Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-08T05:35:43.478Z Has data issue: false hasContentIssue false

Effects of resistant starch on behaviour, satiety-related hormones and metabolites in growing pigs

Published online by Cambridge University Press:  20 May 2014

C. Souza da Silva*
Affiliation:
Adaptation Physiology Group, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands Animal Nutrition Group, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
D. Haenen
Affiliation:
Nutrition, Metabolism and Genomics Group, Division of Human Nutrition, Wageningen University, Bomenweg 2, 6703 HD, Wageningen, The Netherlands
S. J. Koopmans
Affiliation:
Adaptation Physiology Group, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
G. J. E. J. Hooiveld
Affiliation:
Nutrition, Metabolism and Genomics Group, Division of Human Nutrition, Wageningen University, Bomenweg 2, 6703 HD, Wageningen, The Netherlands
G. Bosch
Affiliation:
Animal Nutrition Group, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
J. E. Bolhuis
Affiliation:
Adaptation Physiology Group, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
B. Kemp
Affiliation:
Adaptation Physiology Group, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
M. Müller
Affiliation:
Nutrition, Metabolism and Genomics Group, Division of Human Nutrition, Wageningen University, Bomenweg 2, 6703 HD, Wageningen, The Netherlands
W. J. J. Gerrits
Affiliation:
Animal Nutrition Group, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands
*
Get access

Abstract

Resistant starch (RS) has been suggested to prolong satiety in adult pigs. The present study investigated RS-induced changes in behaviour, satiety-related hormones and metabolites in catheterized growing pigs to explore possible underlying mechanisms for RS-induced satiety. In a cross-over design with two 14-day periods, 10 pigs (initial BW: 58 kg) were assigned to two treatments comprising diets containing either 35% pregelatinized starch (PS) or 34% retrograded starch (RS). Diets were isoenergetic on gross energy. Pigs were fed at 2.8× maintenance. Postprandial plasma response of satiety-related hormones and metabolites was measured at the end of each period using frequent blood sampling. Faecal and urinary energy losses were measured at the end of each period. Behaviour was scored 24 h from video recordings using scan sampling. Energy digestibility and metabolizability were ~6% lower in RS compared with PS diet (P<0.001), and metabolizable energy (ME) intake was ~3% lower in RS-fed than in PS-fed pigs (P<0.001). RS-fed pigs showed less feeder-directed (P=0.001) and drinking (P=0.10) behaviours than PS-fed pigs throughout the day. Postprandial peripheral short-chain fatty acid (SCFA) levels were higher in RS-fed than in PS-fed pigs (P<0.001). Postprandial glucose and insulin responses were lower in RS-fed than in PS-fed pigs (P<0.001). Triglyceride levels were higher in RS-fed than in PS-fed pigs (P<0.01), and non-esterified fatty acid levels did not differ between diets (P=0.90). Glucagon-like peptide-1 (GLP-1) levels were lower in RS-fed than in PS-fed pigs (P<0.001), and peptide tyrosine tyrosine (PYY) levels did not differ between diets (P=0.90). Blood serotonin levels were lower (P<0.001), whereas monoamine oxidase activity (P<0.05) and tryptophan (P<0.01) levels were higher in RS-fed than in PS-fed pigs. Despite a lower ME intake, RS seemed to prolong satiety, based on behavioural observations. Possible underlying mechanisms for RS-induced satiety include increased 24 h plasma SCFA levels, and decreased postprandial glucose and insulin responses. GLP-1 and PYY seemed not to play a role in RS-induced satiety. Low blood serotonin levels in RS-fed pigs suggested a difference in intestinal serotonin release between treatments. Increased postprandial plasma triglyceride levels corresponded with increased SCFA levels, but it is unclear whether triglycerides may have signalled satiety in RS-fed pigs.

