# Assessing the Risk of Occurrence of Bluetongue in Senegal

^{1}

^{2}

^{3}

^{4}

^{5}

^{6}

^{7}

^{*}

^{†}

## Abstract

**:**

## 1. Introduction

_{0}) as a measure of BT epidemic potential and mapped its values. The transmission dynamics are described using a compartmental model in a multi-species context, and we used the Next-Generation Matrix [26] approach to determine R

_{0}. Finally, we combined previous results with mobility and serological data to estimate the risk of occurrence of the disease in the different parts of Senegal due to the introduction of animals from infected zones [27,28].

## 2. Materials and Methods

#### 2.1. Study Area

#### 2.2. Data Collection

#### 2.2.1. Entomological Data

#### 2.2.2. Serological Data

#### 2.2.3. Climatic, Environmental and Livestock Data

#### 2.2.4. Small Ruminants Demographic Data

#### 2.2.5. Mobility Data

#### 2.3. Estimated Vector Abundance, R_{0}, and the Probability of the Occurrence of an Outbreak

#### 2.3.1. Abundance Modeling: Random Forest

#### 2.3.2. Model Host-Vector for Bluetongue Transmission

_{h}), animals either die (D) with a certain probability p, or recover I and acquire lifelong immunity with probability 1-p. Similarly, for the vector population, after infection, susceptible vectors (S) become latent (E), and then infectious for the rest of their lives (I). On top of the transmission dynamics, we considered the demographic dynamics, with animals and vectors being born and dying naturally. Animals born from recovered mothers are protected by maternal antibodies (Imm

_{h}) for the first three months of their lives before becoming susceptible. The resulting compartmental model is a system of nine ordinary differential equations reported in Supplementary Information. A pictorial representation of the model is shown in Figure 3, where the pedex h corresponds to the host-related compartments, and the

**v**one to the vector ones.

_{h}) and for the vectors (λ

_{v}) is estimated as:

_{vh}, P

_{hv}are the probabilities of transmission from vector to host and to host to vector, respectively, ${a}_{s}$ is the biting rate, ${I}_{h},{I}_{v}$ the number of infectious hosts, and vectors ${N}_{h},{N}_{v}$ their populations.

#### 2.3.3. Sensitivity Analysis

#### 2.3.4. Occurrence Probability Map

## 3. Results

#### 3.1. Estimating the Vector Spatial Abundance

#### 3.2. Estimating the Spatial Distribution of R_{0} (Transmission Maps)

_{0}is high in Casamance (mean ${R}_{0}=2.74,1.74$ for the temperature-independent and dependent case) and in the southeastern corner of Senegal (Kédougou region). Indeed, in the latter, the basic reproduction number is higher than 10. Similarly, in Casamance, the value of ${R}_{0}$ is high (above 5 in almost all the area)—possibly linked to the high abundance of C. enderleini. On the other hand, in the northern part of the country (particularly in the Ferlo area), the value of ${R}_{0}$ is low (mean ${R}_{0}=0.66,0.48$ for the temperature-independent and dependent case), meaning there is little risk of an outbreak of BT. Moreover, the map built using temperature-independent values predicts higher values of ${R}_{0}$ in the Casamance area, the groundnut basin (Bassin arachidier) (mean ${R}_{0}=0.80,0.51$ for the temperature-independent and dependent case) and along the Senegal River Valley in the north (mean ${R}_{0}=1.08,0.74$ for the temperature-independent and dependent case), than the map built using temperature-dependent values. The emerging trends reflect the distribution of Culicoides, and any discrepancies between the two approaches could be linked to the different biting rates and latency period. Indeed, areas with high vector abundance (Figure 4) present the highest value of ${R}_{0}$ due to the high vector-host ratio ($\frac{{N}_{V}}{{N}_{h}}$), while areas with low vector abundance (e.g., the Ferlo area) have the lowest risk of Bluetongue transmission.

