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Functional study of a genetic marker allele associated with resistance to Ascaris suum in pigs

Published online by Cambridge University Press:  05 February 2014

PER SKALLERUP*
Affiliation:
Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark Genetics and Bioinformatics, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
STIG M. THAMSBORG
Affiliation:
Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark
CLAUS B. JØRGENSEN
Affiliation:
Genetics and Bioinformatics, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
HEIDI L. ENEMARK
Affiliation:
Section for Bacteriology, Pathology and Parasitology, National Veterinary Institute, Bülowsvej 27, DK-1870 Frederiksberg C, Denmark
AYAKO YOSHIDA
Affiliation:
Department of Infectious Diseases, Division of Parasitology, Faculty of Medicine, University of Miyazaki, Japan
HARALD H. H. GÖRING
Affiliation:
Texas Biomedical Research Institute, 7620 N. W. Loop 410, San Antonio, TX, USA
MERETE FREDHOLM
Affiliation:
Genetics and Bioinformatics, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
PETER NEJSUM
Affiliation:
Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark Genetics and Bioinformatics, Department of Veterinary Clinical and Animal Sciences, University of Copenhagen, Grønnegårdsvej 3, DK-1870 Frederiksberg C, Denmark
*
*Corresponding author. Parasitology and Aquatic Diseases, Department of Veterinary Disease Biology, University of Copenhagen, Dyrlægevej 100, DK-1870 Frederiksberg C, Denmark. E-mail: pesk@sund.ku.dk

Summary

Two single nucleotide polymorphisms (SNP TXNIP and SNP ARNT), both on chromosome 4, have been reported to be associated with roundworm (Ascaris suum) burden in pigs. In the present study, we selected pigs with two SNP TXNIP genotypes (AA; n = 24 and AB; n = 24), trickle-infected them with A. suum from 8 weeks of age until necropsy 8 weeks later, and tested the hypothesis that pigs with the AA genotype would have higher levels of resistance than pigs of AB genotype. We used different indicators of resistance (worm burden, fecal egg counts (FEC), number of liver white spots and A. suum-specific serum IgG antibody levels). Pigs of the AA genotype had lower mean macroscopic worm burden (2·4 vs 19·3; P = 0·06), lower mean total worm burden (26·5 vs 70·1; P = 0·09) and excreted fewer A. suum eggs at week 8 PI (mean number of eggs/g feces: 238 vs 1259; P = 0·14) than pigs of the AB genotype, as expected based on prior associations. The pigs were also genotyped at another locus (SNP ARNT) which showed a similar trend. This study provides suggestive evidence that resistant pigs may be selected using a genetic marker, TXNIP, and provides further support to the quantitative trait locus on chromosome 4.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Ackert, J. E., Eisenbrandt, L. L., Wilmoth, J. H., Glading, B. and Pratt, I. (1935). Comparative resistance of five breeds of chickens to the nematode Ascaridia lineata (Schneider). Journal of Agricultural Research 50, 607624.Google Scholar
Albers, G. A., Gray, G. D., Piper, L. R., Barker, J. S., Le Jambre, L. F. and Barger, I. A. (1987). The genetics of resistance and resilience to Haemonchus contortus infection in young Merino sheep. International Journal for Parasitology 17, 13551363.CrossRefGoogle ScholarPubMed
Almasy, L. and Blangero, J. (1998). Multipoint quantitative-trait linkage analysis in general pedigrees. American Journal of Human Genetics 62, 11981211.Google Scholar
Anderson, R. M. and Schad, G. A. (1985). Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 812825.Google Scholar
Anthony, R. M., Rutitzky, L. I., Urban, J. F. Jr., Stadecker, M. J. and Gause, W. C. (2007). Protective immune mechanisms in helminth infection. Nature Reviews Immunology 7, 975987.CrossRefGoogle ScholarPubMed
