Alternatives to antibiotics as growth promoters for use in swine production: a review

Journal of Animal Science and Biotechnology

Philip A Thacker¹ 

[1] Department of Animal and Poultry Science, University of Saskatchewan, 51 Campus Drive, Saskatoon, Saskatchewan S7N 5A8, Canada

关键词: Recombinant enzymes;    Rare earth elements;    Eucalyptus oil-medium chain fatty acids;    Essential oils;    Egg yolk antibodies;    Clay minerals;    Antimicrobial peptides;   

Others  :  805189
DOI  :  10.1186/2049-1891-4-35

 received in 2013-07-03, accepted in 2013-09-12,  发布年份 2013

【 摘 要 】

In the past two decades, an intensive amount of research has been focused on the development of alternatives to antibiotics to maintain swine health and performance. The most widely researched alternatives include probiotics, prebiotics, acidifiers, plant extracts and neutraceuticals such as copper and zinc. Since these additives have been more than adequately covered in previous reviews, the focus of this review will be on less traditional alternatives. The potential of antimicrobial peptides, clay minerals, egg yolk antibodies, essential oils, eucalyptus oil-medium chain fatty acids, rare earth elements and recombinant enzymes are discussed. Based on a thorough review of the literature, it is evident that a long and growing list of compounds exist which have been tested for their ability to replace antibiotics as feed additives in diets fed to swine. Unfortunately, the vast majority of these compounds produce inconsistent results and rarely equal antibiotics in their effectiveness. Therefore, it would appear that research is still needed in this area and that the perfect alternative to antibiotics does not yet exist.

【 授权许可】

   
2013 Thacker; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Cromwell GL: Why and how antibiotics are used in swine production. Anim Biotechnol 2002, 13:7-27.
• [2]Vondruskova H, Slamova R, Trckova M, Zraly Z, Pavli I: Alternatives to antibiotic growth promotors in prevention of diarrhea in weaned piglets: a review. Vet Med 2010, 55:199-224.
• [3]Van der Fels-Klerx HJ, Puister-Jansen LF, Van Asselt ED, Burgers SL: Farm factors associated with the use of antibiotics in pig production. J Anim Sci 2011, 89:1922-1929.
• [4]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.
• [5]Simon O: An interdisciplinary study on the mode of action of probiotics in pigs. J Anim Feed Sci 2010, 19:230-243.
• [6]Cho JH, Zhao PY, Kim IH: Probiotics as a dietary additive for pigs: a review. J Anim Vet Adv 2011, 10:2127-2134.
• [7]Halas V, Nochta I: Mannan oligosaccharides in nursery pig nutrition and their potential mode of action. Animals 2012, 2:261-274.
• [8]Thacker PA: Recent advances in the use of enzymes with special reference to β-glucanases and pentosanases in swine rations. Asian-Aust J Anim Sci 2000, 13:376-385. (Special Issue)
• [9]Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS: Feed additives for swine: fact sheets-carcass modifers, carbohydrate-degrading enzymes and proteases, and anthelmintics. J Swine Health Prod 2009, 17:325-332.
• [10]Adeola O, Cowieson AJ: Opportunities and challenges in using exogenous enzymes to improve nonruminant animal production. J Anim Sci 2011, 89:3189-3218.
• [11]Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS: Feed additives for swine: fact sheets-acidifiers and antibiotics. J Swine Health Prod 2009, 17:270-275.
• [12]Kil DY, Kwon WB, Kim BG: Dietary acidifiers in weanling pig diets: a review. Revista Colombian de Diencias Pecuarias 2011, 24:1-22.
• [13]Suruanarayana MV, Suresh J, Rajasekhar MV: Organic acids in swine feeding: a review. Agric Sci Res J 2012, 2:523-533.
• [14]Papatsiros VG, Billinis C: The prophylactic use of acidifiers as antibacterial agents in swine. In Antimicrobial agents Edited by Bobbarala V. 2012, 295-310. InTech, DOI:10.5772/32278. Available from: http://www.intechopen.com/books/antimicrobial-agents/the-prophylactic-use-of-acidifiers-as-antibacterial-agents-in-swine webcite. 978-953-51-0723-1
• [15]Windisch W, Schedle K, Plitzner C, Kroismayr A: Use of phytogenic products as feed additives for swine and poultry. J Anim Sci 2008, 86(E. Suppl):E140-E148.
