Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-30T20:31:15.703Z Has data issue: false hasContentIssue false
  • English
  • Français

Natural alternatives to in-feed antibiotics in pig production: can immunomodulators play a role?

Published online by Cambridge University Press:  13 March 2009

M. Gallois ,
H. J. Rothkötter ,
M. Bailey ,
C. R. Stokes  and
I. P. Oswald
M. Gallois
Affiliation:
INRA, UR66, Laboratoire de Pharmacologie-Toxicologie, Centre de Recherche de Toulouse, BP3 31931, Toulouse cedex 9, France
H. J. Rothkötter
Affiliation:
Institut für Anatomie, Medizinische Fakultaet, Otto-von-Guericke-Universitaet Magdeburg, Leipziger Strasse 44, 39120 Magdeburg, Germany
M. Bailey
Affiliation:
Division of Veterinary Pathology Infection & Immunity, University of Bristol, Langford House, Langford BS40 5DU, UK
C. R. Stokes
Affiliation:
Division of Veterinary Pathology Infection & Immunity, University of Bristol, Langford House, Langford BS40 5DU, UK
I. P. Oswald*
Affiliation:
INRA, UR66, Laboratoire de Pharmacologie-Toxicologie, Centre de Recherche de Toulouse, BP3 31931, Toulouse cedex 9, France
*
E-mail: [email protected]
Get access

Abstract

As a result of the European ban of in-feed growth-promoting antibiotics, new strategies are being developed to increase the resistance to disease in farm animals. In pig production, this is of particular importance during the weaning transition when piglets are subjected to major stressful events, making them highly sensitive to digestive disorders. At this time, the development of both innate and adaptive immunity at the mucosal surface is critical in preventing the potential harmful effects of intestinal pathogenic agents. Strategies aiming at stimulating natural host defences through the use of substances able to modulate immune functions have gained increasing interest in animal research, and different bioactive components a priori sharing those properties have been the subject of in vivo nutritional investigations in pig. Among these, yeast derivates (β-glucans and mannans) are able to interact with immune cells, particularly phagocytic cells. However, studies where they have been fed to pigs have shown inconsistent results, suggesting that their ability to target the sensitive immune cells through the oral route is questionable. The plant extracts, which would benefit from a positive image in the public opinion, have also been tested. However, due to a lack of data on the bioactive components of particular plants and the large diversity of species, it has proved difficult to prepare extracts of equivalent potency and thus, the literature on their influence on pig immunity remains inconclusive. In considering piglet immunity and health benefits, the most promising results to date have been obtained with spray-dried animal plasma, whose positive effects would be provided by specific antibodies and non-specific competition of some plasma components with bacteria for intestinal receptors. The major positive effect of spray-dried animal plasma is in reducing the infiltration of gut-associated lymphoid tissue by immune cells, which is likely to be the result of a decreased colonisation by potentially harmful bacteria. This review also highlights the limitations of some of the published in vivo studies on the immunomodulatory activity of certain feed additives. Among those, the lack of standardisation of extracts and the heterogeneity of piglet-rearing conditions (e.g. exposure to pathogens) are likely the most limiting.

Keywords

pigimmunitydisease sensitivityfeed additiveimmunomodulators
Type
Full Paper
Information
animal , Volume 3 , Issue 12 , December 2009 , pp. 1644 - 1661
Copyright
Copyright © The Animal Consortium 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akerreta, S, Cavero, RY, Lopez, V, Calvo, MI 2007. Analyzing factors that influence the folk use and phytonomy of 18 medicinal plants in Navarra. Journal of Ethnobiology and Ethnomedicine 3, 16–35.CrossRefGoogle ScholarPubMed
Amagase, H, Petesch, BL, Matsuura, H, Kasuga, S, Itakura, Y 2001. Intake of garlic and its bioactive components. Journal of Nutrition 131, 955S–962S.CrossRefGoogle ScholarPubMed
