Where are the horses? With the sheep or cows? Uncertain host location, vector-feeding preferences and the risk of African horse sickness transmission in Great Britain.
Abstract: Understanding the influence of non-susceptible hosts on vector-borne disease transmission is an important epidemiological problem. However, investigation of its impact can be complicated by uncertainty in the location of the hosts. Estimating the risk of transmission of African horse sickness (AHS) in Great Britain (GB), a virus transmitted by Culicoides biting midges, provides an insightful example because: (i) the patterns of risk are expected to be influenced by the presence of non-susceptible vertebrate hosts (cattle and sheep) and (ii) incomplete information on the spatial distribution of horses is available because the GB National Equine Database records owner, rather than horse, locations. Here, we combine land-use data with available horse owner distributions and, using a Bayesian approach, infer a realistic distribution for the location of horses. We estimate the risk of an outbreak of AHS in GB, using the basic reproduction number (R0), and demonstrate that mapping owner addresses as a proxy for horse location significantly underestimates the risk. We clarify the role of non-susceptible vertebrate hosts by showing that the risk of disease in the presence of many hosts (susceptible and non-susceptible) can be ultimately reduced to two fundamental factors: first, the abundance of vectors and how this depends on host density, and, second, the differential feeding preference of vectors among animal species.
Publication Date: 2013-04-17 PubMed ID: 23594817PubMed Central: PMC3645429DOI: 10.1098/rsif.2013.0194Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
- African Horse Sickness
- Animal Science
- Animal Species
- Animal Studies
- Bayesian Analysis
- Culicoides
- Diagnosis
- Disease control
- Disease Diagnosis
- Disease Etiology
- Disease Outbreaks
- Disease Transmission
- Epidemiology
- Equine Health
- Horses
- Infectious Disease
- Public Health
- Risk Factors
- Vector-borne disease
- Veterinary Medicine
- Wildlife
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research article attempts to assess the risk of transmission of African horse sickness (AHS) in Great Britain by estimating horse locations using land-use data and the distribution of horse owners, and factoring in the role of non-susceptible vertebrate hosts such as cattle and sheep. Results indicate that using owner addresses as a proxy for horse location can underestimate the risk of AHS transmission.
Understanding the Study
- The study addresses the complex epidemiological issue of understanding the influence of non-susceptible hosts, in this case cattle and sheep, on the transmission of vector-borne diseases, exemplified here by African horse sickness (AHS).
- The complexity is further heightened by uncertainty in the spatial distribution of the hosts, which is the horses in this case.
- The backgrounds to this study are that, (i) the patterns of AHS risk in Great Britain are expected to influence due to non-susceptible hosts, and (ii) inaccurate information on horse distribution because the GB National Equine Database records the locations of horse owners and not the horses.
Methodology and Key Findings
- The researchers used a combination of land-use data and the known distributions of horse owners to infer a more accurate distribution of horses in GB.
- A Bayesian approach, which is a method of statistical inference, was used for the estimation.
- Proponents then used the ‘basic reproduction number’ (R0), which is a term used in epidemiology to denote the expected number of cases directly generated by one case in a population, to estimate AHS outbreak risks in Great Britain.
- The study found that if the locations of the horse owners were used as proxies for the locations of the horses, the risk of AHS transmission would be significantly underestimated.
- The role of the non-susceptible hosts, cattle and sheep, was elucidated, showing that the risk of the disease over many hosts, both susceptible and non-susceptible, could be boiled down to two factors- the abundance of vectors (the Culicoides biting midges) and the dependency of this abundance on host density, and the differential feeding preference of vectors among animal species.
Cite This Article
APA
Lo Iacono G, Robin CA, Newton JR, Gubbins S, Wood JL.
(2013).
Where are the horses? With the sheep or cows? Uncertain host location, vector-feeding preferences and the risk of African horse sickness transmission in Great Britain.
J R Soc Interface, 10(83), 20130194.
https://doi.org/10.1098/rsif.2013.0194 Publication
Researcher Affiliations
- Disease Dynamics Unit, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK. gl334@cam.ac.uk
MeSH Terms
- African Horse Sickness / epidemiology
- African Horse Sickness / prevention & control
- African Horse Sickness / transmission
- Animals
- Cattle / virology
- Ceratopogonidae / physiology
- Ceratopogonidae / virology
- Communicable Disease Control
- Feeding Behavior
- Geography
- Horses / virology
- Insect Vectors / physiology
- Insect Vectors / virology
- Risk Factors
- Seasons
- Sheep / virology
- United Kingdom / epidemiology
- Vaccination / veterinary
- Viral Vaccines / therapeutic use
Grant Funding
- Biotechnology and Biological Sciences Research Council
References
This article includes 57 references
- Tildesley MJ, House TA, Bruhn MC, Curry RJ, O'Neil M, Allpress JLE, Smith G, Keeling MJ. Impact of spatial clustering on disease transmission and optimal control. Proc. Natl Acad. Sci. USA 104, 1041–1046.
