Cattle ticks and associated tick-borne pathogens in Burkina Faso and Benin: Apparent northern spread of Rhipicephalus microplus in Benin and first evidence of Theileria velifera and Theileria annulata

peer reviewedBabesiosis, theileriosis, anaplasmosis, and heartwater are tick-borne diseases that threaten livestock production in sub-Saharan Africa including Burkina Faso and Benin. For over a decade, these two bordering countries have been facing an invasion of the livestock by the tick Rhipicephalus microplus, a major vector for babesiosis, accidentally introduced in Benin in 2004. The molecular identification of tick-borne pathogens in this border area is of particular interest due to animals seasonal migration between the two countries. In this survey, epidemiological features of ticks and tick-borne pathogens in cattle were investigated to compare the eastern Burkina Faso, corresponding to a seasonal migration departure zone, and the northern Benin, which represents a seasonal migration arrival zone. Ticks and peripheral blood were collected from a total of 946 cattle in the two areas. Ticks were morphologically identified and the DNA samples from bovine blood and ticks were analysed by Reverse Line Blot (RLB) hybridization process. A total of 2856 ticks were collected on 490 cattle in Burkina Faso, eight tick species were identified, while 3583 ticks were collected on 456 cattle in North Benin with nine tick species identified. The invasive tick, R. microplus was not found in eastern Burkina Faso, but its spread farthest north in Benin is reported. Six tick-borne pathogen species were found in cattle blood both in eastern Burkina Faso and in northern Benin. Ranked in decreasing order of overall prevalences, they are: Theileria mutans (91.1%), Theileria velifera (77.8%), Babesia bigemina (10.9%), Anaplasma marginale (4.2%), Babesia bovis (3.3%), and Theileria annulata (1.8%). To the best of our knowledge, this survey represents the first report of T. velifera and T. annulata in the region. Overall, the TBP prevalences were significantly higher in northern Benin than in eastern Burkina Faso, indicating a higher parasitological risk in this area. © 2021 Elsevier Gmb

Models for studying the distribution of ticks and tick-borne diseases in animals : a systematic review and a meta-analysis with a focus on Africa

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Cross border transhumance involvement in ticks and tick-borne pathogens dissemination and first evidence of Anaplasma centrale in Burkina Faso

In West Africa, cross-border transhumance, also called seasonal migration, is known to be a very important animal production strategy, as it involves about 70 to 90% of cattle. In spite of the cattle movements, some strategic areas of transhumance remain poorly explored regarding ticks and their associated pathogens investigations. The purpose of this study is to evaluate the involvement of transhumance in the spread of cattle ticks and associated pathogens in Burkina Faso (BF) and Benin (BN), in a context of speedy invasion of West African livestock by Rhipicephalus microplus. A longitudinal survey was performed on 210 cattle from BF, monitored for ticks and tick-borne pathogens (TBP) during one seasonal transhumance. The first sampling coded “T0BF” took place in eastern BF, at the transhumance departure. A second sampling “T1BN” was carried out in northern BN, the transhumance arrival zone. A third sampling “T2BF” was done at the return of cattle in eastern BF. Ticks were morphologically identified and TBP detected with reverse line blot hybridization (RLB) assay. A total of 1027 ticks (7 species), 1006 ticks (11 species) and 1211 ticks (9 species) were respectively found at T0BF, T1BN and T2BF. Some species were collected at the three times of sampling without any significant difference in their relative abundances. However, other tick species appeared only at T1BN and/or T2BF. The TBP species found at the three points surveyed were Theileria annulata, Theileria mutans, Theileria velifera, Babesia bigemina and Anaplasma marginale. The most prevalent was T. mutans with 166/210 (79%), 159/210 (75.7%) and 78/210 (37%) cattle positive respectively at T0BF, T1BN and T2BF. Anaplasma centrale was evidenced with 0.5% and 0.9% respectively at T0BF and T2BF. To our knowledge, this represents its first report in the study area. Overall, the TBP prevalences were significantly lower at T2BF, highlighting the effect of tick populations changes induced by transhumance combined with the seasonal variation influence. © 202

Tiques et maladies associées chez les bovins transhumants entre le Burkina Faso et la République du Bénin : aspects socio-épidémiologiques

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.Appui au réseau de surveillance épidémiologique des maladies animales et aspects sociologiques associés en Afrique de l'Ouest (Acronyme : TransTicks

First tick and tick damage perception survey among sedentary and transhumant pastoralists in Burkina Faso and Benin.