#### 3.3. Estimating the Risk of the Occurrence of BT Outbreaks

## 4. Discussion

_{0}were likely to experience outbreaks with a high probability of occurrence in the south. However, the analysis of the map shows that livestock mobility could play an important role in triggering epidemics. In areas with low ${R}_{0}$ values (between 1 and 2), an epidemic can still occur if enough infected animals are introduced. This is the case in the Ferlo area and at the border with Gambia where there is a high probability of occurrence, despite their low ${R}_{0}$ values. Therefore, despite the fact that BT is a non-contagious disease, livestock mobility can play an important role in its diffusion. To validate our results, we need more information on the epidemiological situation in the region: In fact, we are unable to distinguish if our seroprevalence results are related to epidemic dynamics or low noise circulation or if the animals that were imported were already infected or not. Although our livestock data include information on international movements, in this article, we focused on national movements, since no information was available on the BT epidemiological situation in neighboring countries. Being able to include such, the information would make it possible to assess the risk of introducing the disease from other countries

## 5. Conclusions

## Supplementary Materials

## Author Contributions

## Funding

## Acknowledgments

## Conflicts of Interest

## References

- Stear, M.J. OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals (Mammals, Birds and Bees) 5th Edn. Volumes 1 & 2. World Organization for Animal Health 2004. ISBN 92 9044 622 6. €140. Parasitology
**2005**, 130, 727. [Google Scholar] [CrossRef] - Backx, A.; Heutink, R.; Van Rooij, E.; Van Rijn, P.A. Transplacental and Oral Transmission of Wild-Type Bluetongue Virus Serotype 8 in Cattle after Experimental Infection. Vet. Microbiol.
**2009**, 138, 235–243. [Google Scholar] [CrossRef] [PubMed] [Green Version] - Worwa, G.; Hilbe, M.; Ehrensperger, F.; Chaignat, V.; Hofmann, M.A.; Griot, C.; MacLachlan, N.J.; Thuer, B. Experimental Transplacental Infection of Sheep with Bluetongue Virus Serotype 8. Vet. Rec.
**2009**, 164, 499–500. [Google Scholar] [CrossRef] [PubMed] - Belbis, G.; Breard, E.; Cordonnier, N.; Moulin, V.; Desprat, A.; Sailleau, C.; Viarouge, C.; Doceul, V.; Zientara, S.; Millemann, Y. Evidence of Transplacental Transmission of Bluetongue Virus Serotype 8 in Goats. Vet. Microbiol.
**2013**, 166, 394–404. [Google Scholar] [CrossRef] [PubMed] - Zanella, G.; Durand, B.; Sellal, E.; Breard, E.; Sailleau, C.; Zientara, S.; Batten, C.; Mathevet, P.; Audeval, C. Bluetongue Virus Serotype 8: Abortion and Transplacental Transmission in Cattle in the Burgundy Region, France, 2008–2009. Theriogenology
**2012**, 77, 65–72. [Google Scholar] [CrossRef] [PubMed] - De Clercq, K.; De Leeuw, I.; Verheyden, B.; Vandemeulebroucke, E.; Vanbinst, T.; Herr, C.; Méroc, E.; Bertels, G.; Steurbaut, N.; Miry, C.; et al. Transplacental Infection and Apparently Immunotolerance Induced by a Wild-type Bluetongue Virus Serotype 8 Natural Infection. Transbound. Emerg. Dis.