• [16]Liu HW, Tong JM, Zhou DW: Utilization of Chinese herbal feed additives in animal production. Agric Sci China 2011, 10:1262-1272.
• [17]Pettigrew JE: Reduced use of antibiotic growth promoters in diets fed to weanling pigs: dietary tools, part 1. Anim Biotechnol 2006, 17:207-215.
• [18]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.
• [19]Li YM, Xiang Q, Zhang QH, Huang YD, Su ZJ: Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides 2012, 37:207-215.
• [20]Koczulla AR, Bals R: Antimicrobial peptides: current status and therapeutic potential. Drugs 2003, 63:389-406.
• [21]Wu SD, Zhang FR, Huang ZM, Liu H, Xie CY, Zhang J, Thacker PA, Qiao S: Effect of the antibacterial peptide cecropin AD on performance and intestinal health in weaned piglets challenged with Escherichia coli. Peptides 2012, 35:225-230.
• [22]Yusuf MA, Hamid TH: Lactic acid bacteria: bacteriocin producer: a mini review. IOSR J Pharm 2013, 3:44-50.
• [23]Stahl CH, Callaway TR, Lincoln LM, Lonergan SM, Genovese KJ: Inhibitory activities of colicins against Esherichia coli strains responsible for postweaning diarrhea and edema disease in swine. Antimicrob Agents Chemother 2004, 48:3119-3121.
• [24]Cutler SA, Lonergan SM, Cornick N, Johnson AK, Stahl CH: Dietary inclusion of colicin E1 is effective in preventing postweaning diarrhea caused by F18-positive Esherichia coli in pigs. Antimicrob Agents Chemother 2007, 51:3830-3835.
• [25]Yoon JH, Ingale SL, Kim JS, Kim KH, Lohakare J, Park YK, Park JC, Kwon LK, Chae BJ: Effects of dietary supplementation with antimicrobial peptide-P5 on growth performance, apparent total tract digestibility, faecal and intestinal microflora and intestinal morphology of weanling pigs. J Sci Food Agric 2013, 93:587-592.
• [26]Yoon JH, Ingale SL, Kim JS, Kim KH, Lee SH, Park YK, Kwon IK, Chae BJ: Effects of dietary supplementation of antimicrobial peptide-A3 on growth performance, nutrient digestibility, intestinal and fecal microflora and intestinal morphology in weanling pigs. Anim Feed Sci Technol 2012, 177:98-107.
• [27]Wang JH, Wu CC, Feng J: Effect of dietary antibacterial peptide and zinc-methionine on performance and serum biochemical parameters in piglets. Czech J Anim Sci 2011, 56:30-36.
• [28]Schell TC, Lindemann MD, Kornegay ET, Blodgett DJ: Effects of feeding aflatoxin-contained diets with and without clay to weanling and growing pigs on performance, liver function and mineral metabolism. J Anim Sci 1993, 71:1209-1218.
• [29]Schell TC, Lindemann MD, Kornegay ET, Blodgett DJ: Effects of different types of clay for reducing the detrimental effects of aflatoxin-contained diets on performance and serum profiles of weanling pigs. J Anim Sci 1993, 71:1226-1231.
• [30]Trckova M, Vondruskova H, Zraly Z, Alexa P, Kummer V, Maskova J, Mrlik V, Krizova K, Slana I, Leva L, Pavlik I: The effect of kaolin feeding on efficiency, health status and course of diarrheoal infections caused by enterotoxigenic Esherichia coli strains in weaned piglets. Vet Med 2009, 54:47-63.
• [31]Song M, Liu Y, Soares JA, Che TM, Osuna O, Maddox CW, Pettigrew JE: Dietary clays alleviate diarrhea of weaned pigs. J Anim Sci 2012, 90:345-360.
• [32]Thacker PA: Performance of growing-finishing pigs fed diets containing graded levels of Biotite, and alumninosilicate clay. Asian-Aust J Anim Sci 2003, 16:1666-1672.
