Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-27T07:38:41.094Z Has data issue: false hasContentIssue false
  • English
  • Français

Markers/parameters for the evaluation of natural resistance status of small ruminants against gastrointestinal nematodes

Published online by Cambridge University Press:  08 December 2011

H. A. Saddiqi ,
M. Sarwar ,
Z. Iqbal ,
M. Nisa  and
M. A. Shahzad
H. A. Saddiqi*
Affiliation:
Department of Zoology, GC University, Faisalabad 38040, Pakistan
M. Sarwar
Affiliation:
Institute of Animal Nutrition and Feed Technology, University of Agriculture, Faisalabad 38040, Pakistan
Z. Iqbal
Affiliation:
Department of Parasitology, University of Agriculture, Faisalabad 38040, Pakistan
M. Nisa
Affiliation:
Institute of Animal Nutrition and Feed Technology, University of Agriculture, Faisalabad 38040, Pakistan
M. A. Shahzad
Affiliation:
Institute of Animal Nutrition and Feed Technology, University of Agriculture, Faisalabad 38040, Pakistan
*
†E-mail: abubaker_79@yahoo.com
Get access

Abstract

The high prevalence of anthelmintic-resistant gastrointestinal nematodes (GINs) throughout the world has led to the need for alternative worm control strategies. One of the possible substitutes to reduce the problems of drug resistance and residue is the evaluation/breeding of small ruminants for greater resistance to the GINs (organically produced), which in turn would be a helpful tool to predict the performance of an animal. At present, the existing diversity in the genetic potential to resist/tolerate GINs infection both within and between breeds has been validated. Successful selection of animals to define the genotype and identified resistance is related to the employed markers. A number of phenotypic traits such as faecal egg count (FEC), worm burden, serum antibodies, peripheral eosinophilia, packed cell volume, live weight, serum protein and albumin concentrations have been used for this purpose both in natural and artificial infections. Relatively resistant/tolerant animals have also been found to have mastocytosis, globule leucocytes, high levels of histamine and immunoglobulin (Ig) A and IgE concentrations. Of these traits, the principal and most practical measurement used to assess resistance status in animals undergoing similar parasite challenges is FEC. FEC has a positive/negative correlation with other biochemical, cellular and immunological parameters; however, the reliability of individual trial is often questioned and valuable information regarding the genetic makeup can be obtained from pooled data of a large number of trials and parameters. This paper covers all the aspects reported in the literature on various parameters considered to evaluate the resistance status of a range of small ruminant breeds.

Keywords

gastrointestinal nematodesresistance potentialsmall ruminantsevaluationparameters
Type
Full Paper
Information
animal , Volume 6 , Issue 6 , June 2012 , pp. 994 - 1004
Copyright
Copyright © The Animal Consortium 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, DB, Colditz, IG 1991. Immunity to Haemonchus contortus and the cellular response to helminth antigens in the mammary gland of non lactating sheep. International Journal for Parasitology 21, 631–639.CrossRefGoogle ScholarPubMed
Albers, GA, Gray, GD, Piper, RL, Barker, JSF, Le Jambre, LF, Barger, IA 1987. The genetics of resistance and resilience to Haemonchus contortus infection in young Merino sheep. International Journal for Parasitology 17, 1355–1363.CrossRefGoogle ScholarPubMed
Altaif, KI, Dargie, JD 1978. Genetic resistance to helminthes. The influence of breed and haemoglobin type on the response of sheep to primary infection with Haemonchus contortus. Parasitology 77, 161–175.CrossRefGoogle ScholarPubMed
Amarante, AFT, Barbosa, MA 1995. Seasonal variation in popoulations of infective larvae on pasture and nematode fecal egg output in sheep. Veterinary Zootechnology 7, 127–133.Google Scholar
