Besnoitia besnoiti; bovine besnoitiosis; cattle; clustering analysis; drivers; expert elicitation; multi-criteria decision analysis (MCDA); sensitivity analysis; Immunology and Allergy; Molecular Biology; Immunology and Microbiology (all); Microbiology (medical); Infectious Diseases; General Immunology and Microbiology
Abstract :
[en] Bovine besnoitiosis (BB) is a chronic and debilitating parasitic disease in cattle caused by the protozoan parasite Besnoitia besnoiti. South European countries are affected and have reported clinical cases of BB. However, BB is considered as emerging in other countries/regions of central, eastern and northern Europe. Yet, data on drivers of emergence of BB in Europe are scarce. In this study, fifty possible drivers of emergence of BB in cattle were identified. A scoring system was developed per driver. Then, the scoring was elicited from eleven recognized European experts to: (i) allocate a score to each driver, (ii) weight the score of drivers within each domain and (iii) weight the different domains among themselves. An overall weighted score was calculated per driver, and drivers were ranked in decreasing order of importance. Regression tree analysis was used to group drivers with comparable likelihoods to play a role in the emergence of BB in cattle in Europe. Finally, robustness testing of expert elicitation was performed for the seven drivers having the highest probability to play a key role in the emergence of BB: i.e., (i) legal/illegal movements of live animals from neighbouring/European Union member states or (ii) from third countries, (iii) risk of showing no clinical sign and silent spread during infection and post infection, (iv) as a consequence, difficulty to detect the emergence, (v) existence of vectors and their potential spread, (vi) European geographical proximity of the pathogen/disease to the country, and (vii) animal density of farms. Provided the limited scientific knowledge on the topic, expert elicitation of knowledge, multi-criteria decision analysis, cluster and sensitivity analyses are very important to prioritize future studies, e.g., the need for quantitative import risk assessment and estimation of the burden of BB to evidence and influence policymaking towards changing (or not) its status as a reportable disease, with prevention and control activities targeting, firstly, the top seven drivers. The present methodology could be applied to other emerging animal diseases.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
Evrard, Julien; Regional Association for Animal Registration and Health (ARSIA) asbl, 5590 Ciney, Belgium
Houtain, Jean-Yves; Regional Association for Animal Registration and Health (ARSIA) asbl, 5590 Ciney, Belgium
Alzieu, Jean-Pierre; Laboratoire Vétérinaire Départemental de l'Ariège (LVD09), 09008 Foix, Ariège, France
Bianchini, Juana ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH)
Mpouam, Serge Eugène; School of Veterinary Medicine and Science, University of Ngaoundere, Ngaoundere P.O. Box 454, Cameroon
Schares, Gereon ; Friedrich-Loeffler-Institut, Bundesforschungsinstitut für Tiergesundheit, Federal Research Institute for Animal Health, 17493 Greifswald, Insel Riems, Germany
Liénard, Emmanuel ; UMR INTHERES/DGER, Ecole Nationale Vétérinaire de Toulouse, CEDEX 03, 31076 Toulouse, France
Jacquiet, Philippe; UMR INRA/DGER IHAP 1225, Ecole Nationale Vétérinaire de Toulouse, CEDEX 03, 31076 Toulouse, France
Villa, Luca ; Department of Veterinary Medicine and Animal Sciences, Università degli Studi di Milano, Via dell'Università 6, 26900 Lodi, Italy
Álvarez-García, Gema ; SALUVET Group, Animal Health Department, Faculty of Veterinary Sciences, Complutense University of Madrid, Ciudad Universitaria s/n, 28040 Madrid, Spain
Gazzonis, Alessia Libera ; Department of Veterinary Medicine and Animal Sciences, Università degli Studi di Milano, Via dell'Università 6, 26900 Lodi, Italy
Gentile, Arcangelo ; Department of Veterinary Medical Sciences, University of Bologna, 40064 Ozzano Emilia, BO, Italy
Delooz, Laurent ; Research Unit of Epidemiology and Risk Analysis Applied to Veterinary Science (UREAR-ULiège), Fundamental and Applied Research for Animals & Health (FARAH) Center, Faculty of Veterinary Medicine, University of Liege, 4000 Liege, Belgium ; Regional Association for Animal Registration and Health (ARSIA) asbl, 5590 Ciney, Belgium
Grisez, C.; Bottari, L.; Prévot, F.; Alzieu, J.-P.; Liénard, E.; Corbière, F.; Rameil, M.; Desclaux, X.; Lacz, C.; Boulon, C.; et al. Real-time PCR on skin biopsies for super-spreaders’ detection in bovine besnoitiosis. Parasites Vectors 2020, 13, 529. https://doi.org/10.1186/s13071-020-04405-7.
