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Resistance to ETEC F4/F18–mediated piglet diarrhoea: opening the gene black box

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Abstract

Diarrhoea, a significant problem in pig rearing industry affecting pre- and post-weaning piglets is caused by enterotoxigenic Escherichia coli (ETEC). The ETEC are classified as per the fimbriae types which are responsible for bacterial attachment with enterocytes and release of toxins causing diarrhoea. However, genetic difference exists for susceptibility to ETEC infection in piglets. The different phenotypes found in pigs determine their (pigs’) susceptibility or resistance towards fimbrial subtypes/variants (F4ab, F4ac, F4ad and F18). Specific receptors are present on intestinal epithelium for attachment of these fimbriae, which do not express to same level in all animals. This differential expression is genetically determined and thus their genetic causes (may be putative candidate gene or mutations) render some animals resistant or susceptible to one or more fimbrial subtypes. Genetic linkage studies have revealed the mapping location of the receptor loci for the two most frequent variants F4ab and F4ac to SSC13q41 (i.e. q arm of 13th chromosome of Sus scrofa). Some SNPs have been identified in mucin gene family, transferring receptor gene, fucosyltransferase 1 gene and swine leucocyte antigen locus that are proposed to be linked mutations for resistance/susceptibility towards ETEC diarrhoea. However, owing to the variety of fimbrial types and subtypes, it would be difficult to identify a single causative mutation and the candidate loci may involve more number of genes/regions. In this review, we focus on the genetic mutations in genes involved in imparting resistance/susceptibility to F4 or F18 ETEC diarrhoea and possibilities to use them as marker for selection against susceptible animals.

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References

  • Abonyi, F.O., Omeh, C.V.O. and Machebe, N.S. 2012. Neonatal mortality of pigs in Nsukka, Southeast Nigeria. African Journal of Biotechnology, 11, 13228–13234.

    Article  CAS  Google Scholar 

  • Alustiza, F.E., Picco, N.Y., Bellingeri, R.V., Terzolo, H.R., Vivas, A.B. 2012. Frequency of virulence genes of Escherichia coli among newborn piglets from an intensive pig farm in Argentina. Rev Argent Microbiol. 44, 250–254.

    CAS  PubMed  Google Scholar 

  • Ateba, C.N., Mbewe, M. 2011. Detection of Escherichia coli O157:H7 virulence genes in isolates from beef, pork, water, human and animal species in the northwest province, South Africa: public health implications. Research in Microbiology, 162, 240–248.

    Article  CAS  PubMed  Google Scholar 

  • Bao, W.B., Ye, L., Pan, Z.Y., Zhu, J., Zhu, G.Q., Huang, X.G. and Wu, S.L. 2011. Beneficial genotype of swine FUT1 gene governing resistance to E. coli F18 is associated with important economic traits. Journal of Genetics, 90, 315–318.

    Article  PubMed  Google Scholar 

  • Bao, W.B., Ye, L., Chen, Z. and Liu, L., 2012. Relationship between the expression level of SLA-DQA and Escherichia coli F18 infection in piglets. Gene, 494, 140–144.

    Article  CAS  PubMed  Google Scholar 

  • Bertschinger, H.U., Stamm, M., Vögeli, P. 1993. Inheritance of resistance to oedema disease in the pig: experiments with an Escherichia coli strain expressing fimbriae 107. Veterinary Microbiology, 35, 79–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertschinger, H.U., Hofer, A., Stranzinger, G. and Vogeli, P., 2004. Breeding pigs resistant to Escherichia coli f18 in the field – a progress report from Switzerland. International Society for Animal Hygiène - Saint-Malo, 173–174.

  • Bessone, F.A., Bessone, G., Marini, S., Conde, M.B., Alustiza, F.E., Zielinski, G. 2017. Presence and characterization of Escherichia coli virulence genes isolated from diseased pigs in the central region of Argentina. Veterinary World, 10, 939–945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bijlsma, I.G.W. and Bouw, J., 1987. Inheritance of K88-mediated adhesion of Escherichia coli to jejuna brush borders in pigs: A genetic analysis. Veterinary Research Communication, 11, 509–518.

    Article  CAS  Google Scholar 

  • Bijlsma, I.G., de Nijs, A., van der Meer, C. and Frik, J.F., 1982. Different pig phenotypes affect adherence of Escherichia coli to jejunal brush borders by K88ab, K88ac, or K88ad antigen. Infection and Immunity, 37, 891–894.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bishop, S.C. and Mackenzie, K. A. 2003. Genetic management strategies for controlling infectious diseases in livestock populations. Genetics Selection Evolution, 35, S3–S17.

    Article  Google Scholar 

  • Borie, C., Monreal, Z., Guerrero, P., Sanchez, M.L., Martinez, J., Arellano, T.M., Prado, V., 1997. Prevalence and characterization of enterohaemorrhagic Escherichia coli isoated from healthy cattle and pigs slaughtered in Santiago, Chile. Archivos De Medicina Veterinaria, 29, 205–212.

    Google Scholar 

  • Bosworth, B.T., Dean-Nystrom, E.A., Casey, T.A., Neibergs, H.L. 1998. Differentiation of F18ab+ from F18ac+ Escherichia coli by single-strand conformational polymorphism analysis of the major fimbrial subunit gene (fedA). Clinical and Diagnostic Laboratory Immunology.5, 299–302.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chandler, D.S., Mynott, T.L., Luke, R.K.J. and Craven, J.A., 1994. The distribution and stability of Escherichia coli K88 receptor in the gastrointestinal tract of the pig, Veterinary Microbiology, 38, 203–215.

    Article  CAS  PubMed  Google Scholar 

  • Chen, J., Zhang, C., Zhang, N., Liu, G. 2019. Porcine endemic diarrhea virus infection regulates long noncoding RNA expression. Virology, 15:527:89–97.

  • Chethan, G. E., Garkhal, J., Sircar, S., Malik, Y. P. S., Mukherjee, R., Gupta, V. K., Sahoo, N. R., Agarwal, R. K., De, U. K. 2017a. Changes of haemogram and serum biochemistry in neonatal piglet diarrhoea associated with porcine rotavirus type A. Tropical Animal Health and Production, 49:1517–1522. doi: https://doi.org/10.1007/s11250-017-1357-x.