Amarante, AFT, Bricarello, PA, Rocha, RA, Gennari, SM 2004. Resistance of Santa Ines, Suffolk and Ile de France sheep to naturally acquired gastrointestinal nematode infections. Veterinary Parasitology 120, 91–106.CrossRefGoogle Scholar
Amarante, AFT, Bricarello, PA, Huntley, JF, Mazzolinb, LP, Gomes, JC 2005. Relationship of abomasal histology and parasite-specific immunoglobulin A with the resistance to Haemonchus contortus infection in three breeds of sheep. Veterinary Parasitology 128, 99–107.CrossRefGoogle ScholarPubMed
Amarante, AFT, Craig, TM, El-Sayed, NM, Desouki, AY, Ramsey, WS, Bazer, FW 1999a. Comparison of naturally acquired parasite burdens among Florida Native, Rambouillet and crossbreed ewes. Veterinary Parasitology 85, 61–69.CrossRefGoogle ScholarPubMed
Amarante, AFT, Craig, TM, Ramsey, WS, Davis, SK, Bazer, FW 1999b. Nematode burdens and cellular responses in the abomasal mucosa and blood of Florida Native, Rambouillet and crossbreed lambs. Veterinary Parasitology 80, 311–324.CrossRefGoogle ScholarPubMed
Amarante, AFT, Susin, I, Rocha, RA, Silva, MB, Mendes, CQ, Pires, AV 2009. Resistance of Santa Ines and crossbred ewes to naturally acquired gastrointestinal nematode infections. Veterinary Parasitology 165, 273–280.CrossRefGoogle Scholar
Andronicos, N, Hunt, P, Windon, R 2010. Expression of genes in gastrointestinal and lymphatic tissues during parasite infection in sheep genetically resistant or susceptible to Trichostrongylus colubriformis and Haemonchus contortus. International Journal for Parasitology 40, 417–429.CrossRefGoogle ScholarPubMed
Aumont, G, Gruner, L, Hostache, G 2003. Comparison of the resistance to sympatric and allopatric isolates of Haemonchus contortus of Black Belly sheep in Guadeloupe (FWI) and of INRA 402 sheep in France. Veterinary Parasitology 116, 139–150.CrossRefGoogle Scholar
Baker, RL, Watson, TG, Bisset, SA, Vlassof, A, Douch, PGC 1991. Breeding sheep in New Zealand for resistance to internal parasites, research results and commercial application. In Breeding for disease resistance in sheep (ed. GD Gray and RR Woolaston), pp. 19–32. Australian Wool Corporation, Melbourne.Google Scholar
Baker, RL, Rodriguez-Zas, SL, Southey, BR, Audho, JO, Aduda, EO, Thorpe, W 2003. Resistance and resilience to gastro-intestinal nematode parasites and relationships with productivity of Red Maasai, Dorper and Red Maasai × Dorper crossbred lambs in the sub-humid tropics. Animal Science 76, 119–136.CrossRefGoogle Scholar
Balic, A, Bowles, VM, Meeusen, ENT 2000a. The immunobiology of gastrointestinal nematode infections in ruminants. Advances in Parasitology 45, 181–241.CrossRefGoogle ScholarPubMed
Balic, A, Bowles, VM, Meeusen, ENT 2000b. Cellular profiles in the abomasal mucosa and lymph node during primary infection with Haemonchus contortus in sheep. Veterinary Immunolology and Immunopathololgy 75, 109–120.CrossRefGoogle ScholarPubMed
Bambou, JC, García, EG, Chevrotière, C, Arquet, R, Vachiéry, N, Mandonnet, N 2009. Peripheral immune response in resistant and susceptible Creole kids experimentally infected with Haemonchus contortus. Small Ruminant Research 82, 34–39.CrossRefGoogle Scholar
Barger, IA 1984. Correlation between number of enteric nematode parasites in grazing lambs. International Journal for Parasitology 14, 587–589.CrossRefGoogle ScholarPubMed
Beh, KJ, Maddox, JF 1996. Prospects for the development of genetic markers for resistance to gastrointestinal parasite infection in sheep. International Journal for Parasitology 26, 879–897.CrossRefGoogle ScholarPubMed
Bishop, SC, Morris, CA 2007. Genetics of disease resistance in sheep and goats. Small Ruminant Research 70, 48–59.CrossRefGoogle Scholar
Bishop, SC, Bairden, K, McKellar, QA, Park, M, Stear, MJ 1996. Genetic parameters for fecal egg count following mixed, natural, predominantly Ostertagia circumcincta infection and relationships with live weight in young lambs. Animal Science (Pencaitland) 63, 423–428.CrossRefGoogle Scholar
