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Effects of prefermented cereals or the end products of fermentation on growth and metabolism of enterocyte-like Caco-2 cells and on intestinal health of restrictedly fed weanling pigs

Published online by Cambridge University Press:  16 September 2009

E. M. A. M. Bruininx ,
J. F. J. G. Koninkx ,
G. P. Binnendijk ,
T. Zandstra ,
M. J. W. Heetkamp ,
C. M. C. van der Peet-Schwering  and
W. J. J. Gerrits
E. M. A. M. Bruininx*
Affiliation:
Animal Nutrition and Adaptation Physiology Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands Department of Nutrition and Feed Research, CCL Research B.V., NCB-laan 52, 5462 GE Veghel, The Netherlands
J. F. J. G. Koninkx
Affiliation:
Faculty of Veterinary Medicine, Department of Pathobiology, Division of Pathology, Utrecht University, PO Box 80.158, 3508 TD Utrecht, The Netherlands
G. P. Binnendijk
Affiliation:
Animal Sciences Group, Wageningen University and Research Centre, PO Box 65, 8200 AB Lelystad, The Netherlands
T. Zandstra
Affiliation:
Animal Nutrition and Adaptation Physiology Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
M. J. W. Heetkamp
Affiliation:
Animal Nutrition and Adaptation Physiology Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
C. M. C. van der Peet-Schwering
Affiliation:
Animal Sciences Group, Wageningen University and Research Centre, PO Box 65, 8200 AB Lelystad, The Netherlands
W. J. J. Gerrits
Affiliation:
Animal Nutrition and Adaptation Physiology Group, Wageningen University, PO Box 338, 6700 AH Wageningen, The Netherlands
*
†E-mail: [email protected]
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Abstract

To unravel the underlying mechanisms that explain the positive effects of prefermented cereals on in vivo gastrointestinal (GI) architecture and function, an in vitro experiment using a human small intestinal epithelial cell model (Caco-2) was performed. A range of dilutions (0% to 10%) of the supernatants of three liquid experimental diets, as well as Na-lactate were used in an in vitro experiment to assess their effect on cellular growth, metabolism, differentiation and mucosal integrity using Caco-2. The experimental diets contained, in addition to a protein rich basal diet (60%), (1) a liquid control diet (C) containing 40% of a mixture of barley and wheat (ratio 3 : 1) or (2) a liquid diet (F) containing 40% prefermented barley and wheat or (3) C with the addition of the fermentation end-products (organic acids and ethanol) in concentrations similar to those in the fermented diet (FP). For F, the mixture of barley and wheat was fermented at 35°C for 48 h. Parallel to the in vitro experiment, 18 groups of eight weanling pigs were assigned to one of the experimental diets during a 14-day in vivo experiment. Each group was fed restrictively. The results of the in vitro experiment showed that the lowest dose of both F- and FP-supernatants had no clear effects on the cell proliferation, but incubation with 5% and 10% of the F- and FP-supernatants decreased the cell numbers at day 19. DNA, RNA, protein and glycoprotein synthesis in differentiated Caco-2 cells were stimulated by incubation with the lower concentrations (0.5% to 2.5%) of F- and FP-supernatants whereas the higher concentrations (5% and 10%) had no effect. Both the F- and FP-supernatants decreased the specific sucrase–isomaltase activity in a dose-dependent manner, but the effects on the specific aminopeptidase activities were less clear. Mucosal integrity initially decreased after incubation with the highest F- and FP-supernatants and started to recover between 24 and 48 h. The results of the in vivo experiment showed no dietary effects (P > 0.1) on GI morphology and brush-border enzyme activities at day 5 or at day 14. Time related changes in GI characteristics followed a normal pattern. In conclusion, the supernatants of diets containing either prefermented cereals or their fermentation end-products clearly modulate cellular growth, metabolism, differentiation and mucosal integrity in an in vitro model, although these effects were not observed in the in vivo characteristics measured in weanling pigs.