    Article  CAS  PubMed  Google Scholar 

  • Chethan, G. E., Garkhal, J., Sircar, S., Malik, Y. P. S., Mukherjee, R., Sahoo, N. R., Agarwal, R. K., De, U. K. 2017b. Immunomodulatory potential of β-glucan as supportive treatment in porcine rotavirus enteritis. Veterinary Immunology and Immunopathology, 191:36–43.

    Article  CAS  PubMed  Google Scholar 

  • Chin, J.J.C., Chapman, T.A. 2009. Impact on animal health: Designer probiotics for the management of intestinal health and colibacillosis in weaner pigs. In: Lee YK, Salminen S (eds), Handbook of probiotics and prebiotics. John Wiley & Sons, New Jersey, USA, 406–440.

    Google Scholar 

  • Clements, A., Young, J.C., Constantinou, N, Frankel, G. 2012. Infection strategies of enteric pathogenic Escherichia coli. Gut microbes, 3,71–87.

    Article  PubMed  PubMed Central  Google Scholar 

  • Coddens, A., Verdonck, F., Tiels, P., Rasschaert, K., Goddeeris, B.M., et al. 2007. The age-dependent expression of the F18+ E. coli receptor on porcine gut epithelial cells is positively correlated with the presence of histo-blood group antigens. Veterinary Microbiology, 122, 332–341.

    Article  CAS  PubMed  Google Scholar 

  • Coddens, A., Verdonck, F., Mulinge, M., Goyvaerts, E., Miry, C., Goddeeris, B., Duchateau, L., Cox E. 2008. The possibility of positive selection for both F18+ Escherichia coli and stress resistant pigs opens new perspectives for pig breeding. Veterinary Microbiology, 126, 210–215.

    Article  CAS  PubMed  Google Scholar 

  • Coddens, A., Diswall, M., Angstro¨m, J., Breimer, M. E. Goddeeris, B., Cox, E. and Teneberg S. 2009. Recognition of blood group ABH type 1 determinants by the FedF adhesin of F18-fimbriated Escherichia coli. Journal of Biological Chemistry, 284, 9713–9726.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conway, P.L., Welin, A. and Cohen, P.S., 1990. Presence of K88-specific receptors in porcine ileal mucus is age dependent. Infection and Immunity, 58, 3178–3182.

    CAS  PubMed  PubMed Central  Google Scholar 

  • De, U. K., Mukherjee, R, Prakash, C., Patel, B. H. M., Nandi, S., Dimri, U., Verma, A. K., Verma, M. R. 2019. Adding a bio-response modifier and zinc oxide to piglet weaner diets influences immunological responses to weaning. Animal Production Science, 59: 140–147

    Article  CAS  Google Scholar 

  • Dekker, J.J., Rossen, W., Buller, H.A. and Einerhand, A.W., 2002. The MUC family: an obituary. Trends in Biochemical Sciences, 27, 126–131.

    Article  CAS  PubMed  Google Scholar 

  • Dharmani, P., Srivastava, V., Kissoon-Singh, V. and Chadee, K., 2009. Role of intestinal mucins in innate host defense mechanisms against pathogen. Journal of Innate Immunity, 1, 123–135.

    Article  CAS  PubMed  Google Scholar 

  • Dubreuil, J.D., Isaacson, R.E., Schifferli, D.M. 2016. Animal Enterotoxigenic Escherichia coli. EcoSal Plus, doi:https://doi.org/10.1128/ecosalplus.ESP-0006-2016.

  • Edfors-Lilja, I., Wallgren, P. 2000. Escherichia coli and Salmonella Diarrhoea in Pigs. In: Axford RFE, Bishop SC, Nicholas FW, Owen JB (eds), Breeding for disease resistance in farm animals, 2nd edition. CABI publishing, Wallingford, UK, 253–267.

    Google Scholar 

  • Edfors-Lilja, I., Gustafsson, U., Duval-Iah, Y., Ellergren, H., Johansson, M., Juneja, R.K., Marklund, L. and Andersson, L., 1995. The porcine intestinal receptor for Escherichia coli K88ab, K88ac: regional localization on chromosome 13 and inuence of IgG response to the K88 antigen. Animal Genetics, 16, 237–242.

    Article  Google Scholar 

  • Edfors-Lilja, I., Wattrang, E., Marklund, L., Moller, M., Andersson-Eklund, L., Andersson, L., Fossum, C: 1998. Mapping quantitative trait loci for immune capacity in the pig. Journal of Immunology, 161, 829–835.

    CAS  Google Scholar 

  • Fairbrother, J.M., Nadeau, E., and Carlton L. Gyles. 2005. Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Animal Health Research Reviews, 6, 17–39.

    Article  CAS  PubMed  Google Scholar 

  • FAO, 2013. Food Outlook. URL- http://www.fao.org/docrep/012/ak341e/ak341e09. Accessed 02 Sept 2018.

  • Francis, D.H. 2002. Enterotoxigenic Escherichia coli infection in pigs and its diagnosis. Journal of Swine Health and Production, 10, 171–5.

    Google Scholar 

  • Frydendahl, K., Kare, J.T., Strodl, A.J., Fredholm, M. and Evans, G., 2003. Association between the porcine Escherichia coli F18 receptor genotype and phenotype and susceptibility to colonisation and post-weaning diarrhoea caused by E. coli O138:F18. Veterinary Microbiology, 93, 39–51.

    Article  PubMed  Google Scholar 

  • Fu, W-X., Liu, Y., Lu, X., Niu, X-Y., Ding, X-D., Liu, J-F., Zhang, Q. 2012. A Genome-Wide Association Study Identifies Two Novel Promising Candidate Genes Affecting Escherichia coli F4ab/F4ac Susceptibility in Swine. PLoS ONE 7(3): e32127. doi:https://doi.org/10.1371/journal.pone.0032127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuentes, M., Pijoan, C., Becton, L., Morrison, B. and Pieters, M. 2004. Inoculation of nonpathogenic Escherichia coli to control disease and reduce antibiotic usage. In: Proceedings of the 18th Congress IPVS, Hamburg, Germany, 18, 258.