Anadon, A, Martinez-Larranaga, MR 1999. Residues of antimicrobial drugs and feed additives in animal products: regulatory aspects. Livestock Production Science 59, 183–198.CrossRefGoogle Scholar
Bailey, M, Miller, BG, Telemo, E, Stokes, CR, Bourne, FJ 1993. Specific immunological unresponsiveness following active primary responses to proteins in the weaning diet of piglets. International Archives of Allergy and Immunology 101, 266–271.CrossRefGoogle ScholarPubMed
Bailey, M, Miller, BG, Telemo, E, Stokes, CR, Bourne, FJ 1994. Altered immune response to proteins fed after neonatal exposure of piglets to the antigen. International Archives of Allergy and Immunology 103, 183–187.CrossRefGoogle Scholar
Bailey, M, Haverson, K, Stokes, CR 1996. Immunological functions of the intestinal lamina propria. In Advances in swine in biomedical research (ed. M Tumbleson and L Schook), pp. 267–275. Plenum Press, New York, USA.Google Scholar
Bailey, M, Plunkett, F, Clarke, A, Sturgess, D, Haverson, K, Stokes, C 1998. Activation of T cells from the intestinal lamina propria of the pig. Scandinavian Journal of Immunology 48, 177–182.CrossRefGoogle ScholarPubMed
Bailey, M, Plunkett, FJ, Rothkötter, HJ, Vega-Lopez, MA, Haverson, K, Stokes, CR 2001. Regulation of mucosal immune responses in effector sites. Proceedings of the Nutrition Society 60, 427–435.CrossRefGoogle ScholarPubMed
Bailey, M, Haverson, K, Inman, C, Harris, C, Jones, P, Corfield, G, Miller, B, Stokes, C 2005. The influence of environment on development of the mucosal immune system. Veterinary Immunology and Immunopathology 108, 189–198.CrossRefGoogle ScholarPubMed
Barman, NN, Bianchi, AT, Zwart, RJ, Pabst, R, Rothkötter, HJ 1997. Jejunal and ileal Peyer’s patches in pigs differ in their postnatal development. Anatomy and Embryology (Berlin) 195, 41–50.CrossRefGoogle ScholarPubMed
Baumann, H, Gauldie, J 1994. The acute phase response. Immunology Today 15, 74–80.CrossRefGoogle ScholarPubMed
Baydar, H, Sagdic, O, Ozkan, G, Karadogan, T 2004. Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Control 15, 169–172.CrossRefGoogle Scholar
Bienenstock, J, Befus, D, McDermott, M, Mirski, S, Rosenthal, K 1983. Regulation of lymphoblast traffic and localization in mucosal tissues, with emphasis on IgA. Federation Proceedings 42, 3213–3217.Google ScholarPubMed
Bimczok, D, Sowa, EN, Faber-Zuschratter, H, Pabst, R, Rothkötter, HJ 2005. Site-specific expression of CD11b and SIRPalpha (CD172a) on dendritic cells: implications for their migration patterns in the gut immune system. European Journal of Immunology 35, 1418–1427.CrossRefGoogle ScholarPubMed
Bimczok, D, Post, A, Tschernig, T, Rothkötter, HJ 2006. Phenotype and distribution of dendritic cells in the porcine small intestinal and tracheal mucosa and their spatial relationship to epithelial cells. Cell and Tissue Research 325, 461–468.CrossRefGoogle ScholarPubMed
Blum, KS, Pabst, R 2007. Lymphocyte numbers and subsets in the human blood. Do they mirror the situation in all organs? Immunology Letters 108, 45–51.CrossRefGoogle ScholarPubMed
Bohn, JA, BeMiller, JN 1995. (1→3)-β-D-Glucans as biological response modifiers: a review of structure–functional activity relationships. Carbohydrate Polymers 28, 3–14.CrossRefGoogle Scholar
Bosi, P, Casini, L, Finamore, A, Cremokolini, C, Merialdi, G, Trevisi, P, Nobili, F, Mengheri, E 2004. Spray-dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88. Journal of Animal Science 82, 1764–1772.CrossRefGoogle ScholarPubMed
Boudry, C, Buldgen, A, Portetelle, D, Collard, A, Thewis, A, Dehoux, JP 2007. Effects of oral supplementation with bovine colostrum on the immune system of weaned piglets. Research in Veterinary Science 83, 91–101.CrossRefGoogle ScholarPubMed
Bouhet, S, Hourcade, E, Loiseau, N, Fikry, A, Martinez, S, Roselli, M, Galtier, P, Mengheri, E, Oswald, IP 2004. The mycotoxin fumonisin B1 alters the proliferation and the barrier function of porcine intestinal epithelial cells. Toxicological Sciences 77, 165–171.CrossRefGoogle ScholarPubMed
Brown, GD, Gordon, S 2003. Fungal β-glucans and mammalian immunity. Immunity 19, 311–315.CrossRefGoogle ScholarPubMed
