Ovine Disease Resistance: Integrating Comparative and Functional Genomics Approaches in a Genome Information-Poor Species

  • H.W. Raadsma
  • K.J. Fullard
  • N.M. Kingsford
  • E.T. Margawati
  • E. Estuningsih
  • S. Widjayanti
  • Subandriyo, N. Clairoux
  • T.W. Spithill
  • D. Piedrafita
Part of the Stadler Genetics Symposia Series book series (SGSS)

In combination with goats, sheep represent the two most numerous agricultural species for which no cultural or ethical restrictions apply in their use as a source for milk, fibre and red meat. Particularly, in the developing world these species often represent the sole asset base for small-holder livestock farmers. Despite their global significance, genomic tools and approaches in disease resistance have lagged behind the efforts in the economically more influential beef and dairy cattle industries. In particular, infectious diseases have a significant economic impact on livestock production systems worldwide. The most frequently investigated diseases in sheep have focused on the economically important burdens including gastrointestinal nematodes, dermatophilosis, footrot, myiases and fasciolosis. In this study we describe the use of Indonesian Thin Tail sheep (ITT) as a resource which has been shown to have innate and acquired resistance to tropical fasciolosis (Fasciola gigantica∈dexFasciola gigantica). Using the contrast between the resistant ITT and the highly susceptible Merino in a combined functional and comparative genomics approach, we have identified putative QTL (quantitative trait loci) for an extensive panel of parasite and immune response phenotypes and putative resistance pathways and effector molecules. On refinement of candidate gene analyses and effector mechanisms we propose to map these in the economically important target species, namely cattle and buffalo. In addition we exploit the relative susceptibility of ITT sheep to temperate fasciolosis (Fasciola hepatica∈dexFasciola hepatica) to contrast parasite–host interactions and identify parasite immune evasion strategies to boost the discovery of new vaccine candidates and effector pathways, which may be amenable to exogenous control. The study highlights the power and utility of direct gene discovery in ruminant model systems. To overcome the shortage of genomic tools required for such investigations, we have drawn on the development of integrated comparative maps and alignment to the genome information–rich species such as human, murine and recently cattle. Similarly the use of bovine transcriptome tools have shown cross utility in sheep. The only species-specific requirement is the development of genome-wide high resolution SNP mapping tools which are now under development.


Quantitative Trait Locus Quantitative Trait Locus Analysis Packed Cell Volume Quantitative Trait Locus Region Massively Parallel Signature Sequencing 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Axford, R.F.E., Bishop, S.C., Nicholas, F.W., and Owen, J.B., 2000, Genetics of susceptibility to production diseases in cattle and sheep, in R.F.E. Axford, S.C. Bishop, F.W. Nicholas, and J.B. Owen, eds., Breeding for Disease Resistance in Farm Animals, 418pp.Google Scholar
