Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-26T11:12:46.872Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of dietary betaine and conjugated linoleic acid on insulin sensitivity, protein and fat metabolism of obese pigs

Published online by Cambridge University Press:  03 January 2012

I. Fernández-Fígares ,
M. Lachica ,
A. Martín ,
R. Nieto ,
L. González-Valero ,
J. M. Rodríguez-López  and
J. F. Aguilera
I. Fernández-Fígares*
Affiliation:
Departamento de Fisiología y Bioquímica de la Nutrición Animal, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Camino del Jueves s/n, 18100 Armilla, Granada, Spain
M. Lachica
Affiliation:
Departamento de Fisiología y Bioquímica de la Nutrición Animal, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Camino del Jueves s/n, 18100 Armilla, Granada, Spain
A. Martín
Affiliation:
Servicio de Anatomía Patológica, Hospital Universitario Virgen de las Nieves, Avda. de las Fuerzas Armadas 2, 18014 Granada, Spain
R. Nieto
Affiliation:
Departamento de Fisiología y Bioquímica de la Nutrición Animal, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Camino del Jueves s/n, 18100 Armilla, Granada, Spain
L. González-Valero
Affiliation:
Departamento de Fisiología y Bioquímica de la Nutrición Animal, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Camino del Jueves s/n, 18100 Armilla, Granada, Spain
J. M. Rodríguez-López
Affiliation:
Departamento de Fisiología y Bioquímica de la Nutrición Animal, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Camino del Jueves s/n, 18100 Armilla, Granada, Spain
J. F. Aguilera
Affiliation:
Departamento de Fisiología y Bioquímica de la Nutrición Animal, Estación Experimental del Zaidín, Spanish National Research Council (CSIC), Camino del Jueves s/n, 18100 Armilla, Granada, Spain
*
†E-mail: ifigares@eez.csic.es
Get access

Abstract

To determine possible mechanisms of action that might explain the nutrient partitioning effect of betaine and conjugated linoleic acid (CLA) in Iberian pigs and to address potential adverse effects, twenty gilts were restrictively fed from 20 to 50 kg BW Control, 0.5% betaine, 1% CLA or 0.5% betaine + 1% CLA diets. Serum hormones and metabolites profile were determined at 30 kg BW and an oral glucose test was performed before slaughter. Pigs were slaughtered at 50 kg BW and livers were obtained for chemical and histological analysis. Decreased serum urea in pigs fed betaine and betaine + CLA diets (11%; P = 0.0001) indicated a more efficient N utilization. The increase in serum triacylglycerol (58% and 28%, respectively; P = 0.0098) indicated that CLA and betaine + CLA could have reduced adipose tissue triacylglycerol synthesis from preformed fatty acids. Serum glucose, low-density lipoprotein (LDL) cholesterol and non-esterified fatty acids were unaffected. CLA and betaine + CLA altered serum lipids profile, although liver of pigs fed CLA diet presented no histopathological changes and triglyceride content was not different from Control pigs. Compared with controls, serum growth hormone decreased (20% to 23%; P = 0.0209) for all treatments. Although serum insulin increased in CLA, and especially in betaine + CLA pigs (28% and 83%; P = 0.0001), indices of insulin resistance were unaffected. In conclusion, CLA, and especially betaine + CLA, induced changes in biochemical parameters and hormones that may partially explain a nutrient partitioning effect in young pigs. Nevertheless, they exhibited weak, although detrimental, effects on blood lipids. Moreover, although livers were chemically and histologically normal, pigs fed CLA diet challenged with a glucose load had higher serum glucose than controls.

