1887

Abstract

In Europe and Asia, Ixodid ticks transmit tick-borne encephalitis virus (TBEV), a flavivirus that causes severe encephalitis in humans but appears to show no virulence for livestock and wildlife. In the British Isles, where TBEV is absent, a closely related tick-borne flavivirus, named louping ill virus (LIV), is present. However, unlike TBEV, LIV causes a febrile illness in sheep, cattle, grouse and some other species, that can progress to fatal encephalitis. The disease is detected predominantly in animals from upland areas of the UK and Ireland. This distribution is closely associated with the presence of its arthropod vector, the hard tick . The virus is a positive-strand RNA virus belonging to the genus , exhibiting a high degree of genetic homology to TBEV and other mammalian tick-borne viruses. In addition to causing acute encephalomyelitis in sheep, other mammals and some avian species, the virus is recognized as a zoonotic agent with occasional reports of seropositive individuals, particularly those whose occupation involves contact with sheep. Preventative vaccination in sheep is effective although there is no treatment for disease. Surveillance for LIV in Great Britain is limited despite an increased awareness of emerging arthropod-borne diseases and potential changes in distribution and epidemiology. This review provides an overview of LIV and highlights areas where further effort is needed to control this disease.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.062356-0
2014-05-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/5/1005.html?itemId=/content/journal/jgv/10.1099/vir.0.062356-0&mimeType=html&fmt=ahah

References

  1. Adam K. M., Beasley S. J., Blewett D. A. 1977; The occurrence of antibody to Babesia and to the virus of louping-ill in deer in Scotland. Res Vet Sci 23:133–138[PubMed]
    [Google Scholar]
  2. Balseiro A., Royo L. J., Martínez C. P., Fernández de Mera I. G., Höfle Ú., Polledo L., Marreros N., Casais R., Marín J. F. 2012; Louping ill in goats, Spain, 2011. Emerg Infect Dis 18:976–978 [View Article][PubMed]
    [Google Scholar]
  3. Bannatyne C. C., Wilson R. L., Reid H. W., Buxton D., Pow I. 1980; Louping-ill virus infection of pigs. Vet Rec 106:13 [View Article][PubMed]
    [Google Scholar]
  4. Benavides J., Willoughby K., Underwood C., Newman B., Mitchell G., Carty H. 2011; Encephalitis and neuronal necrosis in a 3-month-old suckled beef calf. Vet Pathol 48:E1–E4 [View Article][PubMed]
    [Google Scholar]
  5. Bertrand Y., Töpel M., Elväng A., Melik W., Johansson M. 2012; First dating of a recombination event in mammalian tick-borne flaviviruses. PLoS ONE 7:e31981 [View Article][PubMed]
    [Google Scholar]
  6. Brotherston J. G., Boyce J. B. 1970; Development of a non-infective protective antigen against louping-ill (arbovirus group B). Laboratory experiments. J Comp Pathol 80:377–388 [View Article][PubMed]
    [Google Scholar]
  7. Brownlee A., Wilson D. R. 1932; Studies of the histopathology of louping ill. J Comp Pathol Ther 45:67–92 [View Article]
    [Google Scholar]
  8. Calisher C. H., Karabatsos N., Zeller H., Digoutte J. P., Tesh R. B., Shope R. E., Travassos da Rosa A. P., St George T. D. 1989; Antigenic relationships among rhabdoviruses from vertebrates and hematophagous arthropods. Intervirology 30:241–257[PubMed]
    [Google Scholar]