    Google Scholar 

  • Fujii, J., Otsu, K., Zorzato, F., de Leon, S., Khanna, V.K., Weiler, J.E., O’Brien, P.J., MacLennan, D.H., 1991. Identification of a mutation in porcine ryanodine receptor associated with malignant hyperthermia. Science, 26, 448–451.

    Article  Google Scholar 

  • Gaastra, W. and Svennerholm A.M., 1996. Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends in Microbiology, 4, 444–452.

    Article  CAS  PubMed  Google Scholar 

  • Gibbons, R.A., Sellwood, R., Burrows, M. and Hunter, P.A., 1977. Inheritance of resistance to neonatal E. coli diarrhoea in the pig: Examination of the genetic system. Theoretical and Applied Genetics, 51, 65–70.

    Article  CAS  PubMed  Google Scholar 

  • Glenn, G.M., Francis, D.H., Danielsen, E.M. 2009. Toxin-mediated effects on the innate mucosal defenses: implications for enteric vaccines. Infection and Immunity, 77, 5206–5215.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goetstouwers, T., Van Poucke, M., Coddens, A., Nguyen, V.U., Melkebeek, V., Deforce, D., Cox, E. and Peelman, L.J. 2014a. Variation in 12 porcine genes involved in the carbohydrate moiety assembly of glycosphingolipids does not account for differential binding of F4 Escherichia coli and their fimbriae. BMC Genetics, 15:103. https://doi.org/10.1186/s12863-014-0103-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goetstouwers, T., Van Poucke, M., Nguyen, V.U., Melkebeek, V., Coddens, A, Deforce, D., Cox, E., Peelman, L.J. 2014b. F4-related mutation and expression analysis of the aminopeptidase N gene in pigs. Journal of Animal Science,, 92(5):1866–1873.

    Article  CAS  PubMed  Google Scholar 

  • Grange, P.A., Erickson, A.K., Anderson, T.J. and Francis, D.H., 1998. Characterization of the carbohydrate moiety of intestinal mucin-type sialoglycoprotein receptors for the K88ac fimbrial adhesin of Escherichia coli. Infection and Immunity, 66, 1613–1621.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grange, P.A., Erickson, A.K., Levery, S.B., Francis, D.H. 1999. Identification of an intestinal neutral glycosphingolipid as a phenotype-specific receptor for the K88ad fimbrial adhesin of Escherichia coli. Infection and Immunity, 67:165–172.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gresse, R., Chaucheyras-Durand, F., Fleury, M.A., van de Wiele, T., Forano, E., Blanquet- Diot, S. 2017. Gut microbiota dysbiosis in postweaning piglets: understanding the keys to health. Trends in Microbiology, 25, 851–873.

    Article  CAS  PubMed  Google Scholar 

  • Guerin, G., Duval-Iflah, Y., Bonneau, M., Bertaud, M., Guillaume, P. and Ollivier, L., 1993. Evidence for linkage between K88ab, K88ac intestinal receptors to Escherichia coli and transferrin loci in pigs, Animal Genetics, 24, 393–396.

    Article  CAS  PubMed  Google Scholar 

  • Guy, S.Z.Y., Thomson, P.C. and Hermesch, S. 2012. Selection of pigs for improved coping with health and environmental challenges: breeding for resistance or tolerance? Frontiers in Genetics, 3, 281, doi: https://doi.org/10.3389/fgene.2012.00281.

    Article  PubMed  PubMed Central  Google Scholar 

  • Henryon, M., P. Berg, J. Jensen and S. Andersen. 2001. Genetic variation for resistance to clinical and subclinical diseases exists in growing pigs. Animal Science, 73: 375–387.

    Article  Google Scholar 

  • Hesselager, M.O., Everest-Dass, A.V., Thaysen-Andersen, M., Bendixen E. and Packer, N.H. 2016. FUT1 genetic variants impact protein glycosylation of porcine intestinal mucosa. Glycobiology, 2016, 26, 607–622.

  • Hopwood, D.E., Hampson, D.J. 2003. Interactions between the intestinal microflora, diet and diarrhoea, and their influences on piglet health in the immediate post-weaning period. In: Pluske, J.R., Le Dividich, J., Verstegen, M.W.A. (eds), Weaning the pig: concepts and consequences. Wageningen Academic Publishers, Wageningen, Netherlands, 199–218.

  • Hu, D., Rampoldi, A., Girard, M., Gutzwiller, A., Neuenschwander, S. 2017; editors. Reduced antibiotic use in piglets: implementation of a breeding programme for E.coli F4ab/ac resistant pigs. In: Klimatwandel und Nutztiere: eine wechselseitige Beeinflussung. Kreuzer M., Lanzini T., Liesegang A., Bruckmaier R., Hess H.D. (eds). ETH-Schriftenreihe zur Tierernährung. 40:157–160.

  • Huang, X.Y., Yang, Q.L., Yuan, J.H. and Gun, S.B., 2015. Polymorphism and haplotype analyses of swine leukocyte antigen DQA exons 2, 3, 4, and their associations with piglet diarrhea in Chinese native pig. Genetics and Molecular Research, 14, 10461–10472.

    Article  CAS  PubMed  Google Scholar 

  • Huang, X., Yang, Q., Yuan, J., Liu, L., Sun, W., Jiang, Y., Zhao, S., Zhang, S., Huang, W. and Gun, S. 2016. Effect of Genetic Diversity in Swine Leukocyte Antigen-DRA Gene on Piglet Diarrhea. Genes, 7, 36, doi:https://doi.org/10.3390/genes7070036.

