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The In Vitro and In Vivo Efficacy of Hen IgY Against Vibrio parahaemolyticus and Vibrio vulnificus

  • Kassim, Neema (Division of Applied Life Science (BK 21 Program), Graduate School of Gyeongsang National University) ;
  • Mtenga, Adelard B. (Division of Applied Life Science (BK 21 Program), Graduate School of Gyeongsang National University) ;
  • Shim, Won-Bo (The College of Human Sciences, Nutrition, Food and Exercise Sciences, Florida State University) ;
  • Chung, Duck-Hwa (Division of Applied Life Science (BK 21 Program), Graduate School of Gyeongsang National University)
  • Received : 2012.04.05
  • Accepted : 2012.05.20
  • Published : 2012.10.28

Abstract

The inhibitory effect of IgY against Vibrio parahaemolyticus and Vibrio vulnificus responsible for seafood-borne diseases was investigated in this study. Water-soluble fractions (WSF) of protein containing IgYs were isolated from the egg yolk of hens initially immunized with formalin-inactivated V. parahaemolyticus or V. vulnificus. Protein, total and specific IgY contents of the WSF were determined. The inhibitory and protective effects of IgYs on the growth of V. parahaemolyticus and V. vulnificus were assayed in liquid medium and in mice. IgYs showed high affinity to their corresponding antigens with high titer from day 28 onwards. Protein contents and total IgY concentrations remained stable throughout the immunization period, whereas specific IgY concentrations increased steadily and reached a plateau at day 49. Specific IgY powder (150 mg/ml) significantly inhibited further multiplication of both V. parahaemolyticus and V. vulnificus in liquid medium as compared with the control IgY. The bacteria count in mice feces was lower in mice pretreated with specific IgYs than in those pretreated with PBS or control IgY. Higher survival of mice was observed in the experimental groups pretreated with either anti-V. parahaemolyticus (75% survival) or anti-V. vulnificus (87% survival) IgYs, compared with those in the control groups pretreated with PBS or nonspecific IgY. All mice in the control groups died within three days after bacteria inoculation; hence, the protective effect of specific IgYs against infection caused by V. parahaemolyticus and V. vulnificus was demonstrated.

Keywords

Acknowledgement

Grant : Cooperative Research Program for Agricultural Science and Technology Development