Bisset, SA, Morris, CA 1996. Feasibility and implications of breeding sheep for resilience to nematode challenge. International Journal for Parasitology 26, 857–868.CrossRefGoogle ScholarPubMed
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 or high faecal worm egg count. Veterinary Parasitology 61, 249–263.CrossRefGoogle ScholarPubMed
Bricarello, PA, Gennari, SM, Oliveira-Sequeira, TCG, Vaz, CMSL, Goncalves de Goncalves, I, Echevarria, FAM 2004. Worm burden and immunological responses in Corriedale and Crioula Lanada sheep following natural infection with Haemonchus contortus. Small Ruminant Research 51, 75–83.CrossRefGoogle Scholar
Bricarello, PA, Zaros, LG, Coutinho, LL, Rocha, RA, Kooyman, FNJ, De Vries, E, Goncalves, JRS, Lima, LG, Pires, AV, Amarante, AFT 2007. Field study on nematode resistance in Nelore-breed cattle. Veterinary Parasitology 48, 272–278.CrossRefGoogle Scholar
Buddle, BM, Jowett, G, Green, RS, Douch, PGC, Risdon, PL 1992. Association of blood eosinophilia with the expression of resistance in Romney lambs to nematodes. International Journal for Parasitology 22, 955–960.CrossRefGoogle ScholarPubMed
Burke, JM, Miller, JE 2004. Relative resistance to gastrointestinal nematode parasites in Dorper, Katahdin, and St. Croix lambs under conditions encountered in the south eastern region of the United States. Small Ruminant Research 54, 43–51.CrossRefGoogle Scholar
Burke, JM, Miller, JE 2008. Use of FAMACHA system to evaluate gastrointestinal nematode resistance/resilience in offspring of stud rams. Veterinary Parasitology 153, 85–92.CrossRefGoogle ScholarPubMed
Burke, JM, Kaplan, RM, Miller, JE, Terrill, TH, Getz, WR, Mobini, S, Valencia, E, Williams, MJ, Williamson, L, Vatta, AF 2007. Accuracy of the FAMACHA system for on-farm use by sheep and goat producers in the southeastern U.S. Veterinary Parasitolology 147, 89–95.CrossRefGoogle Scholar
Chauhan, KK, Rout, PK, Singh, PK, Mandal, A, Singh, HN, Roy, R, Singh, SK 2003. Susceptibility to natural gastro-intestinal nematode infection in different physiological stages in Jamunapari and Barbari goats in the semi-arid tropics. Small Ruminant Research 50, 219–223.CrossRefGoogle Scholar
Chiejina, SN, Behnke, JM, Musongong, GA, Nnadi, PA, Ngongeh, LA 2010. Resistance and resilience of West African dwarf goats of the Nigerian savanna zone exposed to experimental escalating primary and challenge infections with Haemonchus contortus. Veterinary Parasitology 171, 81–90.CrossRefGoogle ScholarPubMed
Cockett, N, Bishop, SC, Davies, G, Hadfield, T, Eng, S, Miller, J 2005. Use of QTL to determine parasite resistance in sheep. Journal of Animal Science 83 (suppl. 1), 128 (Abstract).Google Scholar
Courtney, CH, Parkerm, CF, McLure, KE, Herd, RP 1984. A comparison of the periparturient rise in faecal egg counts of exotic and domestic ewes. International Journal for Parasitology 14, 377–381.CrossRefGoogle ScholarPubMed
Davies, G, Stear, MJ, Bishop, SC 2005. Genetic relationship between indicator traits and nematode parasite infection levels in 6-month old lambs. Animal Science 80, 143–150.CrossRefGoogle Scholar
Dawkins, HJS, Windon, RG, Eagleson, GK 1989. Eosinophil responses in sheep selected for high and low responsiveness to Trichostrongylus colubriformis. International Journal for Parasitology 19, 199–205.CrossRefGoogle ScholarPubMed
Dominik, S 2005. Quantitative trait loci for internal nematode resistance in sheep: a review. Genetic Selection Evolution 37, 83–96.CrossRefGoogle ScholarPubMed
Douch, PGC, Harrison, GBL, Buchanan, LL, Brunsdon, RV 1984. Relationship of histamine in tissues and antiparasitic substances in gastrointestinal mucus to the development of resistance to trichostrongyle infections in young sheep. Veterinary Parasitology 16, 273–288.CrossRefGoogle Scholar
Douch, PGC, Harrison, GBL, Elliott, DC, Buchanan, LL, Greer, KS 1986. Relationship of gastrointestinal histology and mucus antiparasite activity with the development of resistance to trichostrongyle infections in sheep. Veterinary Parasitology 20, 315–331.CrossRefGoogle ScholarPubMed