    Article  CAS  PubMed Central  Google Scholar 

  • Hur, J., Lee, J. H. 2016. Protective efficacy by various doses of Salmonella ghost vaccine candidate carrying enterotoxigenic Escherichia coli fimbrial antigen against neonatal piglet colibacillosis.Canadian Journal of Veterinary Research, 80:245–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hur, J., Barry D. Stein, John Hwa Lee. 2012. A vaccine candidate for post-weaning diarrhea in swine constructed with a live attenuated Salmonella delivering Escherichia coli K88ab, K88ac, FedA, and FedF fimbrial antigens and its immune responses in a murine model. Canadian Journal of Veterinary Research, 76, 186–194.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ikwap, K., Larsson, J., Jacobson, M., Owiny, D. O., Nasinyama, G. W., Nabukenya, I., Mattsson, S., Aspan, A. and Erume, J. 2016. Prevalence of adhesin and toxin genes in E. coli strains isolated from diarrheic and non-diarrheic pigs from smallholder herds in northern and eastern Uganda. BMC Microbiology, 16, 178. DOI https://doi.org/10.1186/s12866-016-0796-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imberechts, H., De Greve, H., Schlicker, C., Bouchet, H., Pohl, P., Charlier, G., Bertschinger, H., Wild, P., Vandekerckhove, J., Van Damme, J., Van Montagu, M. and Lintermans, P., 1992. Characterization of F107 fimbriae of Escherichia coli 107/86, which causes edema disease in pigs, and nucleotide sequence of the F107 major fimbrial subunit gene, fedA. Infection and Immunity, 60, 1963–1971.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobsen, M., Kracht, S.S., Esteso, G., Cirera, S., Edfors, I., Archibald, A., Bendixen, C., Andersson, L., Fredholm, M. and Jorgensen, C.B., 2009. Refined candidate region specified by haplotype sharing for Escherichia coli F4ab/F4ac susceptibility alleles in pigs. Animal Genetics, 41, 21–25.

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen, M., Cirera, S., Joller, D., Esteso, G., Kracht, S.S., Edfors, I., Bendixen, C., Archibald A.L., Vogeli P., Neuenschwander S., Bertschinger H.U., Rampoldi A., Andersson L., Fredholm M. and Jorgensen C.B., 2011. Characterisation of five candidate genes within the ETEC F4ab/ac candidate region in pigs. BMC Research Notes, 4, 225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji, H., Ren, J., Yan, X., Huang, X., Zhang, B., Zhang, Z. and Huang, L., 2011. The porcine MUC20 gene: molecular characterization and its association with susceptibility to enterotoxigenic Escherichia coli F4ab/ac. Molecular Biology Reports, 38, 1593–1601.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, X.P., Liu, Y.G., Xiong, Y.Z. and Deng, C.Y., 2005. Effects of FUT1 gene on meat quality and carcass traits in swine. Hereditas, 27, 566–570.

    CAS  PubMed  Google Scholar 

  • Johnson, A.M., Kaushik, R.S., Francis, D.H., Fleckenstein, J.M., Hardwidge, P.R. 2009. Heat- Labile Enterotoxin Promotes Escherichia coli Adherence to Intestinal Epithelial Cells. Journal of Bacteriology,191, 178–86.

    Article  CAS  PubMed  Google Scholar 

  • Joller, D., Jorgensen, C.B., Bertschinger, H.U., Python, P., Edfors, I., Cirera, S., Archibald, A.L., Burgi, E., Karlskov-Mortensen, P., Andersson, L., Fredholm, M. and Vogeli, P., 2009. Refined localization of the Escherichia coli F4ab/F4ac receptor locus on pig chromosome 13. Animal Genetics, 40, 749–752.

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen, C.B., Cirera, S., Anderson, S.I., Archibald, A.L., Raudsepp, T., Chowdhary, B., Edfors-Lilja, I., Andersson, L. and Fredholm, M., 2003a. Linkage and comparative mapping of the locus controlling susceptibility towards E. coli F4ab/ac diarrhoea in pigs. Cytogenetic and Genome Research, 102, 157–162.

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen, C.B., Cirera, S., Archibald, A., Andersson, L., Fredholm, M., Edfors-Lilja, I., 2003b. Porcine polymorphisms and methods for detecting them. International applications publish under the patent cooperation treaty (PCT). PCT/DK2003/000807 or WO2004/048606 A2.

  • Jorgensen, C.B., Cirera, S., Archibald, A.L., Andersson, L., Fredholm, M. and Edfors- Lilja, I., 2004. Porcine polymorphisms and methods for detecting them. International application published under the patent cooperation treaty (PCT). Journal of Animal Science, 75, 1388–1389.

    Google Scholar 

  • Kijima-Tanaka, M., Ishihara, K., Kojima, A., Morioka, A., Nagata, R., Kawanishi, M., Nakazawa, M., Tamura, Y., Takahashi, T. 2005. A national surveillance of Shiga toxin-producing Escherichia coli in food-producing animals in Japan. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health, 52, 230–237.

    Article  CAS  PubMed  Google Scholar 

  • Knol, E. F., Nielsen, B., Knap, P. W. 2016. Genomic selection in commercial pig breeding. Animal Frontiers, 6 : 15–22,

    Article  Google Scholar 

  • Lee, S.I., Kang, S.G., Kang, M.L. and Yoo, H.S., 2008. Development of multiplex polymerase chain reaction assays for detecting enterotoxigenic Escherichia coli and their application to field isolates from piglets with diarrhea. Journal of Veterinary Diagnostic Investigation, 20, 492–496.

    Article  PubMed  Google Scholar 

  • Li, Y., Qiu, X., Li, H. and Zhang, Q., 2007. Adhesive patterns of Escherichia coli F4 in piglets of three breeds. Journal of Genetics and Genomics, 34, 591–599.

    Article  CAS  PubMed  Google Scholar 

  • Linden, S.K., Florin, T.H. and McGuckin, M.A., 2008. Mucin dynamics in intestinal bacterial infection, PLoS One, 3, e3952. https://doi.org/10.1371/journal.pone.0003952.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Y., Xia, R.W., Yin, X.M., Huo, Y.J., Zhu, G.Q., Wu, S.L., Bao, W.B. 2015a. Expression Level of FUT1 Gene in Different Pig Populations and its Relationship with ETEC F18 Resistance. SOJ Veterinary Science, 1, 1–5. DOI: https://doi.org/10.15226/2381-2907/1/2/00106.

    Article  CAS  Google Scholar 

  • Liu L.X., Zhao, S.G., Lu, H.N., Yang, Q.L., Huang, X.Y., Gun, S.B. 2015b. Association between polymorphisms of the swine MHC-DQA gene and diarrhoea in three Chinese native piglets. International Journal of Immunogenetics, 42, 208–216.