Burkey, TE, Dritz, SS, Nietfeld, JC, Johnson, BJ, Minton, JE 2004. Effect of dietary mannanoligosaccharide and sodium chlorate on the growth performance, acute-phase response, and bacterial shedding of weaned pigs challenged with Salmonella enterica serotype Typhimurium. Journal of Animal Science 82, 397–404.CrossRefGoogle ScholarPubMed
Burt, S 2004. Essential oils: their antibacterial properties and potential applications in foods – a review. International Journal of Food Microbiology 94, 223–253.CrossRefGoogle ScholarPubMed
Churchill, M, Chadburn, A, Bilinski, RT, Bertagnolli, MM 2000. Inhibition of intestinal tumors by curcumin is associated with changes in the intestinal immune cell profile. Journal of Surgical Research 89, 169–175.CrossRefGoogle ScholarPubMed
Coffey, RD, Cromwell, GL 1995. The impact of environment and antimicrobial agents on the growth response of early-weaned pigs to spray-dried porcine plasma. Journal of Animal Science 73, 2532–2539.CrossRefGoogle ScholarPubMed
Coffey, RD, Cromwell, GL 2001. Use of spray-dried animal plasma in diets for weanling pigs. Pig News and Information 22, 39N–48N.Google Scholar
Cosentino, S, Tuberoso, CI, Pisano, B, Satta, M, Mascia, V, Arzedi, E, Palmas, F 1999. In-vitro antimicrobial activity and chemical composition of Sardinian Thymus essential oils. Letters in Applied Microbiology 29, 130–135.CrossRefGoogle ScholarPubMed
Cossart, P, Sansonetti, PJ 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242–248.CrossRefGoogle ScholarPubMed
Craig, WJ 1999. Health-promoting properties of common herbs. American Journal of Clinical Nutrition 70, 491S–499S.CrossRefGoogle ScholarPubMed
Cromwell, GL 2002. Why and how antibiotics are used in swine production. Animal Biotechnology 13, 7–27.CrossRefGoogle ScholarPubMed
Cunningham-Rundles, S, Lin, DH 1998. Nutrition and the immune system of the gut. Nutrition 14, 573–579.CrossRefGoogle ScholarPubMed
Davis, ME, Maxwell, CV, Brown, DC, de Rodas, BZ, Johnson, ZB, Kegley, EB, Hellwig, DH, Dvorak, RA 2002. Effect of dietary mannan oligosaccharides and(or) pharmacological additions of copper sulfate on growth performance and immunocompetence of weanling and growing/finishing pigs. Journal of Animal Science 80, 2887–2894.CrossRefGoogle ScholarPubMed
Davis, ME, Maxwell, CV, Erf, GF, Brown, DC, Wistuba, TJ 2004a. Dietary supplementation with phosphorylated mannans improves growth response and modulates immune function of weanling pigs. Journal of Animal Science 82, 1882–1891.CrossRefGoogle ScholarPubMed
Davis, ME, Brown, DC, Maxwell, CV, Johnson, ZB, Kegley, EB, Dvorak, RA 2004b. Effect of phosphorylated mannans and pharmacological additions of zinc oxide on growth and immunocompetence of weanling pigs. Journal of Animal Science 82, 581–587.CrossRefGoogle ScholarPubMed
Decuypere, J, Dierick, N, Boddez, S 1998. The potentials for immunostimulatory substances (β-α1,3/1,6 glucans) in pig nutrition. Journal of Animal and Feed Sciences 7, 259–265.CrossRefGoogle Scholar
Dewey, CE, Cox, BD, Straw, BE, Bush, EJ, Hurd, HS 1997. Associations between off-label feed additives and farm size, veterinary consultant use, and animal age. Preventive Veterinary Medicine 31, 133–146.CrossRefGoogle ScholarPubMed
Dritz, SS, Shi, J, Kielian, TL, Goodband, RD, Nelssen, JL, Tokach, MD, Chengappa, MM, Smith, JE, Blecha, F 1995. Influence of dietary β-glucan on growth performance, nonspecific immunity, and resistance to Streptococcus suis infection in weanling pigs. Journal of Animal Science 73, 3341–3350.CrossRefGoogle ScholarPubMed
Eicher, SD, McKee, CA, Carroll, JA, Pajor, EA 2006. Supplemental vitamin C and yeast cell wall β-glucan as growth enhancers in newborn pigs and as immunomodulators after an endotoxin challenge after weaning. Journal of Animal Science 84, 2352–2360.CrossRefGoogle ScholarPubMed
El-Abasy, M, Motobu, M, Shimura, K, Na, KJ, Kang, CB, Koge, K, Onodera, T, Hirota, Y 2002. Immunostimulating and growth-promoting effects of sugar cane extract (SCE) in chickens. Journal of Veterinary Medical Science 64, 1061–1063.CrossRefGoogle ScholarPubMed
Fleeton, MN, Contractor, N, Leon, F, Wetzel, JD, Dermody, TS, Kelsall, BL 2004. Peyer’s patch dendritic cells process viral antigen from apoptotic epithelial cells in the intestine of reovirus-infected mice. Journal of Experimental Medicine 200, 235–245.CrossRefGoogle ScholarPubMed
