Hen egg yolk antibodies (IgY), production and use for passive immunization against bacterial enteric infections in chicken: A review;Les anticorps du jaune d'oeuf de poule (IgY), production et utilisation en immunisation passive contre les infections entériques bactériennes: Une revue

Biotechnology, Agronomy, Society and Environment

Volumn 13, Issue 2, 2009, Pages 295-308

  Chalghoumi, Raja ^a,b   Beckers, Yves ^a   Portetelle, Daniel ^a   Théwis, André ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b Funds for the Research in Industry and Agronomy   (Belgium)

Author keywords

Enteric infections; Feed additive; Hen egg yolk antibodies; IgY production; Passive immunization

Indexed keywords

BACTERIA (MICROORGANISMS); GALLUS GALLUS; SALMONELLA;

EID: 70049101359     PISSN: 13706233     EISSN: 17804507     Source Type: Journal    
DOI: None     Document Type: Article

References (110)

1. Akita E.M. & Nakai S., 1992. Immunoglobulins from egg yolks: isolation and purification. J. Food Sci., 57, 629-634.
2. Akita E.M. & Nakai S., 1993. Comparison of four purification methods for the production of immunoglobulins from eggs laid by hens immunized with an enterotoxigenic Escherichia coli strain. J. Immunol. Methods, 160(2), 207-214.
3. Amaral J.A., De Franco M.T., Zapata-Quintanilla L. & Carbonare S.B., 2008. In vitro reactivity and growth inhibition of EPEC serotype O111 and STEC serotypes O111 and O157 by homologous and heterologous chicken egg yolk antibody. Vet. Res. Commun., 32, 281-290.
4. Bade H. & Stegemann H., 1984. Rapid method of extraction of antibodies from hen egg yolk. J. Immunol. Methods, 72(2), 421-426.
5. Barrow P.A., Huggins M.B., Lovell M.A. & Simpson J.M., 1987. Observations on the pathogenesis of experimental Salmonella Typhimurium infection in chickens. Res. Vet. Sci., 42,194-199.
6. Behn I., Hommel U., Oertel M. & Hauschildt S., 1996. Kinetics of IgY formation after immunization of hens with different protein antigens. ALTEX, 13(5), 18-21.
7. Bernardi G. & Cook W.H., 1960. An electrophoretic and ultracentrifugal study on the proteins of the high density fraction of egg yolk. Biochim. Biophys. Acta, 44, 86-96.
8. Brady D. et al., 2002. A lipoprotein-derived anti-microbial factor from hen-egg yolk is active against Streptococcus species. J. Food Sci., 67, 3096-3103.
9. Burley R.W. & Cook W.H., 1961. Isolation and composition of avian egg yolk granules and their constituent alpha-and beta-lipovitellins. Can. J. Biochem. Physiol., 39, 1295-1307.
10. Camenisch G. et al., 1999. General applicability of chicken egg yolk antibodies: the performance of IgY immunoglobulins raised against the hypoxia-induced factor 1α. FASEB J., 13, 81-88.
11. Carlander D., 2002. Avian IgY antibody. In vitro and in vivo. PhD Thesis: University of Uppsala, Faculty of Medecine (Sweden).
12. Chalghoumi R., Théwis A., Portetelle D. & Beckers Y., 2008. Production of hen egg yolk immunoglobulins simultaneously directed against Salmonella Enteritidis and Salmonella Typhimurium in the same egg yolk. Poult. Sci., 87(1), 32-40
13. Chalghoumi R. et al., 2009. Adhesion and growth inhibitory effect of chicken egg yolk antibody (IgY) on Salmonella enterica serovars Enteritidis and Typhimurium in vitro. Foodborne Pathog. Dis., accepted.
14. Chang H.M., Ou-Yang R.F., Chen Y.T. & Chen C.C., 1999. Productivity and some properties of immunoglobulin specific against Streptococcus mutans serotype C in chicken egg yolk (IgY). J. Agric. Food Chem., 47, 61-66.