    Article  CAS  PubMed  Google Scholar 

  • Loos, M., Geens, M., Schauvliege, S., Gasthuys, F., van der Meulen J, Dubreuile, J.D., Goddeeris, B.M., Niewold, T., Cox, E. 2012. Role of heat-stable enterotoxins in the induction of early immune responses in piglets after infection with enterotoxigenic Escherichia coli. PLOS One. 7:e41041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo, Y., Qiu, X., Li, H. and Zhang, Q. 2010. Association between the Polymorphism in FUT1 Gene and the Resistance to PWD and ED in Three Pig Breeds. Asian-Australasian Journal of Animal Sciences, 23, 1268–1275.

    Article  CAS  Google Scholar 

  • Luppi, A. 2017. Swine enteric colibacillosis: diagnosis, therapy and antimicrobial resistance. Porcine Health Management, 3, 16.

    Article  PubMed  PubMed Central  Google Scholar 

  • Luppi, A., Gibellini, M., Gin, T., Vangroenweghe, F., Vandenbroucke, V., Bauerfeind, R., Bonilauri, P., Labarque, G., and Hidalgo, A. 2016. Prevalence of virulence factors in enterotoxigenic Escherichia coli isolated from pigs with post-weaning diarrhea in Europe. Porcine Health Management, 2, 20.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martins, R.P., Da Silva, M.C., Dutra, V., Nakazato, L., Leite Dda, S. 2011. Prevalence of enterotoxigenic and Shiga toxin-producing Escherichia coli in pigs slaughtered in Mato Grosso, Brazil. Journal of Infection in Developing Countries, 5, 123–127.

    Article  PubMed  Google Scholar 

  • Matías, J., Berzosa, M., Pastor, Y., Irache, J. M. and Gamazo C. 2017. Maternal Vaccination. Immunization of Sows during Pregnancy against ETEC Infections. Vaccines, 5, 48.

    Article  CAS  PubMed Central  Google Scholar 

  • Meijerink, E., Fries, R., Vogeli, P., Masabanda, J., Wigger, G., Stricker, C., Neuenschwander, S., Bertschinger H.U. and Stranzinger G., 1997. Two alpha (1,2) fucosyltransferase genes on porcine chromosome 6q11 are closely linked to the blood group inhibitor (S) and Escherichia coli F18 receptor (ECF18R) loci. Mammalian Genome, 8, 736–741.

    Article  CAS  PubMed  Google Scholar 

  • Meijerink, E., Neuenschwander, S., Fries, R., Dinter, A., Bertschinger, H.U., Stranzinger, G. and Vögeli, P. 2000. A DNA polymorphism influencing alpha (1,2) fucosyltransferase activity of the pig FUT1 enzyme determines susceptibility of small intestinal epithelium to Escherichia coli F18 adhesion. Immunogenetics, 52, 129–136.

    Article  CAS  PubMed  Google Scholar 

  • Melkebeek, V., Rasschaert, K., Bellot, P., Tilleman, K., Favoreel, H., Deforce, D., De Geest, B.G., Goddeeris, B.M., Cox, E. 2012. Targeting aminopeptidase N, a newly identified receptor for F4ac fimbriae, enhances the intestinal mucosal immune response. Mucosal Immunology, 5, 635–645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mesonero-Escuredo, S., Strutzberg-Minder, K., Casanovas, C., Segalés, J. 2018.Viral and bacterial investigations on the aetiology of recurrent pig neonatal diarrhoea cases in Spain. Porcine Health Management. 4:5.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moehle, C., Ackermann, N., Langmann, T., Aslanidis, C., Kel, A., Kel-Margoulis, O., Schmitz-Madry, A., Zahn, A., Stremmel, W. and Schmitz, G., 2006. Aberrant intestinal expression and allelic variants of mucin genes associated with inflammatory bowel disease. Journal of Molecular Medicine, 84, 1055–1066.

    Article  CAS  PubMed  Google Scholar 

  • Moncada, D.M., Kammanadiminti, S.J. and Chadee, K., 2003. Mucin and Toll-like receptors in host defense against intestinal parasites. Trends in Parasitology, 19, 305–311.

    Article  CAS  PubMed  Google Scholar 

  • Moredo, F.A., Cappuccio, J.A., Insarralde, L., Perfumo, C.J., Quiroga, M.A., Leotta, G.A. 2012. [Genotypic characterization of toxigenic Escherichia coli isolated from pigs with postweaning diarrhea (PWD) and edema disease (ED)]. Article in Spanish. Rev Argent Microbiology, 44, 85–88.

    Google Scholar 

  • Nagy, B. and Fekete, P.Z., 1999. Enterotoxigenic Escherichia coli (ETEC) in farm animals.Veterinary Research, 30, 259–284.

    CAS  PubMed  Google Scholar 

  • Nagy, B. and Fekete, P.Z., 2005. Enterotoxigenic Escherichia coli in veterinary medicine. International Journal of Medical Microbiology, 295, 443–454.

    Article  CAS  PubMed  Google Scholar 

  • Nagy, B., Whipp, S.C., Imberechts, H., Bertschinger, H.U., Dean-Nystrom, E.A., Casey, T.A. and Salajka, E., 1997. Biological relationship between F18ab and F18ac fimbriae of enterotoxigenic and verotoxigenic Escherichia coli from weaned pigs with oedema disease or diarrhoea. Microbial Pathogenesis, 22, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Nakazawa, M., Akiba, M. 1999. Swine as a potential reservoir of Shiga toxin-producing Escherichia coli O157: H7 in Japan. Emerging Infectious Diseases, 5:833–834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen, V.U., Goetstouwers, T., Coddens, A., Van Poucke, M., Peelman, L., Deforce, D., Melkebeek, V., Cox, E. 2013. Differentiation of F4 receptor profiles in pigs based on their mucin 4 polymorphism, responsiveness to oral F4 immunization and in vitro binding of F4 to villi. Veterinary Immunology and Immunopathology, 152, 93–100.

    Article  CAS  PubMed  Google Scholar 

  • Okello, E., Moonens, K., Erume, J., De Greve, H. 2015. Enterotoxigenic Escherichia coli strains are highly prevalent in Ugandan piggeries but disease outbreaks are masked by antibiotic prophylaxis. Tropical Animal Health and Production, 47, :117–22.

    Article  PubMed  Google Scholar 

  • Olsen, J., Kokholm, K., Noren, O., Sjöström, H. 1997. Structure and expression of aminopeptidase N. Adv Exp Med Biol. 421, 47–57.

