Chicken egg yolk antibodies (IgY) as non-antibiotic production enhancers for use in swine production: a review

Journal of Animal Science and Biotechnology

Yongping Xu²  Shuying Li³  Yuhong Zhen¹  Lili Wang²  Xiaoyu Li² 

[1] Department of Pharmacy, Dalian Medical University, Dalian 116044, China;Ministry of Education Center for Food Safety of Animal Origin, Dalian 116620, China;Dalian SEM Bio-Engineering Technology Co. Ltd, Dalian 116620, China

关键词: Swine;    IgY;    Egg yolk antibodies;    Disease control;    Diarrhea;   

Others  :  1224547
DOI  :  10.1186/s40104-015-0038-8

 received in 2015-06-09, accepted in 2015-07-30,  发布年份 2015

【 摘 要 】

In recent years, the use of in-feed antibiotics for growth and disease prevention in livestock production has been under severe scrutiny. The use and misuse of in-feed antibiotics has led to problems with drug residues in animal products and increased bacterial resistance. Chicken egg yolk antibodies (IgY) have attracted considerable attention as an alternative to antibiotics to maintain swine health and performance. Oral administration of IgY possesses many advantages over mammalian IgG such as cost-effectiveness, convenience and high yield. This review presents an overview of the potential to use IgY immunotherapy for the prevention and treatment of swine diarrhea diseases and speculates on the future of IgY technology. Included are a review of the potential applications of IgY in the control of enteric infections of either bacterial or viral origin such as enterotoxigenic Escherichia coli, Salmonella spp., rotavirus, porcine transmissible gastroenteritis virus, and porcine epidemic diarrhea virus. Some potential obstacles to the adoption of IgY technology are also discussed.

【 授权许可】

   
2015 Li et al.

【 图 表 】

Fig. 1.

