Relationships between immune indicators of parasitic gastroenteritis, nematode burdens and faecal dry matter in sheep
A. R. Williams A E F , D. G. Palmer B , I. H. Williams A , P. E. Vercoe A , D. L. Emery C and L. J. E. Karlsson DA School of Animal Biology, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B Department of Agriculture and Food Western Australia, 3 Baron-Hay Court, South Perth, WA 6151, Australia.
C Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2000, Australia.
D Department of Agriculture and Food Western Australia, 10 Dore Street, Katanning, WA 6317, Australia.
E Present address: The Jenner Institute, University of Oxford, Oxford OX3 7DQ, UK.
F Corresponding author. Email: arwilliams@graduate.uwa.edu.au
Animal Production Science 50(3) 219-227 https://doi.org/10.1071/AN09144
Submitted: 31 October 2009 Accepted: 1 March 2010 Published: 8 April 2010
Abstract
Immune-mediated scouring in sheep is a mucosal hypersensitivity response caused by ingesting infective parasite larvae. In this experiment we tested the hypothesis that levels of parasite-specific antibodies and also interleukin-5 (IL-5) would be negatively correlated with worm numbers, but also faecal dry matter (FDM), in parasite-resistant Merino sheep. Forty Merino rams were challenged with Trichostrongylus colubriformis and Teladorsagia circumcincta larvae every day for 6 weeks, after which they were euthanised and total worm burdens determined. Faecal samples were taken for measurement of worm egg counts and FDM. Serum was collected from the rams before and after the larval challenge commenced, and levels of ovine immunoglobulin light chain, IgG, IgM, IgA and IgE specific for T. colubriformis and T. circumcincta as well as IL-5 were determined by sandwich enzyme-linked immunosorbent assay. IL-5 and all serum antibodies apart from T. colubriformis-specific light chain were significantly increased by the larval challenge. However, none of the antibodies, or IL-5, was correlated with FDM. Negative correlations were observed between the number of adult T. circumcincta and antibody levels; however, there was little relationship between antibodies and numbers of T. colubriformis. It was concluded that serum antibody levels are a poor indicator of the susceptibility of sheep to immune-mediated scouring. Because of these results, sheep breeders should continue to select for low worm egg count and focus on phenotypic indicators of scouring, such as dags, as a means to reduce diarrhoea.
Acknowledgements
The authors are very grateful to Phil Stein, Novartis Animal Health Australia, for supplying infective larvae. Staff at Mt Barker research station and Shenton Park field station are acknowledged for care of the animals. This work was supported by the Australian government and Australian woolgrowers through Australian Wool Innovation Ltd.
Athanasiadou S,
Pemberton A,
Jackson F,
Inglis N,
Miller HRP,
Thevenod F,
MacKellar A, Huntley JF
(2008) Proteomic approach to identify candidate effector molecules during the in vitro immune exclusion of infective Teladorsagia circumcincta in the abomasum of sheep. Veterinary Research 39, 58.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Barger IA,
Le Jambre LF,
Georgi JR, Davies HI
(1985) Regulation of Haemonchus contortus populations in sheep exposed to continuous infection. International Journal for Parasitology 15, 529–533.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Beh KJ
(1987) Production and characterisation of monoclonal antibodies specific for sheep IgG subclasses IgG1 or IgG2. Veterinary Immunology and Immunopathology 14, 187–196.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Beh KJ
(1988) Monoclonal antibodies against sheep immunoglobulin light chain, IgM and IgA. Veterinary Immunology and Immunopathology 18, 19–27.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bendixsen T,
Windon RG,
Huntley JF,
MacKellar A,
Davey RJ,
McClure SJ, Emery DL
(2004) Development of a new monoclonal antibody to ovine chimeric IgE and its detection of systemic and local IgE antibody responses to the intestinal nematode Trichostrongylus colubriformis. Veterinary Immunology and Immunopathology 97, 11–24.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Beraldi D,
Craig BH,
Bishop SC,
Hopkins J, Pemberton JM
(2008) Phenotypic analysis of host-parasite interactions in lambs infected with Teladorsagia circumcincta. International Journal for Parasitology 38, 1567–1577.