15. Chang H.M., Lee Y.C., Chen C.C. & Tu Y.Y., 2002. Microencapsulation protects immunoglobulin in yolk (IgY) specific against Helicobacter pylori urease. J. Food Sci., 67(1), 15-20.
16. Chansarkar N.L., 1998. Studies on structural stability of hen's egg yolk immunoglobulin (IgY). PhD Thesis: University of British Columbia (Canada).
17. Cho Y.H. et al., 2005. Protective effect of microencapsulation consisting of multiple emulsification and heat gelation processes on immunoglobulin in yolk. J. Food Sci., 70(2), 149-151.
18. Collard J.M. et al., 2008. Drastic decrease of Salmonella Enteritidis isolated in humans in Belgium in 2005, shift in phage types and influence on foodborne outbreaks. Epidemiol. Infect., 136, 771-781.
19. Davalos L., Ortega-Vinuesa J.L., Bastos-Gonzalez D. & Hidalgo-Alvarez R., 2000. A comparative study between the adsorption of IgY and IgG on latex particles. J. Biomater. Sci. Polym. Ed., 11(6), 657-673.
20. Davison F., Kaspers B. & Schat K.A., 2008. Avian immunology. Amsterdam: Elsevier.
21. Deignan T., Kelly J., Alwan A. & O'Farrelly C., 2000. Comparative analysis of methods of purification of egg yolk immunoglobulin. Food Agric. Immunol., 12, 77-85.
22. Ebina T. et al., 1990. Gastroenteritis in suckling mice caused by human rotavirus can be prevented with egg yolk immunoglobulin (IgY) and treated with a protein bound polysaccharide preparation (PSK). Microbiol. Immunol., 34, 617-629.
23. Ebina T., 1996. Prophylaxis of rotavirus gastroenteritis using immunoglobulin. Arch. Virol., 12(1), 217-223.
24. EFSA (European Food Safety Authority), 2007. Report of the task force on zoonoses data collection on the analysis of the baseline survey on the prevalence of Salmonella in broiler flocks of Gallus gallus, in the EU, 2005-2006 [1] - Part A: Salmonella prevalence estimates, http://www.efsa.europa.eu/EFSA/Report/zoon_report_ej98_finbroilers_en,0. pdf, (10/05/07).
25. Fu C.Y. et al., 2006. Preparation and evaluation of anti-SARS coronavirus IgY from yolks of immunized SPF chickens. J. Virol. Methods, 133, 112-115.
26. Gallagher J.S. & Voss E.W., 1974. Conformational state of chicken 7S immunoglobulin. Immunochemistry, 11, 461-465.
27. Gassmann M., Thömmes P., Weiser T. & Hübscher U., 1990. Efficient production of chicken egg antibodies against a conserved mammalian protein. FASEB J., 4, 2528-2532.
28. Girard F. et al., 2006. Use of virulence factor-specific egg yolk-derived immunoglobulins as a promising alternative to antibiotics for prevention of attaching and effacing Escherichia coli infections. FEMS Immunol. Med. Microbiol., 46, 340-350.
29. th ed. New York, USA: Freeman W.H. & Company.
30. Gürtler M., Methner U., Kobilke H. & Fehlhaber K., 2004. Effect of orally administered egg yolk antibodies on Salmonella Enteritidis contamination of hen's eggs. J. Vet. Med. B, 51, 129-134.
31. Hanly W.C., Artwohl J.E. & Bennett B.T., 1995. Review of polyclonal antibody production procedures in mammals and poultry. ILAR News, 37, 93-118.
32. Hatta H., Kim M. & Yamamoto T., 1990. A novel isolation method for hen egg yolk antibody, "IgY". Agric. Biol. Chem., 54, 2531-2535.
33. Hatta H. et al., 1993. Productivity and some properties of egg yolk antibody (IgY) against human rotavirus compared with rabbit IgG. Biosci. Biotechnol. Biochem., 57(3), 450-454.
