OMIA 001088-9823 : Neonatal diarrhoea, K88/F4, resistance to in Sus scrofa

See the equivalent entry at NCBI

Mendelian trait/disorder: yes

Mode of inheritance: Autosomal Recessive

Considered a defect: no

Key mutation known: no

Species-specific name: K88 scours

Species-specific symbol: FbcR

Species-specific description: Neonatal diarrhoea in piglets is often caused by strains of Escherichia coli bacteria that have a cell-surface antigen called K88 (renamed F4), which combines with a glycoprotein receptor on the wall of a piglet's intestine, enabling the bacteria to attach themselves to the intestine. Such E. coli are called Enterotoxigenic Escherichia coli (ETEC). Once attached, the ETEC proliferate, releasing enterotoxins and thus producing diarrhoea, which can lead to high mortality. Certain piglets lack the intestinal receptor to F4, and are therefore resistant to F4 bacteria and hence to diarrhoea caused by F4 strains. There are several different antigenic variants of F4 (ab, ac, ad), and it seems that there is a separate receptor for each. The presence or absence of at least two of these receptors (for F4ab and F4ac) is determined for each receptor by one of two closely-linked genes on chromosome 13. The immunological and population-genetic implications of segregation at these loci are very interesting: the result is selection against heterozygotes, as explained by Nicholas (2010, Introduction to Veterinary Genetics, 3rd edn, pp. 132-133).

Inheritance: Gibbons et al. (1977) provided convincing evidence that susceptibility to K88 Escherichia coli, due to the presence of a receptor for K88 E. coli on the brush-border surface of the intestine, is a single-locus autosomal dominant trait; and that resistance (due to lack of the K88 receptor) is recessive. They proposed the symbols S and s for the susceptible and resistant allele, respectively.

Mapping: Gibbons et al. (1977) reported some evidence for linkage of the S/s locus and the transferrin (Tf) locus). Bonneau et al. (1990) reported similar evidence. Vögeli et al. (1992) reported that the K88 locus is loosely linked to the L blood-group-system locus, in what was then called linkage group IV. Marklund et al. (1993) showed that the L blood-group-system locus maps to chromosome SSC4. As Marklund et al. (1993) noted, this evidence did not agree with proposed S/s linkage with Tf, because the Tf locus had by then been mapped to chromosome SSC13. Marklund et al. (1993) concluded that that the K88/blood-group-system L linkage was probably a false positive. This conclusion was reinforced by subsequent evidence supporting linkage to Tf, e.g. by Guérin et al. (1993) and Edfors-Lilja et al. (1995), the latter authors putting the SSC13 location beyond any doubt, with the K88 loci being located 7.4cM proximal to Tf. The SSc13 map location was refined by Python et al. (2002) who located the K88-receptor locus (now called F4acR) between microsatellites S0068 and Sw1030, with recombination fractions 0.04 and 0.05, respectively. Jørgensen et al. (2003) refined the location even further, to 3.8 cM between microsatellites Sw207 and S0075, and physically mapped it to SSC13q41, enabling them to identify two comparative positional regions on human chromosome HSA3, which should provide potential comparative positional candidate genes.

The location was subsequently refined to 14Mb by Joller et al. (2009), to around 1.5Mb by Jacobsen et al. (2010), and to around 620kb by Rampoldi et al. (2010).

A GWAS on 301 phenotyped pigs each genotyped with 62,163 SNPs via the Illumina PorcineSNP60 BeadChip by Fu et al. (2012) confirmed the location to a 2.6Mb region of SSC13q41.

In the same year, Ren et al. (2012) reported a linkage analysis from a genome scan involving 194 microsatellites genotyped on each of 755 phenotyped F2 pigs from a White Duroc × Erhualian resource population, which also confirmed the candidate region. Fine mapping reduced the candidate region to 2.3MB. These same authors then conducted a GWAS and LDLA on the same 755 F2 animals genotyped with the Illumina PorcineSNP60 BeadChip, narrowing down the region to 360kb which contains 4 candidate genes, namely SLC12A8, HEG1, ITGB5 and MUC13.