Type
Research Article
Copyright
© The Animal Consortium 2014 

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

Bertrand, RL, Senadheera, S, Markus, I, Liu, L, Howitt, L, Chen, H, Murphy, TV, Sandow, SL and Bertrand, PP 2011. A western diet increases serotonin availability in rat small intestine. Endocrinology 152, 3647.CrossRefGoogle ScholarPubMed
Bolhuis, JE, van den Brand, H, Staals, S and Gerrits, WJ 2007. Effects of pregelatinized vs. native potato starch on intestinal weight and stomach lesions of pigs housed in barren pens or on straw bedding. Livestock Science 109, 108110.CrossRefGoogle Scholar
Bolhuis, JE, van den Brand, H, Staals, ST, Zandstra, T, Alferink, SJ, Heetkamp, MJ and Gerrits, WJ 2008. Effects of fermentable starch and straw-enriched housing on energy partitioning of growing pigs. Animal 2, 10281036.CrossRefGoogle ScholarPubMed
Bolhuis, JE, van den Brand, H, Bartels, AC, Oostindjer, M, van den Borne, J, Kemp, B and Gerrits, WJ 2010. Effects of fermentable starch on behaviour of growing pigs in barren or enriched housing. Applied Animal Behaviour Science 123, 7786.CrossRefGoogle Scholar
Bosch, G, Verbrugghe, A, Hesta, M, Holst, JJ, van der Poel, AF, Janssens, GP and Hendriks, WH 2009. The effects of dietary fibre type on satiety-related hormones and voluntary food intake in dogs. British Journal of Nutrition 102, 318325.CrossRefGoogle ScholarPubMed
Centraal Veevoeder Bureau 2007. CVB table pigs. Product Board Animal Feed, The Hague, The Netherlands.Google Scholar
Darzi, J, Frost, GS and Robertson, MD 2011. Postgraduate symposium do SCFA have a role in appetite regulation? Proceedings of the Nutrition Society 70, 119128.CrossRefGoogle Scholar
De Leeuw, JA, Jongbloed, AW, Spoolder, HA and Verstegen, MW 2005. Effects of hindgut fermentation of non-starch polysaccharides on the stability of blood glucose and insulin levels and physical activity in empty sows. Livestock Production Science 96, 165174.CrossRefGoogle Scholar
Delzenne, NM, Neyrinck, AM, Backhed, F and Cani, PD 2011. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nature Reviews Endocrinology 7, 639646.CrossRefGoogle ScholarPubMed
Fernstrom, JD and Wurtman, RJ 1972. Brain serotonin content: physiological regulation by plasma neutral amino acids. Science 178, 414416.CrossRefGoogle ScholarPubMed
Foltin, RW 2001. Effects of amphetamine, dexfenfluramine, diazepam, and other pharmacological and dietary manipulations on food “seeking” and “taking” behavior in non-human primates. Psychopharmacology 158, 2838.CrossRefGoogle ScholarPubMed
Gerrits, WJ, Bosch, MW and van den Borne, JJ 2012. Quantifying resistant starch using novel, in vivo methodology and the energetic utilization of fermented starch in pigs. Journal of Nutrition 142, 238244.CrossRefGoogle ScholarPubMed
Giuberti, G, Gallo, A and Masoero, F 2012. Plasma glucose response and glycemic indices in pigs fed diets differing in in vitro hydrolysis indices. Animal 6, 10681076.CrossRefGoogle ScholarPubMed
Haenen, D, Zhang, J, Souza da Silva, C, Bosch, G, van der Meer, IM, van Arkel, J, van den Borne, JJ, Pérez Gutiérrez, O, Smidt, H, Kemp, B, Müller, M and Hooiveld, GJ 2013. A diet high in resistant starch modulates microbiota composition, SCFA concentrations and gene expression in pig intestine. Journal of Nutrition 143, 274283.CrossRefGoogle ScholarPubMed
Higgins, JA 2004. Resistant starch: metabolic effects and potential health benefits. Journal of AOAC International 87, 761768.CrossRefGoogle ScholarPubMed
Keenan, MJ, Martin, RJ, Raggio, AM, McCutcheon, KL, Brown, IL, Birkett, A, Newman, SS, Skaf, J, Hegsted, M, Tulley, RT, Blair, E and Zhou, JN 2012. High-amylose resistant starch increases hormones and improves structure and function of the gastrointestinal tract: a microarray study. Journal of Nutrigenetics and Nutrigenomics 5, 2644.Google ScholarPubMed
Kemperman, RF, Bruins, S, Te Lintelo, JT, Van der Dijs, FP, Erwich, JJ, Landman, H, Muskiet, FD, Kema, IP and Muskiet, FA 2007. Relation between platelet serotonin and feeding mode in newborns suggests that gut motor activity is a determinant of platelet serotonin content. Biogenic Amines 21, 260272.Google Scholar