【 参考文献 】

• [1]Cromwell GL: Why and how antibiotics are used in swine production. Anim Biotechnol 2002, 13:7-27.
• [2]Khachatourians GG: Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria. Can Med Assoc J 1998, 159:1129-1136.
• [3]Casewell M, Friis C, Marco E, McMullin P, Phillips I: The European ban on growth promoting antibiotics and emerging consequences for human and animal health. J Antimicrob Chemother 2003, 52:159-161.
• [4]U.S. Food and Administration. Phasing out certain antibiotic use in farm animals.. http://www.fda.gov/ForConsumers/ConsumerUpdates/ucm378100.htm?source=govdelivery&utm_medium=email&utm_source=govdelivery webcite
• [5]Adeola O, Cowieson AJ: Opportunities and challenges in using exogenous enzymes to improve nonruminant animal production. J Anim Sci 2011, 89:3189-3218.
• [6]Mroz Z: Organic acids as potential alternatives to antibiotic growth promoters for pigs. Adv Pork Prod 2005, 16:169-182.
• [7]Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS: Feed additives for swine: Fact sheets-prebiotics and probiotics, and phytogenics. J Swine Health Prod 2010, 18:132-136.
• [8]Cho JH, Zhao PY, Kim IH: Probiotics as a dietary additive for pigs: Aa review. J Anim Vet Adv 2011, 10:2127-2134.
• [9]Halas V, Nochta I: Mannan oligosaccharides in nursery pig nutrition and their potential mode of action. Animals 2012, 2:261-274.
• [10]Windisch WM, Schedle K, Plitzner C, Kroismayr A: Use of phytogenic products as feed additives for swine and poultry. J Anim Sci 2008, 86:140-148.
• [11]Gong J, Yin F, Hou Y, Yin Y: Review: Chinese herbs as alternatives to antibiotics in feed for swine and poultry production: Potential and challenges in application. Can J Anim Sci 2014, 94:223-241.
• [12]Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS: Feed additives for swine: Fact sheets-High dietary levels of copper and zinc for young pigs, and phytase. J Swine Health Prod 2010, 18:87-91.
• [13]Pettigrew JE: Reduced use of antibiotic growth promoters in diets fed to weanling pigs: Dietary tools, Part 1. Anim Biotechnol 2006, 17:207-215.
• [14]Xu YP, Li XY, Jin LJ, Zhen YH, Lu YN, Li SY, You JS, Wang LH: Application of chicken egg yolk immunoglobulins in the control of terrestrial and aquatic animal diseases: A review. Biotechnol Adv 2011, 29:860-868.
• [15]Carlander D, Kollberg H, Wejaker PE, Larsson A: Peroral immunotherapy with yolk antibodies for the prevention and treatment of enteric infections. Immunol Res 2000, 21:1-6.
• [16]Diraviyam T, Zhao B, Wang Y, Schade R, Michael A, Zhang XY: Effect of chicken egg yolk antibodies (IgY) against diarrhea in domesticated animals: A systematic review and meta-analysis. PloS One 2014., 9Article ID e97716
• [17]Klemperer F: Ueber natürliche Immunität und ihre Verwerthung für die Immunisirungstherapie. Archiv für Experimentelle Pathologie und Pharmakologie 1893, 31:356-382.
• [18]Schade R, Hlinak A: Egg yolk antibodies, state of the art and future prospects. ALTEX 1996, 13(Suppl 1):5-9.
• [19]Schade R, Staak C, Hendriksen C, Erhard MH, Hugel H, Koch G, Larsson A, Pollmann W, van Regenmortel M, Rijke E, Spielmann H, Steinbusch H, Straughan D: The production of avian (egg yolk) antibodies: IgY. The report and recommendations of ECVAM workshop 21. ATLA 1997, 24:925-934.
• [20]Schade R, Calzado EG, Sarmiento R, Chacana PA, Porankiewicz-Asplund J, Terzolo HR: Chicken egg yolk antibodies (IgY-technology): A review of progress in production and use in research and human and veterinary medicine. Altern Lab Anim 2005, 33:129-154.