Keywords

Caco-cellfermented cerealsintestinepigs
Type
Full Paper
Information
animal , Volume 4 , Issue 1 , January 2010 , pp. 40 - 51
Copyright
Copyright © The Animal Consortium 2009

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References

Alley, MC, Scudiero, DA, Monks, A, Hursey, ML, Czerwinski, MJ, Fine, D, Abbott, BJ, Mayo, JG, Shoemaker, RH, Boyd, MR 1988. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Research 48, 589–601.Google ScholarPubMed
Banan, A, Choudharry, S, Zhang, Y, Fields, JZ, Keshavarzian, A 1999. Ethanol induced barrier dysfunction and it’s prevention by growth factor in human intestinal monolayers: evidence for oxidative and cytoskeletal mechanisms. Journal of Pharmacology and Experimental Therapeutics 291, 1075–1085.Google Scholar
Bruininx, EMAM, Binnnendijk, GP, Van der Peet-Schwering, CMC, Schrama, JW, Den Hartog, LA, Everts, H, Beynen, AC 2002. Effect of creep feed consumption on individual feed intake characteristics and performance of group housed weanling pigs. Journal of Animal Science 80, 1413–1418.CrossRefGoogle ScholarPubMed
Canibe, N, Jensen, BB 2003. Fermented and non-fermented liquid feed to growing pigs: effect on aspects of gastrointestinal ecology and growth performance. Journal of Animal Science 81, 2019–2031.CrossRefGoogle Scholar
Canibe, N, HØjberg, O, Badsberg, JH, Jensen, BB 2007. Effects of feeding fermented liquid feed and fermented grain on gastrointestinal ecology and growth performance. Journal of Animal Science 85, 2959–2971.CrossRefGoogle ScholarPubMed
Hampson, DJ 1986. Alterations in piglet small intestinal structure at weaning. Research in Veterinary Science 40, 32–40.CrossRefGoogle ScholarPubMed
Koninkx, JFJG, Brown, DS, Kok, W, Hendriks, HGCJM, Pusztai, A, Bardocz, S 1996. Polyamine metabolism of enterocyte-like Caco-2 cells after exposure to Phaseolus vulgaris lectin. Gut 38, 47–52.CrossRefGoogle ScholarPubMed
Malago, JJ, Koninkx, JFJG, Douma, PM, Dirkzwager, A, Veldman, A, Hendriks, HGCJM, Van Dijk, JE 2003. Differential modulation of enterocyte-like Caco-2 cells after exposure to short chain fatty acids. Food Additives and Contaminants 20, 427–437.CrossRefGoogle ScholarPubMed
Malago, JJ, Koninkx, JFJG, Tooten, PCJ, Van Liere, EA, Van Dijk, JE 2005. Anti-inflammatory properties of heat shock 70 and butyrate on Salmonella-induced interleukin-8 secretion in enterocyte-like Caco-2 cells. Clinical and Experimental Immunology 141, 62–71.CrossRefGoogle ScholarPubMed
Mariadson, JM, Barkla, DH, Gibson, PR 1997. Effect of short chain-fatty acids on paracellular permeability in Caco-2 intestinal epithelium model. American Journal of Physiology 272, G705–G712.Google Scholar
Mikkelsen, LL, Jensen, BB 1997. Effect of fermented liquid feed (FLF) on growth performance and microbial activity in the gastrointestinal tract of weaned piglets. In Proceedings of the 7th International Symposium on Digestive Physiology in Pigs (ed. JP Laplace, C Fevrier, A Barbeau), pp. 639–642. E.A.A.P. Publication no 88. Saint Malo, France.Google Scholar
Mikkelsen, LL, Jensen, BB 1998. Performance and microbial activity in the gastrointestinal tract of piglets fed fermented liquid feed at weaning. Journal of Animal and Feed Sciences 7, 211–215.CrossRefGoogle Scholar