Florkowski, WJ, Elnagheeb, AH, Huang, CL 1998. Risk perception and new food production technologies. Applied Economics Letters 5, 69–73.CrossRefGoogle Scholar
Francis, G, Kerem, Z, Makkar, HP, Becker, K 2002. The biological action of saponins in animal systems: a review. British Journal of Nutrition 88, 587–605.CrossRefGoogle ScholarPubMed
Frank, JW, Carroll, JA, Allee, GL, Zannelli, ME 2003. The effects of thermal environment and spray-dried plasma on the acute-phase response of pigs challenged with lipopolysaccharide. Journal of Animal Science 81, 1166–1176.CrossRefGoogle ScholarPubMed
Gaskins, HR, Collier, CT, Anderson, DB 2002. Antibiotics as growth promotants: mode of action. Animal Biotechnology 13, 29–42.CrossRefGoogle ScholarPubMed
Gebert, A, Rothkötter, HJ, Pabst, R 1994. Cytokeratin 18 is an M-cell marker in porcine Peyer’s patches. Cell and Tissue Research 276, 213–221.CrossRefGoogle ScholarPubMed
Gebert, A, Rothkötter, HJ, Pabst, R 1996. M cells in Peyer’s patches of the intestine. International Review of Cytology 167, 91–159.CrossRefGoogle ScholarPubMed
Greiner, LL, Stahly, TS, Stabel, TJ 2001a. The effect of dietary soy genistein on pig growth and viral replication during a viral challenge. Journal of Animal Science 79, 1272–1279.CrossRefGoogle ScholarPubMed
Greiner, LL, Stahly, TS, Stabel, TJ 2001b. The effect of dietary soy daidzein on pig growth and viral replication during a viral challenge. Journal of Animal Science 79, 3113–3119.CrossRefGoogle ScholarPubMed
Hahn, TW, Lohakare, JD, Lee, SL, Moon, WK, Chae, BJ 2006. Effects of supplementation of β-glucans on growth performance, nutrient digestibility, and immunity in weanling pigs. Journal of Animal Science 84, 1422–1428.CrossRefGoogle ScholarPubMed
Hannant, D 2002. Mucosal immunology: overview and potential in the veterinary species. Veterinary Immunology and Immunopathology 87, 265–267.CrossRefGoogle ScholarPubMed
Hansen, JA, Nelssen, JL, Goodband, RD, Weeden, TL 1993. Evaluation of animal protein supplements in diets of early-weaned pigs. Journal of Animal Science 71, 1853–1862.CrossRefGoogle ScholarPubMed
Haverson, K, Bailey, M, Stokes, CR 1999. T-cell populations in the pig intestinal lamina propria: memory cells with unusual phenotypic characteristics. Immunology 96, 66–73.CrossRefGoogle ScholarPubMed
Haverson, K, Singha, S, Stokes, CR, Bailey, M 2000. Professional and non-professional antigen-presenting cells in the porcine small intestine. Immunology 101, 492–500.CrossRefGoogle ScholarPubMed
Hiss, S, Sauerwein, H 2003. Influence of dietary β-glucan on growth performance, lymphocyte proliferation, specific immune response and haptoglobin plasma concentrations in pigs. Journal of Animal Physiology and Animal Nutrition (Berlin) 87, 2–11.CrossRefGoogle ScholarPubMed
Huang, FP, Platt, N, Wykes, M, Major, JR, Powell, TJ, Jenkins, CD, MacPherson, GG 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. Journal of Experimental Medicine 191, 435–444.CrossRefGoogle Scholar
Huguet, A, Le Normand, L, Fauquant, J, Kaeffer, B, Le Huerou-Luron, I 2007. Influence of bovine colostrum on restoration of intestinal mucosa in weaned piglets. Livestock Science 108, 20–22.CrossRefGoogle Scholar
Ilsley, SE, Miller, HM, Kamel, C 2005. Effects of dietary quillaja saponin and curcumin on the performance and immune status of weaned piglets. Journal of Animal Science 83, 82–88.CrossRefGoogle ScholarPubMed
Jiang, R, Chang, X, Stoll, B, Fan, MZ, Arthington, J, Weaver, E, Campbell, J, Burrin, DG 2000. Dietary plasma protein reduces small intestinal growth and lamina propria cell density in early weaned pigs. Journal of Nutrition 130, 21–26.CrossRefGoogle ScholarPubMed
Kansagra, K, Stoll, B, Rognerud, C, Niinikoski, H, Ou, CN, Harvey, R, Burrin, D 2003. Total parenteral nutrition adversely affects gut barrier function in neonatal piglets. American Journal of Physiology: Gastrointestinal and Liver Physiology 285, G1162–G1170.Google ScholarPubMed
Kelly, D, Coutts, AG 2000. Early nutrition and the development of immune function in the neonate. Proceedings of the Nutrition Society 59, 177–185.CrossRefGoogle ScholarPubMed
Kensil, CR, Mo, AX, Truneh, A 2004. Current vaccine adjuvants: an overview of a diverse class. Frontiers in Bioscience 9, 2972–2988.CrossRefGoogle ScholarPubMed
