The role of mathematical modelling in understanding the epidemiology and control of sheep transmissible spongiform encephalopathies: A review

Veterinary Research

Volumn 41, Issue 4, 2010, Pages

  Gubbins, Simon ^a   Touzeau, Suzanne ^b   Hagenaars, Thomas J ^c  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b UR341 National Agronomical Research Institute (INRA)   (France)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Epidemiology; Mathematical modelling; Scrapie; Sheep; Transmissible spongiform encephalopathy

Indexed keywords

BOVINAE; OVIS ARIES;

ANIMAL; ANIMAL DISEASE; BIOLOGICAL MODEL; PRION DISEASE; REVIEW; SHEEP; SHEEP DISEASE;

ANIMALS; MODELS, BIOLOGICAL; PRION DISEASES; SHEEP; SHEEP DISEASES;

EID: 77953833905     PISSN: 09284249     EISSN: 12979716     Source Type: Journal    
DOI: 10.1051/vetres/2010014     Document Type: Article

References (80)

1. Andreoletti O., Lacroux C., Chabert A., Monnereau L., Tabouret G., Lantier F., et al., PrPSc accumulation in placentas of ewes exposed to natural scrapie: influence of foetal PrP genotype and effect on ewe-to-lamb transmission, J. Gen. Virol. (2002) 83:2607-2616.
2. Anonymous, SEAC Subgroup Report: Research and surveillance for TSEs in sheep, SEAC, London, 1999.
3. Baylis M., Chihota C., Stevenson E., Goldmann W., Smith A., Sivam K., et al., Risk of scrapie in British sheep of different prion protein genotypes, J. Gen. Virol. (2004) 85:2735-2740.
4. Benestad S.L., Arsac J.N., Goldmann W., Nöremark M., Atypical/Nor98 scrapie: properties of the agent, genetics and epidemiology, Vet. Res. (2008) 39:19.
5. Bruce M.E., Boyle A., Cousens S., McConnell I., Foster J., Goldmann W., Fraser H., Strain characterisation of natural sheep scrapie and comparison with BSE, J. Gen. Virol. (2002) 83:695-704.
6. Butler D., Doubts over ability to monitor risk of BSE spread to sheep, Nature (1998) 395:6-7.
7. Caughey B., Baron G.S., Prions and their partners in crime, Nature (2006) 443:803-810.
8. de Jong M.C.M., Kimman T.G., Experimental quantification of vaccine-induced reduction in virus transmission, Vaccine (1994) 12:761-766.
9. del Rio Vilas V.J., Guitian J., Pfeiffer D.U., Wilesmith J.W., Analysis of data from the passive surveillance of scrapie in Great Britain between 1993 and 2002, Vet. Rec. (2006) 159:799-804.
10. Detwiler L.A., Scrapie, Rev. Sci. Tech. Off. Int. Epizoot. (1992) 11:491-537.
11. Detwiler L.A., Baylis M., The epidemiology of scrapie, Rev. Sci. Tech. Off. Int. Epizoot. (2003) 22:121-143.
12. Doeschl-Wilson A., Sawalha R., Gubbins S., Villanueva B., Implications of conflicting associations of the prion protein (PrP) gene with scrapie susceptibility and fitness on the persistence of scrapie, PLoS ONE (2009) 4:e7970.
13. Donnelly C.A., Ferguson N.M., Ghani A.C., Anderson R.M., Implications of BSE infection screening data for the scale of the British BSE epidemic and current European infection levels, Proc. R. Soc. Lond. B (2002) 269:2179-2190.
14. Ducrot C., Arnold M., de Koeijer A., Heim D., Calavas D., Review of the epidemiology and dynamics of BSE epidemics, Vet. Res. (2008) 39:15.
15. Durand B., Dubois M.A., Sabatier P., Calavas D., Ducrot C., Van de Wille A., Multiscale modelling of scrapie epidemiology. II. Geographic level: hierarchical transfer of the herd model to regional disease spread, Ecol. Mod. (2004) 179:515-531.
16. Elliot H., Gubbins S., Ryan J., Ryder S., Tongue S., Watkins G., Wilesmith J., Prevalence of scrapie in sheep in Great Britain: estimates from abattoir surveys during 2002 and 2003, Vet. Rec. (2005) 157:418-419. (Pubitemid 41488668)
17. Eloit M., Adjou K., Coulpier M., Fontaine J.J., Hamel R., Lilin T., et al., BSE agent signatures in a goat, Vet. Rec. (2005) 156:523-524.