**2008**, 55, 352–359. [Google Scholar] [CrossRef] - Purse, B.V.; Mellor, P.S.; Rogers, D.J.; Samuel, A.R.; Mertens, P.P.C.; Baylis, M. Climate Change and the Recent Emergence of Bluetongue in Europe. Nat. Rev. Genet.
**2005**, 3, 171–181. [Google Scholar] [CrossRef] - Purse, B.V.; Brown, H.E.; Harrup, L.; Mertens, P.P.C.; Rogers, D.J. Invasion of Bluetongue and other Orbivirus Infections into Europe: The Role of Biological and Climatic Processes. Rev. Sci. Tech. l’OIE
**2008**, 27, 427–442. [Google Scholar] [CrossRef] - Wilson, A.J.; Mellor, P.S. Bluetongue in Europe: Past, Present and Future. Philos. Trans. R. Soc. B Boil. Sci.
**2009**, 364, 2669–2681. [Google Scholar] [CrossRef] - Coetzee, P.; Stokstad, M.; Venter, E.; Myrmel, M.; Van Vuuren, M. Bluetongue: A Historical and Epidemiological Perspective with the Emphasis on South Africa. Virol. J.
**2012**, 9, 198. [Google Scholar] [CrossRef] [Green Version] - Gambles, R. Bluetongue of Sheep in Cyprus. J. Comp. Pathol. Ther.
**1949**, 59, 176–190. [Google Scholar] [CrossRef] - Roy, P. Bluetongue Virus Genetics and Genome Structure. Virus Res.
**1989**, 13, 179–206. [Google Scholar] [CrossRef] - Saegerman, C.; Berkvens, D.; Mellor, P.S. Bluetongue Epidemiology in the European Union. Emerg. Infect. Dis.
**2008**, 14, 539–544. [Google Scholar] [CrossRef] [PubMed] - Conraths, F.J.; Gethmann, J.; Staubach, C.; Mettenleiter, T.C.; Beer, M.; Hoffmann, B. Epidemiology of Bluetongue Virus Serotype 8, Germany. Emerg. Infect. Dis.
**2009**, 15, 433–435. [Google Scholar] [CrossRef] [PubMed] - Zientara, S.; Sailleau, C.; Bréard, E.; Viarouge, C.; Gorna, K.; Relmy, A.; Desprat, A. Intérêt des Outils Moléculaires Pour l’identification et de Typage des Orbivirus. Rencontres Autour Rech. Rumin.
**2010**, 17, 83–86. [Google Scholar] - Lefevre, P.; Taylor, W. Epidemiological Situation of Bluetongue in Senegal. Rev. Elev. Med. Vet. Pays Trop.
**1983**, 36, 241–245. [Google Scholar] - Lefèvre, P.-C.; Calvez, D. La Fièvre Catarrhale du Mouton (Bluetongue) en Afrique Intertropicale: Influence des Facteurs Écologiques sur la Prévalence de L’infection. Rev. Elev. Méd. vét. P. Trop.
**1986**, 39, 263–268. [Google Scholar] - Bakhoum, M.T.; Fall, A.G.; Fall, M.; Bassene, C.K.; Baldet, T.; Seck, M.T.; Bouyer, J.; Garros, C.; Gimonneau, G. Insight on the Larval Habitat of Afrotropical Culicoides Latreille (Diptera: Ceratopogonidae) in the Niayes Area of Senegal, West Africa. Parasit. Vectors
**2016**, 9, 462. [Google Scholar] [CrossRef] [Green Version] - Fall, M.; Fall, A.G.; Seck, M.T.; Bouyer, J.; Diarra, M.; Lancelot, R.; Gimonneau, G.; Garros, C.; Bakhoum, M.T.; Faye, O.; et al. Host Preferences and Circadian Rhythm of Culicoides (Diptera: Ceratopogonidae), Vectors of African Horse Sickness and Bluetongue Viruses in Senegal. Acta Trop.
**2015**, 149, 239–245. [Google Scholar] [CrossRef] - Diarra, M.; Fall, M.; Fall, A.G.; Diop, A.; Lancelot, R.; Seck, M.T.; Rakotoarivony, I.; Allène, X.; Bouyer, J.; Guis, H. Spatial Distribution Modelling of Culicoides (Diptera: Ceratopogonidae) Biting Midges, Potential Vectors of African Horse Sickness and Bluetongue Viruses in Senegal. Parasit. Vectors
**2018**, 11, 341. [Google Scholar] [CrossRef] - Ciss, M.; Biteye, B.; Fall, A.G.; Fall, M.; Gahn, M.C.B.; Leroux, L.; Apolloni, A. Ecological Niche Modelling to Estimate the Distribution of Culicoides, Potential Vectors of Bluetongue Virus in Senegal. BMC Ecol.