• [21]Gassmann M, Thömmes P, Weiser T, Hübscher U: Efficient production of chicken egg antibodies against a conserved mammalian protein. FASEB J 1990, 4:2528-2531.
• [22]Larsson A, Carlander D, Wilhelmasson M: Immune response in chicken with different amounts of antigen. Food Agricult Immunol 1998, 10:29-36.
• [23]Coleman MA. Oral administration of chicken yolk immunoglobulins to lower somatic cell count in the milk of lactating ruminants. Alexandria, VA: United States Patent and Trademark Office; 1996. US Patent 5,585,098.
• [24]Erhard MH, Schmidt P, Zinsmeister P, Hofmann A, Munster U, Kaspers B: Adjuvant effects of various lipopeptides and interferon-gamma on the humoral immune response of chickens. Poult Sci 2000, 79:1264-1270.
• [25]Fryer J, Firca J, Leventhal J, Blondin B, Malcolm A, Ivancic D, Gandhi R, Shah A, Pao W, Abecassis M, Kaufman D, Stuart F, Anderson B: IgY antiporcine endothelial cell antibodies effectively block human antiporcine xenoantibody binding. Xenotransplantation 1999, 6:98-109.
• [26]Jin LZ, Samuel K, Baidoo K, Marquardt RR, Frohlich AA: In vitro inhibition of adhesion of enterotoxigenic Escherichia coli K88 to piglet intestinal mucus by egg yolk antibodies. FEMS Immunol Med Microbiol 1998, 21:313-321.
• [27]Yokoyama H, Peralta RC, Diaz R, Sendo S, Ikemori Y, Kodama Y: Passive protective effect of chicken egg yolk immunoglobulins against experimental enterotoxigenic Escherichia coli infection in neonatal piglets. Infect Immun 1992, 60:998-1007.
• [28]Alexander TJL: Neonatal diarrhea in pigs. In Escherichia coli in Domestic Animals and Humans. Edited by Gyles CL. CAB International, Wallingford; 1994:151-170.
• [29]Hampson DJ: Postweaning Escherichia coli diarrhea in pigs. In Escherichia coli in Domestic Animals and Humans. Edited by Gyles CL. CAB International, Wallingford; 1994:171-191.
• [30]Zhang W, Berberov EM, Freeling J, He D, Moxley RA, Francis DH: Significance of heat-stable and heat-labile enterotoxins in porcine colibacillosis in an additive model for pathogenicity studies. Infect Immun 2006, 74:3107-3114.
• [31]Rapacz J, Hasler-Rapacz J: Polymorphism and inheritance of swine small intestinal receptors mediating adhesion of three serological variants of Escherichia coli-producing K88 pilus antigen. Anim Genet 1986, 17:305-321.
• [32]Waters JR, Sellwood R. Aspects of genetic resistance to K88 E. coli in pigs. In: Proceedings of the 2nd World Congress on Genetics Applied to Livestock Production. Madrid: International committee for World Congress on Genetics Applied to Livestock Production; 4–8 October 1982. p. 362.
• [33]Imberechts H, Deprez P, van Driessche E, Pohl P: Chicken egg-yolk antibodies against F18ab fimbriae of Escherichia coli inhibit shedding of F18 positive E. coli by experimentally infected pigs. Vet Microbiol 1997, 54:329-341.
• [34]Marquardt RR, Jin LZ, Kim JW, Fang L, Frohlich AA, Baidoo SK: Passive protective effect of egg-yolk antibodies against enterotoxigenic Escherichia coli K88+ infection in neonatal and early-weaned piglets. FEMS Immunol Med Microbiol 1999, 23:283-288.
• [35]Zuniga A, Yokiyama H, Albicker-Rippinger P, Eggenberger E, Bertschinger HU: Reduced intestinal colonisation with F18-positive enterotoxigenic Escherichia coli in weaned pigs fed chicken egg antibody against the fimbriae. FEMS Immunol Med Microbiol 1997, 18:153-161.
• [36]Owusu-Asiedu A, Baidoot SK, Nyachoti CM, Marquardt RR: Response of early-weaned pigs to spray-dried porcine or animal plasma-based diets supplemented with egg-yolk antibodies against enterotoxigenic Escherichia coli. J Anim Sci 2002, 80:2895-2903.