Goetstouwers et al. (2014) conducted a GWAS on 120 F4ab/acR phenotyped pigs (52 non-adhesive and 68 strong adhesive pigs), each genotyped with the Porcine SNP60 BeadChip (Illumina), yielding 55,289 informative SNPs. The authors reported that a "refined candidate region (chr13: 144,810,100–144,993,222) for F4ab/ac ETEC susceptibility was identified with MUC13 adjacent to the distal part of the region. This candidate region lacks annotated genes and contains a sequence gap based on the sequence of the porcine GenomeBuild 10.2."

Molecular basis: By 2000, it was evident that the K88/F4 receptor was a mucin-like glycoprotein (Jin and Zhao, 2000; Van den Broeck et al., 2000). Noticing that a mucin gene called MUC4 was located in the orthologous human HSA3 regions (see Mapping section above), Peng et al. (2007) showed that the porcine MUC4 gene did, indeed, map to the candidate porcine region (SSC13q41), and, as expected with a gene in such close proximity, found strong association of a MUC4 polymorphism with susceptibility/resistance to F4 E. coli. Similar evidence was provided for another mucin gene, MUC13, by Zhang et al. (2008); for three other genes (SLC12A8, MYLK and KPNA1) by Huang et al. (2008); and for yet another mucin gene, MUC20, by Ren et al. (2009) and Ji et al. (2011).

By 2011, the pig genome assembly had revealed a total of 18 annotated genes in the candidate region (Jacobsen et al., 2011). Doubt was cast on MUC13 and MUC20 as causal genes by Schroyen et al. (2012), who showed that expression of these two genes is not associated with resistance/susceptibility.

However, Ren et al. (2012) provided data showing that while MUC13 is expressed in susceptible and resistant pigs, all resistant pigs across a range of breeds are homozygous for a MUC13 allele (called MUC13A) that encodes a MUC13 peptide with a specific tandem repeat structure (ASTSAPAAG). The other allele at this locus (MUC13B) results in a MUC13 peptide with a different tandem repeat structure (TPTPTTTP) to which pathogenic E coli can attach.

(Text written by FN, with very helpful input from Merete Fredholm and Claus Jørgensen)

From the results of their GWAS (see Mapping section above), Goetstouwers et al. (2014) hypothesised "that a porcine orphan gene or trans-acting element present in the identified candidate region has an effect on the glycosylation of F4 binding proteins and therefore determines the F4ab/ac ETEC susceptibility in pigs." Thus the causal mutation for this classic case of genetic resistance remains unknown.

