Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-27T13:45:50.089Z Has data issue: false hasContentIssue false
  • English
  • Français

Feed intake patterns nor growth rates of pigs are affected by dietary resistant starch, despite marked differences in digestion

Published online by Cambridge University Press:  19 December 2019

R. J. J. van Erp Open the ORCID record for R. J. J. van Erp [Opens in a new window] ,
S. de Vries ,
T. A. T. G. van Kempen ,
L. A. Den Hartog  and
W. J. J. Gerrits
R. J. J. van Erp*
Affiliation:
Department of Research & Development, Trouw Nutrition, Stationsstraat 77, 3800 AGAmersfoort, The Netherlands Animal Nutrition Group, Wageningen University, P.O. Box 338, 6700 AHWageningen, The Netherlands
S. de Vries
Affiliation:
Animal Nutrition Group, Wageningen University, P.O. Box 338, 6700 AHWageningen, The Netherlands
T. A. T. G. van Kempen
Affiliation:
Department of Research & Development, Trouw Nutrition, Stationsstraat 77, 3800 AGAmersfoort, The Netherlands Department of Animal Science, North Carolina State University, Raleigh, NC 27695, USA
L. A. Den Hartog
Affiliation:
Department of Research & Development, Trouw Nutrition, Stationsstraat 77, 3800 AGAmersfoort, The Netherlands Animal Nutrition Group, Wageningen University, P.O. Box 338, 6700 AHWageningen, The Netherlands
W. J. J. Gerrits
Affiliation:
Animal Nutrition Group, Wageningen University, P.O. Box 338, 6700 AHWageningen, The Netherlands
*
†E-mail: rik.van.erp@wur.nl
Get access

Abstract

Current feed evaluation systems often assume that fermented starch (i.e. resistant starch (RS)) yields less energy than digested starch. However, growth rates of pigs fed low and high RS diets are often the same when feed is available ad libitum. This may be explained by its effect on digestive processes changing feeding behavior, and consequently energy utilization. This study aims to investigate the effect of RS on nutrient digestion and digesta passage rate in pigs, in combination with its effect on feeding behavior and growth performance under ad libitum conditions. In experiment 1, 20 male pigs (40 ± 2.82 kg) were fed diets containing either 50% waxy maize starch (low in RS (LRS)) or high-amylose maize starch (high in RS (HRS)), and soluble and insoluble indigestible markers. After 14 days of adaptation to the diets, pigs were fed hourly to reach steady state (6 h), dissected, and digesta were collected from eight segments. From the collected samples, nutrient digestion and passage rate of the solid and liquid digesta fraction were determined. In experiment 2, 288 pigs (80 ± 0.48 kg; sex ratio per pen 1 : 1; boar : gilt) were housed in groups of 6. Pigs were ad libitum-fed one of the experimental diets, and slaughtered at approximately 115 kg. Feed intake, growth and carcass parameters were measured. Ileal starch digestibility was greater for LRS-fed than for HRS-fed pigs (98.0% v. 74.0%; P < 0.001), where the additional undigested starch in HRS-fed pigs was fermented in the large intestine. No effects of RS on digesta passage rate of the solid or liquid digesta fraction and on feeding behavior were observed. Growth rate and feed intake did not differ between diets, whereas feed efficiency of HRS-fed pigs was 1%-unit higher than that of LRS-fed pigs (P = 0.041). The efficiency of feed used for carcass gain did not differ between diets indicating that the difference in feed efficiency was determined by the non-carcass fraction. Despite a 30% greater RS intake (of total starch) with HRS than with LRS, carcass gain and feed efficiency used for carcass gain were unaffected. RS did not affect digesta passage rate nor feeding behavior suggesting that the difference in energy intake between fermented and digested starch is compensated for post-absorptively. Our results indicate that the net energy value of fermented starch currently used in pig feed evaluation systems is underestimated and should be reconsidered.

