Ticks and tick-borne diseases in transhumant cattle between Burkina Faso and Republic of Benin : socio-epidemiological aspects

Livestock plays a key role in the macroeconomy of West Africa and provides livelihoods for millions of people. The main cattle rearing strategy in West Africa is pastoralism, including transhumance: i.e. a seasonal migration of cattle with their cattle holders. This adaptive strategy aims to optimize livestock access to water and pastures. However, it can favour pathogens and vectors transboundary spread with many medical and economic consequences to the affected countries.
Using a questionnaire survey and statistical modelling, the first study explored the perception of cattle holders about ticks and tick-borne diseases (TTBD) in cattle, their practices in tick control and the social groups involved in cattle farming in eastern Burkina Faso (46 randomly selected herds) and in northern Benin (44 randomly selected herds). Results show that most of the cattle holders (79%) are from the Fulani social group. The principal and secondary activities of cattle holders are respectively cattle farming and agriculture. The mean age of pastoralists is between 40 and 50 years and 60% of the surveyed herds practice internal or transboundary transhumance. Cattle holders have a clear knowledge of different genus of ticks except for the genus Rhipicephalus. Their knowledge of tick-borne diseases (TBD) is very limited. Amitraz appears to be the main acaricide compound used by cattle holders for tick control (68%) but its use is inappropriate and its source is frequently the unregulated market. All of these findings can induce acaricide resistance especially since the inefficacy of amitraz against R. microplus has already been reported in previous studies. Such results would help to elaborate suitable strategies of control and prevention of TTBD in Burkina Faso and Benin.
The second study aimed to highlight, firstly the corridors and grazing areas used by Burkina Faso transhumant cattle herds going to Benin, secondly the characteristics of departure and arrival areas of transhumance and thirdly, the risk score related to the introduction and spread of the invasive tick species, Rhipicephalus microplus, in free areas. Therefore, GPS (Global Positioning System) devices were given to 27 cattle holders to monitor a full transhumance season between East Burkina Faso and North Benin. GPS devices revealed four main corridors and five main grazing areas used by cattle herds during transhumance. Normalized Difference Vegetation Index (NDVI) and rainfall are significantly higher in Benin than in Burkina Faso whereas temperature is significantly lower. Additionally, using biotic and abiotic parameters, a risk-scoring model was developed to predict the presence of R. microplus at the municipality level. The invasiveness and adaptability of R. microplus added to the frequent stays of transhumant herds in infested areas suggest its potential introduction and establishment in free areas soon. Moreover, frequent intrusions of the transhumant cattle in the wildlife reserves is another risk of vectors and pathogen exchange between domestic and wild animals.
The third study of this thesis aimed to identify epidemiological models developed by researchers to understand the dynamics of TTBD spread. A literature search was implemented with PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analysis) protocol in two online databases (Scopus and PubMed). The selected articles were classified according to country, type of epidemiological models used and the objective of the modelling. Sensitivity, specificity and accuracy available data of these models were investigated using meta-analysis approaches. Results relied on 107 studies in which seven tick genera were modelled, with Ixodes spp. the most studied. Thirteen genera of tick-borne pathogens were modelled, with Borrelia spp. the most frequently modelled. Twenty-four different models were reviewed and the most frequently used are the Generalized Linear Model (GLM) representing 26.67% and the Maximum Entropy (MaxEnt) model representing 24.17%. A focus on TTBD modelling in Africa showed that respectively genus Rhipicephalus and Theileria were the most modelled. A meta-analysis on the quality of 20 models revealed that MaxEnt, Linear Discriminant Analysis (LDA), and the Ecological Niche Factor Analysis (ENFA) models had respectively the highest sensitivity, specificity, and area under the curve effect size among all the selected models. Modelling TTBD is highly relevant for predicting their distribution and preventing their adverse effect on animal and human health and the economy. Related results of such analyses are useful to build prevention and/or control programs by veterinary and public health authorities.
The objectives of the fourth study are to develop models to forecast the habitat distribution of R. microplus. Tick occurrences were assembled from ten different studies conducted in six West African countries in the past decade. Six statistical models (Maximum Entropy MaxEnt, Generalized Linear Model GLM, Generalized Additive Model GAM, Random Forest RF, Boosted Regression Tree BRT et Support Vector Machine SVM) were applied to predict the habitat suitability of R. microplus in West Africa. MaxEnt was used alone and the other five models were used in an ensemble model. The selected models resulted as accurate according to the AUC (Area Under the Receiver Operating Characteristic Curve) and TSS (True Skill Statistic) metrics, respectively above 0.9 and 0.5. The models' predictions show coastal countries of West Africa as more suitable areas for the habitat of R. microplus. We stress the importance of vector surveillance and control in those countries that have not yet detected the tick but are in the areas predicted to host suitable habitats. Indeed, awareness-raising and training of different stakeholders must be reinforced for better prevention and control of this tick in these different countries according to their status.
The objective of the fifth study is to evaluate the clinical and economic impact of ticks and tick-borne diseases in cattle herds and the benefits of controlling these parasites. Using data from an acarological and epidemiological survey conducted in 2017 in eastern Burkina Faso and northern Benin and data collected from various articles, we developed a deterministic model. This model allowed us to evaluate the clinical and economic impact of ticks and tick-borne diseases on herds. Six scenarios were developed depending on whether the animals were treated with only acaricides or with acaricides and against tick-borne diseases. The results of these scenarios were compared in a linear regression to highlight the significant difference. Linear regression revealed a significant gain of 871 euro at herd level (P<0.05) with the acaricide treatment scenarios, compared to the losses if no treatment is done. When preventive treatment of tick-borne pathogens is combined with acaricide treatment there is a significant additional gain of 254 euro (P<0.001) compared to the losses if no treatment is applied at all. It is therefore opportune to set up control strategies adapted to the specificity of each area. The development of these strategies and their implementation must be consensual and participatory for their success.
In conclusion, we can say that this thesis has achieved its overall objective by providing the competent authorities with valuable and relevant decision support tools (epidemiological and economic models) to reduce the incidence of ticks and tick-borne diseases. We, therefore, recommend the following:
• To ECOWAS: better management of veterinary drugs to successfully control ticks and associated diseases and strengthening existing sub-regional agreements on cross-border transhumance;
• To Veterinary Services: strengthening their technical and human resource capacities to face the challenge of ticks and associated diseases and transhumance;
• To livestock keepers: greater responsibility in the supply and use of acaricides and better management of their herds taking into account the level of tick infestation and tick-borne diseases in their respective environments.