Watt, B. Bovine Besnoitiosis, an Emerging Disease. Available online: https://www.ava.com.au/library-resources/library/ava-scientific-journals/acv/2013/bovine-bsnoitiosis-an-emerging-disease/Issue%2068%20Watt.pdf (accessed on 13 December 2021).
Dubey, J.; Sreekumar, C.; Donovan, T.; Rozmanec, M.; Rosenthal, B.; Vianna, M.; Davis, W.; Belden, J. Redescription of Besnoitia bennetti (Protozoa: Apicomplexa) from the donkey (Equus asinus). Int. J. Parasitol. 2005, 35, 659–672. https://doi.org/10.1016/j.ijpara.2005.01.004.
McCully, R.M.; Basson, P.A.; van Niekerk, J.W.; Bigalke, R.D. Observations on Besnoitia cysts in the cardiovascular system of some wild antelopes and domestic cattle. Onderstepoort J. Vet. Res. 1966, 33, 245–276.
Arnal, M.C.; Gutiérrez-Expósito, D.; Martínez-Durán, D.; Regidor-Cerrillo, J.; Revilla, M.; de Luco, D.F.; Jiménez-Meléndez, A.; Ortega-Mora, L.M.; Álvarez-García, G. Systemic Besnoitiosis in a Juvenile Roe Deer (Capreolus capreolus). Transbound. Emerg. Dis. 2016, 64, e8–e14. https://doi.org/10.1111/tbed.12514.
González-Barrio, D.; Köster, P.C.; Habela, M.A.; Martín-Pérez, M.; Fernández-García, J.L.; Balseiro, A.; Barral, M.; Nájera, F.; Figueiredo, A.M.; Palacios, M.J.; et al. Molecular survey of Besnoitia spp. (Apicomplexa) in faeces from European wild meso-carnivores in Spain. Transbound. Emerg. Dis. 2021, 68, 3156–3166. https://doi.org/10.1111/tbed.14206.
Alzieu, J.P.; Cortes, H.; Gottstein, B.; Jacquiet, P.; Dorchies, P.; Schelcher, F.; L’hostis, M. La besnoitiose bovine: Actualités épidé-miologiques et diagnostiques. Bull. G.T.V. Hors Série Parasitol. Bov. Nouv. Approch. 2007, 40, 41–49.
Liénard, E.; Salem, A.; Grisez, C.; Prévot, F.; Bergeaud, J.; Franc, M.; Gottstein, B.; Alzieu, J.; Lagalisse, Y.; Jacquiet, P. A longi-tudinal study of Besnoitia besnoiti infections and seasonal abundance of Stomoxys calcitrans in a dairy cattle farm of southwest France. Veter Parasitol. 2010, 177, 20–27. https://doi.org/10.1016/j.vetpar.2010.11.030.
Liénard, E.; Salem, A.; Jacquiet, P.; Grisez, C.; Prevot, F.; Blanchard, B.; Bouhsira, E.; Franc, M. Development of a protocol testing the ability of Stomoxys calcitrans (Linnaeus, 1758) (Diptera: Muscidae) to transmit Besnoitia besnoiti (Henry, 1913) (Apicomplexa: Sarcocystidae). Parasitol. Res. 2013, 112, 479–486.
Bigalke, R.D. New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field inves-tigations. Onderstepoort J. Veter Res. 1968, 35, 3–137.
Sharif, S.; Jacquiet, P.; Prévot, F.; Grisez, C.; Bouhsira, E.; Franc, M.; Liénard, E. Assessment of persistence of Besnoitia besnoiti (Henry, 1913) bradyzoites in Stomoxys calcitrans (Diptera: Muscidae). Rev. De Med. Vet. 2017, 168, 197-203.