    Article  CAS  PubMed  Google Scholar 

  • Ouyang, J., Zeng, W., Ren, J., Yan, X., Zhang, Z., Yang, M., Han, P., Huang, X., Ai, H. and Huang, L. 2012. Association of B3GNT5 polymorphisms with susceptibility to ETEC F4ab/ac in the white Duroc × Erhualian intercross and 15 outbred pig breeds. Biochemical Genetics, 50, 19–33.

    Article  CAS  PubMed  Google Scholar 

  • Pastoret, S., Ameels, H., Bossiroy, F., Decreux, A., De Longueville, F., Thomas, A. And Desmecht, D. 2012. Detection of disease resistance and susceptibility alleles in pigs using oligonucleotide microarray hybridization. Journal of Veterinary Diagnostic Investigation, 24, 479–488.

    Article  PubMed  Google Scholar 

  • Peelman, L.J. 1999. Genetic investigation of the resistance mechanisms of the pig against diarrhea caused by E. coli. Verh K AcadGeneeskd Belg., 61, 489–515.

  • Peng, Q.L., Ren, J., Yan, X.M., Huang, X., Tang, H., Wang, Y., Zhang, B. and Huang, L.S., 2007. The g.243a>g mutation in intron 17 of MUC4 is significantly associated with susceptibility/resistance to ETEC F4ab/ac infection in pigs. Animal Genetics, 38, 397–400.

    Article  CAS  PubMed  Google Scholar 

  • Pickett, C.L., Twiddy, E.M., Belisle, B.W., Holmes, R.K. 1986. Cloning of genes that encode a new heat-labile enterotoxin of Escherichia coli. Journal of Bacteriology, 165, 348–352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pittman, J.S. 2010. Enteritis in grower-finisher pigs caused by F18-positive Escherichia coli. Journal of Swine Health and Production, 18, 81–86.

    Google Scholar 

  • Pluske, J.R., Diana L. Turpin, Jae-Cheol Kim. 2018. Gastrointestinal tract (gut) health in the young pig. Animal Nutrition, 4, 187–196.

    Article  PubMed  PubMed Central  Google Scholar 

  • Python, P. 2003. Genetic host determinants associated with the adhesion of E. coli with fimbriae F4 in swine. ETH. https://doi.org/10.3929/ethz-a-004630253.

  • Python, P., Jörg, H., Neuenschwander, S., Hagger, C., Stricker, C., Bürgi, E., Bertschinger, H.U., Stranzinger, G. and Vögeli, P. 2002. Fine-mapping of the intestinal receptor locus for enterotoxigenic Escherichia coli F4ac on porcine chromosome 13. Animal Genetics, 33, 441–447.

    Article  CAS  PubMed  Google Scholar 

  • Python, P., Jorg, H., Neuenschwander, S., Asai-Coakwell, M., Hagger, C., Burgi, E., Bertschinger, H.U., Stranzinger, G., & Vogeli, P. 2005. Inheritance of the F4ab, F4ac and F4ad E. coli receptors in swine and examination of four candidate genes for F4acR. Journal of Animal Breeding and Genetics, 122 (Suppl. 1), 5–14.

    Article  CAS  PubMed  Google Scholar 

  • Rampoldi, A., Jacobsen, M.J., Bertschinger, H.U., Joller, D., Burgi, E., Vogeli, P., Andersson, L., Archibald, A.L., Fredholm, M., Jorgensen, C.B. and Neuenschwander, S., 2011. The receptor locus for Escherichia coli F4ab/F4ac in the pig maps distal to the MUC4-LMLN region. Mammalian Genome, 22, 122–129.

    Article  CAS  PubMed  Google Scholar 

  • Rampoldi, A., Bertschinger, H.U., Bürgi, E., Dolf, G., Sidler, X. A., Bratus, A.P., Vögeli, P. and Neuenschwander, S. 2014. Inheritance of porcine receptors for enterotoxigenic Escherichia coli with fimbriae F4ad and their relation to other F4 receptors. Animal, 8, 859–866.

    Article  CAS  PubMed  Google Scholar 

  • Rasschaert, K., Verdonck, F., Goddeeris, B.M., Duchateau, L. and Cox, E., 2007. Screening of pigs resistant to F4 enterotoxigenic Escherichia coli (ETEC) infection. Veterinary Microbiology, 123, 249–253.

    Article  CAS  PubMed  Google Scholar 

  • Ravi, M., Ngeleka, M., Kim, S.H., Gyles, C., Berthiaume, F., Mourez, M., Middleton, D. and Simko, E. 2007. Contribution of AIDA-I to the pathogenicity of a porcine diarrheagenic Escherichia coli and to intestinal colonization through biofilm formation in pigs. Veterinary Microbiology, 120, 308–319.

    Article  CAS  PubMed  Google Scholar 

  • Reik, T.R., Rempel, W.E., McGrath, C.J., Addis, P.B., 1983. Further evidence on the inheritance of halothane reaction in pigs. Journal of Animal Science, 57, 826–831.

    Article  CAS  PubMed  Google Scholar 

  • Reiner, G. 2009. Investigations on genetic disease resistance in swine—A contribution to the reduction of pain, suffering and damage in farm animals. Applied Animal Behaviour Science, 118, 217–221.

    Article  Google Scholar 

  • Ren, J., Yan, X., Ai, H., Zhang, Z., Huang, X., Ouyang, J., Yang, M., Yang, H., Han, P. and Huang, L., 2012. Susceptibility towards enterotoxigenic Escherichia coli F4ac diarrhea is governed by the MUC13 gene in Pig, PLoS ONE, 7(9) :e44573.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renard, C., Hart, E., Sehra, H., Beasley, H., Coggill, P., Howe, K., Harrow, J., Gilbert, J., Sims, S., Rogers, J., Ando, A., Shigenari, A., Shiina, T., Inoko, H., Chardon, P. and Beck, S. 2006. The genomic sequence and analysis of the swine major histocompatibility complex. Genomics, 88, 96–110.