  2. Baker, R.L., Gibson, J.P., Iraqi, F.A., Menge, D.M., Mugambi, J.M., Hanotte, O., Nagda, S., Wakelin, D., and Behnke, J.M., 2003, Exploring the genetic control of resistance to gastrointestinal helminth infections in sheep and mice, Proc. 15th Conf., Assoc. Advan. Anim. Breed. Genet., Melbourne, Australia, 7–11 July 2003, pp. 183–190.Google Scholar
  3. Barillet, F., Arranz, J.J., and Carta, A., 2005, Mapping quantitative trait loci for milk production and genetic polymorphisms of milk proteins in dairy sheep, Genet. Sel. Evol. 37:S109–S123.PubMedCrossRefGoogle Scholar
  4. Barillet, F., Carta, A., Allain, D., Amigues, Y., Bodin, L., Casu, S., Cribiu, E.P., Bed’hom, B., Boichard, D., Boscher, M.Y., Elsen, J.M., Fraghi, A., Gruner, L., Jacquiet, P., Ligios, S., Marie-Etancelin, C., Mura, L., Piredda, G., Roig, A., Rupp, R., Sanna, S.R., Scala, A., Schibler, L., Sechi, T., and Casu, S., 2003, Detection of QTL influencing present and future economic traits in dairy sheep in France and Italy, in 10èemes Rencontres autour des Recherches sur les Ruminants, Institut National de la Recherche Agronomique, Paris, France, 3–4 Décembre 2003, pp. 57–60.Google Scholar
  5. Barthel, R., Feng, J.W., Piedrahita, J.A., McMurray, D.N., Templeton, J.W., and Adams, L.G., 2001, Stable transfection of the bovine NRAMP1 gene into murine RAW264.7 cells: effect on Brucella abortus survival, Infect. Immun. 69:3110–3119.PubMedCrossRefGoogle Scholar
  6. Bayon, Y., Gutierrez-Gil, B., De La Fuente, L.F., San Primitivo Tirados, F., El Zarei, M.F., Alvarez Castelo, L., Arranz, J.J., Perez, J., and Rojo Vasquez, F.A., 2004, Búsqueda de regiones genómicas con influencia sobre la resistencia a las tricostrongilidosis en el ganado ovino de raza churra ITEA, Prod. Anim. 100:197–201.Google Scholar
  7. Beh, K.J., Hulme, D.J., Callaghan, M.J., Leish, Z., Lenane, I., Windon, R.G., and Maddox, J.F., 2002, A genome scan for quantitative trait loci affecting resistance to Trichostrongylus colubriformis in sheep, Anim. Genet. 33:97–106.PubMedCrossRefGoogle Scholar
  8. Benavides, M.V., Weimer, T.A., Borba, M.F.S., Berne, M.E.A., and Sacco, A.M.S., 2002, Association between microsatellite markers of sheep chromosome 5 and faecal egg counts, Small Ruminant Res. 46:97–105.CrossRefGoogle Scholar
  9. Berthier, D., Quere, R., Thevenon, S., Belemsaga, D., Piquemal, D., Marti, J., and Maillard, J.C., 2003, Serial analysis of gene expression (SAGE) in bovine trypanotolerance: preliminary results, Genet. Sel. Evol. 35:S35–S47.PubMedCrossRefGoogle Scholar
  10. Brenig, B., Broad, T.E., Cockett, N.E., and Eggen, A., 2004, Achievements of research in the field of molecular genetics, WAAP Book of the Year, 2003: A Review on Developments and Research in Livestock Systems, Wageningen Universiteit (Wageningen University), Wageningen Netherlands, pp. 73–84.Google Scholar
  11. Butterworth, A.E. 1984. Cell-mediated damage to helminths. Adv. Parasit. 23:143–235.CrossRefGoogle Scholar
  12. Carta, A., Barillet, F., Allain, D., Amigues, B., Bibe, B., Bodin, L., Casu, S., Cribiu, E., Elsen, J.M., Fraghi, A., Gruner, L., Jacuiet, P., Ligios, S., Marie-Etancelin, C., Mura, L., Piredda, G., Rupp, R., Sanna, S.R., Scala, A., Scala, A., Schibler, L., and Casu, S., 2002, QTL Detection with genetic markers in a dairy sheep backcross Sarda × Lacaune Resource Population, Proc. 7th World Congr. Genet. Appl. Livest. Prod. Montpellier, France, August 2002, CD-Rom, Com.No. 09–07.Google Scholar