- Hay SI, Noor AM, Nelson A, Tatem AJ. The accuracy of human population maps for public health application. Trop. Med. Int. Health 10, 1073–1086.
- Tatem AJ, Noor AM, von Hagen C, Di Gregorio A, Hay SI. High resolution population maps for low income nations: combining land cover and census in East Africa. PLoS ONE 2, e1298.
- Riley S. Coping without farm location data during a foot-and-mouth outbreak. Proc. Natl Acad. Sci. USA 107, 957–958.
- Brockmann D, Hufnagel L, Geisel T. The scaling laws of human travel. Nature 439, 462–465.
- Bharti N, Tatem AJ, Ferrari MJ, Grais RF, Djibo A, Grenfell BT. Explaining seasonal fluctuations of measles in Niger using nighttime lights imagery. Science 334, 1424–1427.
- Eagle N, Pentland A. Reality mining: sensing complex social systems. Pers. Ubiquitous Comput. 10, 255–268.
- Robin C, Lo Iacono G, Gubbins S, Wood J, Newton J. The accuracy of the National Equine Database in relation to vector-borne disease risk modelling of horses in Great Britain. Equine Vet. J. 32, 1–7.
- Saegerman C, Berkvens D, Mellor PS. Bluetongue epidemiology in the European Union. Emerg. Infect. Dis. 14, 539–544.
- Wilson AJ, Mellor PS. Bluetongue in Europe: past, present and future. Phil. Trans. R. Soc. B 364, 2669–2681.
- European Food Safety Authority. ‘Schmallenberg’ virus: analysis of the epidemiological data and impact assessment. EFSA J. 10, 2768–2857.
- Hoffmann B. Novel orthobunyavirus in cattle, Europe, 2011. Emerg. Infect. Dis. 18, 469–472.
- Velthuis AGJ, Saatkamp HW, Mourits MCM, de Koeijer AA, Elbers ARW. Financial consequences of the Dutch bluetongue serotype 8 epidemics of 2006 and 2007. Prev. Vet. Med. 93, 294–304.
- Dominguez M, Hendrikx P, Zientara S, Calavas D, Jaÿ M, Touratier A, Languille J, Fediaevsky A. Preliminary estimate of Schmallenberg virus infection impact in sheep flocks: France. Vet. Rec. 171, 426.
- Hanon J, Uyttenhoef A, Fecher-Bourgeois F, Humblet M, Kirschvink N, Haubruge E, Duquesne B, Saegerman C. Quantitative estimation of economical losses consecutive to the 2006–2007 bluetongue epidemics in Wallonia. In Proc. 13th Int. Symp. on Veterinary Epidemiology and Economics, Maastricht, The Netherlands, 20–24 August 2012, p. 81.
- Nevill EM. The use of cattle to protect sheep from bluetongue infection. J. S. Afr. Vet. Assoc. 49, 129–130.
- Diekmann O, Heesterbeek JAP. Mathematical epidemiology of infectious diseases: model building, analysis and interpretation. New York, NY: Wiley.
- Gubbins S, Carpenter S, Baylis M, Wood J, Mellor P. 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 5, 363–371.
- Robin CA, Wylie CE, Wood JLN, Newton JR. Making use of equine population demography for disease control purposes: preliminary observations on the difficulties of counting and locating horses in Great Britain. Equine Vet. J. 43, 372–375.
- Boden LA, Parkin TDH, Yates J, Mellor D, Kao RR. Summary of current knowledge of the size and spatial distribution of the horse population within Great Britain. BMC Vet. Res. 8, 43.
- Fuller R, Smith G, Sanderson J, Hill R, Thomson A. The UK Land Cover Map 2000: construction of a parcel-based vector map from satellite images. Cartographic J. 39, 15–25.
- Park JH, Quinn KM, Martin AD. MCMCpack: Markov chain Monte Carlo in R. J. Stat. Software 42, 323.
- Geyer CJ. An MCMC package for R. Des. Issues 1, 1–7.
- Hartemink NA, Purse BV, Meiswinkel R, Brown HE, de Koeijer A, Elbers ARW, Boenderd G-J, Rogersc DJ, Heesterbeeka JAP. Mapping the basic reproduction number (R0) for vector-borne diseases: a case study on bluetongue virus. Epidemics 1, 153–161.