• [37]Owusu-Asiedu A, Nyachoti CM, Marquardt RR: Response of early-weaned pigs to an enterotoxigenic Esherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody, zinc oxide, fumaric acid or antibiotic. J Anim Sci 2003, 81:1790-1798.
• [38]Owusu-Asiedu A, Nyachoti CM, Baidoo SK, Marquardt RR, Yang X: Response of early-weaned pigs to an enterotoxigenic Esherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody. J Anim Sci 2003, 81:1781-1789.
• [39]Heo JM, Woyengo TA, Kahindi RK, Kiarie E, Maiti P, Nyachoti CM: Ileal amino acid digestibility in egg from hyperimmunized- hens fed to weaned pigs and piglet response to diets contain egg products. Anim Feed Sci Tech 2015, 204:52-61.
• [40]Berberov EM, Zhou Y, Francis DH, Scott MA, Kachman SD, Moxey RA: Relative importance of heat-labile enterotoxin in the causation of severe diarrheal disease in the gnotobiotic piglet model by a strain of enterotoxigenic Escherichia coli that produces multiple enterotoxins. Infect Immun 2004, 72:3914-3924.
• [41]Allen KP, Randolph MM, Fleckenstein JM: Importance of heat-labile enterotoxin in colonization of the adult mouse small intestine by human enterotoxigenic Escherichia coli strains. Infect Immun 2006, 74:869-875.
• [42]Clements JD: Construction of a nontoxic fusion peptide for immunization against Escherichia coli strains that produce heat-labile and heat-stable enterotoxins. Infect Immun 1990, 58:1159-1166.
• [43]Dubreuil JD, Letellier A, Harel J: A recombinant Escherichia coli heat-stable enterotoxin b (STb) fusion protein eliciting neutralizing antibodies. FEMS Immunol Med Mic 1996, 13:317-323.
• [44]You JS, Xu YP, He ML, McAllister TA, Thacker PA, Li XY, Wang TT, Jin LJ: Protection of mice against enterotoxigenic E. coli by immunization with a polyvalent enterotoxin comprising a combination of LTB, STa, and STb. Appl Microbiol Biotechnol 2011, 89:1885-1893.
• [45]You JS, Xu YP, Li HQ, Wang LH, Wu FF, Xu FX, Jin LJ, Li SY, Li XY: Chicken egg yolk immunoglobulin (IgY) developed against fusion protein LTB-STa-STb neutralizes the toxicity of Escherichia coli heat-stable enterotoxins. J Appl Microbiol 2014, 117:320-328.
• [46]Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C: Food-related illness and death in the United States. Emerg Infect Dis 1999, 5:607-625.
• [47]U.S. Department of Agriculture, Economic Research Service: Foodborne illness cost calculator: Salmonella.. http://www.ers.usda.gov webcite
• [48]Besser TE, Goldoft M, Pritchett LC, Khakhria R, Hancock DD, Rice DH: Multiresistant Salmonella typhimurium DT104 infections of humans and domestic animals in the Pacific Northwest of the United States. Epidemiol Infect 2000, 124:193-200.
• [49]Centers for Disease Control and Prevention: Outbreaks of multidrug-resistant Salmonella Typhimurium associated with veterinary facilities—Idaho, Minnesota, and Washington Morb Mortal Wkly Rep 2001, 50:701-704.
• [50]Hurd HS, McKean JD, Griffith RW, Wesley IV, Rostagno MH: Salmonella enterica infections in market swine with and without transport and holding. Appl Environ Microbiol 2002, 68:2376-2381.
• [51]Oosterom J: Epidemiological studies and proposed preventive measures in the fight against human salmonellosis. Int J Food Microbiol 1991, 12:41-51.
• [52]Yokoyama H, Umeda K, Peralta RC, Hashi T, Icatlo FCJ, Kuroki M, Ikemori Y, Kodama Y: Oral passive immunization against experimental salmonellosis in mice using chicken egg-yolk antibodies specific for Salmonella enteritidis and S. typhimurium. Vaccine 1998, 16:388-393.