Douch, PGC, Green, RS, Morris, CA, Mcewan, JC, Windon, RG 1996. Phenotypic markers for selection of nematode-resistant sheep. International Journal for Parasitology 26, 899–911.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Eady, SJ 1995. Phenotypic traits associated with resistance to internal parasites. In Breeding for resistance to infectious diseases in small ruminants (ed. GD Gray, RR Woolaston and BT Eaton), pp. 219–236. ACIAR Monograph series, Canberra.Google Scholar
Eady, SJ, Woolaston, RR, Lewer, RP, Raadsma, HW, Swan, AA, Ponzoni, RW 1998. Resistance to nematode parasites in Merino sheep, correlation with production traits. Australian Journal of Agriculture Research 49, 1201–1211.CrossRefGoogle Scholar
Emery, DL, Wagland, BM, McClure, SJ 1993. Rejection of heterologous nematodes by sheep immunized with larval or adult Trichostrongylus colubriformis. International Journal for Parasitology 23, 841–846.CrossRefGoogle ScholarPubMed
Finkelman, FD, Pearce, EJ, Urban, JF, Sher, A 1991. Regulation and biological function of helminth induced cytokine responses. In Immuno-parasitol today (ed. C Ash and R Gallagher), pp. 62–66. Elsevier, Cambridge.Google Scholar
Gamble, HR, Zajac, AM 1992. Resistance of Saint Croix lambs to Haemonchus contortus in experimentally and naturally acquired infections. Veterinary Parasitology 41, 211–225.CrossRefGoogle Scholar
Gauly, M, Erhardt, G 2001. Genetic resistance to gastrointestinal nematode parasites in Rhön sheep following natural infection. Veterinary Parasitology 102, 253–259.CrossRefGoogle ScholarPubMed
Gauly, M, Kraus, M, Vervelde, L, van Leeuwenb, MAW, Erhardt, G 2002. Estimating genetic differences in natural resistance in Rhön and Merinoland sheep following experimental Haemonchus contortus infection. Veterinary Parasitology 106, 55–67.CrossRefGoogle ScholarPubMed
Gill, HS 1991. Genetic control of acquired resistance to haemonchosis in Merino lambs. Parasite Immunolology 13, 617–628.CrossRefGoogle ScholarPubMed
Gill, HS, Gray, GD, Watson, DL, Husband, AJ 1993. Isotype specific antibody responses to Haemonchus contortus in genetically resistant sheep. Parasite Immunology 15, 61–67.CrossRefGoogle ScholarPubMed
Gill, HS, Husband, AJ, Watson, DL, Gray, GD 1994. Antibody-containing cells in the abomasal mucosa of sheep with genetic resistance to Haemonchus contortus. Research in Veterinary Science 56, 41–47.CrossRefGoogle ScholarPubMed
Gill, HS, Altmann, K, Cross, ML, Husband, AJ 2000. Induction of T helper 1- and T helper 2-type immune responses during Haemonchus contortus infection in sheep. Immunology 99, 458–463.CrossRefGoogle Scholar
Gonzalez, JF, Hernandez, A, Molina, JM, Fernandez, A, Raadsma, HW, Meeusen, ENT, Piedrafita, D 2008. Comparative experimental Haemonchus contortus infection in two sheep breeds native to the Canary Islands. Veterinary Parasitology 153, 374–378.CrossRefGoogle ScholarPubMed
Good, B, Hanrahan, JP, Crowley, BA, Mulcahy, G 2006. Texel sheep are more resistant to natural nematode challenge than Suffolk sheep based on faecal egg count and nematode burden. Veterinary Parasitology 136, 317–327.CrossRefGoogle ScholarPubMed
Gray, GD 1991. Breeding for resistance to Trichostrongyle nematodes in sheep. In Breeding for disease resistance in farm animals (ed. JB Owen and PFE Axford), pp. 139–161. CAB (Commonwealth Agricultural Bureaux) International, Wallingford, UK.Google Scholar
Gray, GD 1995. Genetic variation in resistance to parasites. In Breeding for resistance to infectious in small ruminants (ed. GD Gray, RR Woolaston and BT Eaton), pp. 43–52. ACIAR, Canberra.Google Scholar
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, 417–725.CrossRefGoogle ScholarPubMed
Gruner, J, Cortet, C, Sauve, C, Hoste, H 2004. Regulation of Teladorsagia circumcincta and Trichostrongylus colubriformis worm populations by grazing sheep with differing resistance status. Veterinary Research 35, 91–101.CrossRefGoogle ScholarPubMed