  13. Cockett, N.E., Shay, T.L., and Smit, M., 2001, Analysis of the sheep genome, Physiol. Genomics 7:69–78.PubMedGoogle Scholar
  14. Coltman, D.W., Wilson, K., Pilkington, J.G., Stear, M.J., and Pemberton, J.M., 2001, A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitized population of Soay sheep, Parasitology 122:571–582.PubMedCrossRefGoogle Scholar
  15. Crawford, A.M., and McEwan, J.C., 1998, Identification of animals resistant to nematode parasite infection New Zealand Provisional Patent 330201, New Zealand, p. 46.Google Scholar
  16. Crawford, A.M., McEwan, J.C., Dodds, K.G., Wright, C.S., Bisset, S.A., Macdonald, P.A., Knowler, K.J., Greer, G.J., Green, R.S., Shaw, R.J., Paterson, K.A., Cuthbertson, R.P., Vlassoff, A., Squire, D.R., West, C.J., and Phua, S.H., 1997a, Resistance to nematode parasites in sheep: how important are the MHC genes? Assoc. Advanc. Anim. Breeding and Genet. Proc. Twelfth Conf., Dubbo, NSW, Australia 6–10 April 1997, Part 1, pp. 58–62.Google Scholar
  17. Crawford, A.M., Phua, S.H., McEwan, J.C., Dodds, K.G., Wright, C.C., Morris, C.A., Bisset, S.A., and Green, R.S., 1997b, Finding disease resistance QTL in sheep, Anim. Biotechnol. 8:13–22.CrossRefGoogle Scholar
  18. Crawford, A.M., Paterson, K.A., Dodds, K.G., Tascon, C.D., Williamson, P.A., Thomson, M.R., Bisset, S.A., Beattie, A.E., Greer, G.J., Green, R.S., Wheeler, R., Shaw, R.J., Knowler, K., and McEwan, J.C., 2006, Discovery of quantitative trait loci for resistance to parasitic nematode infection in sheep: I. Analysis of outcross pedigrees, BMC Genomics 7:2164–2178.CrossRefGoogle Scholar
  19. Davies, G., Stear, M.J., Benothman, M., Abuagob, O., Kerr, A., Mitchell, S., and Bishop, S.C., 2006, Quantitative trait loci associated with parasitic infection in Scottish blackface sheep, Hered. 96:252–258.CrossRefGoogle Scholar
  20. Diez-Tascon, C., Keane, O.M., Wilson, T., Zadissa, A., Hyndman, D.L., Baird, D.B., McEwan, J.C., and Crawford, A.M., 2005, Microarray analysis of selection lines from outbred populations to identify genes involved with nematode parasite resistance in sheep, Physiol. Genomics 21:59–69.PubMedCrossRefGoogle Scholar
  21. Diez-Tascon, C., MacDonald, P.A., Dodds, K.G., McEwan, J.C., and Crawford, A.M., 2002, A screen of chromosome 1 for QTL affecting nematode resistance in an ovine outcross population, Proc. 7th World Congr. Genet. Appl. Livestock Prod., Institut National de la Recherche Agronomique (INRA), Montpellier, France, August 2002, Session 13, pp. 1–4, Communication 37.Google Scholar
  22. Donaldson, L., Vuocolo, T., Gray, C., Strandberg, Y., Reverter, A., McWilliam, S., Wang, Y., Byrne, K., and Tellam, R., 2005, Construction and validation of a Bovine Innate Immune Microarray, BMC Genomics 6:135.PubMedCrossRefGoogle Scholar
  23. Dukkipati, V.S.R., Blair, H.T., Johnson, P.L., Murray, A., and Garrick, D.J., 2005, A study on the association of genotypes at the interferon gamma microsatellite locus with faecal strongyle egg counts in sheep, Proc. 16th Conf. Assoc. Advan. Anim. Breeding Genet., Noosa Lakes, Australia, pp. 119–122.Google Scholar