    Article  CAS  PubMed  Google Scholar 

  • Riis Poulsen, A.S., Luise, D., Curtasu, M.V., Sugiharto, S., Canibe, N., Trevisi, P., Lauridsen, C. 2018. Effects of alpha-(1,2)-fucosyltransferase genotype variants on plasma metabolome, immune responses and gastrointestinal bacterial enumeration of pigs pre- and post-weaning. PLoS ONE, 13, e0202970.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ringel, J. and Lohr, M., 2003. The MUC gene family: Their role in diagnosis and early detection of pancreatic cancer. Molecular Cancer, 2, 9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy R., Mondal, T. and Moktan M. W. 2018. Patterns of pre – weaning piglet mortality and economic losses in field condition. African Journal of Agricultural Research, 13, 1291–1296.

    Article  Google Scholar 

  • Ruan, G.R., Y.Y. Xing, Y. Fan, R.M. Qiao, X.F. He, B. Yang, N.S. Ding, J. Ren, L.S. Huang, S.J. Xiao. 2013. Genetic variation at RYR1, IGF2, FUT1, MUC13, and KPL2 mutations affecting production traits in Chinese commercial pig breeds. Czech Journal of Animal Science, 58, 65–70.

    Article  CAS  Google Scholar 

  • Rutter, J.M., Burrows, M.R., Sellwood, R. and Gibbons, R.A., 1975. A genetic basis for resistance to enteric disease caused by E. Coli. Nature, 257, 135–136.

    Article  CAS  PubMed  Google Scholar 

  • Schroyen, M., Stinckens, A., Verhelst, R., Cox, E., Niewold, T. and Buys, N., 2012a. Susceptibility of piglets to enterotoxigenic E. coli is not related to the expression of MUC13 and MUC20. Animal Genetics, 43, 324–327.

    Article  CAS  PubMed  Google Scholar 

  • Schroyen, M., Stinckens, A., Verhelst, R., Niewold, T. and Buys, N., 2012b. The search for the gene mutations underlying enterotoxigenic Escherichia coli F4ab/ac susceptibility in pigs: a review. Veterinary Research, 43, 70. doi: https://doi.org/10.1186/1297-9716-43-70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sellwood, R., Gibbons, R.A., Jones, G.W., Rutter, J.M., 1975. Adhesion of enteropathogenic Escherichia coli to pig intestinal brush borders: the existence of two pig phenotypes. Journal of Medical Microbiology, 8, 405–411.

    Article  CAS  PubMed  Google Scholar 

  • Seo, H., Lu, T., Nandre, R. M., Duan, Q., Zhang, W. 2019.Immunogenicity characterization of genetically fused or chemically conjugated heat-stable toxin toxoids of enterotoxigenic Escherichia coli in mice and pigs.FEMS Microbiology Letters,. 366(4). pii: fnz037.

    Article  Google Scholar 

  • Shakuntala, I., Sanjukta, R.K., Das, S., Puro, K., Ghatak, S. Rajkhowa, S., Milton, A.A.P. and Sen. A. 2017. Occurrence and Characterization of Escherichia coli Isolated from Diarrhoeic Piglets in Meghalaya. Indian Journal of Hill Farming, 88–92.

  • Shi, Q.S. 2003. The review of the receptors of ETEC F4. Pigs and Poultry, 23, 33–35.

    Google Scholar 

  • Shimamura, T., Ito, H., Shibahara, J., Watanabe, A., Hippo, Y., Taniguchi, H., Chen, Y., Kashima, T., Ohtomo, T., Tanioka, F., Iwanari, H., Kodama, T., Kazui, T., Sugimura, H., Fukayama, M. and Aburatani, H., 2005. Over expression of MUC13 is associated with intestinal-type gastric cancer. Cancer Science, 96 , 265–273.

    Article  CAS  PubMed  Google Scholar 

  • Sinha, R., Sahoo, N.R., Kumar, P., Qureshi, S., Kumar, A., Ravikumar, G.V.P.P.S., Bhushan, B., 2018a. Comparative jejunal expression of MUC 13 in Indian native pigs differentially adhesive to diarrhoeagenic E. Coli. Journal of Applied Animal Research, 46, 107–111.

    Article  CAS  Google Scholar 

  • Sinha, R., Sahoo, N.R., Shrivastava, K., Kumar, P., Qureshi, S., Kumar, A., Ravikumar, G.V.P.P.S., and Bhushan, B., 2018b. Effect of Mucin13 gene polymorphism on diarrhoeagenic E. coli adhesion pattern and its expression analysis in native Indian pigs. Archives Animal Breeding, 61, 321–328.

    Article  Google Scholar 

  • Sinha, R., Sahoo, N.R., Shrivastava, K., Kumar, P., Qureshi, S., Kumar, A., Ravikumar, G.V.P.P.S. and Bhushan, B., 2019. Bioinformatic analysis of Mucin 13 gene (partial sequence) in Indian native pig and itsimportance in piglet diarrhoea resistance. Indian Journal of Animal Research, DOI: https://doi.org/10.18805/ijar.B-3757

  • Sun, Y. and Sung Woo Kim. 2017. Intestinal challenge with enterotoxigenic Escherichia coli in pigs, and nutritional intervention to prevent postweaning diarrhea. Animal Nutrition, 3, 322e330.

    Google Scholar 

  • Todorovic, D., Velhner, M., Ljubojević, D., Pajić, M. and Milanov, D., 2015. Resistance to fluoroquinolones in Escherichia coli from pigs. Arhivveterinarske medicine, 8 , 103–112.

    Google Scholar 

  • Toledo, A., Gomez, D., Cruz, C., Carreon, R., Lopez, J., Giono S. and Castro, A.M. 2012. Prevalence of virulence genes in Escherichia coli strains isolated from piglets in the suckling and weaning period in Mexico. Journal of Medical Microbiology, 61, 148–156.

    Article  CAS  PubMed  Google Scholar 

  • Uy, M.R.D., Garcia, G.G., Aquino, J.P., Sampang, J.F., Abuyuan, R.V. and Mingala, C.N. 2018. Gene Expression Analysis of Swine Leukocyte Antigen (SLA-1 and SLA-2) Involved in Porcine Pre-Weaning and Post-Weaning Diarrhea in Nueva Ecija, Philippines. Philippine Journal of Science, 147, 473–481.

    Google Scholar 

  • Van den Broeck, W., Cox, E., Oudega, B., Goddeeris, B.M. 2000. The F4 fimbrial antigen of Escherichia coli and its receptors. Veterinary Microbiology, 71, 223–244.