Gruner, L, Cortet, J, Sauve, C, Limouzin, C, Brunel, JC 2002. Evolution of a nematode community in grazing sheep selected for resistance and susceptibility to Teladorsagia circumcincta and Trichostrongylus colubriformis, a 4-year experiment. Veterinary Parasitology 109, 277–291.CrossRefGoogle ScholarPubMed
Gruner, L, Aumont, G, Getachew, T, Brunel, JC, Pery, C, Cognié, Y, Guérin, Y 2003. Experimental infection of Black Belly and INRA 401 straight and crossbred sheep with trichostrongyle nematode parasites. Veterinary Parasitology 116, 239–249.CrossRefGoogle ScholarPubMed
Haile, A, Tembely, S, Anindo, DO, Mukasa-Mugerwa, E, Rege, JEO, Alemuyami, RL, Baker, RL 2002. Effects of breed and dietary protein supplementation on the responses to gastrointestinal nematode infections in Ethiopian sheep. Small Ruminant Research 44, 247–261.CrossRefGoogle Scholar
Harris, N, Gause, WC 2011. To B or not to B: B cells and the Th2-type immune response to helminthes: a review. Trends in Immunology 32, 80–88.CrossRefGoogle Scholar
Harrison, GBL, Pulford, HD, Gatehouse, TK, Shaw, RJ, Pfeffer, A, Shoemaker, CB 1999. Studies on the role of mucus and mucosal hypersensitivity reactions during ejection of Trichostrongylus colubriformis from the intestine of immune sheep using an experimental challenge model. International Journal for Parasitology 29, 459–468.CrossRefGoogle Scholar
Harrison, GBL, Pulford, HD, Hein, WR, Barber, TK, Shaw, RJ, McNeill, M, Wakefield, STJ, Shoemaker, CB 2003. Immune rejection of Trichostrongylus colubriformis in sheep; a possible role for intestinal mucus antibody against an L3-specific surface antigen. Parasite Immunology 25, 45–53.CrossRefGoogle ScholarPubMed
Hoffman, WE 1981. A partial list of normal values. In Current veterinary therapy, food animal practice (ed. JL Howard) pp. 1168–1171. W.B. Saunders, Philadelphia.Google Scholar
Huntley, JF 1992. Mast cells and basophils: a review of their heterogeneity and function. Journal of Comparative Pathology 107, 349–372.CrossRefGoogle Scholar
Huntley, JF, Newlands, G, Miller, HRP 1984. The isolation and characterization of globule leucocytes, their derivation from mucosal mast cells in parasitized sheep. Parasite Immunology 6, 371–390.CrossRefGoogle ScholarPubMed
Huntley, JF, Newlands, GFJ, Jackson, F, Miller, HRP 1992. The influence of challenge dose, duration of immunity, or steroid treatment on mucosal mast cells and on the distribution of sheep mast cell proteinase in Haemonchus-infected sheep. Parasite Immunology 14, 429–440.CrossRefGoogle ScholarPubMed
Huntley, JF, Redmond, J, Welfare, W, Brennan, G, Jackson, F, Kooyman, F, Vervelde, L 2001. Studies on the immunoglobulin E responses to Teladorsagia circumcincta in sheep, purification of a major high molecular weight allergen. Parasite Immunology 23, 227–235.CrossRefGoogle ScholarPubMed
Hurtado, FA, Escobedo, ER, Munoz-Guzmán, MA, Torres-Hernández, G, Becerril-Pérez, CM 2010. Comparison of parasitological and productive traits of Criollo lambs native to the central Mexican Plateau and Suffolk lambs experimentally infected with Haemonchus contortus. Veterinary Parasitology 172, 277–282.CrossRefGoogle Scholar
Jabbar, A, Iqbal, Z, Kerboeuf, D, Muhammad, G, Khan, MN, Afaq, M 2006. Anthelmintic resistance, the state of play revisited. Life Sciences 79, 2413–2431.CrossRefGoogle ScholarPubMed
Jackson, F, Greer, AW, Huntley, J, McAnulty, RW, Bartley, DJ, Stanley, A, Stenhouse, L, Stankiewicz, M, Sykes, AR 2004. Studies using Teladorsagia circumcincta in an in vitro direct challenge method using abomasal tissue explants. Veterinary Parasitology 124, 73–89.CrossRefGoogle Scholar
Kahn, LP, Knox, MR, Brown, SW, Lea, JM 2003. Regulation of the resistance to nematode parasites of single- and twin-bearing Merino ewes through nutrition and genetic selection. Veterinary Parasitology 15, 15–31.CrossRefGoogle Scholar