• [33]Chen YJ, Kwon OS, Min BJ, Son KS, Cho JH, Hong JW, Kim IH: The effects of dietary Biotite V supplementation as an alternative substance to antibiotics in growing pigs. Asian-Aust J Anim Sci 2005, 18:1642-1645.
• [34]Prvulovic D, Jovanovic-Galovic A, Stanic B, Popovic M, Grubor-Lajsic G: Effects of a clinoptilolite supplement in pig diets on performance and serum parameters. Czech J Anim Sci 2007, 52:159-164.
• [35]Yan L, Hong SM, Kim IH: Effect of bacteriophage supplementation on the growth performance, nutrient digestibility, blood characteristics, and fecal microbial shedding in growing pigs. Asian-Aust J Anim Sci 2012, 25:1451-1456.
• [36]Xu Y, Li X, Jin L, Zhen Y, Lu Y, Li S, You J, Wang L: Application of chicken egg yolk immunoglobulins in the control of terrestrial and aquatic animal diseases: a review. Biotechnol Adv 2011, 29:860-868.
• [37]Chalghoumi R, Beckers Y, Portetelle D, Thewis A: Hen egg yolk antibodies (IgY) production and use for passive immunization against bacterial enteric infections in chicken: a review. Biotechnol Agron Soc Environ 2009, 13:295-308.
• [38]Kovacs-Nolan J, Mine Y: Egg yolk antibodies for passive immunity. Annu Rev Food Sci Technol 2012, 3:163-182.
• [39]Marquardt RR, Jin LZ, Kim JW, Fang L, Frohlich AA, Baidoo SK: Passive protective effect of egg-yolk antibodies against enterotoxigenic Esherichia coli K88+ infection in neonatal and early-weaned piglets. FEMS Immunol Med Microbiol 1999, 23:283-288.
• [40]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.
• [41]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.
• [42]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.
• [43]Zhang ZF, Kim IH: Effects of egg yolk immunoglobulin on growth performance, diarrhea score, diarrhea incidence and serum antibody titer in pre-and post-weaned pigs. Wayamba J Anim Sci 2013, 578X:590-597.
• [44]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.
• [45]Kovacs-Nolan J, Mine Y: Microencapsulation for the gastric passage and controlled intestinal release of immunoglobulin Y. J Immunol Methods 2005, 296:199-209.
• [46]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 evaluatin in a pig model of enteric colibacillosis. Vet Immunol Immunopathol 2009, 129:132-136.
• [47]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 Agric Food Chem 2007, 55:2911-2917.
• [48]Stein HH, Kil DY: Reduced use of antibiotic growth promoters in diets fed to weanling pigs: dietary tools, Part 2. Anim Biotechnol 2006, 17:217-231.
• [49]Gatnau R: Use of plant extracts in swine. 2009. Available at http://www.pig333.com/nutrition/use-of-plant-extracts-in-swine_957/ webcite
• [50]Michiels J, Missotten JA, Fremaut D, De Smet S, Dierick NA: In vitro characterization of the antimicrobial activity of selected essential oil components and binary combinations against the pig gut flora. Anim Feed Sci Technol 2009, 151:111-127.
• [51]Brenes A, Roura E: Essential oils in poultry nutrition: main effects and modes of action. Anim Feed Sci Technol 2010, 158:1-14.
• [52]Ragland D, Stevenson D, Hill MA: Oregano oil and multi-component carbohydrases as alternatives to antimicrobials in nursery diets. Swine Health Prod 2008, 16:238-243.
• [53]Cho JH, Chen YJ, Min BJ, Kim HJ, Kwon OS, Shon KS, Kim IH, Kim SJ, Asamer A: Effects of essential oils supplementation on growth performance, IgG concentration and fecal noxious gas concentration of weaned pigs. Asian-Aust J Anim Sci 2006, 19:80-85.
• [54]Maenner K, Vahjen W, Simon O: Studies on the effects of essential-oil based feed additives on performance, ileal nutrient digestibility, and selected bacterial groups in the gastrointestinal tract of piglets. J Anim Sci 2011, 89:2106-2112.