Bishop, S. C. (2012). Possibilities to breed for resistance to nematode parasite infections in small ruminants in tropical production systems. Animal 6, 741747.CrossRefGoogle ScholarPubMed
Bjorn, H., Roepstorff, A. and Nansen, P. (1996). A possible influence of diet composition on the establishment of nematodes in the pig. Veterinary Parasitology 63, 167171.Google Scholar
Boerwinkle, E., Chakraborty, R. and Sing, C. F. (1986). The use of measured genotype information in the analysis of quantitative phenotypes in man. I. Models and analytical methods. Annals of Human Genetics 50, 181194.Google Scholar
Boes, J., Medley, G. F., Eriksen, L., Roepstorff, A. and Nansen, P. (1998). Distribution of Ascaris suum in experimentally and naturally infected pigs and comparison with Ascaris lumbricoides infections in humans. Parasitology 117, 589596.CrossRefGoogle ScholarPubMed
Brown, H. W. (1927). A study of the regularity of egg-production of Ascaris lumbricoides, Necator americanus and Trichuris trichiura . Journal of Parasitology 14, 110119.Google Scholar
Charlier, C., Coppieters, W., Rollin, F., Desmecht, D., Agerholm, J. S., Cambisano, N., Carta, E., Dardano, S., Dive, M., Fasquelle, C., Frennet, J. C., Hanset, R., Hubin, X., Jorgensen, C., Karim, L., Kent, M., Harvey, K., Pearce, B. R., Simon, P., Tama, N., Nie, H., Vandeputte, S., Lien, S., Longeri, M., Fredholm, M., Harvey, R. J. and Georges, M. (2008). Highly effective SNP-based association mapping and management of recessive defects in livestock. Nature Genetics 40, 449454.CrossRefGoogle ScholarPubMed
Copeman, D. B. and Gaafar, S. M. (1972). Sequential development of hepatic lesions of ascaridosis in colostrum-deprived pigs. Australian Veterinary Journal 48, 263268.Google Scholar
Coppieters, W., Mes, T. H., Druet, T., Farnir, F., Tamma, N., Schrooten, C., Cornelissen, A. W., Georges, M. and Ploeger, H. W. (2009). Mapping QTL influencing gastrointestinal nematode burden in Dutch Holstein-Friesian dairy cattle. BMC Genomics 10, 96.CrossRefGoogle ScholarPubMed
Coustau, C., Chevillon, C. and ffrench-Constant, R. (2000). Resistance to xenobiotics and parasites: can we count the cost? Trends in Ecology and Evolution 15, 378383.Google Scholar
Crofton, H. D. (1971). A model of host–parasite relationships. Parasitology 63, 343364.CrossRefGoogle Scholar
Croll, N. A., Anderson, R. M., Gyorkos, T. W. and Ghadirian, E. (1982). The population biology and control of Ascaris lumbricoides in a rural community in Iran. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 187197.Google Scholar
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. Heredity 96, 252258.Google Scholar
Dawson, H. D., Beshah, E., Nishi, S., Solano-Aguilar, G., Morimoto, M., Zhao, A., Madden, K. B., Ledbetter, T. K., Dubey, J. P., Shea-Donohue, T., Lunney, J. K. and Urban, J. F. Jr. (2005). Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum . Infection and Immunity 73, 11161128.Google Scholar
Dermitzakis, E. T. and Clark, A. G. (2009). Life after GWA studies. Science 326, 239240.CrossRefGoogle ScholarPubMed
Dominik, S., Hunt, P. W., McNally, J., Murrell, A., Hall, A. and Purvis, I. W. (2010). Detection of quantitative trait loci for internal parasite resistance in sheep. I. Linkage analysis in a Romney×Merino sheep backcross population. Parasitology 137, 12751282.CrossRefGoogle Scholar
Dow, C. and Jarrett, W. F. H. (1960). Age, strain and sex differences in susceptibility to Cysticercus fasciolaris in the mouse. Experimental Parasitology 10, 7274.Google Scholar
Eriksen, L., Andersen, S., Nielsen, K., Pedersen, A. and Nielsen, J. (1980). Experimental Ascaris suum infection in pigs. Serological response, eosinophilia in peripheral blood, occurrence of white spots in the liver and worm recovery from the intestine. Nordisk veterinærmedicin 32, 233242.Google Scholar