  24. Elsen, J.M., Moreno, C.R., Bodin, L., François, D., Bouix, J., Barillet, F., Allain, D., Lantier, F., Lantier, I., Schibler, L., Roig, A., Brunel, J.C., and Vitezica, Z.G., 2006, Selectio for scrapie resistance in France, Is there evidence of negative effects on production and health traits?, Proc. 8th World Cong. Genet. Appl. Livestock Prod., Belo Horizonte, MG, Brazil, pp. 15–15.Google Scholar
  25. Fabiyi, J.P., 1987, Production Losses and Control of Helminths in Ruminants of Tropical Regions, Int. J. Parasitol. 17:435–442.PubMedCrossRefGoogle Scholar
  26. Gasbarre, L.C., Sonstegard, T., VanTassell, C.P., and Araujo, R., 2004, Symposium: New approaches in the study of animal parasites, Vet. Parasitol. 125:147–161.CrossRefGoogle Scholar
  27. Gibson, J.R., and Bishop, S.C., 2005, Use of molecular markers to enhance resistance of livestock to disease: a global approach, Rev. Sci. Tech. OIE. 24:343–353.Google Scholar
  28. GLIPHA: Global Livestock Production and Health Atlas Scholar
  29. Gruner, L., Aumont, G., Getachew, T., Brunel, J.C., Pery, C., Cognie, Y., and Guerin, Y., 2003, Experimental infection of Black Belly and INRA 401 straight and crossbred sheep with trichostrongyle nematode parasites, Vet. Parasitol. 116:239–249.PubMedCrossRefGoogle Scholar
  30. Hill, E.W., O’Gorman, G.M., Agaba, M., Gibson, J.P., Hanotte, O., Kemp, S.J., Naessens, J., Coussens, P.M., and MacHugh, D.E., 2005, Understanding bovine trypanosomiasis and trypanotolerance: the promise of functional genomics, Vet. Immun. Immunop. 105:247–258CrossRefGoogle Scholar
  31. Issaq, H.J., Veenstra, T.D., Conrads, T.P., and Felschow, D., 2002, The SELDI-TOF MS approach to proteomics: Protein profiling and biomarker identification, Biochem. Biophys. Res. Commun. 292:587–592.PubMedCrossRefGoogle Scholar
  32. Janssen, M., Weimann, C., Gauly, M., and Erhardt, G., 2002, Associations between infections with Haemonchus contortus and genetic markers on ovine chromosome 20, Proc. 7th World Cong. Genet. Appl. Livestock Prod., Montpellier, France, August 2002, Session 13, pp. 1–4, Communication 11.Google Scholar
  33. Keane, O.M., Zadissa, A., Wilson, T., Hyndman, D.L., Greer, G.J., Baird, D.B., McCulloch, A.F., Crawford, A.M., and McEwan, J.C., 2006, Gene expression profiling of naive sheep genetically resistant and susceptible to gastrointestinal nematodes, BMC Genomics 7:42.PubMedCrossRefGoogle Scholar
  34. Khatkar, M.S., Collins, A., Cavanagh, J.A.L., Hawken, R.J., Hobbs, M., Zenger, K.R., Barris, W., McClintock, A.E., Thomson, P.C., Nicholas, F.W., and Raadsma, H.W., 2006, A first-generation metric linkage disequilibrium map of bovine chromosome 6, Genetics 174:79–85.PubMedCrossRefGoogle Scholar
  35. Khatkar, M.S., Thomson, P.C., Tammen, I., and Raadsma, H.W., 2004, Quantitative trait loci mapping in dairy cattle: review and meta-analysis, Genet. Select. Evol. 36:163–190.CrossRefGoogle Scholar
  36. Lee, H.J., Tokemoto, N., Kurata, H., Kamogawa, Y., Miyatake, S., o’Garra, A., and Arai, N., 2000, GATA-3 induces Thelper cell type 2 (Th_2) cytokine expression and chromatin remodelling in committed Th_i cells, J. Exp. Med. 192:105–115.PubMedCrossRefGoogle Scholar