- Carpenter S, Wilson A, Barber J, Veronesi E, Mellor P, Venter G, Gubbins S. Temperature dependence of the extrinsic incubation period of orbiviruses in Culicoides biting midges. PLoS ONE 6, e27987.
- Baylis M, O'Connell L, Mellor PS. Rates of bluetongue virus transmission between Culicoides sonorensis and sheep. Med. Vet. Entomol. 22, 228–237.
- Backer JA, Nodelijk G. Transmission and control of African horse sickness in the Netherlands: a model analysis. PLoS ONE 6, e23066.
- Venter GJ, Wright IM, Paweska JT. A comparison of the susceptibility of the biting midge Culicoides imicola to infection with recent and historical isolates of African horse sickness virus. Med. Vet. Entomol. 24, 324–328.
- Mullens B, Gerry AC, Lysyk TJ, Schmidtmann ET. Environmental effects on vector competence and virogenesis of bluetongue virus in Culicoides: interpreting laboratory data in a field context. Vet. Ital. 40, 160–166.
- Mellor PS, Hamblin C. African horse sickness. Vet. Res. 35, 445–466.
- Gerry AC, Mullens BA, Maclachlan NJ, Mecham JO. Seasonal transmission of bluetongue virus by Culicoides sonorensis (Diptera: Ceratopogonidae) at a southern California dairy and evaluation of vectorial capacity as a predictor of bluetongue virus transmission. J. Med. Entomol. 38, 197–209.
- Meiswinkel R, Baldet T, de Deken R, Takken W, Delécolle JC, Mellor PS. The 2006 outbreak of bluetongue in northern Europe–the entomological perspective. Prev. Vet. Med. 87, 55–63.
- Gerry AC, Mullens BA. Seasonal abundance and survivorship of Culicoides sonorensis (Diptera: Ceratopogonidae) at a southern California dairy, with reference to potential bluetongue virus transmission and persistence. J. Med. Entomol. 37, 675–688.
- Sanders CJ, Shortall CR, Gubbins S, Burgin L, Gloster J, Harrington R, Reynolds DR, Mellor PS, Carpenter S. Influence of season and meteorological parameters on flight activity of Culicoides biting midges in the United Kingdom. J. Appl. Ecol. 48, 1355–1364.
- Anderson RM, May RM. Infectious diseases of humans: dynamics and control. Oxford, UK: Oxford University Press.
- Lord CC, Woolhouse MEJ, Heesterbeek JAP, Mellor PS. Vector-borne diseases and the basic reproduction number: a case study of African horse sickness. Med. Vet. Entomol. 10, 19–28.
- Lord CC, Woolhouse MEJ, Rawlings P, Mellor PS. Simulation studies of African horse sickness and Culicoides imicola (Diptera: Ceratopogonidae). J. Med. Entomol. 33, 328–338.
- Lord CC, Woolhouse MEJ, Mellor PS. Simulation studies of vaccination strategies in African horse sickness. Vaccine 15, 519–524.
- Purse BV, Mellor PS, Rogers DJ, Samuel AR, Mertens PPC, Baylis M. Climate change and the recent emergence of bluetongue in Europe. Nat. Rev. Microbiol. 3, 171–181.
- Viennet E. Assessment of vector/host contact: comparison of animal-baited traps and UV-light/suction trap for collecting Culicoides biting midges (Diptera: Ceratopogonidae), vectors of Orbiviruses. Parasites Vectors 4, 119.
- van der Rijt R, van den Boom R, Jongema Y, van Oldruitenborgh-Oosterbaan MMS. Culicoides species attracted to horses with and without insect hypersensitivity. Vet. J. 178, 91–97.
- Scheffer EG, Venter GJ, Labuschagne K, Page PC, Mullens BA, MacLachlan NJ, Osterriederh N, Guthrie AJ. Comparison of two trapping methods for Culicoides biting midges and determination of African horse sickness virus prevalence in midge populations at Onderstepoort, South Africa. Vet. Parasite 185, 265–273.
- Zimmer JY. Breeding sites of bluetongue vectors in northern Europe. Vet. Rec. 162, 131.
- Zimmer JY, Saegerman C, Losson B, Haubruge E. Breeding sites of bluetongue virus vectors, Belgium. Emerg. Infect. Dis. 16, 575–576.
- Garcia-Saenz A, McCarter P, Baylis M. The influence of host number on the attraction of biting midges. Culicoides spp, to light traps. Med. Vet. Entomol. 25, 113–115.