Eriksen, L., Lind, P., Nansen, P., Roepstorff, A. and Urban, J. (1992). Resistance to Ascaris suum in parasite naive and naturally exposed growers, finishers and sows. Veterinary Parasitology 41, 137149.CrossRefGoogle ScholarPubMed
Gasbarre, L. C., Leighton, E. A. and Davies, C. J. (1993). Influence of host genetics upon antibody responses against gastrointestinal nematode infections in cattle. Veterinary Parasitology 46, 8191.Google Scholar
Gauly, M., Bauer, C., Preisinger, R. and Erhardt, G. (2002). Genetic differences of Ascaridia galli egg output in laying hens following a single dose infection. Veterinary Parasitology 103, 99107.Google Scholar
Goddard, M. E. and Hayes, B. J. (2007). Genomic selection. Journal of Animal Breeding and Genetics 124, 323330.Google Scholar
Gray, G. D. (1995). Genetic variation in resistance to parasites. In Breeding for Resistance to Infectious Diseases in Small Ruminants (ed. Gray, G. D., Woolaston, R. R. and Eaton, B. T.), pp. 4352. ACIAR Monograph No. 34. Australian Centre for International Agricultural Research, Canberra, Australia.Google Scholar
Groenen, M. A., Archibald, A. L., Uenishi, H., Tuggle, C. K., Takeuchi, Y., Rothschild, M. F., Rogel-Gaillard, C., Park, C., Milan, D., Megens, H. J., Li, S., Larkin, D. M., Kim, H., Frantz, L. A., Caccamo, M., Ahn, H., Aken, B. L., Anselmo, A., Anthon, C., Auvil, L., Badaoui, B., Beattie, C. W., Bendixen, C., Berman, D., Blecha, F., Blomberg, J., Bolund, L., Bosse, M., Botti, S., Bujie, Z. et al. (2012). Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491, 393398.Google Scholar
Hassan, M., Good, B., Hanrahan, J. P., Campion, D., Sayers, G., Mulcahy, G. and Sweeney, T. (2011). The dynamic influence of the DRB1*1101 allele on the resistance of sheep to experimental Teladorsagia circumcincta infection. Veterinary Research 42, 46.Google Scholar
Haugegaard, J. (2010). Prevalence of nematodes in Danish industrialized sow farms with loose housed sows in dynamic groups. Veterinary Parasitology 168, 156159.CrossRefGoogle ScholarPubMed
Havill, L. M., Dyer, T. D., Richardson, D. K., Mahaney, M. C. and Blangero, J. (2005). The quantitative trait linkage disequilibrium test: a more powerful alternative to the quantitative transmission disequilibrium test for use in the absence of population stratification. BMC Genetics 6 (Suppl. 1), S91.CrossRefGoogle Scholar
Helwigh, A. B. and Nansen, P. (1999). Establishment of Ascaris suum in the pig: development of immunity following a single primary infection. Acta Veterinaria Scandinavica 40, 121132.Google Scholar
Hoste, H. and Torres-Acosta, J. F. (2011). Non chemical control of helminths in ruminants: adapting solutions for changing worms in a changing world. Veterinary Parasitology 180, 144154.Google Scholar
Iraqi, F. A., Behnke, J. M., Menge, D. M., Lowe, A. M., Teale, A. J., Gibson, J. P., Baker, L. R. and Wakelin, D. R. (2003). Chromosomal regions controlling resistance to gastro-intestinal nematode infections in mice. Mammalian Genome 14, 184191.Google Scholar
Johnson, J. C. Jr., Stewart, T. B. and Hale, O. M. (1975). Differential responses of Duroc, Hampshire, and crossbred pigs to a superimposed experimental infection with the intestinal threadworm, Strongyloides ransomi . Journal of Parasitology 61, 517524.Google Scholar
Jorgensen, R. J., Nansen, P., Nielsen, K., Eriksen, L. and Andersen, S. (1975). Experimental Ascaris suum infection in pig. Population kinetics following low and high levels of primary infection in piglets. Veterinary Parasitology 1, 151157.Google Scholar
Jungersen, G., Eriksen, L., Nansen, P. and Fagerholm, H. P. (1997). Sex-manipulated Ascaris suum infections in pigs: implications for reproduction. Parasitology 115, 439442.Google Scholar