References


Note: the references are listed in reverse chronological order (from the most recent year to the earliest year), and alphabetically by first author within a year.
2016 Ji, H.Y., Yang, B., Zhang, Z.Y., Ouyang, J., Yang, M., Zhang, X.F., Zhang, W.C., Su, Y., Zhao, K.W., Xiao, S.J., Yan, X.M., Ren, J., Huang, L.S. :
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Nguyen, U.V., Coddens, A., Melkebeek, V., Devriendt, B., Goetstouwers, T., Poucke, M.V., Peelman, L., Cox, E. :
High susceptibility prevalence for F4(+) and F18(+)Escherichia coli in Flemish pigs. Vet Microbiol :, 2016. Pubmed reference: 26822901. DOI: 10.1016/j.vetmic.2016.01.014.
Roubos-van den Hil, P.J., Litjens, R., Oudshoorn, A.K., Resink, J.W., Smits, C.H. :
New perspectives to the enterotoxigenic E. coli F4 porcine infection model: Susceptibility genotypes in relation to performance, diarrhoea and bacterial shedding. Vet Microbiol :, 2016. Pubmed reference: 27665990. DOI: 10.1016/j.vetmic.2016.09.008.
Yang, G.Y., Zhu, Y.H., Zhang, W., Zhou, D., Zhai, C.C., Wang, J.F. :
Influence of orally fed a select mixture of Bacillus probiotics on intestinal T-cell migration in weaned MUC4 resistant pigs following Escherichia coli challenge. Vet Res 47:71, 2016. Pubmed reference: 27424033. DOI: 10.1186/s13567-016-0355-8.
Zhang, W., Zhu, Y.H., Zhou, D., Wu, Q., Song, D., Dicksved, J., Wang, J.F. :
Oral administration of a select mixture of Bacillus probiotics affects the gut microbiota and goblet cell function in newly weaned MUC4 resistant pigs following Escherichia coli challenge. Appl Environ Microbiol :, 2016. Pubmed reference: 27881419. DOI: 10.1128/AEM.02747-16.
2015 Xia, P., Song, Y., Zou, Y., Yang, Y., Zhu, G. :
F4+ enterotoxigenic Escherichia coli (ETEC) adhesion mediated by the major fimbrial subunit FaeG. J Basic Microbiol 55:1118-24, 2015. Pubmed reference: 25847483. DOI: 10.1002/jobm.201400901.
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2011 Jacobsen, M., Cirera, S., Joller, D., Esteso, G., Kracht, SS., Edfors, I., Bendixen, C., Archibald, AL., Vogeli, P., Neuenschwander, S., Bertschinger, HU., Rampoldi, A., Andersson, L., Fredholm, M., Jorgensen, CB. :
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2001 Jaradat, Z.W., Marquardt, R.R. :
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Van, den, Broeck, W., Cox, E., Oudega, B., Goddeeris, B.M. :
The F4 fimbrial antigen of Escherichia coli and its receptors [Review] Veterinary Microbiology 71:223-244, 2000. Pubmed reference: 10703706.
1999 Choi, C., Chae, C. :
Genotypic prevalence of F4 variants (ab, ac, and ad) in Escherichia coli isolated from diarrheic piglets in Korea. Vet Microbiol 67:307-10, 1999. Pubmed reference: 10466506.
Francis, D.H., Erickson, A.K., Grange, P.A. :
K88 adhesins of enterotoxigenic Escherichia coli and their porcine enterocyte receptors. Adv Exp Med Biol 473:147-54, 1999. Pubmed reference: 10659352.
Grange, P.A., Erickson, A.K., Levery, S.B., Francis, D.H. :
Identification of an intestinal neutral glycosphingolipid as a phenotype-specific receptor for the K88ad fimbrial adhesin of Escherichia coli Infection & Immunity 67:165-172, 1999. Pubmed reference: 9864211.
Jeyasingham, M.D., Butty, P., King, T.P., Begbie, R., Kelly, D. :
Escherichia coli K88 receptor expression in intestine of disease-susceptible weaned pigs Veterinary Microbiology 68:219-234, 1999. Pubmed reference: 10510041.
Peelman, L.J. :
[Genetic investigation of the resistance mechanisms of the pig against diarrhea caused by E. coli]. Verh K Acad Geneeskd Belg 61:489-515, 1999. Pubmed reference: 10500474.
1998 Barman, N.N., Sarma, D.K., Rahman, H., Borah, P., Cox, E. :
Elisa and co-agglutination test for detection of K88AC fimbriae in escherichia coli strains Indian Journal of Animal Sciences 68:417-419, 1998.