Alzieu, J.P.; Jacquiet, P.; Boulon, C.; Méjan, F.; Desclaux, X.; Prévot, F.; Franc, M.; Rameil, M.; Grisez, C.; Malaveille, R.; et al. La besnoitiose bovine: Actualités physio-pathogéniques, cliniques et épidémiologiques. Bull. Des. GTV 2016, 84, 67–78.
Gutierrez-Exposito, D.; Ferre, I.; Ortega-Mora, L.-M.; Álvarez-García, G. Advances in the diagnosis of bovine besnoitiosis: Cur-rent options and applications for control. Int. J. Parasitol. 2017, 47, 737–751. https://doi.org/10.1016/j.ijpara.2017.08.003.
Villa, L.; Gazzonis, A.L.; Zanzani, S.A.; Perlotti, C.; Sironi, G.; Manfredi, M.T. Bovine besnoitiosis in an endemically infected dairy cattle herd in Italy: Serological and clinical observations, risk factors, and effects on reproductive and productive perfor-mances. Parasitol. Res. 2019, 118, 3459–3468.
European Food Safety Authority. Scientific statement on Bovine besnoitiosis. EFSA J. 2010, 8, 15.
Salem, A.; Bouhsira, E.; Liénard, E.; Bousquet-Mélou, A.; Jacquiet, P.; Franc, M. Susceptibility of two European strains of Stomoxys calcitrans (L.) to cypermethrin, deltamethrin, fenvalerate, lambda-cyhalothrin, permethrin and phoxim. J. Appl. Res. Vet. Med. Vet. Solut. 2012, 10, 249–257. https://hal.inrae.fr/hal-02645910.
Tainchum, K.; Shukri, S.; Duvallet, G.; Etienne, L.; Jacquiet, P. Phenotypic susceptibility to pyrethroids and organophosphate of wild Stomoxys calcitrans (Diptera: Muscidae) populations in southwestern France. Parasitol. Res. 2018, 117, 4027–4032. https://doi.org/10.1007/s00436-018-6109-y.
Mullens, B.A. Chapter 16: Horse flies and deer flies (Tabanidae). In Medical and Veterinary Entomology, 3rd ed.; Mullen, G.R., Durden, L.A., Eds.; Academic Press: London, UK, 2019; pp. 327–343. https://doi.org/10.1016/B978-0-12-814043-7.00016-9.
Duvallet, G.; Boireau, P. Other vector-borne parasitic diseases: Animal helminthiases, bovine besnoitiosis and malaria. Rev. Sci. Tech. Off. Int. Epiz. 2015, 34, 651-658.
Álvarez-García, G.; Frey, C.; Mora, L.M.O.; Schares, G.R.M. A century of bovine besnoitiosis: An unknown disease re-emerging in Europe. Trends Parasitol. 2013, 29, 407–415. https://doi.org/10.1016/j.pt.2013.06.002.
Mutinelli, F.; Schiavon, E.; Ceglie, L.; Fasolato, M.; Natale, A.; Rampin, F.; Carminato, A. Bovine besnoitiosis in imported cattle in Italy. Veter Parasitol. 2010, 178, 198. https://doi.org/10.1016/j.vetpar.2010.12.019.
Gentile, A.; Militerno, G.; Schares, G.R.M.; Nanni, A.; Testoni, S.; Bassi, P.; Gollnick, N. Evidence for bovine besnoitiosis being endemic in Italy—First in vitro isolation of Besnoitia besnoiti from cattle born in Italy. Veter Parasitol. 2012, 184, 108–115. https://doi.org/10.1016/j.vetpar.2011.09.014.
Anastácio, C.; Bexiga, R.; Nolasco, S.; Zúquete, S.; Delgado, I.L.S.; Nunes, T.; Leitão, A. Impact of Endemic Besnoitiosis on the Performance of a Dairy Cattle Herd. Animals 2022, 12, 1291. https://doi.org/10.3390/ani12101291.
Mehlhorn, H.; Klimpel, S.; Schein, E.; Heydorn, A.O.; Al-Quraishy, S.; Selmair, J. Another African disease in Central Europa: Besnoitiosis of cattle. I. Light and electron microscopical study. Parasitol. Res. 2008, 104, 861–868. https://doi.org/10.1007/s00436-008-1267-y.