• [55]Li PF, Piao XS, Ru YJ, Han X, Xue LF, Zhang HY: Effects of adding essential oil to the diet of weaned pigs on performance, nutrient utilization, immune response and intestinal health. Asian-Aust J Anim Sci 2012, 25:1617-1626.
• [56]Ahmed ST, Hossain ME, Kim GM, Hwang JA, Ji H, Yang CJ: Effect of resveratrol and essential oils on growth performance, immunity, digestibility and fecal microbial shedding in challenged piglets. Asian-Aust J Anim Sci 2013, 26:683-690.
• [57]Huang Y, Yoo JS, Kim HJ, Wang Y, Chen YJ, Cho JH, Kim IH: Effects of dietary supplementation with blended essential oils on growth performance, nutrient digestibility, blood profiles and fecal characteristics in weanling pigs. Asian-Aust J Anim Sci 2010, 23:607-613.
• [58]Salari MH, Amine G, Shirazi MH, Hafezi R, Mohammadypour M: Antibacterial effects of Eucalyptus globulus leaf extract on pathogenic bacteria isolated from specimens of patients with respiratory tract disorders. Clin Microbiol Infect 2006, 12:194-196.
• [59]Serafino A, Vallebona PS, Andreola F, Zonfrillo M, Mercuri L, Federici M, Rasi G, Garaci E, Pierimarchi P: Stimulatory effect of Eucalyptus essential oil on innate cell-mediated immune response. BMC Immunol 2008, 9:17. BioMed Central Full Text
• [60]Abd El-Motaal AM, Ahmed AMH, Bahakaim ASA, Fathi MM: Productive performance and immunocompetence of commercial laying hens given diets supplemented with Eucalyptus. Int J Poult Sci 2008, 7:445-449.
• [61]Dierick NA, Decuypere JA, Molly K, Van Beek E, Vanderbecke E: The combined use of triacylglycerols containing medium-chain fatty acids and exogenous lipolytic enzymes as an alternative for nutritional antibiotics in piglet nutrition: I: in vitro screening of the release of MCFAs from selected fat sources by selected exogenous lipolytic enzymes under simulated pig gastric conditions and their effects on the gut flora of piglets. Livest Prod Sci 2002, 75:129-142.
• [62]Dierick NA, Decuypere JA, Molly K, Van Beek E, Vanderbecke E: The combined use of triacylglycerols containing medium-chain fatty acids and exogenous lipolytic enzymes as an alternative for nutritional antibiotics in piglet nutrition: II: in vivo release of MCFAs in gastric cannulated and slaughtered piglets by endogenous and exogenous lipases: effects on the luminal gut flora and growth performance. Livest Prod Sci 2002, 76:1-16.
• [63]Hong SM, Hwang JH, Kim IH: Effect of medium-chain triglyceride (MCT) on growth performance, nutrient digestibility, blood characteristics in weanling pigs. Asian-Aust J Anim Sci 2012, 25:1003-1008.
• [64]Rossi R, Pastorelli G, Cannata S, Corino C: Recent advances in the use of fatty acids as supplements in pig diets: a review. Anim Feed Sci Technol 2010, 162:1-11.
• [65]Han YK, Hwang UH, Thacker PA: Use of a micro-encapsulated medium chain fatty acid product as an alternative to zinc oxide and antibiotics for weaned pigs. J Swine Health Prod 2011, 19:34-43.
• [66]Redling K: Rare earth elements in agriculture with emphasis on animal husbandry. Muenchen: Diss Ludwig-Maximilians-Universitaet; 2006:325.
• [67]Zhu X, Li D, Yang W, Xiao C, Chen H: Effects of rare earth elements on the growth and nitrogen balance of piglets. Feed Industry 1994, 15:23-25.
• [68]He R, Xia Z: Effects of rare earth elements on growing and fattening of pigs. Guangxi Agric Sci 1998, 5:243-245.
• [69]Rambeck WA, Wehr U: Rare earth elements as alternative growth promoters in pig production. Arch Tierernahr 2000, 53:323-334.
• [70]He ML, Rambeck WA: Rare earth elements: a new generation of growth promoters for pigs. Arch Anim Nutr 2000, 53:323-334.