  37. Li, Y., Miller, J.E., and Franke, D.E., 2001, Epidemiological observation and heterosis of gastrointestinal nematode infection in Suffolk, Gulf Coast Native and crossbred lambs, Vet. Parasitol. 98:273–283.PubMedCrossRefGoogle Scholar
  38. Liao, W., Collins, A., Hobbs, M., Khatkar, M.S., Luo, J., and Nicholas, F.W., 2007, A comparative location database (CompLDB): map integration within and between species, Mamm. Genome 18:287–299.PubMedCrossRefGoogle Scholar
  39. Luhken, G., Stamm, V., Menge, C., and Erhardt, G., 2005, Functional analysis of a single nucleotide polymorphism in a potential binding site for GATA transcription factors in the ovine interleukin 2 gene, Vet. Immun. Immunop. 107:51–56.CrossRefGoogle Scholar
  40. Maddox, J.F., Davies, K.P., Crawford, A.M., Hulme, D.J., Vaiman, D., et al., 2001, An enhanced linkage map of the sheep genome comprising more than 1000 loci, Genome Res. 11:1275–1289.PubMedCrossRefGoogle Scholar
  41. Maizels, R.M., Bundy, D.A.P., Selkirk, M.E., Smith, D.F., and Anderson, R.M., 1993, Immunological modulation and evasion by helminth-parasites in human-populations, Nature 365:797–805.PubMedCrossRefGoogle Scholar
  42. Marshall, K., van der Werf, J.H.J., Maddox, J.F., Graser, H.-U., Zhang, Y., Walkden-Brown, S.W., and Khan, L., 2005, A genome scan for quantitative trait loci for resistance to the gastointestinal parasite Haemonchus contortus in sheep, Proc. Assoc. Advan. Anim. Breed. Genet., Noosa Lakes, Queensland, Australia, pp. 115–118Google Scholar
  43. Meeusen, E.N.T., and Piedrafita, D., 2003, Exploiting natural immunity to helminth parasites for the development of veterinary vaccines, Int. J. Parasitol. 33:1285–1290.PubMedCrossRefGoogle Scholar
  44. Miller, J.E., Cocket, N.E., Walling, G.A., Shay, T.A., McGraw, R.A., Bishop, S.C., and Haley, C.A., 2002, Segregation of resistance to nematode infection in F2 lambs of Suffolk × Gulf Coast Native sheep and associated QTL, Proc. Int. Soc. Anim. Genet., Gottingen, Germany, pp. 160.Google Scholar
  45. Moreno, C.R., Gruner, L., Scala, A., Mura, L., Schibler, L., Amigues, Y., Sechi, T., Jacquiet, P., Francois, D., Sechi, S., Roig, A., Casu, S., Barillet, F., Brunel, J.C., Bouix, J., Carta, A., and Rupp, R., 2006, QTL for resistance to internal parasites in two designs based on natural and experimental conditions of infection, Proc. 8th World Cong. Genet. Appl. Livestock Prod., Belo Horizonte, MG, Brazil, pp. 15–05.Google Scholar
  46. Moreno, C.R., Lantier, F., Berthon, P., Gautier, A.V., Bouchardon, R., Boivin, R., Lantier, I., Brunel, J.-C., Weisbecker, J.-L., François, D., Bouix, J., and Elsen, J.-M., 2003, Genetic parameters for resistance to the salmonella abortosovis vaccinal nstrain RU6 in sheep, Gen. Sel. Evol. 35:199–217.Google Scholar
  47. Nicholas, F.W., 2005, Integrated and comparative maps in livestock genomics, Austr. J. Exper. Agric. 45:1017–1020.CrossRefGoogle Scholar
  48. Overend, D.J., and Bowen, F.L., 1995, Resistance of Fasciola hepatica to Triclabendazole, Aust. Vet. J. 72:275–276.PubMedGoogle Scholar
  49. Paterson, K.A., McEwan, J.C., Dodds, K., Morris, C.A., and Crawford, A.M., 2001, Fine mapping a locus affecting host resistance to internal parasites in sheep, Proc. Assoc. Advan. Anim. Breed. Genet., Queenstown, New Zealand, pp. 91.Google Scholar