Billey, L.O., Erickson, A.K., Francis, D.H. :
Multiple receptors on porcine intestinal epithelial cells for the three variants of Escherichia coli K88 fimbrial adhesin Veterinary Microbiology 59:203-212, 1998. Pubmed reference: 9549860.
Chandler, D.S., Mynott, T.L. :
Bromelain protects piglets from diarrhoea caused by oral challenge with K88 positive enterotoxigenic escherichia coli Gut 43:196-202, 1998. Pubmed reference: 10189844.
Engel, P., Seibert, B., Beuing, R., Senft, B., Erhardt, G. :
Occurrence of escherichia coli F4 receptors in several pig breeds in germany and influence on parameters of reproduction and fattening performance [German] Archiv fur Tierzucht-Archives of Animal Breeding 41:75-87, 1998.
Francis, D.H., Grange, P.A., Zeman, D.H., Baker, D.R., Sun, R., Erickson, A.K. :
Expression of mucin-type glycoprotein K88 receptors strongly correlates with piglet susceptibility to K88(+) enterotoxigenic Escherichia coli, but adhesion of this bacterium to brush borders does not. Infect Immun 66:4050-5, 1998. Pubmed reference: 9712746.
Grange, P.A., Erickson, A.K., Anderson, T.J., Francis, D.H. :
Characterization of the carbohydrate moiety of intestinal mucin-type sialoglycoprotein receptors for the K88AC fimbrial adhesin of escherichia coli Infection & Immunity 66:1613-1621, 1998. Pubmed reference: 9529089.
Jin, L.Z., Baidoo, S.K., Marquardt, R.R., Frohlich, A.A. :
In vitro inhibition of adhesion of enterotoxigenic escherichia coli K88 to piglet intestinal mucus by egg-yolk antibodies FEMS Immunology & Medical Microbiology 21:313-321, 1998.
1997 Andersson, L. :
The use of a wild pig x domestic pig intercross to map phenotypic trait loci Journal of Heredity 88:380-383, 1997. Pubmed reference: 9378913.
Baker, D.R., Billey, L.O., Francis, D.H. :
Distribution of K88-adhesive and non-adhesive phenotypes among four popular breeds of pigs. Adv Exp Med Biol 412:209-11, 1997. Pubmed reference: 9192014.
Baker, D.R., Billey, L.O., Francis, D.H. :
Distribution of K88 Escherichia coli adhesive and nonadhesive phenotypes among pigs of four breeds Veterinary Microbiology 54:123-132, 1997. Pubmed reference: 9057256.
Bertels, A., Jourquin, J., Buys, N., Van Zeveren, A., De Greve, H., Hernalsteens, J.P., Bouquet, Y. :
Selection of swine resistant to F4-positive Escherichia coli. Adv Exp Med Biol 412:427-9, 1997. Pubmed reference: 9192050.
Caloca, M.J., Suarez, S., Soler, J. :
Metabolic changes in red cells in response to adhesion of porcine K88 fimbriated escherichia coli Veterinary Microbiology 58:45-52, 1997. Pubmed reference: 9451460.
Erickson, A.K., Billey, L.O., Srinivas, G., Baker, D.R., Francis, D.H. :
A three-receptor model for the interaction of the K88 fimbrial adhesin variants of Escherichia coli with porcine intestinal epithelial cells. Adv Exp Med Biol 412:167-73, 1997. Pubmed reference: 9192009.
1996 Grange, P.A., Mouricout, M.A. :
Transferrin associated with the porcine intestinal mucosa is a receptor specific for K88AB fimbriae of escherichia coli Infection & Immunity 64:606-610, 1996. Pubmed reference: 8550214.
Mol, O., Oudhuis, W.C., Fokkema, H., Oudega, B. :
The n-terminal beta-barrel domain of the Escherichia coli K88 periplasmic chaperone FaeE determines fimbrial subunit recognition and dimerization Molecular Microbiology 22:379-388, 1996. Pubmed reference: 8930921.
1995 Edfors-Lilja, I., Gustafsson, U., Duvaliflah, Y., Ellergren, H., Johansson, M., Juneja, R.K., Marklund, L., Andersson, L. :
The porcine intestinal receptor for Escherichia coli k88 alpha b, K88 alpha c: Regional localization on chromosome 13 and influence of IgG response to the K88 antigen Animal Genetics 26:237-242, 1995. Pubmed reference: 7661395.
Wittig, W., Klie, H., Gallien, P., Lehmann, S., Timm, M., Tschäpe, H. :