  9. Cranwell M. P., Josephson M., Willoughby K., Marriott L. 2008; Louping ill in an alpaca. Vet Rec 162:28 [View Article][PubMed]
    [Google Scholar]
  10. Davidson M. M., Williams H., Macleod J. A. J. 1991; Louping ill in man: a forgotten disease. J Infect 23:241–249 [View Article][PubMed]
    [Google Scholar]
  11. Davison K. L., Crowcroft N. S., Ramsay M. E., Brown D. W. G., Andrews N. J. 2003; Viral encephalitis in England, 1989–1998: what did we miss?. Emerg Infect Dis 9:234–240 [View Article][PubMed]
    [Google Scholar]
  12. Doherty P. C., Reid H. W. 1971a; Experimental louping-ill in sheep and lambs: II. Neuropathology. J Comp Pathol 81:331–337 [View Article][PubMed]
    [Google Scholar]
  13. Doherty P. C., Reid H. W. 1971b; Louping-ill encephalomyelitis in the sheep: II. Distribution of virus and lesions in nervous tissue. J Comp Pathol 81:531–536 [View Article][PubMed]
    [Google Scholar]
  14. Fleeton M. N., Sheahan B. J., Gould E. A., Atkins G. J., Liljeström P. 1999; Recombinant Semliki Forest virus particles encoding the prME or NS1 proteins of louping ill virus protect mice from lethal challenge. J Gen Virol 80:1189–1198[PubMed]
    [Google Scholar]
  15. Fleeton M. N., Liljeström P., Sheahan B. J., Atkins G. J. 2000; Recombinant Semliki Forest virus particles expressing louping ill virus antigens induce a better protective response than plasmid-based DNA vaccines or an inactivated whole particle vaccine. J Gen Virol 81:749–758[PubMed]
    [Google Scholar]
  16. Fletcher J. M. 1937; Louping-ill in the horse. Vet Rec 49:17–18
    [Google Scholar]
  17. Gao G. F., Hussain M. H., Reid H. W., Gould E. A. 1993a; Classification of a new member of the TBE flavivirus subgroup by its immunological, pathogenetic and molecular characteristics: identification of subgroup-specific pentapeptides. Virus Res 30:129–144 [View Article][PubMed]
    [Google Scholar]
  18. Gao G. F., Jiang W. R., Hussain M. H., Venugopal K., Gritsun T. S., Reid H. W., Gould E. A. 1993b; Sequencing and antigenic studies of a Norwegian virus isolated from encephalomyelitic sheep confirm the existence of louping ill virus outside Great Britain and Ireland. J Gen Virol 74:109–114 [View Article][PubMed]
    [Google Scholar]
  19. Gao G. F., Zanotto P. M. de A., Holmes E. C., Reid H. W., Gould E. A. 1997; Molecular variation, evolution and geographical distribution of louping ill virus. Acta Virol 41:259–268[PubMed]
    [Google Scholar]
  20. Gaunt M. W., Jones L. D., Laurenson K., Hudson P. J., Reid H. W., Gould E. A. 1997; Definitive identification of louping ill virus by RT-PCR and sequencing in field populations of Ixodes ricinus on the Lochindorb estate. Arch Virol 142:1181–1191 [View Article][PubMed]
    [Google Scholar]
  21. Gilbert L., Jones L. D., Hudson P. J., Gould E. A., Reid H. W. 2000; Role of small mammals in the persistence of louping-ill virus: field survey and tick co-feeding studies. Med Vet Entomol 14:277–282 [View Article][PubMed]
    [Google Scholar]
  22. Gilbert L., Jones L. D., Laurenson M. K., Gould E. A., Reid H. W., Hudson P. J. 2004; Ticks need not bite their red grouse hosts to infect them with louping ill virus. Proc Biol Sci 271:Suppl. 4S202–S205 [View Article][PubMed]
    [Google Scholar]
  23. Gould E. A., Moss S. R., Turner S. L. 2004; Evolution and dispersal of encephalitic flaviviruses. Arch Virol Suppl 18:65–84[PubMed]
    [Google Scholar]