Kim, JD, Marshall, MR, Wei, C 1995. Antibacterial activity of some essential oil components against five foodborne pathogens. Journal of Agricultural and Food Chemistry 43, 2839–2845.CrossRefGoogle Scholar
Kim, JD, Hyun, Y, Sohn, KS, Woo, HJ, Kim, TJ, Han, IK 2000. Effects of immunostimulators on growth performance and immune response in pigs weaned at 21 days of age. Journal of Animal and Feed Sciences 9, 333–346.CrossRefGoogle Scholar
Kogan, G, Kocher, A 2007. Role of yeast cell wall polysaccharides in pig nutrition and health protection. Livestock Science 109, 161–165.CrossRefGoogle Scholar
Koh, WS, Yoon, SY, Kwon, BM, Jeong, TC, Nam, KS, Han, MY 1998. Cinnamaldehyde inhibits lymphocyte proliferation and modulates T-cell differentiation. International Journal of Immunopharmacology 20, 643–660.CrossRefGoogle ScholarPubMed
Kommera, SK, Mateo, RD, Neher, FJ, Kim, SW 2006. Phytobiotics and organic acids as potential alternatives to the use of antibiotics in nursery pig diets. Asian-Australasian Journal of Animal Sciences 19, 1784–1789.CrossRefGoogle Scholar
Lallès, JP, Boudry, G, Favier, C, Le Floc’h, N, Luron, I, Montagne, L, Oswald, IP, Pié, S, Piel, C, Sève, B 2004. Gut function and dysfunction in young pigs: physiology. Animal Research 53, 301–316.CrossRefGoogle Scholar
Lallès, JP, Bosi, P, Smidt, H, Stokes, CR 2007. Nutritional management of gut health in pigs around weaning. Proceedings of the Nutrition Society 66, 260–268.CrossRefGoogle ScholarPubMed
Lee, YC 1988. Mannose-binding proteins of animal origin. Advances in Experimental Medicine and Biology 228, 105–121.CrossRefGoogle ScholarPubMed
Levay, PF, Viljoen, M 1995. Lactoferrin: a general review. Haematologica 80, 252–267.Google ScholarPubMed
Li, J, Xing, J, Li, D, Wang, X, Zhao, L, Lv, S, Huang, D 2005. Effects of β-glucan extracted from Saccharomyces cerevisiae on humoral and cellular immunity in weaned piglets. Archives of Animal Nutrition 59, 303–312.CrossRefGoogle ScholarPubMed
Li, J, Li, DF, Xing, JJ, Cheng, ZB, Lai, CH 2006. Effects of β-glucan extracted from Saccharomyces cerevisiae on growth performance, and immunological and somatotropic responses of pigs challenged with Escherichia coli lipopolysaccharide. Journal of Animal Science 84, 2374–2381.CrossRefGoogle ScholarPubMed
Lien, TF, Horng, YM, Wu, CP 2007. Feasibility of replacing antibiotic feed promoters with the Chinese traditional herbal medicine Bazhen in weaned piglets. Livestock Science 107, 97–102.CrossRefGoogle Scholar
Lizardo, R, Nofrarias, M, Guinvarch, J, Justin, AL, Auclair, E, Brufau, J 2008. Influence de l’incorporation de levures Saccharomyces cerevisiae ou de leurs parois dans l’aliment sur la digestion et les performances zootechniques des porcelets en post-sevrage. In 40èmes Journées de la Recherche Porcine, Paris, France, pp. 183–190.Google Scholar
Lo, DY, Chen, TH, Chien, MS, Koge, K, Hosono, A, Kaminogawa, S, Lee, WC 2005. Effects of sugar cane extract on the modulation of immunity in pigs. Journal of Veterinary Medical Science 67, 591–597.CrossRefGoogle ScholarPubMed
Maass, N, Bauer, J, Paulicks, BR, Bohmer, BM, Roth-Maier, DA 2005. Efficiency of Echinacea purpurea on performance and immune status in pigs. Journal of Animal Physiology and Animal Nutrition (Berlin) 89, 244–252.CrossRefGoogle ScholarPubMed
Macdonald, TT, Monteleone, G 2005. Immunity, inflammation, and allergy in the gut. Science 307, 1920–1925.CrossRefGoogle ScholarPubMed
Macpherson, AJ, Uhr, T 2004. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303, 1662–1665.CrossRefGoogle ScholarPubMed
Manzanilla, EG, Nofrarias, M, Anguita, M, Castillo, M, Perez, JF, Martin-Orue, SM, Kamel, C, Gasa, J 2006. Effects of butyrate, avilamycin, and a plant extract combination on the intestinal equilibrium of early-weaned pigs. Journal of Animal Science 84, 2743–2751.CrossRefGoogle Scholar
Mao, XF, Piao, XS, Lai, CH, Li, DF, Xing, JJ, Shi, BL 2005. Effects of β-glucan obtained from the Chinese herb Astragalus membranaceus and lipopolysaccharide challenge on performance, immunological, adrenal, and somatotropic responses of weanling pigs. Journal of Animal Science 83, 2775–2782.CrossRefGoogle ScholarPubMed
