IgY antibodies protect against human rotavirus induced diarrhea in the neonatal gnotobiotic piglet disease model

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Vega, Celina G ^a   Bok, Marina ^a   Vlasova, Anastasia N ^b   Chattha, Kuldeep S ^b   Fernández, Fernando M ^a   Wigdorovitz, Andrés ^a   Parreño, Viviana G ^a   Saif, Linda J ^b  

^a INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN Y; IMMUNOGLOBULIN Y ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; DIARRHEA; DIET SUPPLEMENTATION; DOSE RESPONSE; EGG YOLK; ENZYME LINKED IMMUNOSORBENT ASSAY; GNOTOBIOTICS; HUMAN ROTAVIRUS; IMMUNE RESPONSE; MILK; NEWBORN; NONHUMAN; PASSIVE IMMUNIZATION; VIRUS SHEDDING;

ADMINISTRATION, ORAL; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, VIRAL; ANTIBODY FORMATION; ANTIBODY SPECIFICITY; ANTIBODY-PRODUCING CELLS; ANTIGENS, VIRAL; CAPSID PROTEINS; CELL COUNT; CHICKENS; DIARRHEA; DISEASE MODELS, ANIMAL; DUODENUM; EGG YOLK; ENZYME-LINKED IMMUNOSORBENT ASSAY; GERM-FREE LIFE; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULINS; NEUTRALIZATION TESTS; ROTAVIRUS; ROTAVIRUS INFECTIONS; SUS SCROFA; VIRUS SHEDDING;

ANIMALIA; GALLUS GALLUS; HUMAN ROTAVIRUS A; ROTAVIRUS; ROTAVIRUS A; SUIDAE;

EID: 84864542598     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042788     Document Type: Article

References (63)

1. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, et al. (2010) Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 375: 1969-1987.
2. Santosham M, Chandran A, Fitzwater S, Fischer-Walker C, Baqui AH, et al. (2010) Progress and barriers for the control of diarrhoeal disease. Lancet 376: 63-67.
3. Estes M (2001) Rotavirus and their replication (Cap 54a). In: B. N. Fields DMK, P. M. Howley, editor. Fields Virology. Philadelphia: Lippincott- Raven.
4. Kirkwood CD, (2010) Genetic and antigenic diversity of human rotaviruses: potential impact on vaccination programs. J Infect Dis 202 Suppl: S43-48.
5. Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI, (2003) Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9: 565-572.
6. Stupka JA, Carvalho P, Amarilla AA, Massana M, Parra GI, (2009) National Rotavirus Surveillance in Argentina: high incidence of G9P[8] strains and detection of G4P[6] strains with porcine characteristics. Infect Genet Evol 9: 1225-1231.
7. Santos N, Hoshino Y, (2005) Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 15: 29-56.
8. Dennehy PH, (2008) Rotavirus vaccines: an overview. Clin Microbiol Rev 21: 198-208.
9. Dhama K, Chauhan RS, Mahendran M, Malik SV, (2009) Rotavirus diarrhea in bovines and other domestic animals. Vet Res Commun 33: 1-23.
10. Sarker SA, Pant N, Juneja LR, Hammarstrom L, (2007) Successful treatment of rotavirus-induced diarrhoea in suckling mice with egg yolk immunoglobulin. J Health Popul Nutr 25: 465-468.
11. Anderson EJ, (2009) Prevention and treatment of viral diarrhea in pediatrics. Expert Rev Anti Infect Ther 8: 205-217.
12. Munos MK, Walker CL, Black RE, (2010) The effect of rotavirus vaccine on diarrhoea mortality. Int J Epidemiol 39 Suppl 1: i56-62.
13. Patel MM, Steele D, Gentsch JR, Wecker J, Glass RI, et al. (2011) Real-world impact of rotavirus vaccination. Pediatr Infect Dis J 30: S1-5.
14. Patel NC, Hertel PM, Estes MK, de la Morena M, Petru AM, et al. (2010) Vaccine-acquired rotavirus in infants with severe combined immunodeficiency. N Engl J Med 362: 314-319.
15. Saif LJ, Ward LA, Yuan L, Rosen BI, To TL, (1996) The gnotobiotic piglet as a model for studies of disease pathogenesis and immunity to human rotaviruses. Arch Virol Suppl 12: 153-161.
16. Gonzalez AM, Azevedo MS, Jung K, Vlasova A, Zhang W, et al. (2010) Innate immune responses to human rotavirus in the neonatal gnotobiotic piglet disease model. Immunology 131: 242-256.
17. Franco MA, Angel J, Greenberg HB, (2006) Immunity and correlates of protection for rotavirus vaccines. Vaccine 24: 2718-2731.
18. Hodgins DC, Kang SY, deArriba L, Parreno V, Ward LA, et al. (1999) Effects of maternal antibodies on protection and development of antibody responses to human rotavirus in gnotobiotic pigs. J Virol 73: 186-197.
19. Parreno V, Hodgins DC, de Arriba L, Kang SY, Yuan L, et al. (1999) Serum and intestinal isotype antibody responses to Wa human rotavirus in gnotobiotic pigs are modulated by maternal antibodies. J Gen Virol 80 (Pt 6): 1417-1428.
20. Yuan L, Saif LJ, (2002) Induction of mucosal immune responses and protection against enteric viruses: rotavirus infection of gnotobiotic pigs as a model. Vet Immunol Immunopathol 87: 147-160.
21. Yuan L, Ward LA, Rosen BI, To TL, Saif LJ, (1996) Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J Virol 70: 3075-3083.
22. Desselberger U, Huppertz HI, (2011) Immune responses to rotavirus infection and vaccination and associated correlates of protection. J Infect Dis 203: 188-195.
23. Franco MA, Greenberg HB, (2000) Immunity to homologous rotavirus infection in adult mice. Trends Microbiol 8: 50-52.
24. Parreno V, Marcoppido G, Vega C, Garaicoechea L, Rodriguez D, et al. (2010) Milk supplemented with immune colostrum: protection against rotavirus diarrhea and modulatory effect on the systemic and mucosal antibody responses in calves experimentally challenged with bovine rotavirus. Vet Immunol Immunopathol 136: 12-27.