Jungersen, G., Eriksen, L., Roepstorff, A., Lind, P., Meeusen, E. N., Rasmussen, T. and Nansen, P. (1999). Experimental Ascaris suum infection in the pig: protective memory response after three immunizations and effect of intestinal adult worm population. Parasite Immunology 21, 619630.Google Scholar
Kemper, K. E., Emery, D. L., Bishop, S. C., Oddy, H., Hayes, B. J., Dominik, S., Henshall, J. M. and Goddard, M. E. (2011). The distribution of SNP marker effects for faecal worm egg count in sheep, and the feasibility of using these markers to predict genetic merit for resistance to worm infections. Genetics Research 93, 203219.Google Scholar
Kloosterman, A., Parmentier, H. K. and Ploeger, H. W. (1992). Breeding cattle and sheep for resistance to gastrointestinal nematodes. Parasitology Today 8, 330335.Google Scholar
Lewis, R., Behnke, J. M., Stafford, P. and Holland, C. V. (2006). The development of a mouse model to explore resistance and susceptibility to early Ascaris suum infection. Parasitology 132, 289300.Google Scholar
Manolio, T. A., Collins, F. S., Cox, N. J., Goldstein, D. B., Hindorff, L. A., Hunter, D. J., McCarthy, M. I., Ramos, E. M., Cardon, L. R., Chakravarti, A., Cho, J. H., Guttmacher, A. E., Kong, A., Kruglyak, L., Mardis, E., Rotimi, C. N., Slatkin, M., Valle, D., Whittemore, A. S., Boehnke, M., Clark, A. G., Eichler, E. E., Gibson, G., Haines, J. L., Mackay, T. F., McCarroll, S. A. and Visscher, P. M. (2009). Finding the missing heritability of complex diseases. Nature 461, 747753.Google Scholar
Masure, D., Vlaminck, J., Wang, T., Chiers, K., Van den Broeck, W., Vercruysse, J. and Geldhof, P. (2013). A role for eosinophils in the intestinal immunity against infective Ascaris suum larvae. PLoS Neglected Tropical Diseases 7, e2138.CrossRefGoogle ScholarPubMed
Mejer, H. and Roepstorff, A. (2006). Ascaris suum infections in pigs born and raised on contaminated paddocks. Parasitology 133, 305312.Google Scholar
Miller, S. A., Dykes, D. D. and Polesky, H. F. (1988). A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research 16, 1215.CrossRefGoogle ScholarPubMed
Miquel, N., Roepstorff, A., Bailey, M. and Eriksen, L. (2005). Host immune reactions and worm kinetics during the expulsion of Ascaris suum in pigs. Parasite Immunology 27, 7988.Google Scholar
Mitchell, G. F., Hogarth-Scott, R. S., Edwards, R. D., Lewers, H. M., Cousins, G. and Moore, T. (1976). Studies on immune responses to parasite antigens in mice. I. Ascaris suum larvae numbers and antiphosphorylcholine responses in infected mice of various strains and in hypothymic nu/nu mice. International Archives of Allergy and Applied Immunology 52, 6478.Google Scholar
Mugambi, J. M., Bain, R. K., Wanyangu, S. W., Ihiga, M. A., Duncan, J. L., Murray, M. and Stear, M. J. (1997). Resistance of four sheep breeds to natural and subsequent artificial Haemonchus contortus infection. Veterinary Parasitology 69, 265273.Google Scholar
Nejsum, P., Roepstorff, A., Jorgensen, C. B., Fredholm, M., Goring, H. H., Anderson, T. J. and Thamsborg, S. M. (2009 a). High heritability for Ascaris and Trichuris infection levels in pigs. Heredity 102, 357364.CrossRefGoogle ScholarPubMed
Nejsum, P., Thamsborg, S. M., Petersen, H. H., Kringel, H., Fredholm, M. and Roepstorff, A. (2009 b). Population dynamics of Ascaris suum in trickle-infected pigs. Journal of Parasitology 95, 10481053.CrossRefGoogle ScholarPubMed
Nielsen, B., Jorgensen, C. B., Vernersen, A. and Fredholm, M. (2009). Effect of selection for E. coli F4ab/ac resistance in pigs. 60th Annual Meeting of the European Association for Animal Production, Barcelona, 2008.Google Scholar
Nissen, S., Poulsen, I. H., Nejsum, P., Olsen, A., Roepstorff, A., Rubaire-Akiiki, C. and Thamsborg, S. M. (2011). Prevalence of gastrointestinal nematodes in growing pigs in Kabale District in Uganda. Tropical Animal Health and Production 43, 567572.Google Scholar