Kaplan, RM, Burke, JM, Terrill, TH, Miller, JE, Getz, WR, Mobini, S, Valencia, E, Williams, M, Williamson, LH, Larsen, M, Vatta, AF 2004. Validation of the FAMACHA© eye color chart for detecting clinical anemia on sheep and goat farms in the southern United States. Veterinary Parasitolology 123, 105–120.CrossRefGoogle ScholarPubMed
Kemper, KE, Elwin, RL, Bishop, SC, Goddard, ME, Woolaston, RR 2009. Haemonchus contortus and Trichostrongylus colubriformis did not adapt to long-term exposure to sheep that were genetically resistant or susceptible to nematode infections. International Journal for Parasitology 39, 607–614.CrossRefGoogle ScholarPubMed
Kemper, KE, Palmer, DG, Liu, SM, Greeff, JC, Bishop, SC, Karlsson, LJE 2010. Reduction of faecal worm egg count, worm numbers and worm fecundity in sheep selected for worm resistance following artificial infection with Teladorsagia circumcincta and Trichostrongylus colubriformis. Veterinary Parasitology 171, 238–246.CrossRefGoogle ScholarPubMed
Li, Y, Miller, JE, Franke, DE 2001. Epidemiological observations and heterosis analysis of gastrointestinal nematode parasitism in Suffolk, Gulf Coast Native, and crossbred lambs. Veterinary Parasitology 98, 273–283.CrossRefGoogle ScholarPubMed
Li, RW, Meyer, MJ, Van Tassell, CP, Sonstegard, TS, Conner, EE, Van Amburgh, ME, Boisclair, YR, Capuco, AV 2006. Identification of estrogen-responsive genes in the parenchyma and fat pad of the bovine mammary gland by microarray analysis. Physiological Genomics 27, 42–53.CrossRefGoogle ScholarPubMed
Mandonnet, N, Menendez-Buxadera, A, Arquet, R, Mahieu, M, Bachand, M, Aumont, G 2006. Genetic variability in resistance to gastro-intestinal strongyles during early lactation in Creole goats. Animal Science 82, 283–287.CrossRefGoogle Scholar
Marshall, K, van der Werf, JHF, Maddox, JF, Graser, HU, Zhang, Y, Walkden-Brown, SW, Kahn, L 2005. A genome scan for QTL for resistance to the gastrointestinal parasite Haemonchus contortus in sheep. Proceedings of Association for Advancement of Animal Breeding and Genetics 16, 115.Google Scholar
Matika, O, Pong-Wong, R, Woolliams, JA, and Bishop, SC 2011. Confirmation of two quantitative trait loci regions for nematode resistance in commercial British terminal sire breeds. Animal 8, 1149–1156.CrossRefGoogle Scholar
Matika, O, Nyoni, S, van Wyk, JB, Erasmus, GJ, Baker, RL 2003. Resistance of Sabi and Dorper ewes to gastro-intestinal nematode infections in an African semi-arid environment. Small Ruminant Research 47, 95–110.CrossRefGoogle Scholar
McKenna, PB 1981. The diagnostic value and interpretation of faecal egg counts in sheep. New Zealand Veterinary Journal 29, 129–132.CrossRefGoogle ScholarPubMed
Meeusen, EN, Balic, A 2000. Do eosinophils have a role in the killing of helminth parasites. Parasitology Today 16, 95–101.CrossRefGoogle ScholarPubMed
Miller, HRP 1984. The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Veterinary Immunology and Immunopathology 6, 167–259.CrossRefGoogle ScholarPubMed
Miller, HRP 1996. Mucosal mast cells and the allergic response against nematode parasites. Veterinary Immunology and Immunopathology 54, 331–336.CrossRefGoogle ScholarPubMed
Miller, JE, Bishop, SC, Cockette, NE, McGraw, RA 2006. Segregation of natural and experimental gastrointestinal nematode infection in F2 progeny of susceptible Suffolk and resistant Gulf Coast Native sheep and its usefulness in assessment of genetic variation. Veterinary Parasitology 140, 83–89.CrossRefGoogle ScholarPubMed
Miller, JE, Bahirathan, M, Lemarie, SL, Hembry, FG, Kearney, MT, Barras, SR 1998. Epidemiology of gastrointestinal nematode parasitism in Suffolk and Gulf Coast Native susceptibility to Haemonchus contortus infection. Veterinary Parasitology 74, 55–74.CrossRefGoogle ScholarPubMed
Mugambi, JM, Audho, JO, Baker, RL 2005. Evaluation of the phenotypic performance of a Red Maasai and Dorper double backcross resource population, natural pasture challenge with gastro-intestinal nematode parasites. Small Ruminant Research 56, 239–251.CrossRefGoogle Scholar