  24. Grard G., Moureau G., Charrel R. N., Lemasson J.-J., Gonzalez J.-P., Gallian P., Gritsun T. S., Holmes E. C., Gould E. A., de Lamballerie X. 2007; Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy. Virology 361:80–92 [View Article][PubMed]
    [Google Scholar]
  25. Gray D., Webster K., Berry J. E. 1988; Evidence of louping ill and tick-borne fever in goats. Vet Rec 122:66 [View Article][PubMed]
    [Google Scholar]
  26. Gray J. S. 1991; The development and seasonal activity of the tick Ixodes ricinus: vector of Lyme borreliosis. Rev. Med. Vet. Entomol. 79:323–333 http://www.cabdirect.org/abstracts/19910506476.html
    [Google Scholar]
  27. Greig J. R., Brownlee A., Wilson D. R., Gordon W. S. 1931; The nature of louping ill. Vet Rec 11:325–333
    [Google Scholar]
  28. Gritsun T. S., Venugopal K., Zanotto P. M., Mikhailov M. V., Sall A. A., Holmes E. C., Polkinghorne I., Frolova T. V., Pogodina V. V. other authors 1997; Complete sequence of two tick-borne flaviviruses isolated from Siberia and the UK: analysis and significance of the 5′ and 3′-UTRs. Virus Res 49:27–39 [View Article][PubMed]
    [Google Scholar]
  29. Gritsun T. S., Lashkevich V. A., Gould E. A. 2003a; Tick-borne encephalitis. Antiviral Res 57:129–146 [View Article][PubMed]
    [Google Scholar]
  30. Gritsun T. S., Nuttall P. A., Gould E. A. 2003b; Tick-borne flaviviruses. Adv Virus Res 61:317–371 [View Article][PubMed]
    [Google Scholar]
  31. Health Protection Agency (now Public Health England) 2011; Louping ill virus general information data sheet. [Last updated 14 June 2011]. http://www.hpa.org.uk/Topics/InfectiousDiseases/InfectionsAZ/LoupingIll/GeneralInformation/ Accessed 18 April 2013
    [Google Scholar]
  32. Hudson P. J., Norman R., Laurenson M. K., Newborn D., Gaunt M., Jones L., Reid H., Gould E., Bowers R., Dobson A. 1995; Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping-ill virus in red grouse populations. Parasitology 111:Suppl.S49–S58 [View Article][PubMed]
    [Google Scholar]
  33. Hyde J., Nettleton P., Marriott L., Willoughby K. 2007; Louping ill in horses. Vet Rec 160:532 [View Article][PubMed]
    [Google Scholar]
  34. Jensen P. M., Skarphedinsson S., Semenov A. 2004; [Densities of the tick (Ixodes ricinus) and coexistence of the louping ill virus and tick borne encephalitis virus on the island of Bornholm]. Ugeskr Laeger 166:2563–2565 [in Danish] [PubMed]
    [Google Scholar]
  35. Johnson N., Wakeley P. R., Mansfield K. L., McCracken F., Haxton B., Phipps L. P., Fooks A. R. 2010; Assessment of a novel real-time pan-flavivirus RT-polymerase chain reaction. Vector Borne Zoonotic Dis 10:665–671 [View Article][PubMed]
    [Google Scholar]
  36. Johnson N., Voller K., Phipps L. P., Mansfield K., Fooks A. R. 2012; Rapid molecular detection methods for arboviruses of livestock of importance to northern Europe. J Biomed Biotechnol 2012:719402 [View Article][PubMed]
    [Google Scholar]
  37. Jones L. D., Gaunt M., Hails R. S., Laurenson K., Hudson P. J., Reid H., Henbest P., Gould E. A. 1997; Transmission of louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Med Vet Entomol 11:172–176 [View Article][PubMed]
    [Google Scholar]
  38. Krueger N., Reid H. W. 1994; Detection of louping ill virus in formalin-fixed, paraffin wax-embedded tissues of mice, sheep and a pig by the avidin-biotin-complex immunoperoxidase technique. Vet Rec 135:224–225 [View Article][PubMed]
    [Google Scholar]