Oksanen, A., Eriksen, L., Roepstorff, A., Ilsoe, B., Nansen, P. and Lind, P. (1990). Embryonation and infectivity of Ascaris suum eggs. A comparison of eggs collected from worm uteri with eggs isolated from pig faeces. Acta Veterinaria Scandinavica 31, 393398.Google Scholar
Oliveira, M. C., Alencar, M. M., Chagas, A. C., Giglioti, R. and Oliveira, H. N. (2009). Gastrointestinal nematode infection in beef cattle of different genetic groups in Brazil. Veterinary Parasitology 166, 249254.Google Scholar
O'Lorcain, P. and Holland, C. V. (2000). The public health importance of Ascaris lumbricoides . Parasitology 121, S51S71.Google Scholar
Peng, W., Zhou, X., Cui, X., Crompton, D. W., Whitehead, R. R., Xiong, J., Wu, H., Peng, J., Yang, Y., Wu, X., Xu, K. and Yan, Y. (1996). Ascaris, people and pigs in a rural community of Jiangxi Province, China. Parasitology 113, 545557.Google Scholar
Pérez, J., García, P. M., Mozos, E., Bautista, M. J. and Carrasco, L. (2001). Immunohistochemical characterization of hepatic lesions associated with migrating larvae of Ascaris suum in pigs. Journal of Comparative Pathology 124, 200206.Google Scholar
Petkevicius, S., Bjorn, H., Roepstorff, A., Nansen, P., Bach Knudsen, K. E., Barnes, E. H. and Jensen, K. (1995). The effect of two types of diet on populations of Ascaris suum and Oesophagostomum dentatum in experimentally infected pigs. Parasitology 111, 395401.Google Scholar
Pulendran, B. and Artis, D. (2012). New paradigms in type 2 immunity. Science 337, 431435.Google Scholar
Quinnell, R. J. (2003). Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33, 12191231.Google Scholar
R Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Riggio, V., Matika, O., Pong-Wong, R., Stear, M. J. and Bishop, S. C. (2013). Genome-wide association and regional heritability mapping to identify loci underlying variation in nematode resistance and body weight in Scottish Blackface lambs. Heredity 110, 420429.Google Scholar
Roepstorff, A. (1998). Natural Ascaris suum infections in swine diagnosed by coprological and serological (ELISA) methods. Parasitology Research 84, 537543.Google Scholar
Roepstorff, A. and Murrell, K. D. (1997). Transmission dynamics of helminth parasites of pigs on continuous pasture: Ascaris suum and Trichuris suis . International Journal for Parasitology 27, 563572.Google Scholar
Roepstorff, A. and Nansen, P. (1998). Epidemiology, Diagnosis and Control of Helminth Parasites of Swine. Food and Agriculture Organization (FAO), Rome.Google Scholar
Roepstorff, A., Eriksen, L., Slotved, H. C. and Nansen, P. (1997). Experimental Ascaris suum infection in the pig: worm population kinetics following single inoculations with three doses of infective eggs. Parasitology 115, 443452.Google Scholar
Ronéus, O. (1966). Studies on the aetiology and pathogenesis of white spots in the liver of pigs. Acta Veterinaria Scandinavica 7 (Suppl. 16), 1112.Google Scholar
Saddiqi, H. A., Jabbar, A., Sarwar, M., Iqbal, Z., Muhammad, G., Nisa, M. and Shahzad, A. (2011). Small ruminant resistance against gastrointestinal nematodes: a case of Haemonchus contortus . Parasitology Research 109, 14831500.Google Scholar
Sallé, G., Jacquiet, P., Gruner, L., Cortet, J., Sauvé, C., Prévot, F., Grisez, C., Bergeaud, J. P., Schibler, L., Tircazes, A., Francois, D., Pery, C., Bouvier, F., Thouly, J. C., Brunel, J. C., Legarra, A., Elsen, J. M., Bouix, J., Rupp, R. and Moreno, C. R. (2012). A genome scan for QTL affecting resistance to Haemonchus contortus in sheep. Journal of Animal Science 90, 46904705.Google Scholar
Schwartz, B. (1959). Experimental infection of pigs with Ascaris suum . American Journal of Veterinary Research 20, 713.Google Scholar