Keywords

fermented starchdigesta passage ratenet energy valueswinefeeding behavior
Type
Research Article
Information
animal , Volume 14 , Issue 7 , July 2020 , pp. 1402 - 1412
Copyright
© The Animal Consortium 2019

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

Bird, AR, Vuaran, M, Brown, I and Topping, DL 2007. Two high-amylose maize starches with different amounts of resistant starch vary in their effects on fermentation, tissue and digesta mass accretion, and bacterial populations in the large bowel of pigs. British Journal of Nutrition 97, 134–144.10.1017/S0007114507250433CrossRefGoogle ScholarPubMed
Black, J, Williams, B and Gidley, M 2009. Metabolic regulation of feed intake in monogastric mammals. In Voluntary feed intake in pigs (eds. D Torrallardona and E Roura), pp. 189–214. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Blok, MC, Brandsma, G, Bosch, G, Gerrits, WJJ, Jansman, AJM, Fledderus, J and Everts, H 2015. A new Dutch net energy formula for feed and feedstuffs for growing and fattening pigs. Centraal Veevoeder Bureau, Wageningen, The Netherlands.Google Scholar
Bolhuis, JE, van den Brand, H, Bartels, AC, Oostindjer, M, van den Borne, JJ, 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, 77–86.10.1016/j.applanim.2010.01.010CrossRefGoogle Scholar
Bolhuis, JE, Van den Brand, H, Staals, S and Gerrits, W 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, 108–110.10.1016/j.livsci.2007.01.100CrossRefGoogle Scholar
Bolhuis, JE, Van den Brand, H, Staals, STM, Zandstra, T, Alferink, SJJ, Heetkamp, MJW and Gerrits, WJJ 2008. Effects of fermentable starch and straw-enriched housing on energy partitioning of growing pigs. Animal 2, 1028–1036.10.1017/S175173110800222XCrossRefGoogle ScholarPubMed
Brand-Miller, J, Thomas, M, Swan, V, Ahmad, Z, Petocz, P and Colagiuri, S 2003. Physiological validation of the concept of glycemic load in lean young adults. The Journal of Nutrition 133, 2728–2732.10.1093/jn/133.9.2728CrossRefGoogle ScholarPubMed
Brüning, JC, Gautam, D, Burks, DJ, Gillette, J, Schubert, M, Orban, PC, Klein, R, Krone, W, Müller-Wieland, D and Kahn, CR 2000. Role of brain insulin receptor in control of body weight and reproduction. Science 289, 2122–2125.10.1126/science.289.5487.2122CrossRefGoogle ScholarPubMed
Centraal Veevoeder Bureau 2018. CVB table pigs. Centraal Veevoeder Bureau, Wageningen, The Netherlands.Google Scholar
Champ, MM-J 2004. Physiological aspects of resistant starch and in vivo measurements. Journal of AOAC International 87, 749–755.10.1093/jaoac/87.3.749CrossRefGoogle ScholarPubMed
Chan, HT, Leh, CP, Bhat, R, Senan, C, Williams, PA and Karim, AA 2011. Molecular structure, rheological and thermal characteristics of ozone-oxidized starch. Food Chemistry 126, 1019–1024.10.1016/j.foodchem.2010.11.113CrossRefGoogle Scholar
Da Silva, CS, Bosch, G, Bolhuis, J, Stappers, L, van Hees, H, Gerrits, W and Kemp, B 2014a. Effects of alginate and resistant starch on feeding patterns, behaviour and performance in ad libitum-fed growing pigs. Animal 8, 1917–1927.10.1017/S1751731114001840CrossRefGoogle Scholar
Da Silva, CS, Haenen, D, Koopmans, SJ, Hooiveld, GJ, Bosch, G, Bolhuis, JE, Kemp, B, Müller, M and Gerrits, WJ 2014b. Effects of resistant starch on behaviour, satiety-related hormones and metabolites in growing pigs. Animal 8, 1402–1411.10.1017/S1751731114001116CrossRefGoogle Scholar
da Silva, CS, 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 and Behavior 107, 218–230.10.1016/j.physbeh.2012.07.001CrossRefGoogle ScholarPubMed
de Vries, S, Gerrits, WJJ, Kabel, MA, Vasanthan, T and Zijlstra, RT 2016. β-Glucans and resistant starch alter the fermentation of recalcitrant fibers in growing pigs. PloS One 11, e0167624.CrossRefGoogle ScholarPubMed