• [71]He ML, Ranz D, Rambeck WA: Study on the performance enhancing effect of rare earth elements in growing and finishing pigs. J Anim Physiol Anim Nutr 2001, 85:263-270.
• [72]Kraatz M, Taras D, Manner K, Simon O: Weaning pig performance and faecal microbiota with and without in-feed addition of rare earth elements. J Anim Physiol Anim Nutr 2006, 90:361-368.
• [73]Han YK, Thacker PA: Effect of antibiotics, zinc oxide and rare earth mineral yeast on performance, nutrient digestibility and blood parameters in weaned pigs. Asian-Aust J Anim Sci 2010, 23:1057-1065.
• [74]Buhler M, Limper J, Muller A, Schwarz G, Simon O, Sommer M, Spring W: Enzymes in animal nutrition. German Feed Additives Association Fact Sheet; 2013. Available at http://www.awt-feedadditives.de/Publikationen/Enzymbro-engl.pdf webcite
• [75]Choct M: Feed non-starch polysaccharides: chemical structures and nutritional significance. Singapore: Proceedings of the Feed Ingredients Asia 97 Conference; 1997.
• [76]Metzler B, Bauer B, Mosenthin R: Microflora management in the gastrointestinal tract of piglets. Asian-Aust J Anim Sci 2005, 18:1353-1362.
• [77]Kiarie E, Nyachoti CM, Slominski BA, Blank G: Growth performance, gastrointestinal microbial activity, and nutrient digestibility in early-weaned pigs fed diets containing flaxseed and carbohydrase enzyme. J Anim Sci 2007, 85:2982-2993.
• [78]Emiola IA, Opapeju FO, Slominski BA, Nyachoti CM: Growth performance and nutrient digestibility in swine fed wheat distillers dried grains with solubles-based diets supplemented with a multi-carbohydrase enzyme. J Anim Sci 2009, 87:2315-2322.
• [79]Thacker PA: Effect of enzyme supplementation on the performance of growing-finishing pigs fed barley based diets supplemented with soybean meal or canola meal. Asian-Aust J Anim Sci 2001, 14:1008-1013.
• [80]Olukosi OA, Sands JS, Adeola O: Supplementation of carbohydrases or phytase individually or in combination to diets for weanling and growing-finishing pigs. J Anim Sci 2007, 85:1702-1711.
• [81]Jones CK, Bergstrom JR, Tokach MD, DeRouchey JM, Goodband RD, Nelssen JL, Dritz SS: Efficacy of commercial enzymes in diets containing various concentrations and sources of dried distillers grains with solubles for nursery pigs. J Anim Sci 2010, 88:2084-2091.
• [82]Baas TC, Thacker PA: Impact of gastric pH on dietary enzyme activity and survivability in swine fed β-glucanase supplemented diets. Can J Anim Sci 1996, 76:245-252.
• [83]Thacker PA, Baas TC: Effect of gastric pH on the activity of exogenous pentosanase and the effect of pentosanase supplementation of the diet on the performance of growing-finishing pigs. Anim Feed Sci Technol 1996, 63:187-200.
• [84]He J, Yin J, Wang L, Yu B, Chen D: Functional characterization of a recombinant xylanase from Pichia pastoris and effect of the enzyme on nutrient digestibility in weaned pigs. Brit J Nutr 2010, 103:1507-1513.
• [85]Lv JN, Chen YQ, Guo XJ, Piao XS, Cao YH, Dong B: Effects of supplementation of β-mannanase in corn-soybean meal diets on performance and nutrient digestibility in growing pigs. Asian-Aust J Anim Sci 2013, 26:579-587.
• [86]Cai H, Shi P, Luo H, Bai Y, Huang H, Yang P, Yao B: Acidic β-mannanase from penicillium pinophilum C1: cloning, characterization and assessment of its potential for animal feed application. J Biosci Bioeng 2011, 112:551-557.
• [87]Pettey LA, Carter SD, Senne BW, Shriver JA: Effect of beta-mannanase adding to corn-soybean meal diets on growth performance, carcass traits and apparent nutrient digestibility in growing-finishing pigs. J Anim Sci 2002, 80:1012-1019.