Keywords

betaineCLAinsulin sensitivityliver histologypig
Type
Full Paper
Information
animal , Volume 6 , Issue 7 , 28 May 2012 , pp. 1058 - 1067
Copyright
Copyright © The Animal Consortium 2012

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

Ahima, RS, Flier, JS 2000. Leptin. Annual Reviews of Physiology 62, 413–437.CrossRefGoogle ScholarPubMed
Association of Official Analytical Chemists (A OAC) 1990. Official methods of analysis, 15th edition. AOAC, Washington, DC.Google Scholar
Barak, AJ, Beckenhauer, HC, Junnila, M, Tuma, DJ 1993. Dietary betaine promotes generation of hepatic S-adenosylmethionine and protects the liver from ethanol-induced fatty infiltration. Alcoholism, Clinical and Experimental Research 17, 552–555.CrossRefGoogle ScholarPubMed
Barb, CR, Hausmann, GJ, Houseknecht, KL 2001. Biology of leptin in the pig. Domestic Animal Endocrinology 21, 297–317.CrossRefGoogle ScholarPubMed
Barb, CR, Barrett, JB, Kraeling, RR, Rampacek, GB 1999. Role of leptin in modulating neuroendocrine function: a metabolic link between the brain-pituitary and adipose tissue. Reproduction in Domestic Animals 34, 111–125.CrossRefGoogle Scholar
Berg, EP, McFadin, EL, Maddock, KR, Goodwin, RN, Baas, TJ, Keisler, DH 2003. Serum concentrations of leptin in six genetic lines of swine and relationship with growth and carcass characteristics. Journal of Animal Science 81, 167–171.CrossRefGoogle ScholarPubMed
Boletín Oficial del Estado 2005. Real Decreto Español 1201/2005 sobre la protección de los animales utilizados para experimentación y otros fines científicos. Boletín Oficial del Estado 252, 34367–34391.Google Scholar
Bontempo, V, Sciannimanico, D, Pastorelli, G, Rossi, R, Rosi, F, Corino, C 2004. Dietary conjugated linoleic acid positively affects immunological variables in lactating sows and piglets. Journal of Nutrition 134, 817–824.CrossRefGoogle ScholarPubMed
Bremer, J, Osmundsen, H 1984. Fatty acid oxidation and its regulation. In Fatty acid metabolism and its regulation (ed. S Numa), pp. 113–153. Elsevier Science Publishers, Amsterdam, The Netherlands.CrossRefGoogle Scholar
Brook, CG, Hindmarsh, PC, Stanhope, R 1988. Growth and growth hormone secretion. Journal of Endocrinology 119, 179–184.CrossRefGoogle ScholarPubMed
Ceddia, RB 2005. Direct metabolic regulation in skeletal muscle and fat tissue by leptin: implications for glucose and fatty acids homeostasis. International Journal of Obesity 29, 1175–1183.CrossRefGoogle ScholarPubMed
Clément, L, Poirier, H, Niot, I, Bocher, V, Guerre-Millo, M, Krief, S, Staels, B, Besnard, P 2002. Dietary trans-10,cis-12 conjugated linoleic acid induces hyperinsulinemia and fatty liver in the mouse. Journal of Lipid Research 43, 1400–1409.CrossRefGoogle ScholarPubMed
Coma, J, Carrion, D, Zimmerman, DR 1995. Use of plasma urea nitrogen as a rapid response criterion to determine the lysine requirement of pigs. Journal of Animal Science 73, 472–481.CrossRefGoogle ScholarPubMed
Conde-Aguilera, JA, Lachica, M, Nieto, R, Fernández-Fígares, I 2011. Metabolic regulation of fatty acid esterification and effects of CLA on glucose homeostasis in pig hepatocytes. Animal, In press. doi:10.1017/S1751731111001613.Google Scholar
Davis, TA, Suryawan, A, Orellana, RA, Fiorotto, ML, Burrin, DG 2010. Amino acids and insulin are regulators of muscle protein synthesis in neonatal pigs. Animal 4, 1790–1796.CrossRefGoogle ScholarPubMed
Delany, JP, Blohm, F, Truett, AA, Scimeca, JA, West, DB 1999. Conjugated linoleic acid rapidly reduces body fat content in mice without affecting energy intake. American Journal of Physiology 276, 1172–1179.Google ScholarPubMed
Dugan, MER, Aalhus, JL, Schaefer, AL, Kramer, JKG 1997. The effect of conjugated linoleic acid on fat to lean repartitioning and feed conversion in pigs. Canadian Journal of Animal Science 77, 723–725.CrossRefGoogle Scholar