Keszthelyi, D, Troost, FJ and Masclee, AA 2009. Understanding the role of tryptophan and serotonin metabolism in gastrointestinal function. Neurogastroenterology & Motility 21, 12391249.CrossRefGoogle ScholarPubMed
Koopmans, SJ, Van Der Meulen, J, Dekker, R, Corbijn, H and Mroz, Z 2006. Diurnal variation in insulin-stimulated systemic glucose and amino acid utilization in pigs fed with identical meals at 12-hour intervals. Hormone and Metabolic Research 38, 607613.CrossRefGoogle ScholarPubMed
Leonhardt, M and Langhans, W 2004. Fatty acid oxidation and control of food intake. Physiology & Behavior 83, 645651.CrossRefGoogle ScholarPubMed
Magalhaes, CP, de Freitas, MF, Nogueira, MI, Campina, RC, Takase, LF, de Souza, SL and de Castro, RM 2010. Modulatory role of serotonin on feeding behavior. Nutritional Neuroscience 13, 246255.CrossRefGoogle ScholarPubMed
Morand, C, Rémésy, C, Levrat, M-A and Demigné, C 1992. Replacement of digestible wheat starch by resistant cornstarch alters splanchnic metabolism in rats. Journal of Nutrition 122, 345354.CrossRefGoogle ScholarPubMed
Näslund, E, Bogefors, J, Skogar, S, Grybäck, P, Jacobsson, H, Holst, JJ and Hellström, PM 1999. GLP-1 slows solid gastric emptying and inhibits insulin, glucagon, and PYY release in humans. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 277, R910R916.CrossRefGoogle ScholarPubMed
O’Hea, EK and Leveille, GA 1969. Significance of adipose tissue and liver as sites of fatty acid synthesis in the pig and the efficiency of utilization of various substrates for lipogenesis. Journal of Nutrition 99, 338344.CrossRefGoogle ScholarPubMed
Onaga, T, Zabielski, R and Kato, S 2002. Multiple regulation of peptide YY secretion in the digestive tract. Peptides 23, 279290.CrossRefGoogle ScholarPubMed
Regmi, PR, van Kempen, T, Matte, JJ and Zijlstra, RT 2011. Starch with high amylose and low in vitro digestibility increases short-chain fatty acid absorption, reduces peak insulin secretion, and modulates incretin secretion in pigs. Journal of Nutrition 141, 398405.CrossRefGoogle ScholarPubMed
Sappok, MA 2012. In vitro fermentation capacity of hindgut microbiota in pigs in relation to dietary fibre. PhD Thesis, Wageningen University, The Netherlands.Google Scholar
Serena, A, Jorgensen, H and Bach Knudsen, KE 2009. Absorption of carbohydrate-derived nutrients in sows as influenced by types and contents of dietary fiber. Journal of Animal Science 87, 136147.CrossRefGoogle ScholarPubMed
Sleeth, ML, Thompson, EL, Ford, HE, Zac-Varghese, SE and Frost, G 2010. Free fatty acid receptor 2 and nutrient sensing: a proposed role for fibre, fermentable carbohydrates and short-chain fatty acids in appetite regulation. Nutrition Research Reviews 23, 135145.CrossRefGoogle ScholarPubMed
Souza da Silva, C, Van den Borne, JJ, Gerrits, WJ, Kemp, B and Bolhuis, JE 2012. Effects of dietary fibers with different physicochemical properties on feeding motivation in adult female pigs. Physiology & Behavior 107, 218230.CrossRefGoogle Scholar
Souza da Silva, C, Bolhuis, JE, Gerrits, WJ, Kemp, B and Van den Borne, JJ 2013. Effects of dietary fibers with different fermentation characteristics on feeding motivation in adult female pigs. Physiology & Behavior 110, 148157.CrossRefGoogle ScholarPubMed
Topping, DL and Clifton, PM 2001. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiological Reviews 81, 10311064.CrossRefGoogle ScholarPubMed
Wanders, AJ, van den Borne, JJ, de Graaf, C, Hulshof, T, Jonathan, MC, Kristensen, M, Mars, M, Schols, HA and Feskens, EJ 2011. Effects of dietary fibre on subjective appetite, energy intake and body weight: a systematic review of randomized controlled trials. Obesity Reviews 12, 724739.CrossRefGoogle ScholarPubMed
Supplementary material: File

Souza da Silva Supplementary Material

Supplementary Material

Download Souza da Silva Supplementary Material(File)
File 34.9 KB