Doti, S, Suárez-Belloch, J, Latorre, M, Guada, J and Fondevila, M 2014. Effect of dietary starch source on growth performances, digestibility and quality traits of growing pigs. Livestock Science 164, 119–127.10.1016/j.livsci.2014.03.016CrossRefGoogle Scholar
Englyst, HN, Kingman, S and Cummings, J 1992. Classification and measurement of nutritionally important starch fractions. European Journal of Clinical Nutrition 46, S33–50.Google ScholarPubMed
Everts, H 2015. Energy requirement for maintenance in growing pigs, no. 57. Centraal Veevoeder Bureau, Wageningen, The Netherlands.Google Scholar
Fouhse, JM, Gänzle, MG, Regmi, PR, van Kempen, TA and Zijlstra, RT 2015. High amylose starch with low in vitro digestibility stimulates hindgut fermentation and has a bifidogenic effect in weaned pigs. The Journal of Nutrition 145, 2464–2470.10.3945/jn.115.214353CrossRefGoogle Scholar
Galgani, J, Aguirre, C and Díaz, E 2006. Acute effect of meal glycemic index and glycemic load on blood glucose and insulin responses in humans. Nutrition Journal 5, 22.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. The Journal of Nutrition 142, 238–244.10.3945/jn.111.147496CrossRefGoogle ScholarPubMed
Heijnen, M-LA and Beynen, AC 1997. Consumption of retrograded (RS3) but not uncooked (RS2) resistant starch shifts nitrogen excretion from urine to feces in cannulated piglets. The Journal of Nutrition 127, 1828–1832.CrossRefGoogle Scholar
Holdsworth, S 1971. Applicability of rheological models to the interpretation of flow and processing behaviour of fluid food products. Journal of Texture Studies 2, 393–418.10.1111/j.1745-4603.1971.tb00589.xCrossRefGoogle ScholarPubMed
ISO 6496 1999. ISO 6496: Animal feeding stuffs – determination of moisture and other volatile matter content. International Organization for Standardization, Geneva, Switzerland.Google Scholar
ISO 15914 2004. ISO 15914: animal feeding stuffs – determination of total starch content. International Organization for Standardization, Geneva, Switzerland.Google Scholar
ISO 16634-1:2008 2008. ISO 16634-1:2008: Food products – determination of the total nitrogen content by combustion according to the Dumas principle and calculation of the crude protein content – Part 1: Oilseeds and animal feeding stuffs. International Organization for Standardization, Geneva, Switzerland.Google Scholar
Jonathan, MC, Haenen, D, da Silva, CS, Bosch, G, Schols, HA and Gruppen, H 2013. Influence of a diet rich in resistant starch on the degradation of non-starch polysaccharides in the large intestine of pigs. Carbohydrate Polymers 93, 232–239.10.1016/j.carbpol.2012.06.057CrossRefGoogle Scholar
Kidder, D and Manners, M 1980. The level and distribution of carbohydrases in the small intestine mucosa of pigs from 3 weeks of age to maturity. British Journal of Nutrition 43, 141–153.10.1079/BJN19800073CrossRefGoogle Scholar
Kotb, A and Luckey, T 1972. Markers in nutrition. Nutrition Abstracts and Reviews 42, 813–845.Google ScholarPubMed
Lambooij, E, Engel, B, Buist, WG and Vereijken, PFG 2011. Uitsnijden van varkenskarkassen voor het opstellen van een formule om het vleespercentage met de HGP7 (Hennessy Grading Probe), CGM (Capteur Gras/Maigre-Sydel) en de CSB (Image Meater) te schatten = Lean meat equation for the Hennessy Grading Probe (HGP7), Capteur Gras/Maigre-Sydel (CGM and CSB-Image-Meater (CSB)), Wageningen UR Livestock Research, Lelystad, The Netherlands.Google Scholar
Li, T, Dai, QZ, Yin, YL, Zhang, J, Huang, R, Ruan, Z, Deng, Z and Xie, M 2008. Dietary starch sources affect net portal appearance of amino acids and glucose in growing pigs. Animal 2, 723–729.10.1017/S1751731108001614CrossRefGoogle ScholarPubMed