Lesser, M.; Braun, U.; Deplazes, P.; Gottstein, B.; Hilbe, M.; Basso, W. First cases of besnoitiosis in cattle in Switzerland. Schweiz. Arch. Tierheilkd. 2012, 154, 469–474.
Cortes, H.; Leitão, A.; Gottstein, B.; Hemphill, A. A review on bovine besnoitiosis: A disease with economic impact in herd health management, caused byBesnoitia besnoiti (Franco and Borges). Parasitology 2014, 141, 1406–1417. https://doi.org/10.1017/s0031182014000262.
Ryan, E.G.; Lee, A.; Carty, C.; O’Shaughnessy, J.; Kelly, P.; Cassidy, J.P.; Sheehan, M.; Johnson, A.; de Waal, T. Bovine besnoi-tiosis (Besnoitia besnoiti) in an Irish dairy herd. Veter Rec. 2016, 178, 608–608. https://doi.org/10.1136/vr.103683.
Vanhoudt, A.; Pardon, B.; De Schutter, P.; Bosseler, L.; Sarre, C.; Vercruysse, J.; Deprez, P. First confirmed case of bovine besno-itiosis in an imported bull in Belgium. Vlaams Diergeneeskd. Tijdschr. 2015, 84, 205–211. https://doi.org/10.21825/vdt.v84i4.16596.
Delooz, L.; Evrard, J.; Mpouam, S.E.; Saegerman, C. Emergence of Besnoitia besnoiti in Belgium. Pathogens 2021, 10, 1529. https://doi.org/10.3390/pathogens10121529.
Bianchini, J.; Humblet, M.; Cargnel, M.; Van Der Stede, Y.; Koenen, F.; De Clercq, K.; Saegerman, C. Prioritization of livestock transboundary diseases in Belgium using a multicriteria decision analysis tool based on drivers of emergence. Transbound. Emerg. Dis. 2019, 67, 344–376. https://doi.org/10.1111/tbed.13356.
Saegerman, C.; Bianchini, J.; Snoeck, C.J.; Moreno, A.; Chiapponi, C.; Zohari, S.; Ducatez, M.F. First expert elicitation of knowledge on drivers of emergence of influenza D in Europe. Transbound. Emerg. Dis. 2020, 68, 3349–3359. https://doi.org/10.1111/tbed.13938.
Cox, R.; Sánchez, J.; Revie, C.W. Multi-Criteria Decision Analysis Tools for Prioritising Emerging or Re-Emerging Infectious Diseases Associated with Climate Change in Canada. PLoS ONE 2013, 8, e68338. https://doi.org/10.1371/journal.pone.0068338.
European Centre for Disease Prevention and Control. Best Practices in Ranking Emerging Infectious Disease Threats. A Litera-ture Review. European Centre for Disease Prevention and Control. 2015. Available online: https://ecdc.europa.eu/sites/por-tal/files/media/en/publications/Publi cations/emerging-infectious-disease-threats-best-practices-ranking.pdf (accessed on 1 June 2022).
Avila, L.N.; Gonçalves, V.S.P.; Perez, A.M. Risk of Introduction of Bovine Tuberculosis (TB) Into TB-Free Herds in Southern Bahia, Brazil, Associated with Movement of Live Cattle. Front. Veter Sci. 2018, 5, 230. https://doi.org/10.3389/fvets.2018.00230.
Beltran-Alcrudo, D.; Falco, J.R.; Raizman, E.; Dietze, K. Transboundary spread of pig diseases: The role of international trade and travel. BMC Veter-Res. 2019, 15, 64. https://doi.org/10.1186/s12917-019-1800-5.
Saegerman, C.; Bertagnoli, S.; Meyer, G.; Ganière, J.-P.; Caufour, P.; De Clercq, K.; Jacquiet, P.; Fournié, G.; Hautefeuille, C.; Etore, F.; et al. Risk of introduction of lumpy skin disease in France by the import of vectors in animal trucks. PLoS ONE 2018, 13, e0198506. https://doi.org/10.1371/journal.pone.0198506.
Saegerman, C.; Bertagnoli, S.; Meyer, G.; Ganière, J.-P.; Caufour, P.; De Clercq, K.; Jacquiet, P.; Hautefeuille, C.; Etore, F.; Casal, J.; et al. Risk of introduction of Lumpy Skin Disease into France through imports of cattle. Transbound. Emerg. Dis. 2019, 66, 957– 967. https://doi.org/10.1111/tbed.13111.