- Bartsch S, Bauer B, Wiemann A, Clausen PH, Steuber S. Feeding patterns of biting midges of the Culicoides obsoletus and Culicoides pulicaris groups on selected farms in Brandenburg, Germany. Parasite Res. 105, 373–380.
- Ninio C, Augot D, Delecolle JC, Dufour B, Depaquit J. Contribution to the knowledge of Culicoides (Diptera: Ceratopogonidae) host preferences in France. Parasite Res. 108, 657–663.
- Lassen SB, Nielsen S, Skovgård H, Kristensen M. Molecular identification of bloodmeals from biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasite Res. 108, 823–829.
- Garros C, Gardès L, Allène X, Rakotoarivony I, Viennet E, Rossi S, Balenghien T. Adaptation of a species-specific multiplex PCR assay for the identification of blood meal source in Culicoides (Ceratopogonidae: Diptera): applications on Palaearctic biting midge species, vectors of Orbiviruses. Infect. Gen. Evol. 11, 1103–1110.
- Guthrie AJ. Protective immunization of horses with a recombinant canarypox virus vectored vaccine co-expressing genes encoding the outer capsid proteins of African horse sickness virus. Vaccine 27, 4434–4438.
- Scanlen M, Paweska J, Verschoor J, van Dijk A. The protective efficacy of a recombinant VP2-based African horsesickness subunit vaccine candidate is determined by adjuvant. Vaccine 20, 1079–1088.
- Roy P, Bishop DHL, Howard S, Aitchison H, Erasmus B. Recombinant baculovirus-synthesized African horsesickness virus (AHSV) outer-capsid protein VP2 provides protection against virulent AHSV challenge. J. Gen. Virol. 77, 2053–2057.
- Weyer CT, Quan M, Joone C, Lourens CW, Maclachlan NJ, Guthrie AJ. African horse sickness in naturally infected, immunised horses. Equine Vet. J. 45, 117–119.
- Sedda L, Brown HE, Purse BV, Burgin L, Gloster J, Rogers DJ. A new algorithm quantifies the roles of wind and midge flight activity in the bluetongue epizootic in northwest Europe. Proc. R. Soc. B 279, 2354–2362.
- Barbu CM. The effects of city streets on an urban disease vector. PLoS Comput. Biol. 9, e1002801.
- de Vos CJ, Hoek CA, Nodelijk G. Risk of introducing African horse sickness virus into the Netherlands by international equine movements. Prev. Vet. Med. 106, 108–122.
- HMSO. The African Horse Sickness (England) Regulations 2012. Statutory Instruments no. 2629.
Citations
This article has been cited 22 times.- Mojsiejczuk L, Whitlock F, Chen H, Magill C, Aranday-Cortes E, Bone J, Tong L, Da Silva Filipe A, Bryant N, Newton JR, Chambers TM, Reedy SE, Nemoto M, Yamanaka T, Hughes J, Murcia PR. Multiple introductions of equine influenza virus into the United Kingdom resulted in widespread outbreaks and lineage replacement. PLoS Pathog 2025 Jun;21(6):e1013227.
- Archana M, Nayankumar, Sundarraj R, Mruthyunjaya AG, Ghosal T, Mazumdar A, Hemadri D, Sengupta PP, Prasad M, Reddy YN, Yarabolu KR, Ummer J, Misri J, Rahman H, Shome BR, Shivachandra SB, Chanda MM. Abundance and Diversity of Culicoides Species (Diptera: Ceratopogonidae) in Different Forest Landscapes of Karnataka, India: Implications for Culicoides Borne Diseases. Transbound Emerg Dis 2023;2023:6250963.
- Gubbins S. Using the basic reproduction ratio to quantify transmission and identify data gaps for epizootic haemorrhagic disease virus. R Soc Open Sci 2024 Oct;11(10):241217.
- Elbers ARW, Gonzales JL. Culicoides (Diptera: Ceratopogonidae) Abundance Is Influenced by Livestock Host Species and Distance to Hosts at the Micro Landscape Scale. Insects 2023 Jul 14;14(7).
- Lee EC, Arab A, Colizza V, Bansal S. Spatial aggregation choice in the era of digital and administrative surveillance data. PLOS Digit Health 2022 Jun;1(6):e0000039.
- Nelson E, Thurston W, Pearce-Kelly P, Jenkins H, Cameron M, Carpenter S, Guthrie A, England M. A Qualitative Risk Assessment for Bluetongue Disease and African Horse Sickness: The Risk of Entry and Exposure at a UK Zoo. Viruses 2022 Feb 28;14(3).