Scott, J. A. and Headlee, W. H. (1938). Studies in Egypt on the correction of helminth egg count data for the size and consistency of stools. American Journal of Hygiene 27, 176195.Google Scholar
Silva, M. V., Sonstegard, T. S., Hanotte, O., Mugambi, J. M., Garcia, J. F., Nagda, S., Gibson, J. P., Iraqi, F. A., McClintock, A. E., Kemp, S. J., Boettcher, P. J., Malek, M., Van Tassell, C. P. and Baker, R. L. (2012). Identification of quantitative trait loci affecting resistance to gastrointestinal parasites in a double backcross population of Red Maasai and Dorper sheep. Animal Genetics 43, 6371.CrossRefGoogle Scholar
Skallerup, P., Nejsum, P., Jorgensen, C. B., Goring, H. H., Karlskov-Mortensen, P., Archibald, A. L., Fredholm, M. and Thamsborg, S. M. (2012). Detection of a quantitative trait locus associated with resistance to Ascaris suum infection in pigs. International Journal for Parasitology 42, 383391.Google Scholar
Slotved, H. C., Barnes, E. H., Eriksen, L., Roepstorff, A., Nansen, P. and Bjorn, H. (1997). Use of an agar-gel technique for large scale application to recover Ascaris suum larvae from intestinal contents of pigs. Acta Veterinaria Scandinavica 38, 207212.Google Scholar
Stankiewicz, M. and Jeska, E. L. (1990). Evaluation of pyrantel-tartrate abbreviated Ascaris suum infections for the development of resistance in young pigs against migrating larvae. International Journal for Parasitology 20, 7781.Google Scholar
Stear, M. J., Bairden, K., Duncan, J. L., Holmes, P. H., McKellar, Q. A., Park, M., Strain, S., Murray, M., Bishop, S. C. and Gettinby, G. (1997). How hosts control worms. Nature 389, 27.Google Scholar
Stear, M. J., Strain, S. and Bishop, S. C. (1999). How lambs control infection with Ostertagia circumcincta . Veterinary Immunology and Immunopathology 72, 213218.Google Scholar
Thamsborg, S. M., Nejsum, P. and Mejer, H. (2013). Impact of Ascaris suum in livestock. In Ascaris: The Neglected Parasite (ed. Holland, C. V.), pp. 363381. Elsevier, London, UK.Google Scholar
Urban, J. F. Jr., Alizadeh, H. and Romanowski, R. D. (1988). Ascaris suum: development of intestinal immunity to infective second-stage larvae in swine. Experimental Parasitology 66, 6677.Google Scholar
Vlaminck, J., Nejsum, P., Vangroenweghe, F., Thamsborg, S. M., Vercruysse, J. and Geldhof, P. (2012). Evaluation of a serodiagnostic test using Ascaris suum haemoglobin for the detection of roundworm infections in pig populations. Veterinary Parasitology 189, 267273.CrossRefGoogle ScholarPubMed
Williams-Blangero, S., Subedi, J., Upadhayay, R. P., Manral, D. B., Rai, D. R., Jha, B., Robinson, E. S. and Blangero, J. (1999). Genetic analysis of susceptibility to infection with Ascaris lumbricoides . American Journal of Tropical Medicine and Hygiene 60, 921926.Google Scholar
Wolc, A., Arango, J., Settar, P., Fulton, J. E., O'Sullivan, N. P., Preisinger, R., Habier, D., Fernando, R., Garrick, D. J., Hill, W. G. and Dekkers, J. C. (2012). Genome-wide association analysis and genetic architecture of egg weight and egg uniformity in layer chickens. Animal Genetics 43 (Suppl. 1), 8796.CrossRefGoogle ScholarPubMed
Yoshida, A., Nagayasu, E., Horii, Y. and Maruyama, H. (2012). A novel C-type lectin identified by EST analysis in tissue migratory larvae of Ascaris suum . Parasitology Research 110, 15831586.Google Scholar
Zaros, L. G., Bricarello, P. A., Amarante, A. F., Rocha, R. A., Kooyman, F. N., De Vries, E. and Coutinho, L. L. (2010). Cytokine gene expression in response to Haemonchus placei infections in Nelore cattle. Veterinary Parasitology 171, 6873.CrossRefGoogle ScholarPubMed
Zinsstag, J., Ankers, P., Njie, M., Smith, T., Pandey, V. S., Pfister, K. and Tanner, M. (2000). Heritability of gastrointestinal nematode faecal egg counts in West African village N'Dama cattle and its relation to age. Veterinary Parasitology 89, 7178.Google Scholar