Duncan, DB 1955. Multiple range and multiple F-test. Biometrics 11, 1–42.CrossRefGoogle Scholar
Dunshea, FR, Harris, DM, Bauman, DE, Boyd, RD, Bell, AW 1992. Effect of porcine somatotropin on in vivo glucose kinetics and lipogenesis in the growing pig. Journal of Animal Science 70, 141–151.CrossRefGoogle Scholar
Dunshea, FR, D'Souza, DN, Pethick, DW, Harper, GS, Warner, RD 2005. Effects of dietary factors and other metabolic modifiers on quality and nutritional value of meat. Meat Science 71, 8–38.CrossRefGoogle ScholarPubMed
Fernández-Fígares, I, Lachica, M, Nieto, R, Rivera-Ferre, M, Aguilera, JF 2007. Serum profile of metabolites and hormones in obese (Iberian) and lean (Landrace) growing gilts fed balanced or lysine deficient diets. Livestock Science 110, 73–81.CrossRefGoogle Scholar
Fernández-Fígares, I, Conde-Aguilera, JA, Nieto, R, Lachica, M, Aguilera, JF 2008. Synergistic effects of betaine and conjugated linoleic acid on growth and carcass composition of growing Iberian pigs. Journal of Animal Science 86, 102–111.CrossRefGoogle ScholarPubMed
Fernández-Fígares, I, Wray-Cahen, D, Steele, NC, Campbell, RG, Hall, DD, Virtanen, E, Caperna, TJ 2002. Effect of dietary betaine on energy utilization and partitioning in the young growing feed restricted pig. Journal of Animal Science 80, 421–428.CrossRefGoogle Scholar
Florini, JR, Ewton, DZ, Coolican, SA 1996. Growth hormone and the insulin-like growth factor system in myogenesis. Endocrine Reviews 17, 481–517.Google ScholarPubMed
Garlick, PJ, Grant, I 1988. Amino acid infusion increases the sensitivity of muscle protein synthesis in vivo to insulin. Effect of branched-chain amino acids. Biochemical Journal 254, 579–584.CrossRefGoogle ScholarPubMed
Huang, QC, Xu, ZR, Han, XY, Lia, WF 2006. Changes in hormones, growth factor and lipid metabolism in finishing pigs fed betaine. Livestock Science 105, 78–85.CrossRefGoogle Scholar
Huang, QC, Xu, ZR, Han, XY, Li, WF 2007. Effect of betaine on growth hormone pulsatile secretion and serum metabolites in finishing pigs. Journal of Animal Physiology and Animal Nutrition 91, 85–90.CrossRefGoogle ScholarPubMed
Kang, K, Pariza, MW 2002. Trans-10, cis-12 conjugated linoleic acid reduces leptin secretion from 3T3-L1 adipocytes. Biochemical and Biophysical Research Communications 287, 377–382.CrossRefGoogle Scholar
Katz, A, Nambi, SS, Mather, K, Baron, AD, Follmann, DA, Sullivan, G, Quon, MJ 2000. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. Journal of Clinical Endocrinology and Metabolism 85, 2402–2410.CrossRefGoogle ScholarPubMed
Kersten, S 2001. Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Reports 2, 282–286.CrossRefGoogle ScholarPubMed
Kidd, MT, Ferket, PR, Garlich, JD 1997. Nutritional and osmoregulatory functions of betaine. World's Poultry Science Journal 53, 125–139.CrossRefGoogle Scholar
Kinosian, B, Glick, H, Garland, G 1994. Cholesterol and coronary heart disease: predicting risks by levels and ratios. Annals of Internal Medicine 121, 641–647.CrossRefGoogle ScholarPubMed
Kostogrys, RB, Pisulewski, PM 2010. Effect of conjugated linoleic acid (CLA) on lipid profile and liver histology in laboratory rats fed high-fructose diet. Environmental Toxicology and Pharmacology 30, 245–250.CrossRefGoogle ScholarPubMed
Larsen, TM, Toubro, S, Astrup, A 2003. Efficacy and safety of dietary supplements containing CLA for the treatment of obesity: evidence from animal and human studies. Journal of Lipid Research 44, 2234–2241.CrossRefGoogle ScholarPubMed
Li, Y, Seifert, MF, Ney, DM, Grahn, M, Grant, AL, Allen, KG, Watkins, BA 1999. Dietary conjugated linoleic acids alter serum IGF-I and IGF binding protein concentrations and reduce bone formation in rats fed (n-6) or (n-3) fatty acids. Journal of Bone Mineral Research 14, 1153–1162.CrossRefGoogle ScholarPubMed