Masihi, KN 2000. Immunomodulatory agents for prophylaxis and therapy of infections. International Journal of Antimicrobial Agents 14, 181–191.CrossRefGoogle ScholarPubMed
Milgate, J, Roberts, DCK 1995. The nutritional & biological significance of saponins. Nutrition Research 15, 1223–1249.CrossRefGoogle Scholar
Muhl, A, Liebert, F 2007. No impact of a phytogenic feed additive on digestion and unspecific immune reaction in piglets. Journal of Animal Physiology and Animal Nutrition (Berlin) 91, 426–431.CrossRefGoogle ScholarPubMed
Neutra, MR, Mantis, NJ, Kraehenbuhl, JP 2001. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nature Immunology 2, 1004–1009.CrossRefGoogle ScholarPubMed
Niedergang, F, Kweon, MN 2005. New trends in antigen uptake in the gut mucosa. Trends in Microbiology 13, 485–490.CrossRefGoogle ScholarPubMed
Niess, JH, Reinecker, HC 2005. Lamina propria dendritic cells in the physiology and pathology of the gastrointestinal tract. Current Opinion in Gastroenterology 21, 687–691.CrossRefGoogle ScholarPubMed
Niewold, TA 2007. The nonantibiotic anti-inflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis. Poultry Science 86, 605–609.CrossRefGoogle ScholarPubMed
Niewold, TA, van Dijk, AJ, Geenen, PL, Roodink, H, Margry, R, van der Meulen, J 2007. Dietary specific antibodies in spray-dried immune plasma prevent enterotoxigenic Escherichia coli F4 (ETEC) post weaning diarrhoea in piglets. Veterinary Microbiology 124, 362–369.CrossRefGoogle ScholarPubMed
Nofrarias, M, Manzanilla, EG, Pujols, J, Gibert, X, Majo, N, Segales, J, Gasa, J 2006. Effects of spray-dried porcine plasma and plant extracts on intestinal morphology and on leukocyte cell subsets of weaned pigs. Journal of Animal Science 84, 2735–2742.CrossRefGoogle ScholarPubMed
Nofrarias, M, Manzanilla, EG, Pujols, J, Gibert, X, Majo, N, Segales, J, Gasa, J 2007. Spray-dried porcine plasma affects intestinal morphology and immune cell subsets of weaned pigs. Livestock Science 108, 299–302.CrossRefGoogle Scholar
Nollet, H, Deprez, P, Van Driessche, E, Muylle, E 1999. Protection of just weaned pigs against infection with F18+Escherichia coli by non-immune plasma powder. Veterinary Microbiology 65, 37–45.CrossRefGoogle ScholarPubMed
Oswald, IP 2006. Role of intestinal epithelial cells in the innate immune defence of the pig intestine. Veterinary Research 37, 359–368.CrossRefGoogle ScholarPubMed
Pakkanen, R, Aalto, J 1997. Growth factors and antimicrobial factors of bovine colostrum. International Dairy Journal 7, 285–297.CrossRefGoogle Scholar
Pié, S, Lallès, JP, Blazy, F, Laffitte, J, Seve, B, Oswald, IP 2004. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. Journal of Nutrition 134, 641–647.Google ScholarPubMed
Pié, S, Awati, A, Vida, S, Falluel, I, Williams, BA, Oswald, IP 2007. Effects of added fermentable carbohydrates in the diet on intestinal proinflammatory cytokine-specific mRNA content in weaning piglets. Journal of Animal Science 85, 673–683.CrossRefGoogle ScholarPubMed
Pierce, JL, Cromwell, GL, Lindemann, MD, Russell, LE, Weaver, EM 2005. Effects of spray-dried animal plasma and immunoglobulins on performance of early weaned pigs. Journal of Animal Science 83, 2876–2885.CrossRefGoogle ScholarPubMed
Pluske, JR, Hampson, DJ, Williams, IH 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215–236.CrossRefGoogle Scholar
Polo, J, Quigley, JD, Russell, LE, Campbell, JM, Pujols, J, Lukert, PD 2005. Efficacy of spray-drying to reduce infectivity of pseudorabies and porcine reproductive and respiratory syndrome (PRRS) viruses and seroconversion in pigs fed diets containing spray-dried animal plasma. Journal of Animal Science 83, 1933–1938.CrossRefGoogle ScholarPubMed
Pugh, DM 2002. The EU precautionary bans of animal feed additive antibiotics. Toxicology Letters 128, 35–44.CrossRefGoogle ScholarPubMed
Regulation (EC) No. 1774/2002, European Parliament and Council 2002. Regulation (EC) No. 1774/2002 of the European Parliament and of the Council of 3 October 2002 laying down health rules concerning animal by-products not intended for human consumption. Official Journal of the European Union L273, 1–95.Google Scholar