  39. Labuda M., Danielova V., Jones L. D., Nuttall P. A. 1993; Amplification of tick-borne encephalitis virus infection during co-feeding of ticks. Med Vet Entomol 7:339–342 [View Article][PubMed]
    [Google Scholar]
  40. Laurenson M. K., Norman R. A., Gilbert L., Reid H. W., Hudson P. J. 2003; Identifying disease reservoirs in complex systems: mountain hares as reservoirs of ticks and louping-ill virus, pathogens of red grouse. J Anim Ecol 72:177–185 [View Article]
    [Google Scholar]
  41. Laurenson M. K., McKendrick I. J., Reid H. W., Challenor R., Mathewson G. K. 2007; Prevalence, spatial distribution and the effect of control measures on louping-ill virus in the Forest of Bowland, Lancashire. Epidemiol Infect 135:963–973 [View Article][PubMed]
    [Google Scholar]
  42. Lawson J. H., Manderson W. G., Weston Hurst E. 1949; Louping-ill meningo-encephalitis: a further case and a serological survey. Lancet 254:696–699 [View Article][PubMed]
    [Google Scholar]
  43. Macaldowie C., Patterson I. A. P., Nettleton P. F., Low H., Buxton D. 2005; Louping ill in llamas (Lama glama) in the Hebrides. Vet Rec 156:420–421[PubMed] [CrossRef]
    [Google Scholar]
  44. MacKenzie C. P., Lewis N. D., Smith S. T., Muir R. W. 1973; Louping-ill in a working collie. Vet Rec 92:354–356 [View Article][PubMed]
    [Google Scholar]
  45. MacLeod J. 1935; Ixodes ricinus in relation to its physical environment: II. The factors governing survival and activity. Parasitology 27:123–144 [View Article]
    [Google Scholar]
  46. Macleod J., Gordon W. S. 1932; Studies in louping ill: II. Transmission by the sheep tick, Ixodes ricinus L. J Comp Pathol Ther 45:240–252 [View Article]
    [Google Scholar]
  47. Mansfield K. L., Johnson N., Phipps L. P., Stephenson J. R., Fooks A. R., Solomon T. 2009; Tick-borne encephalitis virus – a review of an emerging zoonosis. J Gen Virol 90:1781–1794 [View Article][PubMed]
    [Google Scholar]
  48. Mansfield K. L., Horton D. L., Johnson N., Li L., Barrett A. D. T., Smith D. J., Galbraith S. E., Solomon T., Fooks A. R. 2011; Flavivirus-induced antibody cross-reactivity. J Gen Virol 92:2821–2829 [View Article][PubMed]
    [Google Scholar]
  49. Marin M. S., McKenzie J., Gao G. F., Reid H. W., Antoniadis A., Gould E. A. 1995; The virus causing encephalomyelitis in sheep in Spain: a new member of the tick-borne encephalitis group. Res Vet Sci 58:11–13 [View Article][PubMed]
    [Google Scholar]
  50. Marriott L., Willoughby K., Chianini F., Dagleish M. P., Scholes S., Robinson A. C., Gould E. A., Nettleton P. F. 2006; Detection of Louping ill virus in clinical specimens from mammals and birds using TaqMan RT-PCR. J Virol Methods 137:21–28 [View Article][PubMed]
    [Google Scholar]
  51. Marston D. A., Mansfield K. L., Mearns R., Ellis R. J., Fooks A. R., Johnson N. 2013; Louping ill virus genome sequence derived from the spinal cord of an infected lamb. Genome Announc 1:e00454-e13 [View Article][PubMed]
    [Google Scholar]
  52. McGuire K., Holmes E. C., Gao G. F., Reid H. W., Gould E. A. 1998; Tracing the origins of louping ill virus by molecular phylogenetic analysis. J Gen Virol 79:981–988[PubMed]
    [Google Scholar]
  53. Moseley M. H., Marriott L., Nettleton P., Dukes J., Irvine R. J., Mougeot F. 2007; Use of real-time RT-PCR to determine the prevalence of louping ill virus in live red grouse chicks. Vet Rec 161:660–661 [View Article][PubMed]