34. Hatta H. et al., 1997. Passive immunization against dental plaque formation in humans: effect of mouth rinse containing egg yolk antibodies (IgY) specific to Streptococcus mutans. Caries Res., 31, 268-274.
35. Horikoshi T., Hiraoka J., Saito M. & Hamada S., 1993. IgG antibody from hen egg yolks: purification by ethanol fractionation. J. Food Sci., 58, 739-742.
36. Ikemori Y. et al., 1992. Protection of neonatal calves against fatal enteric colibacillosis by administration of egg yolk powder from hens immunized with K99-piliated enterotoxigenic Escherichia coli. Am. J. Vet. Res., 53(11), 2005-2008.
37. Ikemori Y. et al., 1997. Passive protection of neonatal calves against bovine coronavirus-induced diarrhea by administration of egg yolk or colostrum antibody powder. Vet. Microbiol., 58, 105-111.
38. Imberechts H., Deprez P., Van Driessche E. & Pohl P., 1997. Chicken egg yolk antibodies against F18ab fimbriae of Escherichia coli inhibit shedding of F18 positive Escherichia coli by experimentally infected pigs. Vet. Microbiol., 54, 329-341.
39. th ed. Berlin; Heidelberg, Deutschland: Spektrum Akademischer Verlag.
40. Jaradat Z.W. & Marquardt R.R., 2000. Studies on the stability of chicken IgY in different sugars, complex carbohydrates and food materials. Food Agric. Immunol., 12, 263-272.
41. Jensenius J.C. et al., 1981. Eggs: conveniently packaged antibodies. Methods for purification of yolk IgG. J. Immunol. Methods, 46, 63-68.
42. Kapoor P., Compton M.M. & Howarth B.,2000. Immunization of chickens with quail and turkey perivitelline membrane proteins: production of anti-bodies and their effects on fertility. Poult. Sci., 79, 245-256.
43. Kassaify Z.G. & Mine Y., 2004a. Effect of food protein supplements on Salmonella Enteritidis infection and prevention in laying hens. Poult. Sci., 83, 753-760.
44. Kassaify Z.G. & Mine Y., 2004b. Non-immunized egg yolk powder can suppress the colonization of Salmonella Typhimurium, Escherichia coli O157:H7, and Campylobacter jejuni in laying hens. Poult. Sci., 83, 1497-1506.
45. Kassaify Z.G., Li E.W.Y. & Mine Y., 2005. Identification of antiadhesive fraction(s) in non-immunized egg yolk powder: in vitro study. J. Agric. Food Chem., 53, 4607-4614.
46. Kim H. & Nakai S., 1996. Immunoglobulin separation from egg yolk: a serial filtration system. J. Food Sci., 61(3), 510-512.
47. Klemperer F., 1893. Ueber natürliche Immunität und ihre Verwertung für die Immunisierungstherapie. Arch. Exp. Pathol. Pharmakol., 31, 356-382.
48. Kovacs-Nolan J. & Mine Y., 2005. Microencapsulation for the gastric passage and controlled intestinal release of immunoglobulin Y. J. Immunol. Methods, 296, 199-209.
49. Kubo R.T., Zimmerman B. & Grey H.M., 1973. Phylogeny of immunoglobulins. In: Sela M., ed. The antigens. San Diego, CA, USA: Academic Press, 117-177.
50. Kuroki M. et al., 1993. Passive protection against bovine rotavirus-induced diarrhea in murine model by specific immunoglobulins from chicken egg yolk. Vet. Microbiol., 37, 135-146.
51. Kuroki M. et al., 1994. Passive protection against bovine rotavirus in calves by specific immunoglobulins from chicken egg yolk. Arch. Virol., 138, 143-148.
52. Lee E.N., Sunwoo H.H., Menninen K. & Sim J.S., 2002a. In vitro studies of chicken egg yolk antibody (IgY) against Salmonella Enteritidis and Salmonella Typhimurium. Poult. Sci., 81, 632-641.