25. Sarker SA, Casswall TH, Juneja LR, Hoq E, Hossain I, et al. (2001) Randomized, placebo-controlled, clinical trial of hyperimmunized chicken egg yolk immunoglobulin in children with rotavirus diarrhea. J Pediatr Gastroenterol Nutr 32: 19-25.
26. Vega C, Bok M, Chacana P, Saif L, Fernandez F, et al. (2011) Egg yolk IgY: protection against rotavirus induced diarrhea and modulatory effect on the systemic and mucosal antibody responses in newborn calves. Vet Immunol Immunopathol 142: 156-169.
27. Inagaki M, Yamamoto M, Xijier Cairangzhuoma, Uchida K, et al. (2010) In vitro and in vivo evaluation of the efficacy of bovine colostrum against human rotavirus infection. Biosci Biotechnol Biochem 74: 680-682.
28. Mrukowicz J, Szajewska H, Vesikari T, (2008) Options for the prevention of rotavirus disease other than vaccination. J Pediatr Gastroenterol Nutr 46 Suppl 2: S32-37.
29. Mine Y, Kovacs-Nolan J, (2002) Chicken egg yolk antibodies as therapeutics in enteric infectious disease: a review. J Med Food 5: 159-169.
30. Schade R, Calzado EG, Sarmiento R, Chacana PA, Porankiewicz-Asplund J, et al. (2005) Chicken egg yolk antibodies (IgY-technology): a review of progress in production and use in research and human and veterinary medicine. Altern Lab Anim 33: 129-154.
31. Sesarman A, Mihai S, Chiriac MT, Olaru F, Sitaru AG, et al. (2008) Binding of avian IgY to type VII collagen does not activate complement and leucocytes and fails to induce subepidermal blistering in mice. Br J Dermatol 158: 463-471.
32. Carlander D, Stalberg J, Larsson A, (1999) Chicken antibodies: a clinical chemistry perspective. Ups J Med Sci 104: 179-189.
33. Schade R, Burger W, Schoneberg T, Schniering A, Schwarzkopf C, et al. (1994) Avian egg yolk antibodies. The egg laying capacity of hens following immunisation with antigens of different kind and origin and the efficiency of egg yolk antibodies in comparison to mammalian antibodies. ALTEX 11: 75-84.
34. Tini M, Jewell UR, Camenisch G, Chilov D, Gassmann M, (2002) Generation and application of chicken egg-yolk antibodies. Comp Biochem Physiol A Mol Integr Physiol 131: 569-574.
35. Dean KL, (2000) Hyperimmune eggs capture natural immune support. Alternative & Complementary therapies pp. 118-124.
36. Akita EM, Jang CB, Kitts DD, Nakai S, (1999) Evaluation of the allergenicity of egg yolk immunoglobulin Y and other egg proteins by passive cutaneous anaphylaxis. Food and Agricultural Immunology 11: 191-201.
37. Schade R, Henklein P, Hlinak A, de Vente J, Steinbusch H, (1996) Specificity of Chicken (IgY) versus Rabbit (IgG) Antibodies Raised against Cholecystokinin Octapeptide (CCK-8). ALTEX 13: 80-85.
38. Schade R, Hlinak A, (1996) Egg Yolk Antibodies, State of the Art and Future Prospects. ALTEX 13: 5-9.
39. Meyer RC, Bohl EH, Kohler EM, (1964) Procurement and Maintenance of Germ-Free Seine for Microbiological Investigations. Appl Microbiol 12: 295-300.
40. Jensen AR, Elnif J, Burrin DG, Sangild PT, (2001) Development of intestinal immunoglobulin absorption and enzyme activities in neonatal pigs is diet dependent. J Nutr 131: 3259-3265.
41. Mulder IE, Schmidt B, Lewis M, Delday M, Stokes CR, et al. (2011) Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity. PLoS One 6: e28279.
42. Cornaglia EM, Barrandeguy M, Fijtman N, Schudel A, (1989) Enzyme linked immunosorbent assay, immunofluorescent test and electrophoresis analysis of rotaviral RNA in the diagnosis and characterization of the bovine rotavirus. Revista Latinoamericana de Microbiologia pp. 59-62.
43. Saif L, Yuan L, Ward L, To T, (1997) Comparative studies of the pathogenesis, antibody immune responses, and homologous protection to porcine and human rotaviruses in gnotobiotic piglets. Adv Exp Med Biol 412: 397-403.
44. Littell RC, Henry PR, Ammerman CB, (1998) Statistical analysis of repeated measures data using SAS procedures. J Anim Sci 76: 1216-1231.