References

  1. Akita, E. M. and S. Nakai. 1992. Immunoglobulins from egg yolk: Isolation and purification. J. Food Sci. 57: 629-634. https://doi.org/10.1111/j.1365-2621.1992.tb08058.x
  2. Allen, J. C. and C. J. Smith. 1987. Enzyme-linked immunoassay kits for routine food analysis. Trends Biotechnol. 5: 193-199. https://doi.org/10.1016/S0167-7799(87)80007-0
  3. Austin, B. 2010. Vibrios as causal agents of zoonoses. Vet. Microbiol. 140: 310-317. https://doi.org/10.1016/j.vetmic.2009.03.015
  4. Bae, H. D., K. Kitaguchi, F. Horio, and A. Murai. 2009. Higher incorporation of heterologous chicken immunoglobulin Y compared with homologous quail immunoglobulin Y into egg yolks of Japanese quail (Coturnix japonica). Poultry Sci. 88: 1703-1711. https://doi.org/10.3382/ps.2008-00238
  5. Bauer, A., O. Ostensvik, M. Florvag, O. Ormen, and L. M. ROrvik. 2006. Occurrence of Vibrio parahaemolyticus, V. cholerae, and V. vulnificus in Norwegian Blue Mussels (Mytilus edulis). Appl. Environ. Microbiol. 72: 3058-3061. https://doi.org/10.1128/AEM.72.4.3058-3061.2006
  6. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  7. Chalghoumi, R., Y. Beckers, D. Portetelle, and A. Thewis. 2009. Hen egg yolk antibodies (IgY), production and use for passive immunization against bacterial enteric infections in chicken: A review. Biotechnol. Agron. Soc. Environ. 13: 295-308.
  8. Chalghoumi, R., A. Thewis, Y. Beckers, C. Marcq, D. Portetelle, and Y. Schneider, 2009. Adhesion and growth inhibitory effect of chicken egg yolk antibody (IgY) on Salmonella enterica serovars Enteritidis and Typhimurium in vitro. Foodborne Pathog. Dis. 6: 593-604. https://doi.org/10.1089/fpd.2008.0258
  9. Chang, H. M., R. F. Ou-Yang, Y. T. Chen, and C. C. Chen. 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. https://doi.org/10.1021/jf980153u
  10. Deignan, T., J. Kelly, A. Alwan, and C. O'Farrelly. 2000. Comparative analysis of methods of purification of egg yolk immunoglobulin. J. Agric. Food Chem. 12: 77-85.
  11. De Meulenaer, B., K. Baert, H. Lanckriet, V. Van Hoed, and A. Huyghebaert. 2002. Development of an enzyme-linked immunosorbent assay for bisphenol A using chicken immunoglobulins. J. Agric. Food Chem. 50: 5273-5282. https://doi.org/10.1021/jf0202739
  12. Dias da Silva, W. and D. V. Tambourgi. 2010. IgY: A promising antibody for use in immunodiagnostic and in immunotherapy. Vet. Immunol. Immunopathol.135: 173-180. https://doi.org/10.1016/j.vetimm.2009.12.011
  13. Dong, D., H. Liu, Q. Xiao, and R. Li. 2008. Affinity purification of egg yolk immunoglobulins (IgY) with a stable synthetic ligand. J. Chromatogr. B 870: 51-54. https://doi.org/10.1016/j.jchromb.2008.05.036
  14. Grey, H. M. 1967. Duck immunoglobulins. II. Biologic and immunochemical studies. Eur. J. Immunol. 98: 820-826.
  15. Guimaraes, M. C. C., L. G. Amaral, L. B. A. Rangel, I. V. Silva, C. G. F. Matta, and M. F. R. Matta. 2009. Growth inhibition of Staphylococcus aureus by chicken egg yolk antibodies. Arch. Immunol. Ther. Exp. 57: 377-382. https://doi.org/10.1007/s00005-009-0041-x
  16. Hassan, Z. H., J. T. M. Zwartkruis-Nahuis, and E. De Boer. 2012. Occurrence of Vibrio parahaemolyticus in retailed seafood in The Netherlands. Int. Food Res. J. 19: 39-43.
  17. Hirai, K., H. Arimitsu, K. Umeda, K. Yokota, L. Shen, K. Ayada, et al. 2010. Passive oral immunization by egg yolk immunoglobulin (IgY) to Vibrio cholerae effectively prevents cholera. Acta Med. Okayama 64: 163-170.
  18. Javier Hernández-Campos, F., E. Brito-De La Fuente, and B. Torrestiana-Sánchez. 2010. Purification of egg yolk immunoglobulin (IgY) by ultrafiltration: Effect of pH, ionic strength, and membrane properties. J. Agric. Food Chem. 58: 187-193. https://doi.org/10.1021/jf902964s
  19. Kassim, N., A. B. Mtenga, W. G. Lee, J. S. Kim, W. B. Shim, and D. H. Chung. 2011. Production of coturnix quail immunoglobulins Y (IgYs) against Vibrio parahaemolyticus and Vibrio vulnificus. Food Sci. Biotechnol. 20: 1577-1583. https://doi.org/10.1007/s10068-011-0218-z
  20. Kass, P. H. and H. P. Riemann. 2006. Epidemiology of foodborne diseases, pp. 3-26. In H. P. Riemann, and D. O. Cliver (eds). Foodborne Infections and Intoxications, 3rd Ed. Academic Press, New York.
  21. Kirkman, T. W. 1996. Statistics to Use. Accessed Jan. 20, 2012, from http://www.physics.csbsju.edu/stats/.
  22. Larsson, A., L. Jonsson, and J. Sjoquist. 1988. Determination of circulating immune complexes by chicken anti-human C3 and anti-human C1q micro ELISA. J. Immunol. Methods 113: 93-99. https://doi.org/10.1016/0022-1759(88)90385-7