53. Lee K.A. et al., 2002b. Acid stability of anti-Helicobacter pyroli IgY in aqueous polyol solution. J. Biochem. Mol. Biol., 35, 488-493.
54. Leenaars M., Claassen E. & Boersma W.J.A.,1996. Modulation of the humoral immune response: antigens and antigen presentation. In: Lefkovits I., ed. Immunology methods manual. London: Academic Press Ltd, 989-1013.
55. Leslie G.A. & Martin L.N., 1973. Studies on the secretory immunologic system of fowl. 3. Serum and secretory IgA of the chicken. J. Immunol., 110(1), 1-9.
56. Lévesque S., Martinez G. & Fairbrother J.M.,2007. Improvement of adjuvant systems to obtain a cost-effective production of high levels of specific IgY. Poult. Sci., 86, 630-635.
57. Li X., Shuai J. & Fang W., 2006. Protection of Carassius auratus Gibelio against infection by Aeromonas hydrophila using specific immunoglobulins from hen egg yolk. J. Zheijiang Univ. Sci. B, 7, 922-928.
58. Lösch U., Schranner I., Wanke I. & Jügens L., 1986. The chicken egg, an antibody source. J. Vet. Med. B, 33, 609-619.
59. Mahn K., 1998. Etablierung eines Immunisierungsschemas für Legehennen. PhD Thesis: University of Munich (Germany).
60. Marquardt R.R. et al., 1999. Passive protective effect of egg-yolk antibodies against enterotoxigenic Escherichia coli K88+ infection in neonatal and early weaned piglets. FEMS Immunol. Med. Microbiol., 23, 283-288.
61. Matsuda H. et al., 1999. A chicken monoclonal antibody with specificity for the N-terminal of human prion protein. FEMS Immunol. Med. Microbiol., 23, 89-194.
62. Mayrhofer S., Paulsen P., Smulders F.J.M. & Hilbert F., 2003. Antimicrobial resistance profile of five major food-borne pathogens isolated from beef, pork and poultry. Int. J. Food Microbiol., 97(1), 23-29.
63. McCully K.A., Mok C.C. & Common R.H., 1962. Paper electrophoretic characterization of proteins and lipoproteins of hen's egg yolk. Can. J. Biochem. Physiol., 40, 937-952.
64. McLaren R.D., Prosser C.G., Grieve R.C.J. & Borrisenko M., 1994. The use of caprylic acid for the extraction of the immunoglobulin fraction from egg yolk of chickens immunized with ovine α-lactalbumin. J. Immunol. Methods, 177, 175-184.
65. Mohammed S.M. et al., 1998. Deposition of genetically engineered human antibodies into the egg yolk of hens. Immunotechnology, 4, 115-125.
66. Morrison S.L. et al., 2001. Sequences in antibody molecules important for receptor-mediated transport into the chicken egg yolk. Mol. Immunol., 38, 619-625.
67. O'Farrelly C., Branton D. & Wanke C.A., 1992. Oral ingestion of egg yolk immunoglobulin from hens immunized with an enterotoxigenic Escherichia coli strain prevents diarrhea in rabbits challenged with the same strain. Infect. Immun., 60, 2593-2597.
68. Olbrich C. et al., 2002. Stable biocompatible adjuvants: a new type of adjuvant based on solid lipid nanoparticles: a study on cytotoxicity, compatibility and efficacy in chicken. ATLA, 30, 443-458.
69. Otani H., Matsumoto K., Saeki A. & Hosono A., 1991. Comparative studies on properties of hen egg yolk IgY and rabbit serum IgG antibodies. Lebensm. Wiss. Technol., 24, 152-158.
70. Özpinar H. et al., 1996. Dose-dependent effects of specific egg-yolk antibodies on diarrhea of newborn calves. Prev. Vet. Med., 27, 67-73.