BACKGROUND: Transhumance, a main ancestral animal production strategy of the West African Countries (WAC), can favour the spread of vectors and vector-borne diseases within and/or across countries. Transhumance has been implicated in such spread as well as that of related tick-borne diseases (TBD). METHODS AND PRINCIPAL FINDINGS: Using a questionnaire survey and statistical modelling, this study explores the perception of herders about ticks and TBD in cattle, their practices in tick control and the social groups involved in cattle farming in eastern Burkina Faso (46 random herds) and in the northern Benin (44 random herds). Results show that most of the herders (79%) are from the Fulani social group. The principal and secondary activities of herders are respectively cattle farming and agriculture. The mean age of pastoralists is between 40 and 50 years depending on the province of origin and 60% of the surveyed herds practice internal or transboundary transhumance. Herders have a clear knowledge of different genus of ticks except the genus Rhipicephalus. Their knowledge of TBD is very limited. These results also reveal that herders in Benin use less acaricides treatment calendar compared with those in Burkina Faso. Transhumant pastoralists (i.e. transhumant cattle farmers) plan more acaricide treatment and have more cows with lost teats (i.e. tick damage) than the sedentary ones. In addition, amitraz appears to be the main acaricide compound used by herders for tick control (68%) but its use is inappropriate and its source is frequently the unregulated market. CONCLUSIONS AND SIGNIFICANCE: All of these findings can induce acaricide resistance especially as the inefficacy of amitraz against Rhipicephalus (Boophilus) microplus has already been reported in previous studies. Such results would help to elaborate suitable strategies of control and prevention of ticks and TBD in Burkina Faso and Benin

Efficacy of two commercial synthetic pyrethroids (cypermethrin and deltamethrin) on Amblyomma variegatum and Rhipicephalus microplus strains of the south-western region of Burkina Faso

Since 2011, period of the livestock invasion by the cattle tick Rhipicephalus microplus in Burkina Faso (BF), tick-control problems were exacerbated. Based on farmer’s reports, most commonly used commercial acaricides were found to be ineffective in Western South part of the country. To investigate the occurrence and extent of such acaricidal ineffectiveness, we performed the standardized larval packet test (LPT) with commercial deltamethrin (vectocid) and cypermethrin (cypertop), on two cattle tick species, the native Amblyomma variegatum and the invasive R. microplus. The resistance ratios (RR) were computed with susceptible Hounde strain of Rhipicephalus geigyi as reference. The R. microplus population showed resistance to the two acaricides tested with the highest lethal concentration (LC) values, and different resistance ratios higher than 4 (deltamethrin: RR50 = 28.18 and RR90 = 32.41; cypermethrin: RR50 = 8.79 and RR90 = 23.15). In the contrary, A. variegatum population was found to be highly susceptible to acaricides tested with low lethal concentrations and resistance ratio values (deltamethrin: RR50 = 0.5 and RR90 = 0.48; cypermethrin: RR50 = 0.68 and RR90 = 0.79). These data demonstrate high synthetic pyrethroid resistance in R. microplus strain, leading to conclude that the acaricide ineffectiveness in tick populations control remains a concern in BF. © 2021, The Author(s)

First digital characterization of the transhumance corridors through Benin used by cattle herds from Burkina Faso and associated risk scoring regarding the invasion of Rhipicephalus (Boophilus) microplus.

BACKGROUND: Livestock plays a key role in the macro economy 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 herders. This adaptive strategy aims to optimize livestock access to water and pastures. However, it can favour pathogens and vectors transboundary spread. This study aim is 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 introduction and spread of the invasive tick species, Rhipicephalus (Boophilus) microplus, in free areas. METHODS AND PRINCIPAL FINDINGS: Therefore, GPS devices were given to 27 herders to monitor a full transhumance season between East Burkina Faso and North Benin. The analysis of 14,966 spots generated by the GPS devices revealed four main corridors and five main grazing areas used by cattle herds during transhumance. Statistical analysis of normalized difference vegetation index (NDVI), rainfall and temperature data, highlighted significant differences between departure and arrival areas. NDVI and rainfall are significantly higher in Benin than Burkina Faso whereas temperature is significantly lower. Additionally, using biotic and abiotic parameters, a risk scoring was developed to predict the presence of Rhipicephalus (Boophilus) microplus at municipality level. CONCLUSIONS AND SIGNIFICANCE: The better vegetation, temperature and rainfall conditions during the dry seasons in Benin attract cattle herds from Burkina Faso. The invasiveness and adaptability of Rhipicephalus (Boophilus) 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

Modelling habitat suitability of the invasive tick Rhipicephalus microplus in West Africa.

peer reviewedTicks have medical and economic importance due to their ability to transmit pathogens to humans and animals. In tropical and sub-tropical countries, tick-borne diseases (TBD) are among the most important diseases affecting livestock and humans. The fast spread of ticks and TBD requires a quick development and application of efficient prevention and/or control programs. Therefore, prior investigations on TBD and related vectors epidemiology, for instance, through accurate epidemiological models, are mandatory. This study aims to develop models to forecast suitable habitat for Rhipicephalus microplus distribution in West Africa. Tick occurrences were assembled from 10 different studies carried out in six West African countries in the past decade. Six statistical models (maximum entropy in a single model and generalised linear model, generalised additive model, random forest, boosted regression tree and support vector machine model in an ensemble model) were applied and compared to predict the habitat suitability of R. microplus distribution in West Africa. Each model was evaluated with the area under the receiver operating characteristic curve (AUC), the true skill statistic (TSS) and the Boyce index (BI). The selected models had good performance according to their AUC (above .8), TSS (above .7) and BI (above .8). Temperature played a key role in MaxEnt model, whereas normalised difference vegetation index (NDVI) was the most important variable in the ensemble model. The model predictions showed coastal countries of West Africa as more suitable for R. microplus. However, some Sahelian areas seems also favourable. We stress the importance of vector surveillance and control in countries that have not yet detected R. microplus but are in the areas predicted to host suitable habitat. 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