Mugambi, JM, Wanyangu, SW, Bain, RK, Owango, MO, Duncan, JL, Stear, MJ 1996. Response of Dorper and Red Maasai lambs to trickle Haemonchus contortus infections. Research in Veterinary Science 6, 218–221.CrossRefGoogle Scholar
Notter, DR, Andrew, SA, Zajac, AM 2003. Responses of hair and wool sheep to a single fixed dose of infective larvae of Haemonchus contortus. Small Ruminant Research 47, 221–225.CrossRefGoogle Scholar
Pfeffer, A, Douch, PGC, Shaw, RJ, Gatehouse, TK, Rabel, B, Green, RS, Shirer, CL, Jonas, WE, Bisset, S 1996. Sequential cellular and humoral responses in the abomasal mucosa and blood of Romney sheep dosed with Trichostrongylus axei. International Journal for Parasitology 26, 765–773.CrossRefGoogle ScholarPubMed
Preston, JM, Allonby, EW 1978. The influence of breed on the susceptibility of sheep and goats to a single experimental infection with Haemonchus contortus. Veterinary Record 103, 509–512.CrossRefGoogle ScholarPubMed
Rainbird, MA, Macmillan, D, Meeusen, ENT 1998. Eosinophil-mediated killing of Haemonchus contortus larvae: effect of eosinophil activation and role of antibody, complement and interleukin-5. Parasite Immunology 20, 93–110.CrossRefGoogle ScholarPubMed
Rege, JEO, Tembely, S, Mukasa-Mugerwa, E, Sovani, S, Anindo, D, Lahlou-Kassi, A, Nagda, S, Baker, RL 2002. Effect of breed and season on production and response to infection with gastrointestinal nematode parasites in sheep in the highlands of Ethiopia. Livestock Production Science 78, 159–174.CrossRefGoogle Scholar
Reynolds, L, Baker, RL, Sherington, J, Njubi, D 1992. Resistance to gastro-intestinal parasites in Dorper and Red Maasai–Dorper crossbred sheep. Proceedings of the 10th Scientific Workshop of the Small Ruminant Collaborative Research Support Programme, Nairobi, Kenya, 131–137.Google Scholar
Rocha, RA, Amarante, AFT, Bricarello, PA 2004. Comparison of the susceptibility of Santa Ines and Ile de France ewes to nematode parasitism around periparturition and during lactation. Small Ruminant Research 55, 65–75.CrossRefGoogle Scholar
Saddiqi, HA, Iqbal, Z, Khan, MN, Muhammad, G 2010a. Comparative resistance of sheep breeds to Haemonchus contortus in a natural pasture infection. International Journal of Agriculture and Biology 12, 739–773.Google Scholar
Saddiqi, HA, Iqbal, Z, Khan, MN, Sarwar, M, Muhammad, G, Yaseen, M, Jabbar, A 2010b. Evaluation of three Pakistani sheep breeds for their natural resistance to artificial infection of Haemonchus contortus. Veterinary Parasitology 168, 141–145.CrossRefGoogle ScholarPubMed
Saddiqi, HA, Jabbar, A, Iqbal, Z, Babar, W, Sindhu, Z, Abbas, RZ 2006. Comparative efficacy of five anthelmintics against trichostrongylid nematodes in sheep. Canadian Journal of Animal Science 86, 471–477.CrossRefGoogle Scholar
Sayers, G, Sweeney, T 2005. Gastrointestinal nematode infection in sheep – a review of the alternatives to anthelmintics in parasite control. Animal Health Research Reviews 6, 159–171.CrossRefGoogle ScholarPubMed
Stear, MJ, Bishop, SC 1999. The curvilinear relationship between worm length and fecundity of Teladorsagia circumcincta. International Journal for Parasitology 29, 777–780.CrossRefGoogle ScholarPubMed
Stear, MJ, Strain, S, Bishop, SC 1999. Mechanisms underlying resistance to nematode infection. International Journal for Parasitology 29, 51–56.CrossRefGoogle ScholarPubMed
Stear, MJ, Mitchell, S, Strain, S, Bishop, SC, Mckellar, QA 2000. The influence of age on the variation among sheep in susceptibility to natural nematode infection. Veterinary Parasitology 89, 31–36.CrossRefGoogle ScholarPubMed
Stear, MJ, Bairden, K, Bishop, SC, Buitkamp, J, Epplen, JT, Gostomski, D, Mckellar, QA, Schwaiger, FW, Wallace, DS 1996. An ovine lymphocyte antigen is associated with reduced faecal egg counts in four-month-old lambs following natural, predominantly Ostertagia circumcincta infection. International Journal for Parasitology 26, 423–428.CrossRefGoogle ScholarPubMed