**2019**, 19, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version] - Akakpo, A.; Toukam, W.C.; Mankor, A.; Ly, C. Impact Économique de L’épizootie de Peste Équine de 2007 au Sénégal. Bull. Anim. Health Prod. Afr.
**2011**, 59, 1–16. [Google Scholar] [CrossRef] - Diouf, N.D.; Etter, E.; Akakpo, A.J.; Lo, M.M. Outbreaks of African Horse Sickness in Senegal, and Methods of Control of the 2007 Epidemic. Vet. Rec.
**2012**, 172, 152. [Google Scholar] [CrossRef] [PubMed] - Diarra, M.; Fall, M.; Fall, A.G.; Diop, A.; Seck, M.T.; Garros, C.; Balenghien, T.; Allène, X.; Rakotoarivony, I.; Lancelot, R.; et al. Seasonal Dynamics of Culicoides (Diptera: Ceratopogonidae) Biting Midges, Potential Vectors of African Horse Sickness and Bluetongue Viruses in the Niayes Area of Senegal. Parasites Vectors
**2014**, 7, 147. [Google Scholar] [CrossRef] [Green Version] - Diarra, M.; Fall, M.; Lancelot, R.; Diop, A.; Fall, A.G.; Dicko, A.H.; Seck, M.T.; Garros, C.; Allène, X.; Rakotoarivony, I.; et al. Modelling the Abundances of Two Major Culicoides (Diptera: Ceratopogonidae) Species in the Niayes Area of Senegal. PLoS ONE
**2015**, 10, e0131021. [Google Scholar] [CrossRef] [PubMed] [Green Version] - Diekmann, O.; Heesterbeek, H.; Roberts, M.G. The Construction of Next-Generation Matrices for Compartmental Epidemic Models. J. R. Soc. Interface
**2009**, 7, 873–885. [Google Scholar] [CrossRef] [Green Version] - Brugger, K.; Rubel, F. Bluetongue Disease Risk Assessment Based on Observed and Projected Culicoides obsoletus spp. Vector Densities. PLoS ONE
**2013**, 8, e60330. [Google Scholar] [CrossRef] [Green Version] - Colizza, V.; Barthelemy, M.; Barrat, A.; Vespignani, A. Epidemic Modeling in Complex Realities. Comptes Rendus Boil.
**2007**, 330, 364–374. [Google Scholar] [CrossRef] [Green Version] - Fall, M.; Diarra, M.; Fall, A.G.; Balenghien, T.; Seck, M.T.; Bouyer, J.; Garros, C.; Gimonneau, G.; Allène, X.; Mall, I.; et al. Culicoides (Diptera: Ceratopogonidae) Midges, the Vectors of African Horse Sickness Virus--a Host/Vector Contact Study in the Niayes Area of Senegal. Parasit. Vectors
**2015**, 8, 39. [Google Scholar] [CrossRef] - Vandenbussche, F.; Vanbinst, T.; Verheyden, B.; Van Dessel, W.; Demeestere, L.; Houdart, P.; Bertels, G.; Praet, N.; Berkvens, D.; Mintiens, K.; et al. Evaluation of Antibody-ELISA and Real-Time RT-PCR for the Diagnosis and Profiling of Bluetongue Virus Serotype 8 during the Epidemic in Belgium in 2006. Vet. Microbiol.
**2008**, 129, 15–27. [Google Scholar] [CrossRef] [Green Version] - Gahn, M.C.B.; Seck, M.T.; Ciss, M.; Fall, A.G.; Lo, M.M.; Ndiaye, M.; Fall, M.; Biteye, B.; Sailleau, C.; Viarouge, C.; et al. Insight Bluetongue Virus Transmission in Small Ruminants in Senegal (to be submitted). Microorganism
**2020**. [Google Scholar] - Lancelot, R.; Faye, B.; Juanes, X.; Ndiaye, M.; Pérochon, L.; Tillard, E. La Base de Données BAOBAB: Un Outil Pour Modéliser la Production et la Santé des Petits Ruminants dans les Systèmes D’élevage Traditionnels au Sénégal. Revue d’Elevage Méd. Vét. Pays Trop.