18. European Commission, Report on the monitoring and testing of ruminants for the presence of transmissible spongiform encephalopathy (TSE) in the EU in 2006, European Commission, Brussels, Belgium, 2007.
19. Fediaevsky A., Tongue S.C., Nöremark M., Calavas D., Ru G., Hopp P., A descriptive study of the prevalence of atypical and classical scrapie in sheep in 20 European countries, BMC Vet. Res. (2008) 4:19.
20. Ferguson N.M., Ghani A.C., Donnelly C.A., Hagenaars T.J., Anderson R.M., Estimating the human health risk from possible BSE infection of the British sheep flock, Nature (2002) 415:420-424.
21. Ferguson N.M., Donnelly C.A., Assessment of the risk posed by bovine spongiform encephalopathy in cattle in Great Britain and the impact of potential changes to current control measures, Proc. R. Soc. Lond. B (2003) 270:1579-1584.
22. Foster J.D., Dickinson A.G., Age at death from natural scrapie in a flock of Suffolk sheep, Vet. Rec. (1989) 125:415-417.
23. Foster J.D., Hope J., Fraser H., Transmission of bovine spongiform encephalopathy to sheep and goats, Vet. Rec. (1993) 133:339-341.
24. Foster J.D., Parnham D., Chong A., Goldmann W., Hunter N., Clinical signs, histopathology and genetics of experimental transmission of BSE and natural scrapie to sheep and goats, Vet. Rec. (2001) 148:165-171.
25. Fryer H., Baylis M., Sivam K., McLean A.R., Quantifying the risk from ovine BSE and the impact of control strategies, Proc. R. Soc. Lond. B (2007) 274:1497-1503.
26. Gonzalez L., Dagleish M.P., Martin S., Dexter G., Steele P., Finlayson J., Jeffrey M., Diagnosis of preclinical scrapie in live sheep by the immunohistochemical examination of rectal biopsies, Vet. Rec. (2008) 162:397-403.
27. Gravenor M.B., Cox D.R., Hoinville L.J., Hoek A., McLean A.R., The flock-to-flock force of infection for scrapie in Britain, Proc. R. Soc. Lond. B (2001) 268:587-592.
28. Gravenor M.B., Papasozomenos P., McLean A.R., Neophytu G., A scrapie epidemic in Cyprus, Epidemiol. Infect. (2004) 132:751-760.
29. Green D.M., del Rio Vilas V.J., Birch C.P.D., Johnson J., Kiss I.Z., McCarthy N.D., Kao R.R., Demographic risk factors for classical and atypical scrapie in Great Britain, J. Gen. Virol. (2007) 88:3486-3492.
30. Gubbins S., Simmons M.M., Sivam K., Webb C.R., Hoinville L.J., Prevalence of scrapie infection in Great Britain: interpreting the results of the 1997-1998 abattoir survey, Proc. R. Soc. Lond. B (2003) 270:1919-1924.
31. Gubbins S., A modelling framework to describe the spread of scrapie between sheep flocks in Great Britain, Prev. Vet. Med. (2005) 67:143-156.
32. Gubbins S., Webb C.R., Simulation of the options for a national control programme to eradicate scrapie from Great Britain, Prev. Vet. Med. (2005) 69:175-187.
33. Gubbins S., Roden J.A., Breeding programmes for TSE resistance in British sheep. II. Assessing the impact on the prevalence and incidence of scrapie, Prev. Vet. Med. (2006) 73:17-31. (Pubitemid 43138756)
34. Gubbins S., Clark A.M., Eglin R.D., Sivam S.K., Results of a postal survey of scrapie in the Shetland Isles in 2003, Vet. Rec. (2006) 158:255-260.
35. Gubbins S., Prevalence of sheep infected with classical scrapie in Great Britain: integrating multiple sources of surveillance data for 2002, J. R. Soc. Interface (2008) 5:1343-1351.
36. Gubbins S., McIntyre K.M., Prevalence of sheep infected with classical scrapie in Great Britain, 1993-2007, Epidemiol. Infect. (2009) 137:787-791.
37. Hagenaars T.J., Donnelly C.A., Ferguson N.M., Anderson R.M., The transmission dynamics of the aetiological agent of scrapie in a sheep flock, Math. Biosci. (2000) 168:117-135.
38. Hagenaars T.J., Ferguson N.M., Donnelly C.A., Anderson R.M., Persistence patterns of scrapie in a sheep flock, Epidemiol. Infect. (2001) 127:157-167.