    [Google Scholar]
  54. Norberg P., Roth A., Bergström T. 2013; Genetic recombination of tick-borne flaviviruses among wild-type strains. Virology 440:105–116 [View Article][PubMed]
    [Google Scholar]
  55. Orlinger K. K., Hofmeister Y., Fritz R., Holzer G. W., Falkner F. G., Unger B., Loew-Baselli A., Poellabauer E. M., Ehrlich H. J. other authors 2011; A tick-borne encephalitis virus vaccine based on the European prototype strain induces broadly reactive cross-neutralizing antibodies in humans. J Infect Dis 203:1556–1564 [View Article][PubMed]
    [Google Scholar]
  56. Papa A., Pavlidou V., Antoniadis A. 2008; Greek goat encephalitis virus strain isolated from Ixodes ricinus, Greece. Emerg Infect Dis 14:330–332 [View Article][PubMed]
    [Google Scholar]
  57. Patel P., Landt O., Kaiser M., Faye O., Koppe T., Lass U., Sall A. A., Niedrig M. 2013; Development of one-step quantitative reverse transcription PCR for the rapid detection of flaviviruses. Virol J 10:58 [View Article][PubMed]
    [Google Scholar]
  58. Porter R., Norman R. A., Gilbert L. 2013; A model to test how ticks and louping ill virus can be controlled by treating red grouse with acaricide. Med Vet Entomol 27:237–246 [View Article][PubMed]
    [Google Scholar]
  59. Randolph S. E., Green R. M., Hoodless A. N., Peacey M. F. 2002; An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus . Int J Parasitol 32:979–989 [View Article][PubMed]
    [Google Scholar]
  60. Reid H. W. 1975; Experimental infection of red grouse with louping-ill virus (Flavivirus group): I. The viraemia and antibody response. J Comp Pathol 85:223–229 [View Article][PubMed]
    [Google Scholar]
  61. Reid H. 1984; Epidemiology of louping-ill. In Vectors in Virus Biology pp. 161–178 Edited by Mayo M. A., Harrap K. A. London: Academic Press;
    [Google Scholar]
  62. Reid H. W. 1991; Louping Ill. In Practice 13:157–160 [View Article][PubMed]
    [Google Scholar]
  63. Reid H. W. 2011; Louping ill (ovine encephalomyelitis): etiology and transmission. The Merck Veterinary Manual. [Last full review/revision July 2011] http://www.merckmanuals.com/vet/nervous_system/louping_ill_ovine_encephalomyelitis/overview_of_louping_ill.html Accessed 19 April 2013
    [Google Scholar]
  64. Reid H. W., Boyce J. B. 1974; Louping-ill virus in red grouse in Scotland. Vet Rec 95:150 [View Article][PubMed]
    [Google Scholar]
  65. Reid H. W., Chianini F. 2007; Louping ill. In Diseases of Sheep, 4th edn. pp. 250–255 Edited by Aitken I. D. Oxford: Blackwell Publishing; [View Article]
    [Google Scholar]
  66. Reid H. W., Doherty P. C. 1971; Experimental louping-ill in sheep and lambs: I. Viraemia and the antibody response. J Comp Pathol 81:291–298 [View Article][PubMed]
    [Google Scholar]
  67. Reid H. W., Gibbs C. A., Burrells C., Doherty P. C. 1972; Laboratory infections with louping-ill virus. Lancet 299:592–593 [View Article][PubMed]
    [Google Scholar]
  68. Reid H. W., Barlow R. M., Boyce J. B. 1976; Isolation of louping-ill virus from a roe deer (Capreolus capreolus). Vet Rec 98:116 [View Article][PubMed]
    [Google Scholar]
  69. Reid H. W., Barlow R. M., Pow I. 1978a; Isolation of louping-ill virus from red deer (Cervus elaphus). Vet Rec 102:463–464 [View Article][PubMed]
    [Google Scholar]
  70. Reid H. W., Duncan J. S., Phillips J. D. P., Moss R., Watson A. 1978b; Studies of louping-ill virus (Flavivirus group) in wild red grouse (Lagopus lagopus scoticus). J Hyg (Lond) 81:321–329 [View Article][PubMed]