Louveau, I, Gondret, F 2004. Regulation of development and metabolism of adipose tissue by growth hormone and the insulin-like growth factor system. Domestic Animal Endocrinology 27, 241–255.CrossRefGoogle ScholarPubMed
Martins, JM, Neves, JA, Freitas, A, Tirapicos, JL 2010. Betaine supplementation affects the cholesterol but not the lipid profile of pigs. European Journal of Lipid Science and Technology 112, 295–303.CrossRefGoogle Scholar
Matthews, JO, Southern, LL, Pontif, JE, Higbie, AD, Bidner, TD 1998. Interactive effects of betaine, crude protein, and net energy in finishing pigs. Journal of Animal Science 76, 2444–2455.CrossRefGoogle ScholarPubMed
Matthews, JO, Southern, LL, Higbie, AD, Persica, MA, Bidner, TD 2001. Effects of betaine on growth, carcass characteristics, pork quality, and plasma metabolites of finishing pigs. Journal of Animal Science 79, 722–728.CrossRefGoogle ScholarPubMed
Matthews, DR, Hosker, JP, Rudenki, AS, Naylor, BA, Treacher, DF, Turner, RC 1985. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419.CrossRefGoogle ScholarPubMed
Medina, EA, Horn, WF, Keim, NL, Havel, PJ, Benito, P, Kelley, DS, Nelson, GJ, Erickson, KL 2000. Conjugated linoleic acid supplementation in humans: effects on circulating leptin concentrations and appetite. Lipids 35, 783–788.CrossRefGoogle ScholarPubMed
Mitchell, AD, Pursel, VG, Elsasser, TH, Mcmurtry, JP, Bee, G 2005. Effects of dietary conjugated linoleic acid on growth and body composition of control and IGF-I transgenic pigs. Animal Research 54, 395–411.CrossRefGoogle Scholar
Nagao, K, Inoue, N, Wang, YM, Shirouchi, B, Yanagita, T 2005. Dietary conjugated linoleic acid alleviates nonalcoholic fatty liver disease in Zucker (fa/fa) rats. Journal of Nutrition 135, 9–13.CrossRefGoogle ScholarPubMed
Nieto, R, Miranda, A, García, MA, Aguilera, JF 2002. The effect of dietary protein content and feeding level on the rate of protein deposition and energy utilization in growing Iberian pigs from 15 to 50 kg body weight. British Journal of Nutrition 88, 39–49.CrossRefGoogle ScholarPubMed
Nieto, R, Lara, L, García, MA, Gómez, F, Zalvide, M, Cruz, M, Pariente, JM, Moreno, A, Aguilera, JF 2001. Evaluation of an integrated feeding system in the Iberian pig. Study of food consumption and productive parameters. Solo Cerdo Iberico 6, 57–69.Google Scholar
National Research Council (NRC) 1998. Nutrient requirements of swine, 10th edition. National Academy Press, Washington, DC.Google Scholar
Ostrowska, E, Muralitharan, M, Cross, RF, Baumann, DE, Dunshea, FR 1999. Dietary conjugated linoleic acids increase lean tissue and decrease fat deposition in growing pigs. Journal of Nutrition 129, 2037–2042.CrossRefGoogle ScholarPubMed
Ostrowska, E, Cross, RF, Muralitharan, M, Bauman, DE, Dunshea, FR 2002. Effects of dietary fat and conjugated linoleic acid on plasma metabolite concentrations and metabolic responses to homeostatic signals in pigs. British Journal of Nutrition 88, 625–634.CrossRefGoogle ScholarPubMed
Ostrowska, E, Suster, D, Muralitharan, M, Cross, RF, Leury, BJ, Bauman, DE, Dunshea, FR 2003. Conjugated linoleic acid decreases fat accretion in pigs: evaluation by dual-energy X-ray absorptiometry. British Journal of Nutrition 89, 219–229.CrossRefGoogle ScholarPubMed
Øverland, M, Rørvik, KA, Skrede, A 1999. Effect of trimethylamine oxide and betaine in swine diets on growth performance, carcass characteristics, nutrient digestibility, and sensory quality of pork. Journal of Animal Science 77, 2143–2153.CrossRefGoogle ScholarPubMed
Park, Y, Albright, KJ, Liu, W, Storkson, JM, Cook, ME, Pariza, MW 1997. Effect of conjugated linoleic acid on body composition in mice. Lipids 32, 853–858.CrossRefGoogle ScholarPubMed
Petronini, PG, de Angelis, EM, Borghetti, P, Borghetti, AF, Wheelers, KP 1992. Modulation by betaine of cellular responses to osmotic stress. Biochemical Journal 282, 69–73.CrossRefGoogle ScholarPubMed