• [88]Van Dijk AJ, Everts H, Nabuurs MJA, Margry RJ, Beynen AC: Growth performance of weanling pigs fed spray-dried animal plasma: a review. Livest Prod Sci 2001, 68:263-274.
• [89]Torrallardona D: Spray dried animal plasma as an alternative to antibiotics in weanling pigs: a review. Asian-Aust J Anim Sci 2010, 23:131-148.
• [90]Bontempo V, Di Giancamillo A, Savoini G, Dell’Orto V, Domeneghini C: Live yeast supplementation acts upon intestinal morpho-functional aspects and growth in weanling piglets. Anim Feed Sci Technol 2006, 129:224-236.
• [91]Li JY, Li DF, Gong LM, Ma YX, He YH, Zhai HX: Effects of live yeast on the performance, nutrient digestibility, gastrointestinal microbiota and concentration of volatile fatty acids in weanling pigs. Arch Anim Nutr 2006, 60:277-288.
• [92]Shen YB, Piao XS, Kim SW, Wang L, Liu P, Yoon I, Zhen YG: Effects of yeast culture supplementation on growth performance, intestinal health, and immune response of nursery pigs. J Anim Sci 2009, 87:2614-2624.
• [93]Yan L, Han DL, Meng QW, Lee JH, Park CJ, Kim IH: Effects of anion supplementation on growth performance, nutrient digestibility, meat quality and fecal noxious gas content in growing-finishing pigs. Asian-Aust J Anim Sci 2010, 23:1073-1079.
• [94]Nyachoti CM, Kiarie E, Bhandari SK, Zhang G, Krause DO: Weaned pig responses to Esherichia coli K88 oral challenge when receiving a lysozyme supplement. J Anim Sci 2012, 90:252-260.
• [95]Huguet A, Le Dividich J, Le Huerou-Luron I: Improvement of growth performance and sanitary status of weaned piglets fed a bovine colostrum-supplemented diet. J Anim Sci 2012, 90:1513-1520.
• [96]Wang Y, Shan T, Xu Z, Liu J, Feng J: Effect of lactoferrin on the growth performance, intestinal morphology and expression of PR-39 and protegrin-1 genes in weaned piglets. J Anim Sci 2006, 84:2636-2641.
• [97]Shan T, Wang Y, Liu J, Xu Z: Effect of dietary lactoferrin on the immune functions and serum iron level of weanling piglets. J Anim Sci 2007, 85:2140-2146.
• [98]Garcia-Montoya IA, Cendon TS, Arevalo-Gallegos S, Rascon-Cruz Q: Lactoferrin a multiple bioactive protein: an overview. Biochim Biophys Acta 1820, 2012:226-236.
• [99]Lai CH, Yin JD, Li DF, Zhao LD, Qiao SY, Xing JJ: Conjugated linoleic acid attenuates the production and gene expression of pro-inflammatory cytokines in weaned pigs challenged with lipopolysaccharide. J Nutr 2005, 135:239-244.
• [100]Lai CH, Yin JD, Li DF, Zhao LD, Chen XJ: Effects of dietary conjugated linoleic acid supplementation on the performance and immunological responses of weaned pigs after an escherichia coli lipopolysaccharide challenge. J Anim Vet Adv 2005, 2:299-305.
• [101]Liu P, Piao XS, Thacker PA, Zheng ZK, Wong D, Kim SW: Chito-oligosaccharide reduces diarrhea incidence and attenuates the immune response of weanling pigs challenged with E. coli K88. J Anim Sci 2010, 88:3871-3879.
• [102]Liu P, Piao XS, Kim SW, Li XJ, Wang L, Shen YB, Lee HS, Li SY: Effects of chito-oligosaccharide supplementation on the growth performance, nutrient digestibility, intestinal morphology, and fecal shedding of Escherichia coli and Lactobacilli in weaning pigs. J Anim Sci 2008, 86:2609-2618.
• [103]O’Doherty JV, Dillon S, Figat S, Callan JJ, Sweeney T: The effects of lactose inclusion and seaweed extract derived from Laminaria spp. on performance, digestibility of diet components and microbial populations in newly weaned pigs. Anim Feed Sci Technol 2010, 157:173-180.