    [Google Scholar]
  71. Reid H. W., Buxton D., Pow I., Brodie T. A., Holmes P. H., Urquhart G. M. 1986; Response of sheep to experimental concurrent infection with tick-borne fever (Cytoecetes phagocytophila) and louping-ill virus. Res Vet Sci 41:56–62[PubMed]
    [Google Scholar]
  72. Rivers T. M., Schwentker F. F. 1934; Louping ill in man. J Exp Med 59:669–685 [View Article][PubMed]
    [Google Scholar]
  73. Ross H. M., Evans C. C., Spence J. A., Reid H. W., Krueger N. 1994; Louping ill in free-ranging pigs. Vet Rec 134:99–100 [View Article][PubMed]
    [Google Scholar]
  74. Sargison N. 2008 Sheep Flock Health: A Planned Approach Oxford: Blackwell Publishing; [View Article]
    [Google Scholar]
  75. Shaw B., Reid H. W. 1981; Immune responses of sheep to louping-ill virus vaccine. Vet Rec 109:529–531[PubMed]
    [Google Scholar]
  76. Sheahan B. J., Moore M., Atkins G. J. 2002; The pathogenicity of louping ill virus for mice and lambs. J Comp Pathol 126:137–146 [View Article][PubMed]
    [Google Scholar]
  77. Simpson E., Schock A., Nettleton P. F., Holliman A., Watson P. J., Scholes S. F. 2003; Ovine louping ill encephalitis: Lesion mapping and antigen distribution. In European Society of Veterinary Pathology, 21st Annual Meeting, Dublin, 2003
    [Google Scholar]
  78. Smith C. E., McMahon D. A., O’Reilly K. J., Wilson A. L., Robertson J. M. 1964a; The epidemiology of louping ill in Ayrshire: the first year of studies in sheep. J Hyg (Lond) 62:53–68 [View Article][PubMed]
    [Google Scholar]
  79. Smith C. E., Varma M. G., McMahon D. 1964b; Isolation of louping ill from small mammals in Ayrshire, Scotland. Nature 203:992–993 [View Article][PubMed]
    [Google Scholar]
  80. Stockman S. 1918; Louping-ill. J. Comp. Pathol. Therap. 31:137–193 [View Article]
    [Google Scholar]
  81. Timoney P. J., Donnelly W. J., Clements L. O., Fenlon M. 1976; Encephalitis caused by louping ill virus in a group of horses in Ireland. Equine Vet J 8:113–117 [View Article][PubMed]
    [Google Scholar]
  82. Twomey D. F., Cranwell M. P., Reid H. W., Tan J. F. V. 2001; Louping ill on Dartmoor. Vet Rec 149:687[PubMed]
    [Google Scholar]
  83. Walkington J., Hulgur M., Yates D. 2013; A case of refractory seizures caused by an unusual zoonosis. J Intensive Care Soc 14:65–67 http://journal.ics.ac.uk/pdf/1401065.pdf [CrossRef]
    [Google Scholar]
  84. Whitby J. E., Whitby S. N., Jennings A. D., Stephenson J. R., Barrett A. D. T. 1993; Nucleotide sequence of the envelope protein of a Turkish isolate of tick-borne encephalitis (TBE) virus is distinct from other viruses of the TBE virus complex. J Gen Virol 74:921–924 [View Article][PubMed]
    [Google Scholar]
  85. Williams H., Thorburn H. 1962; Serum antibodies to louping-ill virus. Scott Med J 7:353–355[PubMed]
    [Google Scholar]
  86. Williams H., Thorburn H., Ziffo G. S. 1963; Isolation of louping ill from the red grouse. Nature 200:193–194 [View Article][PubMed]
    [Google Scholar]
  87. Zanotto P. M. de A., Gao G. F., Gritsun T., Marin M. S., Jiang W. R., Venugopal K., Reid H. W., Gould E. A. 1995; An arbovirus cline across the northern hemisphere. Virology 210:152–159 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.062356-0
Loading
/content/journal/jgv/10.1099/vir.0.062356-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error