- de Vos CJ, Hennen WHGJ, van Roermund HJW, Dhollander S, Fischer EAJ, de Koeijer AA. Assessing the introduction risk of vector-borne animal diseases for the Netherlands using MINTRISK: A Model for INTegrated RISK assessment. PLoS One 2021;16(11):e0259466.
- Thongsripong P, Hyman JM, Kapan DD, Bennett SN. Human-Mosquito Contact: A Missing Link in Our Understanding of Mosquito-Borne Disease Transmission Dynamics. Ann Entomol Soc Am 2021 Jul;114(4):397-414.
- More S, Bicout D, Bøtner A, Butterworth A, Calistri P, De Koeijer A, Depner K, Edwards S, Garin-Bastuji B, Good M, Gortazar Schmidt C, Michel V, Miranda MA, Nielsen SS, Raj M, Sihvonen L, Spoolder H, Thulke HH, Velarde A, Willeberg P, Winckler C, Bau A, Beltran-Beck B, Carnesecchi E, Casier P, Czwienczek E, Dhollander S, Georgiadis M, Gogin A, Pasinato L, Richardson J, Riolo F, Rossi G, Watts M, Lima E, Stegeman JA. Vector-borne diseases. EFSA J 2017 May;15(5):e04793.
- Bessell PR, Auty HK, Roberts H, McKendrick IJ, Bronsvoort BMC, Boden LA. A Tool for Prioritizing Livestock Disease Threats to Scotland. Front Vet Sci 2020;7:223.
- England ME, Pearce-Kelly P, Brugman VA, King S, Gubbins S, Sach F, Sanders CJ, Masters NJ, Denison E, Carpenter S. Culicoides species composition and molecular identification of host blood meals at two zoos in the UK. Parasit Vectors 2020 Mar 16;13(1):139.
- Porphyre T, Grewar JD. Assessing the potential of plains zebra to maintain African horse sickness in the Western Cape Province, South Africa. PLoS One 2019;14(10):e0222366.
- Lo Iacono G, Cunningham AA, Bett B, Grace D, Redding DW, Wood JLN. Environmental limits of Rift Valley fever revealed using ecoepidemiological mechanistic models. Proc Natl Acad Sci U S A 2018 Jul 31;115(31):E7448-E7456.
- Lo Iacono G, Armstrong B, Fleming LE, Elson R, Kovats S, Vardoulakis S, Nichols GL. Challenges in developing methods for quantifying the effects of weather and climate on water-associated diseases: A systematic review. PLoS Negl Trop Dis 2017 Jun;11(6):e0005659.
- Chapman GE, Archer D, Torr S, Solomon T, Baylis M. Potential vectors of equine arboviruses in the UK. Vet Rec 2017 Jan 7;180(1):19.
- Zhang Z, Manjourides J, Cohen T, Hu Y, Jiang Q. Spatial measurement errors in the field of spatial epidemiology. Int J Health Geogr 2016 Jul 1;15(1):21.
- Baker T, Carpenter S, Gubbins S, Newton R, Lo Iacono G, Wood J, Harrup LE. Can insecticide-treated netting provide protection for Equids from Culicoides biting midges in the United Kingdom?. Parasit Vectors 2015 Nov 25;8:604.
- Faverjon C, Leblond A, Hendrikx P, Balenghien T, de Vos CJ, Fischer EA, de Koeijer AA. A spatiotemporal model to assess the introduction risk of African horse sickness by import of animals and vectors in France. BMC Vet Res 2015 Jun 4;11:127.
- Guichard S, Guis H, Tran A, Garros C, Balenghien T, Kriticos DJ. Worldwide niche and future potential distribution of Culicoides imicola, a major vector of bluetongue and African horse sickness viruses. PLoS One 2014;9(11):e112491.
- Bessell PR, Auty HK, Searle KR, Handel IG, Purse BV, de C Bronsvoort BM. Impact of temperature, feeding preference and vaccination on Schmallenberg virus transmission in Scotland. Sci Rep 2014 Jul 18;4:5746.
- Thompson GM, Jess S, Gordon AW, Murchie AK. Sticky-trapping biting midges (Culicoides spp.) alighting on cattle and sheep: effects of trap colour and evidence for host preference. Parasitol Res 2014 Aug;113(8):3085-94.
- Gubbins S, Turner J, Baylis M, van der Stede Y, van Schaik G, Abrahantes JC, Wilson AJ. Inferences about the transmission of Schmallenberg virus within and between farms. Prev Vet Med 2014 Oct 15;116(4):380-90.
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