71. Panada A.K. & Reddy M.R., 2007. Boosting the chick's immune system through early nutrition. Poult. Int., http://www.poultryinternationaldigital.com/poultryinternational/200707/? pg=23, (10/06/08).
72. Patterson R., Youngner J.S., Weigle W.O. & Dixon F.J., 1962. Antibody production and transfer to egg yolk in chickens. J. Immunol., 89, 272-278.
73. Peralta R.C. et al., 1994. Passive immunisation against experimental Salmonellosis in mice by orally adminis-tered hen egg-yolk antibodies specific for 14-kDa fimbriae of Salmonella Enteritidis. J. Med. Microbiol., 41, 29-35.
74. Polson A., Von Wechmar M.B. & Regenmortel M.H.V.V., 1980. Isolation of viral IgY antibodies from yolks of immunized hens. Immunol. Commun., 9, 475-493.
75. Polson A. et al., 1985. Improvements in the isolation of IgY from the yolks of eggs laid by immunized hens. Immunol. Invest., 14(4), 323-327.
76. Polson A., 1990. Isolation of IgY from the yolks of eggs by a chloroform polyethylene glycol procedure. Immunol. Invest., 19(3), 253-258.
77. Rahimi S. et al., 2007. Prevention of Salmonella infection in poultry by specific egg-derived antibody. Int. J. Poult. Sci., 6, 230-235.
78. th ed. London: Blackie Academic & Professional.
79. Rose M.E., Orlans E. & Buttress N., 1974. Immunoglobulin classes in the hen's egg: their segregation in yolk and white. Eur. J. Immunol., 4, 521-523.
80. Rose M.E. & Orlans E., 1981. Immunoglobulins in the egg, embryo, and young chick. Dev. Comp. Immunol., 5, 15-20.
81. Schade R. & Hlinak A., 1996. Egg yolk antibodies, state of the art and future prospects. ALTEX, 13(1), 5-9.
82. Schade R. et al., 2005. Chicken egg yolk antibodies (IgY-technology): a review of progress in production and use in research and human and veterinary medicine. ATLA, 33, 129-154.
83. Schwarzkopf C., Staak C., Behn I. & Erhard M., 2000. Immunization. In: Schade R. et al., eds. Chicken egg yolk antibodies, production and application: IgY Technology. Berlin; Heidelberg, Deutschland; New York, USA: Springer Lab Manuals, 25-64.
84. Shimizu M., Nakai S. & Fitzsimmons R.C., 1988. An-E. coli immunoglobulin Y isolated from egg yolk of immunized chickens as a potential food ingredient. J. Food Sci., 5, 1360-1366.
85. Shimizu M. et al., 1992. Molecular stability of chicken and rabbit immunoglobulins G. Biosci. Biotechnol. Biochem., 56, 270-274.
86. Shimizu M., Nagashima H., Sano K. & Hashimoto K., 1993. Comparative studies on molecular stability of immunoglobulin G from different species. Comp. Biochem. Physiol., 106(2), 255-261.
87. Shimizu M., Nagashima H., Hashimoto K. & Suzuki T., 1994. Egg yolk antibody (IgY) stability in aqueous solution with high sugar concentrations. J. Food Sci., 59(4), 763-772.
88. Sim J.S., Sunwoo H.H. & Lee E.N., 2000. Ovoglobulin Y. In: Naidu A.S., ed. Natural food antimicrobial systems. New York, USA: CRC Press, 227-252.
89. Skrabanja A.T, De Meere A.L, De Ruiter R.A. & Van Den Oetelaar P.J., 1994. Lyophilization of biotechnology products. PDA J. Pharm. Sci. Technol., 48(6), 311-317.
90. nd ed. Westport, CT, USA: AVI Pub. Co.
91. Sugita-Konishi Y. et al., 2000. Blockade of Salmonella Enteritidis passage across the basolateral barriers of human intestinal epithelial cells by specific antibody. Microbiol. Immunol., 44, 473-479.