Prevalence of the fimbrial antigens F18 and K88 and of enterotoxins and verotoxins among Escherichia coli isolated from weaned pigs. Zentralbl Bakteriol 283:95-104, 1995. Pubmed reference: 9810650.
1994 Alexander, T.J.L., Gyles, C.L. :
Neonatal Diarrhoea in Pigs Escherichia Coli in Domestic Animals and Humans :151-170, 1994.
Deannystrom, E.A., Samuel, J.E. :
Age-related resistance to 987P fimbria-mediated colonization correlates with specific glycolipid receptors in intestinal mucus in swine Infection and Immunity 62:4789-4794, 1994. Pubmed reference: 7927756.
Erickson, A.K., Baker, D.R., Bosworth, B.T., Casey, T.A., Benfield, D.A., Francis, D.H. :
Characterization of porcine intestinal receptors for the K88ac fimbrial adhesin of Escherichia coli as mucin-type sialoglycoproteins Infection and Immunity 62:5404-5410, 1994. Pubmed reference: 7960120.
Seignole, D., Grange, P., Duvaliflah, Y., Mouricout, M. :
Characterization of O-glycan moieties of the 210 and 240 kDa pig intestinal receptors for Escherichia coli K88ac fimbriae Microbiology - UK 140:2467-2473, 1994.
1993 Blomberg, L., Henriksson, A., Conway, P.L. :
Inhibition of Adhesion of Escherichia coli K88 to Piglet Ileal Mucus by Lactobacillus spp Applied and Environmental Microbiology 59:34-39, 1993. Pubmed reference: 8439162.
Blomberg, L., Krivan, H.C., Cohen, P.S., Conway, P.L. :
Piglet Ileal Mucus Contains Protein and Glycolipid (Galactosylceramide) Receptors Specific for Escherichia-Coli K88 Fimbriae Infection and Immunity 61:2526-2531, 1993. Pubmed reference: 8099067.
Guerin, G., Duvaliflah, Y., Bonneau, M., Bertaud, M., Guillaume, P., Ollivier, L. :
Evidence for Linkage Between K88Ab, K88Ac Intestinal Receptors to Escherichia Coli and Transferrin Loci in Pigs Animal Genetics 24:393-396, 1993. Pubmed reference: 7904804.
Hu, Z.L., Hasler-Rapacz, J., Huang, S.C., Rapacz, J. :
Studies in Swine on Inheritance and Variation in Expression of Small Intestinal Receptors Mediating Adhesion of the K88 Enteropathogenic Escherichia coli Variants Journal of Heredity 84:157-165, 1993. Pubmed reference: 8228168.
Marklund, L., Wintero, A.K., Thomsen, P.D., Johansson, M., Fredholm, M., Gustafsson, U., Andersson, L. :
A Linkage Group on Pig Chromosome 4 Comprising the Loci for Blood Group L, Gba, Atp1B1 and Three Microsatellites Animal Genetics 24:333-338, 1993. Pubmed reference: 7904798.
Payne, D., O'Reilly, M., Williamson, D. :
The K88 Fimbrial Adhesin of Enterotoxigenic Escherichia-coli Binds to beta-1-Linked Galactosyl Residues in Glycosphingolipids Infection and Immunity 61:3673-3677, 1993. Pubmed reference: 8103039.
Stamm, M., Sorg, I. :
Intestinal Receptors for Adhesive Fimbriae of Escherichia coli in Pigs - A Review Schweizer Archiv Fur Tierheilkunde 135:89-95, 1993. Pubmed reference: 8096652.
1992 Runnels, P.L., Vijtiuk, N., Valpotic, I. :
Association of Porcine Intestinal F4 Receptor with Escherichia-Coli Induced Diarrheal Disease and Body Weight Gain in Weaned Pigs Periodicum Biologorum 94:141-148, 1992.
Valpotic, I., Frankovic, M., Vrbanac, I. :
Identification of Infant and Adult Swine Susceptible to Enterotoxigenic Escherichia coli by Detection of Receptors for F4(K88)ac Fimbriae in Brush Borders or Feces Comparative Immunology Microbiology and Infectious Diseases 15:271-279, 1992.
Vogeli, P., Kuhn, B., Kuhne, R., Obrist, R., Stranzinger, G., Huang, S.C., Hu, Z.L., Hasler-Rapacz, J., Rapacz, J. :
Evidence for Linkage Between the Swine L-Blood Group and the Loci Specifying the Receptors Mediating Adhesion of K88 Escherichia coli Pilus Antigens Animal Genetics 23:19-29, 1992. Pubmed reference: 1349202.
Willemsen, P.T.J., Degraaf, F.K. :
Age and Serotype Dependent Binding of K88 Fimbriae to Porcine Intestinal Receptors Microbial Pathogenesis 12:367-375, 1992. Pubmed reference: 1354324.