• [53]Mathew AG, Rattanatabtimtong S, Nyachoti CM, Fang L: Effects of in-feed egg yolk antibodies on Salmonella shedding, bacterial antibiotic resistance, and health of pigs. J Food Protect 2009, 72:267-273.
• [54]Letellier A, Messier S, Lessard L, Quessy S. Assessment of different treatments to reduce Salmonella in swine. In: Proceedings of the 3rd International Symposium on the Epidemiology and Control of Salmonella in Pork. Washington, DC: Iowa State University; 5-7 August 1999. p. 321–325.
• [55]Wood RL, Pospischil A, Rose R: Distribution of persistent Salmonella typhimurium infection in internal organs of swine. Am J Vet Res 1989, 50:1015-1021.
• [56]Fedorka-Cray PJ, Kelley LC, Stabel TJ, Gray JT, Laufer JA: Alternate routes of invasion may affect pathogenesis of Salmonella typhimurium in swine. Infect Immun 1995, 63:2658-2664.
• [57]Jensen VB, Harty JT, Jones BD: Interactions of the invasive pathogens Salmonella typhimurium, Listeria monocytogenes, and Shigella flexneri with M cells and murine Peyer’s patches. Infect Immun 1998, 66:3758-3766.
• [58]Saif LJ, Wesley RD: Transmissible gastroenteritis and porcine respiratory coronavirus. In Disease of Swine. 8th edition. Iowa State University Press, Ames; 1999:295-325.
• [59]Yan QG, Ou Y, Guo WZ, Feng T, Fan WQ, Lai WL, Cao HZ, Li B: Isolation of SC-1strain of transmissible gastroenteritis virus of swine and characteristic analysis of gene7. Chin J Vet Sci 2007, 27:613-616.
• [60]Yang LL, Guo FS, Sun SF, Wu B, Chen HC: Comparsion of antigenicity between expressed proteins of the fragment including S gene whole antigenic sites and the deleted fragment in porcine respiratory coronavirus of transmissible gastroeritis virus. Chin J Virol 2005, 21:384-388.
• [61]Zuo Y, Fan J, Fan H, Li T, Zhang X: Prophylactic and therapeutic effects of egg yolk immunoglobulin against porcine transmissible gastroenteritis virus in piglets. Front Agric China 2009, 3:104-108.
• [62]Cui HZ, Jiang HL, Zhang JL, Zhang H, Qin GX: Study and application of the hyperimmunized yolk antibodies against TGEV and PEDV in piglets. China Anim Husbandry Vet Med 2012, 39:173-175.
• [63]Wood EN: An apparently new syndrome of porcine epidemic diarrhea. Vet Rec 1977, 100:243-244.
• [64]DeBouck P, Pensaert M: Experimental infection of pigs with a new porcine enteric coronavirus CV 777. Am J Vet Res 1980, 41:219-223.
• [65]Pigpers A, van Nieuwstadt AP, Terpstra C, Verheijden JHM: Porcine epidemic diarrhea in a herd of breeding and finishing pigs. Vet Rec 1993, 132:129-131.
• [66]Kweon CH, Kwon BJ, Woo SR, Kim JM, Woo GH, Son DH, Hur W, Lee YS: Immunoprophylactic effect of chicken egg yolk immunoglobulin (Ig Y) against porcine epidemic diarrhea virus (PEDV) in piglets. J Vet Med Sci 2000, 62:961-964.
• [67]Song WP, Xu FZ, Wang JL, Yang B, Lai PA: Effect of IgY treatment on porcine epidemic diarrhea virus (PEDV) in piglets. Acta Agriculturae Boreali- Sinica 2003, 18:114-115.
• [68]Santosham M, Chandran A, Fitzwater S, Fischer-Walker C, Baqui AH, Black R: Progress and barriers for the control of diarrhoeal disease. Lancet 2010, 376:63-67.
• [69]Kaminjolo JS, Adesiyun AA: Rotavirus infection in calves, piglets, lambs and goat kids in Trinidad. Br Vet J 1994, 150:293-299.
• [70]Kuroki M, Ohta Y, Ikemori Y, Peralta RC, Yokoyama H, Kodama Y: Passive protection against bovine rotavirus in calves by specific immunoglobulins from chicken egg yolk. Arch Virol 1994, 138:143-148.
• [71]Yolken RH, Leister F, Wee SB, Miskuff R, Vonderfecht S: Antibodies to rotavirus in chickens’ eggs: A potential source of antiviral immunoglobulins suitable for human consumption. Pediatrics 1988, 81:291-295.