Maroux, S, Louvard, D, Barratti, J 1973. The aminopeptidase of hog intestinal brush border. Biochimica et Biophysica Acta 321, 282–295.CrossRefGoogle ScholarPubMed
Messer, M, Dahlqvist, A 1966. A one step ultra-micromethod for the assay of intestinal disacharidases. Analytical Biochemistry 14, 376–392.CrossRefGoogle Scholar
Ovelgönne, JH, Koninkx, JFJG, Pusztai, A, Bardocz, S, Kok, W, Ewen, SWB, Hendriks, HGCJM, Van Dijk, JE 2000. Decreased levels of heat shock proteins in gut epithelial cells after exposure to plant lectins. Gut 46, 679–687.CrossRefGoogle ScholarPubMed
Pinto, M, Robine-Leon, S, Appay, MD, Kedinger, M, Triadou, N, Dussaulx, E, Lacroix, B, Simon-Assmann, P, Haffan, K, Fogh, J, Zweibaum, A 1983. Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biology of the Cell 47, 323–330.Google Scholar
Pusztai, A, Koninkx, J, Hendriks, H, Kok, W, Hulscher, S, Van Damme, EJM, Peumans, WJ, Grant, G, Bardocz, S 1996. Effect of the insecticidal Galanthus nivalis agglutinin on metabolism and activities of brush border enzymes in the rat small intestine. Journal of Nutritional Biochemistry 7, 677–682.CrossRefGoogle Scholar
Scholten, RHJ 2001. Fermentation of liquid diets for pigs. PhD Thesis, Wageningen Institute of Animal Science, Department of Animal Nutrition, Wageningen University, Wageningen, The Netherlands.Google Scholar
Scholten, RHJ, Van der Peet-Schwering, CMC, Den Hartog, LA, Balk, M, Schrama, JW, Verstegen, MWA 2002. Fermented wheat in liquid diets: effects on gastroinstestinal characteristics in weanling piglets. Journal of Animal Science 80, 1179–1186.CrossRefGoogle Scholar
Scholten, RHJ, Rijnen, MMJA, Schrama, JW, Boer, H, Van der Peet-Schwering, CMC, Vesseur, PC, Den Hartog, LA, Verstegen, MWA 2001a. Fermentation of liquid co-products and liquid compound diets: 1. Effects on chemical composition during a 6-day storage period. Journal of Animal Physiology and Animal Nutrition 85, 111–123.CrossRefGoogle Scholar
Scholten, RHJ, Rijnen, MMJA, Schrama, JW, Boer, H, Van der Peet-Schwering, CMC, Den Hartog, LA, Vesseur, PC, Verstegen, MWA 2001b. Fermentation of liquid co-products and liquid compound diets: 2. Effects on pH, acid-binding capacity, organic acids and ethanol during a 6-day storage period. Journal of Animal Physiology and Animal Nutrition 85, 124–134.CrossRefGoogle Scholar
Stevens, A 1982. The haematoxylins. Standard haematoxylin and eosin stain for paraffin sections. In Theory and Practice of Histological Techniques (ed. JD Bancroft and A Stevens), pp. 113–114. Churchill Livingstone, Edinburgh; London; Melbourne; New York.Google Scholar
Verdonk, JMAJ, Spreeuwenberg, MAM, Bakker, GCM, Verstegen, MWA 2000. Effect of protein source and feed intake level on histology of the small intestine in newly weaned piglets. In Proceedings of the 8th International Symposium on Digestive Physiology in Pigs (ed. JE Lindberg and B Ogle), pp. 332–334, Uppsala, Sweden.CrossRefGoogle Scholar
Verstegen, MWA, Van der Hel, W, Brandsma, H, Henken, AM, Bransen, AM 1987. The Wageningen respiration unit for animal production research: a description of the equipment and its possibilities. In Energy metabolism in farm animals: effects of housing, stress and disease (ed. MWA Verstegen and AM Henken), pp. 21–48. Martinus Nijhoff Publishers, Dordrecht, The Netherlands.CrossRefGoogle Scholar