1991 Bertin, A.M., Duchetsuchaux, M.F. :
Relationship Between Virulence and Adherence of Various Enterotoxigenic Escherichia-Coli Strains to Isolated Intestinal Epithelial Cells from Chinese Meishan and European Large White Pigs American Journal of Veterinary Research 52:45-49, 1991. Pubmed reference: 2021252.
Conway, P.L., Wadstrom, T., Blomberg, L., Makela, P.H., Welin, A., Svennerholm, A.M., Cohen, P.S., Wolfwatz, H. :
The Role of Piglet Intestinal Mucus in the Pathogenicity of Escherichia-Coli K88 Molecular Pathogenesis of Gastrointestinal Infections 58:335-337, 1991.
Duchetsuchaux, M.F., Bertin, A.M., Menanteau, P.S. :
Susceptibility of Chinese Meishan and European Large White Pigs to Enterotoxigenic Escherichia-Coli Strains Bearing Colonization Factor K88, 987P, K99, or F41 American Journal of Veterinary Research 52:40-44, 1991. Pubmed reference: 2021251.
Edfors-Lilja, I., Owen, J.B., Axford, R.F.E. :
Escherichia-coli Resistance in Pigs :424-435, 1991.
Lingaas, F. :
Epidemiological and Genetical Studies in Norwegian Pig Herds .4. Breed Effects, Recurrence of Disease, and Relationship Between Disease and Some Performance Traits Acta Veterinaria Scandinavica 32:107-114, 1991. Pubmed reference: 1950843.
Lingaas, F., Ronningen, K. :
Epidemiological and Genetical Studies in Norwegian Pig Herds .5. Estimates of Heritability and Phenotypic Correlations of the Most Common Diseases in Norwegian Pigs Acta Veterinaria Scandinavica 32:115-122, 1991. Pubmed reference: 1950844.
Metcalfe, J.W., Krogfelt, K.A., Krivan, H.C., Cohen, P.S., Laux, D.C. :
Characterization and Identification of a Porcine Small Intestine Mucus Receptor for the K88ab Fimbrial Adhesin Infection and Immunity 59:91-96, 1991. Pubmed reference: 1670931.
Mouricout, M. :
Swine and Cattle Enterotoxigenic Escherichia-Coli-Mediated Diarrhea - Development of Therapies Based on Inhibition of Bacteria-Host Interactions European Journal of Epidemiology 7:588-604, 1991. Pubmed reference: 1723693.
Ollivier, L., Renjifo, X. :
Use of Genetic Resistance to K88 Colibacillosis in Pig Breeding Schemes Genetics Selection Evolution 23:235-248, 1991.
1990 Bakker, D., Vanzijderveld, F.G., Vanderveen, S., Oudega, B., Degraaf, F.K. :
K88 Fimbriae As Carriers of Heterologous Antigenic Determinants Microbial Pathogenesis 8:343-352, 1990. Pubmed reference: 1699108.
Bonneau, M., Duval-Iflah, Y., Guerin, G., Ollivier, L., Renard, C., Renjifo, X. :
Aspects ghetiques et microbiologiques de la colibacillose K88 chez le porc. Annales de Recherches Vbtbrinaires 21:302-303, 1990.
Duvaliflah, Y., Heidt, P.J., Vossen, J.M., Derycke, J., Fontaine, J.J., Rusch, V.C., Guillaume, P., Ouriet, M.F., Raibaud, P. :
In Vivo Adherence of Nonenterotoxigenic Escherichia Coli - K88 to Piglet Intestinal Epithelium - Pathogenic Effect Microecology and Therapy, Vol 20 20:427-429, 1990.
Valpotic, I., Dean, E.A., Whipp, S.C., Moon, H.W. :
Screening of Porcine Feces for K88 Resistant Phenotype by ELISA Periodicum Biologorum 92:43-44, 1990.
1989 Valpotic, I., Runnels, P.L., Moon, H.W. :
Invitro Adhesion of K88Ac+ Escherichia-Coli to Peyers Patch and Peripheral Blood Lymphocytes, Buccal and Rectal Epithelial Cells or Intestinal Epithelial Brush Borders of Weaned Pigs Veterinary Microbiology 20:357-368, 1989. Pubmed reference: 2678726.
1987 Bijlsma, I.G.W., Bouw, J. :
Inheritance of K88-mediated adhesion of Escherichia coli to jejunal brush borders in pigs: a genetic analysis Veterinary Research Communications 11:509-518, 1987. Pubmed reference: 2897739.
1986 Chandler, D.S., Chandler, H.M., Luke, R.K., Tzipori, S.R., Craven, J.A. :
Screening of pig intestines for K88 non-adhesive phenotype by enzyme immunoassay. Vet Microbiol 11:153-61, 1986. Pubmed reference: 3518224.
Edfors-Lilja, I. :