| Crossref | GoogleScholarGoogle Scholar |
Bisset SA,
Vlassoff A,
Douch PGC,
Jonas WE,
West CJ, Green RS
(1996) Nematode burdens and immunological responses following natural challenge in Romney lambs selectively bred for low of high faecal worm egg count. Veterinary Parasitology 61, 249–263.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Doligalska M,
Moskwa B, Stear MJ
(1999) Relationships among peripheral eosinophilia, eosinophil peroxidise activity, interleukin-5 concentration and faecal nematode egg count during natural, mixed gastrointestinal nematode infection. Veterinary Immunology and Immunopathology 70, 299–308.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Douch PGC,
Green RS,
Morris CA,
Bisset SA,
Vlassoff A,
Baker RL,
Watson TG,
Hurford AP, Wheeler M
(1995) Genetic and phenotypic relationships among anti-Trichostrongylus colubriformis antibody level, faecal egg count and body weight traits in grazing Romney sheep. Livestock Production Science 41, 121–132.
| Crossref | GoogleScholarGoogle Scholar |
Emery DL
(1996) Vaccination against worm parasites of animals. Veterinary Parasitology 64, 31–45.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Emery DL,
Bendixsen T, McClure SJ
(1991) The use of electroblotted antigens of Trichostrongylus colubriformis to induce proliferative responses in sensitised lymphocytes from sheep. International Journal for Parasitology 21, 179–185.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Emery DL,
McClure SJ,
Wagland BM, Jones WO
(1992) Studies of stage-specific immunity against Trichostrongylus colubriformis in sheep: immunisation by normal and truncated infections. International Journal for Parasitology 22, 215–220.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gisbert JP, McNicholl AG
(2009) Questions and answers on the role of faecal calprotectin as a biological marker in inflammatory bowel disease. Digestive and Liver Disease 41, 56–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gounni AS,
Lamkhloued B,
Ochiai K,
Tanaka Y,
Delaporte E,
Capron A,
Kinet JP, Capron M
(1994) High-affinity IgE receptor on eosinophils is involved in defence against parasites. Nature 367, 183–186.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gray GD,
Barger IA,
Le Jambre LF, Douch PGC
(1992) Parasitological and immunological responses of genetically resistant Merino sheep on pastures contaminated with parasitic nematodes. International Journal for Parasitology 22, 417–425.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Greeff JC, Karlsson LJE
(2006) Breeding for worm resistance – whole farm benefits. International Journal of Sheep and Wool Science 54, 7–14.
Harrison GBL,
Pulford HD,
Doolin EE,
Pernthaner A,
Shoemaker CB, Hein WR
(2008) Antibodies to surface epitopes of the carbohydrate larval antigen CarLA are associated with passive protection in strongylid nematode challenge infections. Parasite Immunology 30, 577–584.
| PubMed |
Henderson NG, Stear MJ
(2006) Eosinophil and IgA responses in sheep infected with Teladorsagia circumcincta. Veterinary Immunology and Immunopathology 112, 62–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jackson F, Miller JE
(2006) Alternative approaches to control – Quo Vadit? Veterinary Parasitology 139, 371–384.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Karlsson LJE, Greeff JC
(2006) Selection response in faecal worm egg counts in the Rylington Merino parasite-resistant flock. Australian Journal of Experimental Agriculture 46, 809–811.
| Crossref | GoogleScholarGoogle Scholar |
Karlsson LJE,
Pollott GE,
Eady SJ,
Bell A, Greeff JC
(2004) Relationship between faecal worm egg counts and scouring in Australian Merino sheep. Animal Production in Australia 25, 100–103.