  23. Lee, E. N., H. H. Sunwoo, K. Menninen, and J. S. Sim. 2002. In vitro studies of chicken egg yolk antibody (IgY) against Salmonella Enteritidis and Salmonella Typhymurium. Poult. Sci. 81: 632-641.
  24. Lee, J. K., D. W. Jung, S. Y. Eom, S. W. Oh, Y. Kim, H. S. Kwak, and Y. H. Kim. 2008. Occurrence of Vibrio parahaemolyticus in oysters from Korean retail outlets. Food Cont. 19: 990-994. https://doi.org/10.1016/j.foodcont.2007.10.006
  25. Lee, S. B., Y. Mine, and R. M. W. Stevenson. 2000. Effects of hen egg yolk immunoglobulin in passive protection of rainbow trout against Yersinia ruckeri. J. Agric. Food Chem. 48: 110-115. https://doi.org/10.1021/jf9906073
  26. Lee, S. H., H. S. Lillehoj, D. W. Park, S. I. Jang, A. Morales, D. García, et al. 2009. Induction of passive immunity in broiler chickens against Eimeria acervulina by hyperimmune egg yolk immunoglobulin Y. Poult. Sci. 88: 562-566. https://doi.org/10.3382/ps.2008-00340
  27. Mahdavi, A. H., H. R. Rahmani, N. Nili, A. H. Samie, and S. Soleimanian-Zad. 2010. Chicken egg yolk antibody (IgY) powder against Escherichia coli 078:K80. J. Anim. Vet. Adv. 9: 366-373. https://doi.org/10.3923/javaa.2010.366.373
  28. Meenatchisundaram, S., V. Shanmugam, and V. M. Anjali. 2011. Development of chicken egg yolk antibodies against Streptococcus mitis-purification and neutralizing efficacy. J. Basic Clin. Pharm. 2: 109-114.
  29. Michael, A., S. Meenatchisundaram, G. Parameswari, T. Subbraj, R. Selvakumaran, and S. Ramalingam. 2010. Chicken egg yolk antibodies (IgY) as an alternative to mammalian antibodies. Indian J. Sci. Technol. 3: 468-474.
  30. Michael, H., M. D. Bross, K. M. D. Soch, R. M. D. Morales, and R. B. M. D. Mitchell. 2007. Vibrio vulnificus infection: Diagnosis and treatment. Am. Fam. Physician 76: 539-544.
  31. Min, S., S. Cheon, J. Kim, W. I. Cho, and H. H. Sunwoo. 2009. Growth inhibition of Clostridium perfringens vegetative cells and spores using chicken immunoglobulin Y. J. Food Safety 29: 511-520. https://doi.org/10.1111/j.1745-4565.2009.00173.x
  32. Na, H. S., Y. J. Lim, Y. S. Yun, Y. H. Choi, J. S. Oh, J. H. Rhee, and H. C. Lee. 2009. Protective effect of ginsan against Vibrio vulnificus infection. J. Bacteriol. Virol. 39: 113-118. https://doi.org/10.4167/jbv.2009.39.2.113
  33. Nair, G. B. N., S. M. Faruque, and D. A. Sack. 2006. Vibrios, pp. 332-372. In Y. Motarjemi and M. Adams (eds.). Emerging Foodborne Pathogens. CRC Press, Cambrige, England.
  34. Nishibuchi, M. and A. DePaola. 2005. Vibrio species, pp. 251-271. In P. M. Fratamico, A. K. Bhunia, and J. L. Smith (eds.). Foodborne Pathogens: Microbiology and Molecular Biology. Caister Academic Press, Norflok, UK.
  35. Oliver, J. D. and J. Kaper. 2007. Vibrio species, pp. 343-379. In M. P. Doyle and L. R. Beuchat (eds.). Food Microbiology: Fundamentals and Frontiers, 3rd Ed. ASM Press, Washington, DC.
  36. Pauly, D., M. Dorner, X. Zhang, A. Hlinak, B. Dorner, and R. Schade. 2009. Monitoring of laying capacity, immunoglobulin Y concentration, and antibody titer development in chickens immunized with ricin and botulinum toxins over a two-year period. Poult. Sci. 88: 281-290. https://doi.org/10.3382/ps.2008-00323
  37. Shin, J., M. Yang, S. W. Nam, J. T. Kim, N. H. Myung, W. G. Bang, and I. H. Roe. 2002. Use of egg yolk-derived immunoglobulin as an alternative to antibiotic treatment for control of Helicobacter pylori infection. Clin. Diagn. Lab. Immunol. 9: 1061-1066.
  38. Sunwoo, H. H., E. N. Lee, N. Gujral, and M. R. Suresh. 2010. Growth inhibition of Escherichia coli 987P by neutralizing IgY antibodies. Open Immunol. J. 3: 1-8.
  39. Sunwoo, H. H., E. N. Lee, K. Menninen, M. R. Suresh, and J. S. Sim. 2002. Growth inhibitory effect of chicken egg yolk antibody (IgY) on Escherichia coli O157:H7. J. Food Sci. 67: 1486-1494. https://doi.org/10.1111/j.1365-2621.2002.tb10310.x
  40. Sunwoo, H. H., W. W. Wang, and J. S. Sim. 2006. Detection of Escherichia coli O157:H7 using chicken immunoglobulin Y. Immunol. Lett. 106: 191-193. https://doi.org/10.1016/j.imlet.2006.05.005
  41. Tunung, R., S. Margaret, P. Jeyaletchumi, L. C. Chai, Z. T. C. Tuan, F. M. Ghazali, et al. 2010. Prevalence and quantification of Vibrio parahaemolyticus in raw salad vegetables at retail level. J. Microbiol. Biotechnol. 20: 391-396.
  42. Vikrama, C. P., K. Shanmugasundaram, and S. Malmarugan. 2010. In vitro assessment of bacteriostatic potency of egg yolk immunoglobulin against Escherichia coli. Vet. World 3: 460-462.

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