**1998**, 51, 135–146. [Google Scholar] [CrossRef] - O’Farrell, H.; Gourley, S.A. Modelling the Dynamics of Bluetongue Disease and the Effect of Seasonality. Bull. Math. Boil.
**2014**, 76, 1981–2009. [Google Scholar] [CrossRef] [PubMed] - González-Parra, G.; Aranda, D.F.; Chen-Charpentier, B.; Díaz-Rodríguez, M.; Castellanos, J.E. Mathematical Modeling and Characterization of the Spread of Chikungunya in Colombia. Math. Comput. Appl.
**2019**, 24, 6. [Google Scholar] [CrossRef] [Green Version] - Gubbins, S.; Carpenter, S.; Baylis, M.; Wood, J.L.; Mellor, P.S. Assessing the Risk of Bluetongue to UK Livestock: Uncertainty and Sensitivity Analyses of a Temperature-Dependent Model for the Basic Reproduction Number. J. R. Soc. Interface
**2007**, 5, 363–371. [Google Scholar] [CrossRef] [PubMed] [Green Version] - Hartemink, N.; Purse, B.; Meiswinkel, R.; Brown, H.E.; De Koeijer, A.; Elbers, A.; Boender, G.-J.; Rogers, D.; Heesterbeek, J. Mapping the Basic Reproduction Number (R0) for Vector-Borne Diseases: A Case Study on Bluetongue Virus. Epidemics
**2009**, 1, 153–161. [Google Scholar] [CrossRef] - Santman-Berends, I.; Stegeman, J.; Vellema, P.; Van Schaik, G. Estimation of the Reproduction Ratio (R0) of Bluetongue Based on Serological Field Data and Comparison with Other BTV Transmission Models. Prev. Vet. Med.
**2013**, 108, 276–284. [Google Scholar] [CrossRef] - Charron, M.V.; Seegers, H.; Langlais, M.; Ezanno, P. Seasonal Spread and Control of Bluetongue in Cattle. J. Theor. Boil.
**2011**, 291, 1–9. [Google Scholar] [CrossRef] - Hammami, P.; Lancelot, R.; Lesnoff, M. Modelling the Dynamics of Post-Vaccination Immunity Rate in a Population of Sahelian Sheep after a Vaccination Campaign against Peste des Petits Ruminants Virus. PLoS ONE
**2016**, 11, e0161769. [Google Scholar] [CrossRef] [Green Version] - Dean, A.S.; Fournié, G.; Kulo, A.E.; Boukaya, G.A.; Schelling, E.; Bonfoh, B. Potential Risk of Regional Disease Spread in West Africa through Cross-Border Cattle Trade. PLoS ONE
**2013**, 8, e75570. [Google Scholar] [CrossRef] [Green Version] - Cianci, D.; Hartemink, N.; Ibáñez-Justicia, A. Modelling the Potential Spatial Distribution of Mosquito Species Using Three Different Techniques. Int. J. Health Geogr.
**2015**, 14, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version] - Peters, J.; De Baets, B.; Van Doninck, J.; Calvete, C.; Lucientes, J.; De Clercq, E.M.; Ducheyne, E.; Verhoest, N.E.C. Absence Reduction in Entomological Surveillance Data to Improve Niche-Based Distribution Models for Culicoides Imicola. Prev. Veter Med.
**2011**, 100, 15–28. [Google Scholar] [CrossRef] [PubMed] - Breiman, L. Random forests. Mach. Learn.
**2001**, 45, 5–32. [Google Scholar] [CrossRef] [Green Version] - Basille, M.; Calenge, C.; Marboutin, E.; Andersen, R.; Gaillard, J. Assessing Habitat Selection Using Multivariate Statistics: Some Refinements of the Ecological-Niche Factor Analysis. Ecol. Model.
**2008**, 211, 233–240. [Google Scholar] [CrossRef] - Phillips, S.J.; Dudík, M. Modeling of Species Distributions with Maxent: New Extensions and a Comprehensive Evaluation. Ecography
**2008**, 31, 161–175. [Google Scholar] [CrossRef]