• [72]Ebina T: Prophylaxis of rotavirus gastroenteritis using immunoglobulin. Arch Virol Suppl 1996, 12:217-223.
• [73]Ozpinar H, Erhard MN, Aytug N, Ozpinar A, Baklaci C, Karamuptuoglu S, Hofmann A, Losch V: Dose-dependent effects of specific egg-yolk antibodies on diarrhea of newborn calves. Prevent Vet Med 1996, 27:67-73.
• [74]Vega CG, Bok M, Vlasova AN, Chattha KS, Fernández FM, Wigdorovitz A, Parreño VG, Saif LJ: IgY antibodies protect against human rotavirus induced diarrhea in the neonatal gnotobiotic piglet disease model. PloS One 2012., 7Article ID e42788
• [75]Hong JW, Kwon OS, Min BJ, Lee WB, Shon KS, Kim IH, Kim JW: Evaluation effects of spray-dried egg protein containing specific egg yolk antibodies as a substitute for spray-dried plasma protein or antibiotics in weaned pigs. Asian-Aust J Anim Sci 2004, 17:1139-1144.
• [76]Chernysheva LV, Friendship RM, Dewey CE, Gyles CL: The effect of dietary chicken egg-yolk antibodies on the clinical response in weaned pigs challenged with a K88+ Esherichia coli isolate. J Swine Health Prod 2003, 12:119-122.
• [77]Kovacs-Nolan J, Mine Y: Microencapsulation for the gastric passage and controlled intestinal release of immunoglobulin Y. J Immunol Methods 2005, 296:199-209.
• [78]Shimizu M, Fitzsimmons RC, Nakai S: Anti-E. coli immunoglobulin Y isolated from egg yolk of immunized chickens as a potential food ingredient. J Food Sci 1988, 53:1360-1366.
• [79]Yokoyama H, Peralta RC, Sendo S, Ikemori Y, Kodama Y: 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 1993, 54:867-872.
• [80]Chang HM, Lee YC, Chen CC, Tu YY: Microencapsulation protects immunoglobulin in yolk (IgY) specific against Helicobacter pylori urease. J Food Sci 2002, 67:15-20.
• [81]Cho YH, Lee JJ, Park IB, Huh CS, Baek YJ, Park J: Protective effect of microencapsulation consisting of multiple emulsification and heat gelation processes on immunoglobulin in yolk. J Food Sci 2005, 70:148-151.
• [82]Li XY, Jin LJ, McAllister TA, Stanford K, Xu JY, Lu YN, Zhen YH, Sun YX, Xu YP: Chitosan-alginate microcapsules for oral delivery of egg yolk immunoglobulin (IgY). J Agr Food Chem 2007, 55:2911-2917.
• [83]Li XY, Jin LJ, Uzonna JE, Li SY, Liu JJ, Li HQ, Lu YN, Zhen YH, Xu YP: Chitosan- alginate microcapsules for oral delivery of egg yolk immunoglobulin (IgY): in vivo evaluation in a pig model of enteric colibacillosis. Vet Immunol Immunop 2009, 29:132-136.
• [84]Marquardt RR, Li S. Control of diarrhea in young pigs using therapeutic antibodies. In: Proceedings of Allen D. Leman Swine Conference. Minneapolis, MN: University of Minnesota. 15–18 September 2001. p. 227-239.
• [85]Hatta H, Kapoor MP, Juneja LR: Bioactive components in egg yolk. In Egg Bioscience and Biotechnology. Edited by Mine Y. John Wiley & Sons Inc, New Jersey; 2008:185-237.
• [86]Chu WH, Gao GF: Application of chicken egg yolk immunoglobulins against Enterotoxigenic Escherichia coli in piglets. Chin J Vet Sci 2006, 26:616-618.
• [87]Yokoyama H, Hashi T, Umeda K, Icatlo FC Jr, Kuroki M, Ikemori Y, Kodama Y: Effect of oral egg antibody in experimental F18+ Escherichia coli infection in weaned pigs. J Vet Med Sci 1997, 59:917-921.
• [88]Yang BL, Zhang YF, Wu JM: Research of hyperimmunized yolk antibodies for prevention and treatment of piglet dysentery. Am Sci Vet Med 2002, 10:37-38.
• [89]Xu FZ, Wang JL, Yang B, Song WP, Lai PA, Qin ZR, Meng YN: Preparation and application of chicken egg yolk immunoglobulins against enterotoxigenic Escherichia coli in piglets. Acta Agr Boreali-Sinica 2002, 17:108-112.