Larsen JWA,
Anderson N,
Vizard AL,
Anderson GA, Hoste H
(1994) Diarrhoea in Merino ewes during winter: association with trichostrongylid larvae. Australian Veterinary Journal 71, 365–372.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Larsen JWA,
Vizard AL, Anderson N
(1995) Production losses in Merino ewes and financial penalties caused by trichostrongylid infections during winter and spring. Australian Veterinary Journal 72, 58–63.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Larsen JWA,
Anderson N, Vizard AL
(1999) The pathogenesis and control of diarrhoea and breech soiling in adult Merino sheep. International Journal for Parasitology 29, 893–902.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
MacKinnon KM,
Burton JL,
Zajac AM, Notter DR
(2009) Microarray analysis reveals difference in gene expression profiles of hair and wool sheep infected with Haemonchus contortus. Veterinary Immunology and Immunopathology 130, 210–220.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Meeusen ENT
(1999) Immunology of helminth infections, with special reference to immunopathology. Veterinary Parasitology 84, 259–273.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pollott GE,
Karlsson LJE,
Eady SJ, Greeff JC
(2004) Genetic parameters for indicators of host resistance to parasites from weaning to hogget age in Merino sheep. Journal of Animal Science 82, 2852–2864.
| PubMed |
Prussin C, Metcalfe DD
(2006) IgE, mast cells, basophils, eosinophils. The Journal of Allergy and Clinical Immunology 117, S450–S456.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rothwell TLW,
Windon RG,
Horsburgh BA, Anderson BH
(1993) Relationship between eosinophilia and responsiveness to infection with Trichostrongylus colubriformis in sheep. International Journal for Parasitology 23, 203–211.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Scobie DR,
O’Connell D,
Morris CA, Hickey SM
(2008) Dag score is negatively correlated with breech bareness score of sheep. Australian Journal of Experimental Agriculture 48, 999–1003.
| Crossref | GoogleScholarGoogle Scholar |
Snoeck V,
Peters IR, Cox E
(2006) The IgA system: a comparison of structure and function in different species. Veterinary Research 37, 455–467.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stear MJ,
Bishop SC,
Doligalska M,
Duncan JL,
Holmes PH,
Irvine J,
McCririe L,
MacKellar A,
Sinski E, Murray M
(1995) Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643–652.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stear MJ,
Strain S, Bishop SC
(1999) Mechanisms underlying resistance to nematode infection. International Journal for Parasitology 29, 51–56.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sykes AR,
Xie HL,
Stankiewicz M,
Huntley JF,
MacKellar A,
Sedcole JR,
McAnulty RW, Green RS
(2007) The effect of vaccinating infection during pregnancy and dietary protein supply on the peri-parturient immune response of sheep to infection with Teladorsagia circumcincta and Trichostrongylus colubriformis larvae. Animal 1, 249–260.
| Crossref | GoogleScholarGoogle Scholar |
Whitlock HV
(1948) Some modifications of the McMaster helminth egg counting technique and apparatus. Journal of the Council for Scientific and Industrial Research 21, 177–180.
Williams AR,
Karlsson LJE,
Palmer DG,
Williams IH,
Vercoe PE,
Greeff JC, Emery DL
(2008) Increased levels of cysteinyl leukotrienes and prostaglandin E2 in gastrointestinal tract mucus are associated with decreased faecal dry matter in Merino rams during nematode infection. Australian Journal of Experimental Agriculture 48, 873–878.
| Crossref | GoogleScholarGoogle Scholar |
Williams AR,
Greeff JC,
Vercoe PE,
Dobson RJ, Karlsson LJE
(2010a) Merino ewes bred for parasite-resistance reduce larval contamination onto pasture during the peri-parturient period. Animal 4, 122–127.
| Crossref | GoogleScholarGoogle Scholar |
Williams AR,
Karlsson LJE,
Palmer DG,
Vercoe PE,
Williams IH,
Greeff JC, Emery DL
(2010b) Relationships between faecal dry matter, worm burdens and inflammatory mediators and cells in parasite-resistant Merino rams. Veterinary Parasitology in press. ,
| Crossref | GoogleScholarGoogle Scholar | PubMed |