Jacquiet, P.; Liénard, E.; Franc, M. Bovine besnoitiosis: Epidemiological and clinical aspects. Veter Parasitol. 2010, 174, 30–36. https://doi.org/10.1016/j.vetpar.2010.08.013.
García-Lunar, P.; Ortega-Mora, L.-M.; Schares, G.; Gollnick, N.S.; Jacquiet, P.; Grisez, C.; Prevot, F.; Frey, C.F.; Gottstein, B.; Álvarez-García, G. An Inter-Laboratory Comparative Study of Serological Tools Employed in the Diagnosis of Besnoitia besnoiti Infection in Bovines. Transbound. Emerg. Dis. 2012, 60, 59–68. https://doi.org/10.1111/j.1865-1682.2012.01318.x.
Schares, G.; Maksimov, A.; Basso, W.; Moré, G.; Dubey, J.; Rosenthal, B.; Majzoub, M.; Rostaher, A.; Selmair, J.; Langenmayer, M.; et al. Quantitative real time polymerase chain reaction assays for the sensitive detection of Besnoitia besnoiti infection in cattle. Veter Parasitol. 2011, 178, 208–216. https://doi.org/10.1016/j.vetpar.2011.01.038.
OIE. Terrestrial Animal Health Code. Criteria for the Inclusion of Diseases, Infections and Infestations in the OIE list. Chapter 1.2. Available online: https://www.oie.int/fileadmin/Home/eng/Health_standards/tahc/2018/en_chapitre_criteria_dis-eases.htm#chapitre_criteria_diseases (accessed on 12 December 2021).
Waap, H.; Nunes, T.; Cortes, H.; Leitão, A.; Vaz, Y. Prevalence and geographic distribution of Besnoitia besnoiti infection in cattle herds in Portugal. Parasitol. Res. 2014, 113, 3703–3711. https://doi.org/10.1007/s00436-014-4035-1.
Waap, H.; Nunes, T.; Vaz, Y.; Leitão, A. Serological survey of Toxoplasma gondii and Besnoitia besnoiti in a wildlife conservation area in southern Portugal. Veter Parasitol. Reg. Stud. Rep. 2016, 3–4, 7–12. https://doi.org/10.1016/j.vprsr.2016.05.003.
Gutierrez-Exposito, D.; Arnal, M.C.; Martínez-Durán, D.; Cerrillo, J.R.; Revilla, M.; de Luco, D.L.F.; Jiménez-Meléndez, A.; Ber-nal, R.C.; Habela, M.A.; García-Bocanegra, I.; et al. The role of wild ruminants as reservoirs of Besnoitia besnoiti infection in cattle. Veter Parasitol. 2016, 223, 7–13. https://doi.org/10.1016/j.vetpar.2016.04.005.
Humblet, M.-F.; Losson, B.; Saegerman, C. Integrated Management of Blood-Feeding Arthropods in Veterinary Teaching Facil-ities—Part 1: Overview of Haematophagous Arthropods of Interest in North-Western Europe. Rev. Sci. Tech. 2020, 39, 737–756. Available online: www.oie.int/app/uploads/2021/12/06122021-00190-en-humblet-1-ang.pdf (accessed on 9 December 2021).
Humblet, M.-F.; Losson, B.; Saegerman, C. Integrated Management of Blood-Feeding Arthropods in Veterinary Teaching Facil-ities—Part 2: Overview of Control Methods against Adults and Immature Stages. Rev. Sci. Tech. 2020, 39, 757–777. Available online: www.oie.int/app/uploads/2021/12/07122021-00191-en-humblet-2-ang.pdf (accessed on 9 December 2021).
Humblet, M.-F.; Losson, B.; Saegerman, C. Integrated Management of Blood-Feeding Arthropods in Veterinary Teaching Facil-ities—Part 3: Proposal for a Coherent and Affordable Control Plan. Rev. Sci. Tech. 2020, 39, 779–793. Available online: www.oie.int/app/uploads/2021/12/09122021-00192-en-humblet-3-ang.pdf (accessed on 9 December 2021).
Gore, S.M. Biostatistics and the Medical Research Council. MRC News 1987, 35, 19–20.