39. Hagenaars T.J., Donnelly C.A., Ferguson N.M., Anderson R.M., Dynamics of a scrapie outbreak in a flock of Romanov sheep - estimation of transmission parameters, Epidemiol. Infect. (2003) 131:1015-1022.
40. Hagenaars T.J., Donnelly C.A., Ferguson N.M., Epidemiological analysis of data for scrapie in Great Britain, Epidemiol. Infect. (2006) 134:359-367.
41. Healy A.M., Hannon D., Morgan K.L., Weavers E., Collins J.D., Doherty M.L., A paired case-control study of risk factors for scrapie in Irish sheep flocks, Prev. Vet. Med. (2004) 64:73-83.
42. Hoinville L.J., A review of the epidemiology of scrapie in sheep, Rev. Sci. Tech. Off. Int. Epizoot. (1996) 15:827-852.
43. Hopp P., Ulvund M.J., Jarp J., A case-control study on scrapie in Norwegian sheep flocks, Prev. Vet. Med. (2001) 51:183-198.
44. Hopp P., Webb C.R., Jarp J., Monte Carlo simulation of surveillance strategies for scrapie in Norwegian sheep, Prev. Vet. Med. (2003) 61:103-125.
45. Houston F., Goldmann W., Chong A., Jeffrey M., Gonzalez L., Foster J., et al., BSE in sheep bred for resistance to infection, Nature (2003) 423:498.
46. Hunter N., Cairns D., Scrapie-free Merino and Poll Dorset sheep from Australia and New Zealand have normal frequencies of scrapie-susceptible PrP genotypes, J. Gen. Virol. (1998) 79:2079-2082.
47. Hunter N., Scrapie - uncertainties, biology and molecular approaches, Biochim. Biophys. Acta (2007) 1772:619-628.
48. Jeffrey M., Martin S., Thomson J.R., Dingwall W.S., Bagara-McGorum I., Gonzalez L., Onset and distribution of PrP accumulation in scrapie-affected Suffolk sheep as demonstrated by sequential necropsies and tonsillar biopsies, J. Comp. Pathol. (2001) 125:48-57.
49. Jeffrey M., Martin J., Gonzalez L., Foster J., Langeveld J.P.M., van Zijderveld F., et al., Immunohistochemical features of PrPd accumulation in natural and experimental goat transmissible spongiform encephalopathies, J. Comp. Pathol. (2005) 134: 171-181.
50. Kao R.R., Gravenor M.B., McLean A.R., Modelling the national scrapie eradication programme in the UK, Math. Biosci. (2001) 174:61-76.
51. Kao R.R., Gravenor M.B., Baylis M., Bostock C.J., Chihota C.M., Evans J.C., et al., The potential size and duration of an epidemic of bovine spongiform encephalopathy in British sheep, Science (2002) 295:332-335.
52. Kao R.R., Houston F., Baylis M., Chihota C.M., Goldmann W., Gravenor M.B., et al., Epidemiological implications of the susceptibility to BSE of putatively resistant sheep, J. Gen. Virol. (2003) 84:3503-3512.
53. Kao R.R., Green D.M., Johnson J., Kiss I.Z., Disease dynamics over very different time-scales: foot-and-mouth disease and scrapie on the network of livestock movements in the UK, J. R. Soc. Interface (2007) 4:907-916.
54. Konold T., Moore S.J., Bellworthy S.J., Simmons H.A., Evidence of scrapie transmission via milk, BMC Vet. Res. (2008) 4:14.
55. Krebs J.R., May R.M., Stumpf M.P.H., Theoretical models of sheep BSE reveal possibilities, Nature (2002) 415:115.
56. Man W.Y.N., Nicholls N., Woolhouse M.E.J., Lewis R.M., Villanueva B., Evaluating different PrP genotype selection strategies for expected severity of scrapie outbreaks and genetic progress in performance in commercial sheep, Prev. Vet. Med. (2009) 91: 161-171.
57. Matthews L., Woolhouse M.E.J., Hunter N., The basic reproduction number for scrapie, Proc. R. Soc. Lond. B (1999) 266:1085-1090.
58. Matthews L., Coen P.G., Foster J.D., Hunter N., Woolhouse M.E.J., Population dynamics of a scrapie outbreak, Arch. Virol. (2001) 146:1173-1186.
59. McIntyre K.M., Gubbins S., Sivam S.K., Baylis M., Flock-level risk factors for scrapie in Great Britain: analysis of a 2002 anonymous postal survey, BMC Vet. Res. (2006) 2:25.