92. Sugita-Konishi Y. et al., 2002. Inhibition of bacterial adhesion and Salmonella infection in BALB/c mice by sialyoligosaccharides and their derivatives from chicken egg yolk. J. Agric. Food Chem., 50, 3607-3613.
93. Sunwoo H.H. et al., 2002. Growth inhibitory effect of chicken egg yolk antibody (IgY) on Escherichia coli O157:H7. J. Food Sci., 75, 342-345.
94. Svendsen L., Crowley A., Stodulski G. & Hau J., 1996. Antibody production in rabbits and chickens immunized with human IgG. A comparison of titre and avidity development in rabbit serum, chicken serum and egg yolk using three different adjuvants. J. Immunol. Methods, 191, 113-120.
95. Tini M. et al., 2002. Generation and application of chicken egg-yolk antibodies. Com. Biochem. Physiol. A, 131, 569-574.
96. Tressler R.L. & Roth T.F., 1987. IgG receptors on the embryonic chick yolk sac. J. Biol. Chem., 262, 15406-15412.
97. Tsubokura K. et al., 1997. Oral administration of antibodies as prophylaxis and therapy in Campylobacter jejuni-infected chickens. Clin. Exp. Immunol., 108, 451-455.
98. Vieira J.G.H. et al., 1984. Egg yolk as a source of antibodies for human parathyroid hormone (hPTH) radioimmunoassay. J. Immunoassay, 5, 121-129.
99. Wang X.Z. et al., 2008. In vitro inhibition of oral Candida albicans by chicken egg yolk antibody (IgY). Mycopathologia, 165, 381-387.
100. Wanke R. et al., 1996. Freund's complete adjuvant in the chicken: efficient immunostimulation with severe local inflammatory reaction. Zent. Veterinarmed A, 43(4), 243-253.
101. Wiedemann V. et al., 1991. Chicken egg antibodies for prophylaxis and therapy of infectious intestinal diseases. J. Vet. Med., 38, 283-291.
102. Wilkie D.C., 2006. Non-antibiotic approaches to control pathogens in the gastrointestinal tract of the broiler chicken. PhD Thesis: University of Saskatchewan (Canada).
103. Woolley J.A. & Landon J., 1995. Comparison of antibody production to human interleukin-6 (IL-6) by sheep and chickens. J. Immunol. Methods, 178, 253-265.
104. Yokoyama H. et al., 1992. Passive protective effect of chicken egg yolk immunoglobulins against experimental enterotoxigenic Escherichia coli infection in neonatal piglets. Infect. Immun., 60, 998-1007.
105. Yokoyama H. et al., 1993. Detection of passage and absorption of chicken egg yolk immunoglobulins in the gastrointestinal tract of pigs by use of enzyme-linked immunosorbent assay and fluorescent antibody testing. Am. J. Vet. Res., 54(6), 867-872.
106. Yokoyama H. et al., 1998a. Prevention of fatal Salmonellosis in neonatal calves, using orally administered chicken egg yolk Salmonella: specific antibodies. Am. J. Vet. Res., 59(4), 416-420.
107. Yokoyama H. et al., 1998b. Oral passive immunization against experimental Salmonellosis in mice using chicken egg yolk antibodies specific for Salmonella Enteritidis and S. Typhimurium. Vaccine, 16(4), 388-393.
108. Yolken R.H. et al., 1988. Antibodies to rotaviruses in chicken's eggs: a potential source of antiviral immunoglobulins suitable for human consumption. Pediatrics, 81, 291-295.
109. Ziprin R.L., Corrier D.E. & Elissalde M.H., 1989. Maturation of resistance to Salmonellosis in newly hatched chicks: inhibition by cyclosporine. Poult. Sci., 68, 1637-1642.
110. Zuniga A. et al., 1997. Reduced intestinal colonization with F18-positive enterotoxigenic Escherichia coli in weaned pigs fed chicken egg antibody against the fimbriae. FEMS Immunol. Med. Microbiol., 18, 153-161.