**Figure 1.**Seroprevalence, entomological, and demographic data. The circles show regional BT seroprevalence based on data collected during the national sero-survey in 2018. The squares show the distribution of the four Culicoides species of interest; the square’s size is proportional to the logarithm of the number of Culicoides collected during the national entomological survey in 2012. The background colors (red and blue) delimit the two pastoral zones with different birth and mortality rates. Dashed lines delimit the six agro-ecological zones in Senegal (Ferlo, Senegal River Valley, Eastern Senegal, Casamance, Groundnut Basin, Niayes), while the thin solids lines identify the administrative regions.

**Figure 2.**Mobility data. On top (

**a**) representation of livestock mobility network, each line corresponds to movements existing between the department, and the color is relative to the number of animals exchanged. The bottom part, departments are colored based on: (

**b**) The incoming volume (number of animals arriving in the department); (

**c**) outgoing volume (number of animals leaving the department), na: data not available.

**Figure 3.**Pictorial representation of the mathematical model. Host dynamics are at the top of the figure, vector dynamics at the bottom.

**Figure 4.**Maps of abundance of the four main Bluetongue virus (BTV) vector species in Senegal: (

**a**) C. imicola; (

**b**) C. oxystoma; (

**c**) C. enderleini, and (

**d**) C. miombo.

**Figure 5.**Transmission maps (${R}_{0}$) (

**a**) realized using temperature-independent parameters; (

**b**) using temperature-dependent parameters.

**Figure 6.**Tornado plot of sensitivity analysis in the 2 cases when parameters used in the model are temperature-independent (

**a**) or temperature-dependent (

**b**). The name of the epidemiological parameters that are varied on shown on the y-axis. The variation in the number of pixels at risk is shown on the x-axis. For each parameter, the bars represent the variation in the number of at risk pixels following a decrease or increase in a parameter value. The color of the bar indicates if the variation in the number of pixels at risk is due to an increase (red) or a decrease (blue) in the corresponding parameter value. The length of the bar is proportional to the variation in the number of pixels at risk (expressed as a percentage).

**Figure 7.**Probability of outbreaks due to the introduction of infected animals. (

**a**) using R

_{0}temperature-independent values, (

**b**) using R

_{0}temperature-dependent values. Livestock movements from infected areas could explain why areas with a low value of R

_{0}could have a high risk of outbreak occurrence. White areas correspond to areas where the outbreak probability has not been estimated because of missing information.

Parameter | Description | Temperature Independent | Temperature-Dependent | ||
---|---|---|---|---|---|

Values | References | Values | References | ||

${d}_{v}$ | Vector mortality rate | 0.16 [0.1–0.5] | [36,37] | $0.009{e}^{0.16T}$ | [36] |

b_{v} | Vector fertility rate | 6.1 eggs/year | [38] | ||

α_{v} | Latency rate for vector | 0.09 [0.06–0.1] | [33,36] | $0.0003T\left(T-10.4\right)$ | [35,36] |

P_{vh} | Transmission Vector-host | 0.9 [0.8–1.0] | [36] | ||

a_{s} | Biting rate | 0.17 [0.05–0.4] | [36] | $0.0002\times T\times \left(T-3.7\right)\times {\left(41.9-T\right)}^{\raisebox{1ex}{$1$}\!\left/ \!\raisebox{-1ex}{$27$}\right.}$ | [36] |

d_{h} | Host mortality rate | 0.0005 (Sylvo-pastoral area) 0.0008 (Agro-pastoral area) | [39] | ||

b_{h} | Host fertility rate | 0.002 (Sylvo-pastoral area) 0.0015 (Agro-pastoral area) | [39] | ||

α_{h} | Latency rate for host | 0.0625 | [33] | ||

r_{h} | Recovery rate for host | 0.125 | [27,36] | ||

d_{h} | Host mortality rate | 0.0005 (Sylvo-pastoral area) 0.0008 (Agro-pastoral area) | [39] | ||

b_{h} | Host fertility rate | 0.002 (Sylvo-pastoral area) 0.0015 (Agro-pastoral area) | [39] | ||

α_{h} | Latency rate for host | 0.0625 | [33] | ||

r_{h} | Recovery rate for host | 0.125 | [27,36] | ||

P_{hv} | Transmission Host Vector | 0.05 [0.001–0.15] | [36,37] | ||

p_{h} | Disease induced mortality | 0.01 [0.001–0.01] | [36] | ||

${\eta}_{h}$ | Rate of immunity loss | 1/90 | [39] |

© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

## Share and Cite

**MDPI and ACS Style**

Gahn, M.C.B.; Niakh, F.; Ciss, M.; Seck, I.; Lo, M.M.; Fall, A.G.; Biteye, B.; Fall, M.; Ndiaye, M.; Ba, A.;
et al. Assessing the Risk of Occurrence of Bluetongue in Senegal. *Microorganisms* **2020**, *8*, 1766.
https://doi.org/10.3390/microorganisms8111766

**AMA Style**

Gahn MCB, Niakh F, Ciss M, Seck I, Lo MM, Fall AG, Biteye B, Fall M, Ndiaye M, Ba A,
et al. Assessing the Risk of Occurrence of Bluetongue in Senegal. *Microorganisms*. 2020; 8(11):1766.
https://doi.org/10.3390/microorganisms8111766

**Chicago/Turabian Style**

Gahn, Marie Cicille Ba, Fallou Niakh, Mamadou Ciss, Ismaila Seck, Modou Moustapha Lo, Assane Gueye Fall, Biram Biteye, Moussa Fall, Mbengué Ndiaye, Aminata Ba,
and et al. 2020. "Assessing the Risk of Occurrence of Bluetongue in Senegal" *Microorganisms* 8, no. 11: 1766.
https://doi.org/10.3390/microorganisms8111766