  50. Paterson, S., Wilson, K., and Pemberton, J.M., 1998, Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.), Proc. Nat. Acad. Sci. USA 95:3714–3719.PubMedCrossRefGoogle Scholar
  51. Pholpark, M., and Srikitjakarn, L., 1989, The control of parasitism in swamp buffalo and cattle in north-east Thailand, International Seminar on Animal Health and Production Services for Village Livestock, ,l>Khon Kaen, Thailan, pp. 244–249.Google Scholar
  52. Piedrafita, D., Estuningsih, E., Pleasance, J., Prowse, R., Raadsma, H.W., Meeusen E.N.T., and Spithill, T.W., 2007, Peritoneal lavage cells of Indonesian thin-tail sheep mediateantibody-dependent superoxide radical cytotoxicity in vitro against newly excysted juvenile Fasciola gigantica but not juvenile Fasciola hepatica,Infect. Immun. 75:1954–1963.Google Scholar
  53. Piedrafita, D., Parsons, J.C., Sandeman, R.M., Wood, P.R., Estuningsih, S.E., Partoutomo, S., and Spithill, T.W., 2001, Anti body-dependent cell-mediated cytotoxicity to newly excysted juvenile Fasciola hepatica in vitro is mediated by reactive nitrogen intermediates, Parasite Immun. 23:473–482.CrossRefGoogle Scholar
  54. Piedrafita, D., Raadsma, H.W., Prowse, R., and Spithill, T.W., 2004, Immunology of the host-parasite relationship in fasciolosis (Fasciola hepatica and Fasciola gigantica), Can. J. Zoo. 82:233–250.CrossRefGoogle Scholar
  55. Piedrafita, D., Spithill, T.W., Dalton, J.P., Brindley, P.J., Sandeman, M.R., Wood, P.R., and Parsons, J.C., 2000, Juvenile Fasciola hepatica are resistant to killing in vitro by free radicals compared with larvae of Schistosoma mansoni, Parasite Immun. 22:287–295.CrossRefGoogle Scholar
  56. Raadsma, H.W., Margawati, E.T., Piedrafita, D., Estuningsih, E., Widjayanti, S., Beriajaja, Subandriyo, Thomson, P., and Spithill, T., 2002, Towards molecular genetic characterisation of high resistance to internal parasites in Indonesian Thin Tail sheep, Proc. 7th World Cong. Genet. Appl. Livest. Prod., August 2002, Institut National de la Recherche Agronomique (INRA), Montpellier, France, Session 13, pp. 1–4, Communication 18.Google Scholar
  57. Raadsma, H.W., Piedrafita, D., Kingsford, N.M., Fullard, K.J., Margawati, E.T., Estuningsih, E., Widjayanti, S., Subandriyo, Clairoux, N., and Spithill, T., 2005, A functional and comparative genomics approach to characterize the high resistance of Indonesian Thin Tail (ITT) sheep to fasciolosis as a model for ruminants, In Brief and In Depth, CABI Publishing, AgBiotechNet.Google Scholar
  58. Roberts, J.A., Estuningsih, E., Widjayanti, S., Wiedosari, E., Partoutomo, S., and Spithill, T.W., 1997a, Resistance of Indonesian thin tail sheep against Fasciola gigantica and F. hepatica, Vet. Parasitol. 68:69–78.CrossRefGoogle Scholar
  59. Roberts, J.A., Estuningsih, E., Wiedosari, E., and Spithill, T.W., 1997b, Acquisition of resistance against Fasciola gigantica by Indonesian thin tail sheep, Vet. Parasitol. 73:215–224.CrossRefGoogle Scholar
  60. Roberts, J.A., Widjayanti, S., Estuningsih, E., and Hetzel, D.J., 1997c, Evidence for a major gene determining the resistance of Indonesian thin tail sheep against Fasciola gigantica, Vet. Parasitol. 68:309–314.CrossRefGoogle Scholar