60. McIntyre K.M., Gubbins S., Goldmann W., Stevenson E., Baylis M., The time-course of a scrapie outbreak, BMC Vet. Res. (2006) 2:20.
61. McIntyre K.M., Gubbins S., Goldmann W., Hunter N., Baylis M., Epidemiological characteristics of classical scrapie outbreaks in 30 sheep flocks in the United Kingdom, PLoS ONE (2008) 3:e3994.
62. McLean A.R., Hoek A., Hoinville L.J., Gravenor M.B., Scrapie transmission in Britain: a recipe for a mathematical model, Proc. R. Soc. Lond. B (1999) 266:2531-2538.
63. Medley G., Predicting the unpredictable, Science (2001) 294:1663-1664.
64. O'Rourke K.I., Duncan J.V., Logan J.R., Anderson A.K., Norden D.K., Williams E.S., et al., Active surveillance for scrapie by third eyelid biopsy and genetic susceptibility testing of flocks of sheep in Wyoming, Clin. Diagn. Lab. Immunol. (2002) 9: 966-971.
65. Ortiz-Pelaez A., del Rio Vilas V.J., Withinholding prevalence of sheep classical scrapie in Great Britain, BMC Vet. Res. (2009) 5:1.
66. Sabatier P., Durand B., Dubois M.A., Ducrot C., Calavas D., Van de Wille A., Multiscale modelling of scrapie epidemiology. I. Herd level: a discrete model of disease transmission in a sheep flock, Ecol. Mod. (2004) 180:233-252.
67. St Rose S.G., Hunter N., Matthews L., Foster J.D., Chase-Topping M.E., Kruuk L.E.B., et al., Comparative evidence for a link between Peyer's patch development and susceptibility to transmissible spongiform encephalopathies, BMC Infect. Dis. (2006) 6:5.
68. Schreuder B.E.C., van Keulen L.J.M., Vromans M.E.W., Langeveld J.P.M., Smits M.A., Tonsillar biopsy and PrPSc detection in the preclinical diagnosis of scrapie, Vet. Rec. (1998) 142:564-568.
69. Stack M.J., Jeffery M., Gubbins S., Grimmer S., Gonzalez L., Martin S., et al., Monitoring for bovine spongiform encephalopathy in sheep in Great Britain, 1998-2004, J. Gen. Virol. (2006) 87:2099-2107.
70. Stamp J.T., Scrapie: a transmissible disease of sheep, Vet. Rec. (1962) 74:357-362.
71. Stringer S.M., Hunter N., Woolhouse M.E.J., A mathematical model of the dynamics of scrapie in a sheep flock, Math. Biosci. (1998) 153:79-98. (Pubitemid 28527372)
72. Sweeney T., Hanrahan J.P., The evidence of associations between prion protein genotype and production, reproduction and health traits in sheep, Vet. Res. (2008) 39:28.
73. Tongue S.C., Pfeiffer D.U., Warner R., Elliott H., del Rio Vilas V.J., Estimation of the relative risk for developing clinical scrapie: the role of prion protein (PrP) genotype and selection bias, Vet. Rec. (2006) 158:43-50.
74. Touzeau S., Chase-Topping M.E., Matthews L., Lajous D., Eychenne F., Hunter N., et al., Modelling the spread of scrapie in a sheep flock: evidence for increased transmission during lambing seasons, Arch. Virol. (2006) 151:735-751.
75. Truscott J.E., Ferguson N.M., Transmission dynamics and mechanisms of endemicity of scrapie in the UK sheep population, Epidemiol. Infect. (2009) 137:762-774.
76. Truscott J.E., Ferguson N.M., Control of scrapie in the UK sheep population, Epidemiol. Infect. (2009) 137:775-786.
77. Van Keulen L.J.M., Vromans M.E.W., van Zijderveld F.G., Early and late pathogenesis of natural scrapie infection in sheep, APMIS (2002) 110:23-32.
78. Webb C.R., Wilesmith J.W., Simmons M.M., Hoinville L.J., A stochastic model to estimate the prevalence of scrapie in Great Britain using the results of an abattoir-based survey, Prev. Vet. Med. (2001) 51:269-287.
79. Woolhouse M.E.J., Stringer S.M., Matthews L., Hunter N., Anderson R.M., Epidemiology and control of scrapie within a sheep flock, Proc. R. Soc. Lond. B (1998) 265:1205-1210. (Pubitemid 28340102)
80. Woolhouse M.E.J., Matthews L., Coen P., Stringer S.M., Foster J.D., Hunter N., Population dynamics of scrapie in a sheep flock, Philos. Trans. R. Soc. Lond. B Biol. Sci. (1999) 354:751-756.