Stear, MJ, Bishop, SC, Doligalska, M, Duncan, JL, Holmes, PH, Irvine, J, McVririe, L, McKellar, QA, Sinski, E, Murray, M 1995. Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia cricumcincta. Parasite Immunology 17, 643–652.CrossRefGoogle Scholar
Strain, SA, Stear, MJ 1999. The recognition of molecules from fourth-stage larvae of Ostertagia circumcincta by IgA from infected sheep. Parasite immunology 21, 163–168.CrossRefGoogle ScholarPubMed
Strain, SAJ, Stear, MJ 2001. The influence of protein supplementation on the immune response to Haemonchus contortus. Parasite Immunology 23, 527–531.CrossRefGoogle ScholarPubMed
Taylor, EL 1939. Technique for the estimation of pasture infestation by strongyloid larvae. Parasitology 31, 473–478.CrossRefGoogle Scholar
Taylor, MA, Hunt, KR, Wilson, CA, Quick, JM 1990. Clinical observations, diagnosis and control of Haemonchus contortus infections in periparturient ewes. Veterinary Record 126, 555–556.Google ScholarPubMed
Terefe, G, Lacroux, C, Andreoletti, O, Grisez, C, Prevot, F, Bergeaud, JP, Penicaud, J, Rouillon, V, Gruner, L, Brunel, JC, Francois, D, Bouix, J, Dorchies, P, Jacquiet, P 2007. Immune response to Haemonchus contortus infection in susceptible (INRA 401) and resistant (Barbados Black Belly) breeds of lambs. Parasite Immunology 29, 415–424.CrossRefGoogle ScholarPubMed
Urban, JF Jr, Madden, KB, Svetic, A, Cheever, A, Trotta, PP, Gause, WC, Katona, IM, Finkelman, FD 1992. The importance of Th2 cytokines in protective immunity to nematodes. Immunological Reviews 127, 205–220.CrossRefGoogle ScholarPubMed
van Wyk, JA, Malan, FS, Bath, GF 1997. Rampant anthelmintic resistance in sheep in South Africa – what are the options? In Proceedings of the Workshop held at the 16th international Conference of the World Association for the Advancement of Parasitology – Managing Anthelmintic Resistance in Endoparasites (ed. JA van Wyk and PC Van Schalkwyk), pp. 51–63. 10–15 August 1997, Sun City, South Africa.Google Scholar
Vanimisetti, HB, Greiner, SP, Zajac, AM, Notter, DR 2004. Performance of hair sheep composite breeds, resistance of lambs to Haemonchus contortus. Journal of Animal Science 82, 595–604.CrossRefGoogle ScholarPubMed
Vatta, AF, Letty, BA, van der Linde, MJ, van Wijk, EF, Hansen, JW, Krecek, RC 2001. Testing for clinical anaemia caused by Haemonchus spp. in goats farmed under resource-poor conditions in South Africa using an eye colour chart developed for sheep. Veterinary Parasitology 99, 1–14.CrossRefGoogle ScholarPubMed
Wanyangu, SW, Mugambi, JM, Bain, RK, Duncan, JL, Murray, M, Stear, MJ 1997. Response to artificial and subsequent natural infection with Haemonchus contortus in Red Maasai and Dorper ewes. International Journal for Parasitology 69, 275–282.Google ScholarPubMed
Woolaston, RR 1992. Selection of Merino sheep for increased and decreased resistance to Haemonchus contortus, periparturient effects on faecal egg counts. International Journal for Parasitology 22, 947–953.CrossRefGoogle ScholarPubMed
Woolaston, RR, Baker, RL 1996. Prospects of breeding small ruminants for resistance to internal parasites. International Journal for Parasitology 26, 845–855.CrossRefGoogle ScholarPubMed
Yacob, HT, Duranton-Grisez, C, Prevot, F, Bergeaud, JP, Bleuart, C, Jacquiet, P, Dorchies, P, Hoste, H 2002. Experimental concurrent infections of sheep with Oestrus ovis and Trichostrongylus colubriformis, negative interactions between parasite populations and related changes in the cellular responses of nasal and digestive mucosae. Veterinary Parasitology 104, 307–317.CrossRefGoogle ScholarPubMed
Zajac, AM, Herd, RP, McClure, KE 1988. Trichostrongylid parasite populations in pregnant or lactating and unmated Florida Native and Dorset/Rambouillet ewes. International Journal for Parasitology 18, 981–985.CrossRefGoogle ScholarPubMed
Zajac, AM, Krakowka, S, Herd, RP, McClure, KE 1990. Experimental Haemonchus contortus infection in three breeds of sheep. Veterinary Parasitology 36, 221–235.CrossRefGoogle ScholarPubMed