    Article  PubMed  Google Scholar 

  • van Zijderveld, F.G., Anakotta, J., Brouwers, R.A., van Zijderveld, A.M., Bakker, D. and de Graaf, F.K. 1990. Epitope analysis of the F4 (K88) fimbrial antigen complex of enterotxigenic Escherichia coli by using monoclonal antibodies. Infection and Immunity, 58, 1870–1878.

    PubMed  PubMed Central  Google Scholar 

  • Vidotto, M.C., Natália C.S. de Lima; Juliana T.T. Fritzen; Júlio C. de Freitas; Emerson J. Venâncio; Mario A. Ono. 2009. Frequency of virulence genes in Escherichia coli strains isolated from piglets with diarrhea in the North Parana State, Brazil. Brazilian Journal of Microbiology, 40, 199–204.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vӧgeli, P., Bertschinger, H.U., Stamm, M., Stricker, C., Hagger, C., Fries, R., Rapacz, J. and Stranzinger, G., 1996. Genes specifying receptors for F18 fimbriated Escherichia coli, causing oedema disease and postweaning diarrhoea in pigs, map to chromosome 6. Animal Genetics, 27, 321–328.

    Google Scholar 

  • Vogeli, P., Meijerink, E., Fries, R., Neuenschwander, S., Vorlander, N., Stranzinger, G., Bertschinger, H.U., 1997. A molecular test for the detection of E. coli F18 receptors: a breakthrough in the struggle against edema disease and post-weaning diarrhea. Schweizer Arch. Tierheilk., 139, 479–484.

    CAS  Google Scholar 

  • Vu-Khac, H., Holoda, E., Pilipcinec, E., Blanco, M., Blanco, J.E., Dahbi, G., Mora, A., Lopez, C., Gonzalez, E.A, and Blanco, J. 2007. Serotypes, virulence genes, intimin types and pfge profiles of Escherichia coli isolated from piglets with diarrhoea in Slovakia. The Veterinary Journal, 174,176–187.

    Article  CAS  PubMed  Google Scholar 

  • Walsh, M.D., Young, J.P., Leggett, B.A., Williams, S.H., Jass, J.R. and McGuckin, M.A., 2007. The MUC13 cell surface mucin is highly expressed by human colorectal carcinomas. Human Pathology, 38, 883–892.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Ren, J., Lan, L., Yan, X., Huang, X., Peng, Q., Tang, H., Zhang, B., Ji, H. and Huang, L. 2007. Characterization of polymorphisms of transferrin receptor and their association with susceptibility to ETEC F4ab/ac in pigs. Journal of Animal Breeding and Genetics, 124, 225–229.

    Article  CAS  PubMed  Google Scholar 

  • Wang, H., Zhong, Z., Luo, Y., Cox, E., Devriendt, B. 2019. Heat-Stable Enterotoxins of Enterotoxigenic Escherichia coli and Their Impact on Host Immunity. Toxins, 11: 24; doi:https://doi.org/10.3390/toxins11010024

    Article  CAS  PubMed Central  Google Scholar 

  • Wu, Z., Feng, H., Cao, Y., Huang, Y., Dai, C., Wu, S. and Bao, W. 2018. New Insight into the Molecular Mechanism of the FUT2 Regulating Escherichia coli F18 Resistance in Weaned Piglets. International Journal of Molecular sciences, 19, 3301.

    Article  CAS  PubMed Central  Google Scholar 

  • Yan, X.M., Ren, J., Guo, Y.M., Ding, N.S., Chen, K.F., Gao, J., Ai, H.S., Chen, C.Y., Ma, J.W. and Huang, L.S., 2003. Research on the genetic variations of a1-fucosytransferase (FUT1) gene in 26 pig breeds. Yi Chuan Xue Bao, 30, 830–840.

    CAS  PubMed  Google Scholar 

  • Yan, X., Huang, X., Ren, J., Zou, Z., Yang, S., Ouyang, J., Zeng, W., Yang, B., Xiao, S., Huang, L. 2009. Distribution of Escherichia coli F4 adhesion phenotypes in pigs of 15 Chinese and Western breeds and a White Duroc x Erhualian intercross. Journal of Medical Microbiology, 58, 1112–1117.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Q.L., Kong, J.J., Wang, D.W., Zhao, S.G. and Gun, S.B. 2013. Swine Leukocyte Antigen-DQA Gene Variation and Its Association with Piglet Diarrhea in Large White, Landrace and Duroc. Asian- Australasian Journal of Animal Sciences, 26, 1065–1071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, Q.L., Zhao, S.G., Wang, D.W. and Feng, Y., 2014. Association between genetic polymorphism in the swine leukocyte antigen-DRA gene and piglet diarrhoea in three Chinese pig breeds. Asian- Australasian Journal of Animal Sciences, 27, 1228–1235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, W., Berberov, E.M., Freeling, J., He, D., Moxley, R.A. and Francis, D.H. 2006. Significance of heat-stable and heat-labile enterotoxins in porcine colibacillosis in an additive model for pathogenicity studies. Infection and Immunity, 74:3107–3114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, W., Zhao, M., Ruesch, L., Omot, A. and Francis, D. 2007. Prevalence of virulence genes in Escherichia coli strains recently isolated from young pigs with diarrhea in the US. Veterinary Microbiology, 123, 145–152.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, B., Ren, J., Yan, X., Huang, X., Ji, H., Peng, Q., Zhang, Z. and Huang, L. 2008. Investigation of the porcine MUC13 gene: isolation, expression, polymorphisms and strong association with susceptibility to enterotoxigenic Escherichia coli F4ab/ac. Animal Genetics, 39, 258–266.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H., Xu, Y., Zhang, Z., You, J., Yang, Y., Li, X. 2018. Protective immunity of a Multivalent Vaccine Candidate against piglet diarrhea caused by enterotoxigenic Escherichia coli (ETEC) in a pig model. Vaccine,36:723–728.

    Article  CAS  PubMed  Google Scholar 

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Sinha, R., Sahoo, N.R., Shrivastava, K. et al. Resistance to ETEC F4/F18–mediated piglet diarrhoea: opening the gene black box. Trop Anim Health Prod 51, 1307–1320 (2019). https://doi.org/10.1007/s11250-019-01934-x

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