Regulation (EC) No. 1831/2003, European Parliament and Council 2003. Regulation (EC) No. 1831/2003 of the European Parliament and of the Council of 22 September 2003 on additives for use in animal nutrition. Official Journal of the European Union L268, 29–43.Google Scholar
Rodriguez-Fragoso, L, Reyes-Esparza, J, Burchiel, SW, Herrera-Ruiz, D, Torres, E 2008. Risks and benefits of commonly used herbal medicines in Mexico. Toxicology and Applied Pharmacology 227, 125–135.CrossRefGoogle ScholarPubMed
Rothkötter, HJ, Pabst, R 1989. Lymphocyte subsets in jejunal and ileal Peyer’s patches of normal and gnotobiotic minipigs. Immunology 67, 103–108.Google ScholarPubMed
Rothkötter, HJ, Ulbrich, H, Pabst, R 1991. The postnatal development of gut lamina propria lymphocytes: number, proliferation, and T and B cell subsets in conventional and germ-free pigs. Pediatric Research 29, 237–242.CrossRefGoogle Scholar
Rothkötter, HJ, Mollhoff, S, Pabst, R 1999a. The influence of age and breeding conditions on the number and proliferation of intraepithelial lymphocytes in pigs. Scandinavian Journal of Immunology 50, 31–38.CrossRefGoogle ScholarPubMed
Rothkötter, HJ, Hriesik, C, Barman, NN, Pabst, R 1999b. B and also T lymphocytes migrate via gut lymph to all lymphoid organs and the gut wall, but only IgA+ cells accumulate in the lamina propria of the intestinal mucosa. European Journal of Immunology 29, 327–333.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Rothkötter, HJ, Sowa, EN, Pabst, R 2005. The pig as a model developmental immunotoxicology. In Developmental immunotoxicology (ed. S Holladay), pp. 103–115. CRC Press, Boca Raton, FL, USA.Google Scholar
Sahin, AA, Ro, JY, el-Naggar, AK, Wilson, PL, Teague, K, Blick, M, Ayala, AG 1991. Tumor proliferative fraction in solid malignant neoplasms. A comparative study of Ki-67 immunostaining and flow cytometric determinations. American Journal of Clinical Pathology 96, 512–519.CrossRefGoogle ScholarPubMed
Sansonetti, PJ 2004. War and peace at mucosal surfaces. Nature Reviews Immunology 4, 953–964.CrossRefGoogle ScholarPubMed
Sauerwein, H, Schmitz, S, Hiss, S 2007. Effects of a dietary application of a yeast cell wall extract on innate and acquired immunity, on oxidative status and growth performance in weanling piglets and on the ileal epithelium in fattened pigs. Journal of Animal Physiology and Animal Nutrition (Berlin) 91, 369–380.CrossRefGoogle ScholarPubMed
Shah, U, Walker, WA 2002. Pathophysiology of intestinal food allergy. Advances in Pediatrics 49, 299–316.Google ScholarPubMed
Shan, T, Wang, Y, Liu, J, Xu, Z 2007. Effect of dietary lactoferrin on the immune functions and serum iron level of weanling piglets. Journal of Animal Science 85, 2140–2146.CrossRefGoogle ScholarPubMed
Singh, B, Bhat, TK, Singh, B 2003. Potential therapeutic applications of some antinutritional plant secondary metabolites. Journal of Agricultural and Food Chemistry 51, 5579–5597.CrossRefGoogle ScholarPubMed
Sohn, KS, Kim, MK, Kim, JD, Han, IK 2000. The role of immunostimulants in monogastric animal and fish – review. Asian-Australasian Journal of Animal Sciences 13, 1178–1187.CrossRefGoogle Scholar
Stein, HH 2002. Experience of feeding pigs without antibiotics: a European perspective. Animal Biotechnology 13, 85–95.CrossRefGoogle ScholarPubMed
Stein, HH, Kil, DY 2006. Reduced use of antibiotic growth promoters in diets fed to weanling pigs: dietary tools, part 2. Animal Biotechnology 17, 217–231.CrossRefGoogle ScholarPubMed
Stockwin, LH, McGonagle, D, Martin, IG, Blair, GE 2000. Dendritic cells: immunological sentinels with a central role in health and disease. Immunology and Cell Biology 78, 91–102.CrossRefGoogle ScholarPubMed
Stokes, CR, Bailey, M, Haverson, K, Harris, C, Jones, P, Inman, C, Pié, S, Oswald, IP, Williams, BA, Akkermans, ADL, Sowa, E, Rothkötter, HJ, Miller, BG 2004. Postnatal development of intestinal immune system in piglets: implications for the process of weaning. Animal Research 53, 325–334.CrossRefGoogle Scholar
Torrallardona, D, Conde, R, Esteve-Garcia, E, Brufau, J 2002. Use of spray dried animal plasma as an alternative to antimicrobial medication in weanling pigs. Animal Feed Science and Technology 99, 119–129.CrossRefGoogle Scholar
