffective in terms of yield increase after wheat flowering. After suitable validation, which will require some further years of observations, the model will be used to forecast aphid densities in real time at any date or growth stage of the crop anywhere in the country. It will be the backbone of a decision support system, forecasting yield losses at the level of a field. The model intends then to complete the punctual forecasting provided by older models by a comprehensive spatial view on a large area and leads to the diminution of insecticide sprayings in wheat crops.