Martens, BM, Gerrits, WJ, Bruininx, EM and Schols, HA 2018. Amylopectin structure and crystallinity explains variation in digestion kinetics of starches across botanic sources in an in vitro pig model. Journal of Animal Science and Biotechnology 9, 91.10.1186/s40104-018-0303-8CrossRefGoogle Scholar
Martin, LJ, Dumon, HJ and Champ, MM 1998. Production of short-chain fatty acids from resistant starch in a pig model. Journal of the Science of Food and Agriculture 77, 71–80.10.1002/(SICI)1097-0010(199805)77:1<71::AID-JSFA3>3.0.CO;2-H3.0.CO;2-H>CrossRefGoogle Scholar
Martínez-Puig, D, Castillo, M, Nofrarias, M, Creus, E and Pérez, JF 2007. Long-term effects on the digestive tract of feeding large amounts of resistant starch: a study in pigs. Journal of the Science of Food and Agriculture 87, 1991–1999.CrossRefGoogle Scholar
Mathers, J, Smith, H and Carter, S 1997. Dose–response effects of raw potato starch on small-intestinal escape, large-bowel fermentation and gut transit time in the rat. British Journal of Nutrition 78, 1015–1029.10.1079/BJN19970215CrossRefGoogle ScholarPubMed
Mohd. Azemi, B and Wootton, M 1984. In vitro digestibility of hydroxypropyl maize, waxy maize and high amylose maize starches. Starch-Stärke 36, 273–275.10.1002/star.19840360805CrossRefGoogle Scholar
Mosenthin, R, Sauer, W, Henkel, H, Ahrens, F and De Lange, C 1992. Tracer studies of urea kinetics in growing pigs: II. The effect of starch infusion at the distal ileum on urea recycling and bacterial nitrogen excretion. Journal of Animal Science 70, 3467–3472.10.2527/1992.70113467xCrossRefGoogle ScholarPubMed
Myers, W, Ludden, P, Nayigihugu, V and Hess, B 2004. A procedure for the preparation and quantitative analysis of samples for titanium dioxide. Journal of Animal Science 82, 179–183.10.2527/2004.821179xCrossRefGoogle ScholarPubMed
Regmi, PR, Metzler-Zebeli, BU, Gänzle, MG, van Kempen, TA and Zijlstra, RT 2011. Starch with high amylose content and low in vitro digestibility increases intestinal nutrient flow and microbial fermentation and selectively promotes bifidobacteria in pigs. The Journal of Nutrition 141, 1273–1280.CrossRefGoogle ScholarPubMed
Saltiel, AR and Kahn, CR 2001. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799.10.1038/414799aCrossRefGoogle ScholarPubMed
Schirra, J and Göke, B 2005. The physiological role of GLP-1 in human: incretin, ileal brake or more? Regulatory Peptides 128, 109–115.10.1016/j.regpep.2004.06.018CrossRefGoogle ScholarPubMed
Schop, M, Jansman, AJ, De Vries, S and Gerrits, WJ 2019. Increasing intake of dietary soluble nutrients affects digesta passage rate in the stomach of growing pigs. British Journal of Nutrition 121, 529–537.10.1017/S0007114518003756CrossRefGoogle Scholar
Schrama, JW and Bakker, GC 1999. Changes in energy metabolism in relation to physical activity due to fermentable carbohydrates in group-housed growing pigs. Journal of Animal Science 77, 3274–3280.CrossRefGoogle ScholarPubMed
Shelat, KJ, Nicholson, T, Flanagan, BM, Zhang, D, Williams, BA and Gidley, MJ 2015. Rheology and microstructure characterisation of small intestinal digesta from pigs fed a red meat-containing Western-style diet. Food Hydrocolloids 44, 300–308.CrossRefGoogle Scholar
Shi, Y-C, Capitani, T, Trzasko, P and Jeffcoat, R 1998. Molecular structure of a low-amylopectin starch and other high-amylose maize starches. Journal of Cereal Science 27, 289–299.10.1006/jcrs.1997.9998CrossRefGoogle Scholar
So, P-W, Yu, W-S, Kuo, Y-T, Wasserfall, C, Goldstone, AP, Bell, JD and Frost, G 2007. Impact of resistant starch on body fat patterning and central appetite regulation. PloS One 2, e1309.10.1371/journal.pone.0001309CrossRefGoogle ScholarPubMed
Solà-Oriol, D, van Kempen, T and Torrallardona, D 2010. Relationships between glycaemic index and digesta passage of cereal-based diets in pigs. Livestock Science 134, 41–43.10.1016/j.livsci.2010.06.091CrossRefGoogle Scholar