[Improved disease resistance in pigs by exploitation of genetic variation in immune defences] Konsulentavdelningens Rapporter, Sveriges Lantbruksuniversitet 82:1-5, 1986.
Rapacz, J., Hasler-Rapacz, J. :
Polymorphism and inheritance of swine small intestine receptors mediating adhesion of three serological variants of Escherichia coli producing K88 pilus antigen Animal Genetics 17:305-321, 1986. Pubmed reference: 2881506.
1985 Bijlsma, I.G., de Nijs, A., Frik, J.F. :
The prevalence of different porcine phenotypes in the Netherlands concerning adherence of K88-positive Escherichia coli to intestinal epithelium. Vet Q 7:246-8, 1985. Pubmed reference: 3901499. DOI: 10.1080/01652176.1985.9693994.
1984 Chappuis, J.P., Duval-Iflah, Y., Ollivier, L., Legault, C. :
Escherichia coli K88 adhesion: comparison of Chinese and Large White piglets Genetique, Selection, Evolution 16:385-390, 1984.
Sellwood, R. :
Inhibition of adhesion of Escherichia coli K88 antigen by mammary secretions of susceptible and resistant sows. Vet Microbiol 9:477-86, 1984. Pubmed reference: 6388142.
Walters, J.R., Sellwood, R. :
The performance of pigs genetically resistant to K88 E. coli :2 pp., 1984.
Wilson, I.B., Staley, T.E., Bush, L.J., Gilliland, S.E. :
Recovery of intestinal membrane binding sites for K88 E. coli from pig mucosal organ cultures. Mol Cell Biochem 62:57-65, 1984. Pubmed reference: 6146093.
1983 Sellwood, R. :
Genetic and immune factors in the susceptibility of piglets to Escherichia coli diarrhoea Annales de Recherches Veterinaires 14:512-518, 1983. Pubmed reference: 6375530.
1982 Edfors-Lilja, I., Paterson, H., Gahne, B. :
The intestinal receptor for E. coli K88 in relation to performance of SW, Yorkshire x SW, Landrace pigs :390-394, 1982.
Walters, J.R., Sellwood, R. :
Aspects of genetic resistance to K88 in pigs :362-367, 1982.
1981 Snodgrass, D.R., Chandler, D.S., Makin, T.J. :
Inheritance of Esherichia coli K88 adhesion in pigs: identification of nonadhesive phenotypes in a commercial herd Veterinary Record 109:461-463, 1981. Pubmed reference: 7046202.
1980 Anderson, M.J., Whitehead, J.S., Kim, Y.S. :
Interaction of Escherichia coli K88 antigen with porcine intestinal brush border membranes. Infect Immun 29:897-901, 1980. Pubmed reference: 7000707.
Sellwood, R. :
The interaction of the K88 antigen with porcine intestinal epithelial cell brush borders. Biochim Biophys Acta 632:326-35, 1980. Pubmed reference: 6774765.
Sellwood, R. :
Breeding for E coli resistance Pig Farming Supplement :?, 1980.
1979 Kearns, M.J., Gibbons, R.A. :
The possible nature of the pig intestinal receptor for the K88 antigen of escherichia coli FEMS Microbiology Letters 6:165-168, 1979.
Sellwood, R. :
Escherichia coli diarrhoea in pigs with or without the K88 receptor Veterinary Record 105:228-230, 1979. Pubmed reference: 399711.
1977 Gibbons, R.A., Sellwood, R., Burrows, M., Hunter, P.A. :
Inheritance of resistance to neonatal E. coli diarrhoea in the pig: examination of the genetic system Theoretical and Applied Genetics 51:65-70, 1977.
1976 Tedeschi, G.G., Amici, D., Santarelli, I. :
Unstable L-forms of micrococci in human foetal blood. Experientia 32:925-7, 1976. Pubmed reference: 954986.
1975 Sellwood, R., Gibbons, R.A., Jones, G.W., Rutter, J.M. :
Adhesion of enteropathogenic Escherichia coli to pig intestinal brush borders: the existence of two pig phenotypes Journal of Medical Microbiology 8:405-511, 1975. Pubmed reference: 1100837.
1972 Jones, G.W., Rutter, J.M. :
Role of the K88 antigen in the pathogenesis of neonatal diarrhoea caused by Escherichia coli in piglets Infection and Immunity 6:918-927, 1972. Pubmed reference: 4629393.
1968 Sweeney, E.J. :
Escherichia coli in enteric disease of swine: observations on herd resistance Irish Veterinary Journal 22:42-46, 1968.

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