45. Wolfinger R, Chang M, Cary N, (1998) Comparing the SAS GLM and Mixed procedures for Repeted Measures. SAS Institute Inc.
46. Westfall P, Tobias R, Rom D, Wolfinger R, Hochberg Y, (1999) Multiple Comparisons and Multiple Tests. SAS Institute, Inc.
47. Hatta H, Tsuda K, Akachi S, Kim M, Yamamoto T, et al. (1993) Oral passive immunization effect of anti-human rotavirus IgY and its behavior against proteolytic enzymes. Biosci Biotechnol Biochem 57: 1077-1081.
48. Losonsky GA, Vonderfecht SL, Eiden J, Wee SB, Yolken RH, (1986) Homotypic and heterotypic antibodies for prevention of experimental rotavirus gastroenteritis. J Clin Microbiol 24: 1041-1044.
49. Coste A, Cohen J, Reinhardt M, Kraehenbuhl JP, Sirard JC, (2001) Nasal immunisation with Salmonella typhimurium producing rotavirus VP2 and VP6 antigens stimulates specific antibody response in serum and milk but fails to protect offspring. Vaccine 19: 4167-4174.
50. Coste A, Sirard JC, Johansen K, Cohen J, Kraehenbuhl JP, (2000) Nasal immunization of mice with virus-like particles protects offspring against rotavirus diarrhea. J Virol 74: 8966-8971.
51. Fernandez FM, Conner ME, Hodgins DC, Parwani AV, Nielsen PR, et al. (1998) Passive immunity to bovine rotavirus in newborn calves fed colostrum supplements from cows immunized with recombinant SA11 rotavirus core-like particle (CLP) or virus-like particle (VLP) vaccines. Vaccine 16: 507-516.
52. Fleming FE, Graham KL, Taniguchi K, Takada Y, Coulson BS, (2007) Rotavirus-neutralizing antibodies inhibit virus binding to integrins alpha 2 beta 1 and alpha 4 beta 1. Arch Virol 152: 1087-1101.
53. Iosef C, Van Nguyen T, Jeong K, Bengtsson K, Morein B, et al. (2002) Systemic and intestinal antibody secreting cell responses and protection in gnotobiotic pigs immunized orally with attenuated Wa human rotavirus and Wa 2/6-rotavirus-like-particles associated with immunostimulating complexes. Vaccine 20: 1741-1753.
54. Redmond MJ, Ijaz MK, Parker MD, Sabara MI, Dent D, et al. (1993) Assembly of recombinant rotavirus proteins into virus-like particles and assessment of vaccine potential. Vaccine 11: 273-281.
55. Tosser G, Delaunay T, Kohli E, Grosclaude J, Pothier P, et al. (1994) Topology of bovine rotavirus (RF strain) VP6 epitopes by real-time biospecific interaction analysis. Virology 204: 8-16.
56. Jacoby H, Moore J, Wnorowski G, (2001) Inhibition of diarrhea by immune egg: a castor oil mouse model. Journal of Nutraceuticals, Functional & Medical Foods 3: 47-52.
57. Torche AM, Le Dimna M, Le Corre P, Mesplede A, Le Gal S, et al. (2006) Immune responses after local administration of IgY loaded-PLGA microspheres in gut-associated lymphoid tissue in pigs. Vet Immunol Immunopathol 109: 209-217.
58. Helm RM, Furuta GT, Stanley JS, Ye J, Cockrell G, et al. (2002) A neonatal swine model for peanut allergy. J Allergy Clin Immunol 109: 136-142.
59. Nelson K, Mine Y, Duarte J, Matar C, (2007) Immunomodulating effects of egg yolk low lipid peptic digests in a murine model. Food and Agricultural Immunology 18: 15.
60. Xu YP, Zou WM, Zhan XJ, Yang SH, Xie DZ, et al. (2006) Preparation and determination of immunological activities of anti-HBV egg yolk extraction. Cell Mol Immunol 3: 67-71.
61. Bernhisel-Broadbent J, Yolken RH, Sampson HA, (1991) Allergenicity of orally administered immunoglobulin preparations in food-allergic children. Pediatrics 87: 208-214.
62. El-Merhibi A, Lymn K, Kanter I, Penttila IA, (2012) Early oral ovalbumin exposure during maternal milk feeding prevents spontaneous allergic sensitization in allergy-prone rat pups. Clin Dev Immunol pp. 396232.
63. Rahman S, Higo-Moriguchi K, Htun KW, Taniguchi K, Icatlo FC Jr, et al. (2012) Randomized placebo-controlled clinical trial of immunoglobulin Y as adjunct to standard supportive therapy for rotavirus-associated diarrhea among pediatric patients. Vaccine 30: 4661-4669.