  61. Roy, B., and Tandon, V., 1992, Seasonal prevalence of some zoonotic trematode infections in cattle and pigs in the north-east Montane zone in India, Vet. Parasitol. 41:69–76.PubMedCrossRefGoogle Scholar
  62. Sayers, G., Good, B., Hanrahan, J.P., Ryan, M., and Sweeney, T., 2005, Intron 1 of the interferon gamma gene: its role in nematode resistance in Suffolk and Texel sheep breeds, Res. Vet. Sci. 79:191–196.PubMedCrossRefGoogle Scholar
  63. Schillhorn van Veen, T.W., 1980, Fascioliasis (Fasciola gigantica) in West Africa: a review, Vet. Bull. 50:529–533.Google Scholar
  64. Schwerin, M., Czernek-Schafer, D., Goldammer, T., Kata, S.R., Womack, J.E., Pareek, R., Pareek, C., Walawski, K., and Brunner, R.M., 2003, Application of disease-associated differentially expressed genes – Mining for functional candidate genes for mastitis resistance in cattle, Genet. Sel. Evol. 35:S19–S34.PubMedCrossRefGoogle Scholar
  65. Seaton, G., Haley, C.S., Knott, S.A., Kearsey, M., and Visscher, P.M., 2002, QTL Express: mapping quantitative trait loci in of simple and complex pedigrees, Bioinform. 18:339–340.CrossRefGoogle Scholar
  66. Shay, T.L., Miller, J.E., McGraw, R.A., Walling, G.A., Bishop, S.C., Haley, C.A., and Cocket, N.E., 2002, Characterisation of QTL associated with resistance to nematode infection in sheep, Int. Soc. Anim. Genet., Gottingen, Germany, pp. 174.Google Scholar
  67. Soesetya, R.H.B., 1975, The prevalence of Fasciola gigantica infection in cattle in East Java, Indonesia, Malay. Vet. J. 6:5–8.Google Scholar
  68. Spithill, T.W., and Dalton, J.P., 1998, Progress in development of liver fluke vaccines, Parasitol. Today 14:224–228.PubMedCrossRefGoogle Scholar
  69. Spithill, T.W., Piedrafita, D., and Smooker, P.M.,1997, Immunological approaches for the control of fasciolosis, Int. J. Parasitol. 27:1221–1235.Google Scholar
  70. Spithill, T.W., Smooker, P.M., and Copeman, D.B., 1999, Fasciola gigantica: epidemiology, control, immunology and molecular biology, in J.P. Dalton, ed., Fasciolosis, CAB International, Oxford, pp. 465–525.Google Scholar
  71. Stear, M.J., Abuagob, O., Ben Othman, M., and Bishop, S.C., 2006, Major genes and resistance to nematode infection in naturally infected Scottish Blackface lambs, Proc. 8th World Cong. Genet. Appl. Livest. Prod., Belo Horizonte, M.G., Brazil, pp. 15–21.Google Scholar
  72. Sukhapesna, V., Tantasuvan, D., Sarataphan, N., and Imsup, K., 1994, Economic impact of fasciolosis in buffalo production, J. Thai Vet. Med. Assoc. 45:45–52.Google Scholar
  73. Tang, N., Tornatore, P., and Weinberger, S.R., 2004, Current developments in SELDI affinity technology, Mass Spect. Rev. 23:34–44.CrossRefGoogle Scholar
  74. Wiedosari, E., and Copeman, D.B., 1990, High-resistance to experimental-infection with Fasciola gigantica in Javanese thin-tailed sheep, Vet. Parasitol. 37:101–111.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • H.W. Raadsma
    • 1
  • K.J. Fullard
  • N.M. Kingsford
  • E.T. Margawati
  • E. Estuningsih
  • S. Widjayanti
  • Subandriyo, N. Clairoux
  • T.W. Spithill
  • D. Piedrafita
  1. 1.Reprogen-Centre for Advanced Technologies in Animal Genetics and Reproduction, Faculty of Veterinary ScienceUniversity of SydneyAustralia

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