Torrallardona, D, Conde, R, Badiola, I, Polo, J 2007. Evaluation of spray dried animal plasma and calcium formate as alternatives to colistin in piglets experimentally infected with Escherichia coli K99. Livestock Science 108, 303–306.CrossRefGoogle Scholar
Touchette, KJ, Carroll, JA, Allee, GL, Matteri, RL, Dyer, CJ, Beausang, LA, Zannelli, ME 2002. Effect of spray-dried plasma and lipopolysaccharide exposure on weaned pigs: I. Effects on the immune axis of weaned pigs. Journal of Animal Science 80, 494–501.CrossRefGoogle ScholarPubMed
Trevisi, P, Merialdi, G, Mazzoni, M, Casini, L, Tittarelli, C, De Filippi, S, Minieri, L, Lalatta-Costerbosa, G, Bosi, P 2007. Effect of dietary addition of thymol on growth, salivary and gastric function, immune response and excretion of Salmonella enterica serovar Typhimurium, in weaning pigs challenged with this microbe strain. Italian Journal of Animal Science 6 suppl. 1, 374–376.CrossRefGoogle Scholar
Turner, JL, Dritz, SS, Higgins, JJ, Minton, JE 2002a. Effects of Ascophyllum nodosum extract on growth performance and immune function of young pigs challenged with Salmonella typhimurium. Journal of Animal Science 80, 1947–1953.CrossRefGoogle ScholarPubMed
Turner, JL, Dritz, SS, Higgins, JJ, Herkelman, KL, Minton, JE 2002b. Effects of a Quillaja saponaria extract on growth performance and immune function of weanling pigs challenged with Salmonella typhimurium. Journal of Animal Science 80, 1939–1946.CrossRefGoogle ScholarPubMed
Tzianabos, AO 2000. Polysaccharide immunomodulators as therapeutic agents: structural aspects and biologic function. Clinical Microbiology Reviews 13, 523–533.CrossRefGoogle ScholarPubMed
van Dijk, AJ, Everts, H, Nabuurs, MJA, Margry, RJCF, Beynen, AC 2001. Growth performance of weanling pigs fed spray-dried animal plasma: a review. Livestock Production Science 68, 263–274.CrossRefGoogle Scholar
van Dijk, AJ, Enthoven, PMM, Van den Hoven, SGC, Van Laarhoven, MMMH, Niewold, TA, Nabuurs, MJA, Beynen, AC 2002. The effect of dietary spray-dried porcine plasma on clinical response in weaned piglets challenged with a pathogenic Escherichia coli. Veterinary Microbiology 84, 207–218.CrossRefGoogle ScholarPubMed
Walter, BM, Bilkei, G 2004. Immunostimulatory effect of dietary oregano etheric oils on lymphocytes from growth-retarded, low-weight growing-finishing pigs and productivity. Tijdschrift Voor Diergeneeskunde 129, 178–181.Google ScholarPubMed
Wang, YZ, Shan, TZ, Xu, ZR, Feng, J, Wang, ZQ 2007. Effects of the lactoferrin (LF) on the growth performance, intestinal microflora and morphology of weanling pigs. Animal Feed Science and Technology 135, 263–272.CrossRefGoogle Scholar
Wenk, C 2003. Herbs and botanicals as feed additives in monogastric animals. Asian-Australasian Journal of Animal Sciences 16, 282–289.CrossRefGoogle Scholar
White, LA, Newman, MC, Cromwell, GL, Lindemann, MD 2002. Brewers dried yeast as a source of mannan oligosaccharides for weanling pigs. Journal of Animal Science 80, 2619–2628.Google ScholarPubMed
Williams, DL 1997. Overview of (1→3)-β-D-glucan immunobiology. Mediators of Inflammation 6, 247–250.CrossRefGoogle Scholar
Windisch, WM, Schedle, K, Plitzner, C, Kroismayr, A 2008. Use of phytogenic products as feed additives for swine and poultry. Journal of Animal Science 86, E140–E148.CrossRefGoogle ScholarPubMed
Woollard, AC, Tatham, KC, Barker, S 2007. The influence of essential oils on the process of wound healing: a review of the current evidence. Journal of Wound Care 16, 255–257.CrossRefGoogle ScholarPubMed
Yi, GF, Carroll, JA, Allee, GL, Gaines, AM, Kendall, DC, Usry, JL, Toride, Y, Izuru, S 2005. Effect of glutamine and spray-dried plasma on growth performance, small intestinal morphology, and immune responses of Escherichia coli K88+-challenged weaned pigs. Journal of Animal Science 83, 634–643.CrossRefGoogle ScholarPubMed
Yoshizawa, Y, Enomoto, A, Todoh, H, Ametani, A, Kaminogawa, S 1993. Activation of murine macrophages by polysaccharide fractions from marine algae (Porphyra yezoensis). Bioscience Biotechnology and Biochemistry 57, 1862–1866.CrossRefGoogle ScholarPubMed
Yuan, SL, Piao, XS, Li, DF, Kim, SW, Lee, HS, Guo, PF 2006. Effects of dietary Astragalus polysaccharide on growth performance and immune function in weaned pigs. Animal Science 62, 501–507.CrossRefGoogle Scholar