Solomon, TPJ, Chambers, ES, Jeukendrup, AE, Toogood, AA and Blannin, AK 2008. The effect of feeding frequency on insulin and ghrelin responses in human subjects. British Journal of Nutrition 100, 810–819.10.1017/S000711450896757XCrossRefGoogle ScholarPubMed
Strubbe, JH and van Dijk, G 2002. The temporal organization of ingestive behaviour and its interaction with regulation of energy balance. Neuroscience and Biobehavioral Reviews 26, 485–498.CrossRefGoogle ScholarPubMed
Sun, T, Lærke, HN, Jørgensen, H and Knudsen, KEB 2006. The effect of extrusion cooking of different starch sources on the in vitro and in vivo digestibility in growing pigs. Animal Feed Science and Technology 131, 67–86.CrossRefGoogle Scholar
Tolkamp, BJ and Kyriazakis, I 1999. To split behaviour into bouts, log-transform the intervals. Animal Behaviour 57, 807–817.CrossRefGoogle ScholarPubMed
van Bussel, W, Kerkhof, F, van Kessel, T, Lamers, H, Nous, D, Verdonk, H, Verhoeven, B, Boer, N and Toonen, H 2010. Accurate determination of titanium as titanium dioxide for limited sample size digestibility studies of feed and food matrices by inductively coupled plasma optical emission spectrometry with real-time simultaneous internal standardization. Atomic Spectroscopy 31, 81–88.Google Scholar
Van der Meulen, J, Bakker, G, Bakker, J, De Visser, H, Jongbloed, A and Everts, H 1997. Effect of resistant starch on net portal-drained viscera flux of glucose, volatile fatty acids, urea, and ammonia in growing pigs. Journal of Animal Science 75, 2697–2704.CrossRefGoogle ScholarPubMed
van Erp, RJ, Kempen, TA, de Vries, S and Gerrits, WJ 2019. Pigs ferment enzymatically digestible starch when it is substituted for resistant starch The Journal of Nutrition.CrossRefGoogle Scholar
van Erp, RJJ, van Hees, HMJ, Zijlstra, RT, van Kempen, TATG, van Klinken, JB and Gerrits, WJJ 2018. Reduced feed intake, rather than increased energy losses, explains variation in growth rates of normal-birth-weight piglets. The Journal of Nutrition 148, 1794–1803.CrossRefGoogle ScholarPubMed
Van Kempen, T, Pujol, S, Tibble, S and Balfagon, A 2007. In vitro characterization of starch digestion and its implications for pigs. In Paradigms in Pig Science (eds. Wiseman, J, Varley, M, Mcorist, S and Kemp, B 2007. In vitro characterization of starch digestion and its implications for pigs. In Paradigms in Pig Science (eds. ), pp. 515–526. Nottingham University Press, Nottingham, UK.Google Scholar
van Kempen, TA, Regmi, PR, Matte, JJ and Zijlstra, RT 2010. In vitro starch digestion kinetics, corrected for estimated gastric emptying, predict portal glucose appearance in pigs. The Journal of Nutrition 140, 1227–1233.CrossRefGoogle ScholarPubMed
Vicari, T, van den Borne, JJGC, Gerrits, WJJ, Zbinden, Y and Blum, JW 2008. Postprandial blood hormone and metabolite concentrations influenced by feeding frequency and feeding level in veal calves. Domestic Animal Endocrinology 34, 74–88.CrossRefGoogle ScholarPubMed
Wilfart, A, Montagne, L, Simmins, H, Noblet, J and van Milgen, J 2007. Digesta transit in different segments of the gastrointestinal tract of pigs as affected by insoluble fibre supplied by wheat bran. British Journal of Nutrition 98, 54–62.10.1017/S0007114507682981CrossRefGoogle ScholarPubMed
Williams, C, David, DJ and Iismaa, O 1962. The determination of chromic oxide in faeces samples by atomic absorption spectrophotometry. The Journal of Agricultural Science 59, 381–385.CrossRefGoogle Scholar
Yin, F, Zhang, Z, Huang, J and Yin, Y 2010. Digestion rate of dietary starch affects systemic circulation of amino acids in weaned pigs. British Journal of Nutrition 103, 1404–1412.10.1017/S0007114509993321CrossRefGoogle ScholarPubMed