Purushotham, A, Shrode, GE, Wendel, AA, Liu, LF, Belury, MA 2007. Conjugated linoleic acid does not reduce body fat but decreases hepatic steatosis in adult Wistar rats. Journal of Nutritional Biochemistry 18, 676–684.CrossRefGoogle Scholar
Ramsay, TG, Evock-Clover, CM, Steele, NC, Azain, MJ 2001. Dietary conjugated linoleic acid alters fatty acid composition of pig skeletal muscle and fat. Journal of Animal Science 79, 2152–2161.CrossRefGoogle ScholarPubMed
Stangl, GI, Muller, H, Kirchgessner, M 1999. Conjugated linoleum acid effects on circulating hormones, metabolites and lipoproteins, and its proportion in fasting serum and erythrocyte membranes of swine. European Journal of Nutrition 38, 271–277.CrossRefGoogle Scholar
Steinberg, GR, Dyck, DJ 2000. Development of leptin resistance in rat soleus muscle in response to high-fat diets. American Journal of Physiology Endocrinology and Metabolism 279, 1374–1382.CrossRefGoogle ScholarPubMed
Suster, D, Leury, BJ, King, RH, Mottram, M, Dunshea, FR 2004. Interrelationships between porcine somatotropin (pST), betaine and energy level on body composition and tissue distribution of finisher boars. Australian Journal of Agricultural Research 55, 983–990.CrossRefGoogle Scholar
Tesseraud, S, Métayer, S, Duchêne, S, Bigot, K, Grizard, J, Dupont, J 2007. Regulation of protein metabolism by insulin: value of different approaches and animal models. Domestic Animal Endocrinology 33, 123–142.CrossRefGoogle ScholarPubMed
Thiel-Cooper, RL, Parrish, JRFC, Sparks, JC, Wiegand, BR, Ewan, RC 2001. Conjugated linoleic acid changes swine performance and carcass composition. Journal of Animal Science 79, 1821–1828.CrossRefGoogle ScholarPubMed
Tischendorf, F, Möckel, P, Schöne, F, Plonné, M, Jahreis, G 2002. Effect of dietary conjugated linoleic acids on the distribution of fatty acids in serum lipoprotein fractions and different tissues of growing pigs. Journal of Animal Physiology and Animal Nutrition 86, 313–325.CrossRefGoogle ScholarPubMed
Tsuboyama-Kasaoka, N, Miyazaki, H, Kasaoka, S, Ezaki, O 2003. Increasing the amount of fat in a conjugated linoleic acid-supplemented diet reduces lipodystrophy in mice. Journal of Nutrition 133, 1793–1799.CrossRefGoogle Scholar
Tsuboyama-Kasaoka, N, Takahashi, M, Tanemura, K, Kim, HJ, Tange, T, Okuyama, H, Kasai, M, Ikemoto, S, Ezaki, O 2000. Conjugated linoleic acid supplementation reduces adipose tissue by apoptosis and develops lipodystrophy in mice. Diabetes 49, 1534–1542.CrossRefGoogle ScholarPubMed
Turpin, G 1985. A double blind study of the effectiveness of Beaufor betaine citrate ampoules in the treatment of type IV hyperlipidaemias. Semaine des Hopitaux 61, 2429–2433.Google Scholar
Wang, YM, Nagao, K, Inoue, N, Ujino, Y, Shimada, Y, Nagao, T, Iwata, T, Kamegai, T, Yamauchi-Sato, Y, Yanagita, T 2006. Isomer-specific anti-obese and hypolipidemic properties of conjugated linoleic acid in obese OLETF rats. Bioscience, Biotechnology and Biochemistry 70, 355–362.CrossRefGoogle ScholarPubMed
Wray-Cahen, D, Fernández-Fígares, I, Virtanen, E, Steele, NC, Caperna, TJ 2004. Betaine improves growth, but does not induce whole body or hepatic palmitate oxidation in swine (Sus scrofa domestica). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 137, 131–140.CrossRefGoogle ScholarPubMed
Yamasaki, M, Mansho, K, Mishima, H, Kimura, G, Sasaki, M, Kasai, M, Tachibana, H, Yamada, K 2000a. Effect of dietary conjugated linoleic acid on lipid peroxidation and histological change in rat liver tissues. Journal of Agricultural and Food Chemistry 48, 6367–6371.CrossRefGoogle ScholarPubMed
Yamasaki, M, Mansho, K, Ogino, Y, Kasai, M, Tachibana, H, Yamada, K 2000b. Acute reduction of serum leptin level by dietary conjugated linoleic acid in Sprague-Dawley rats. Journal of Nutritional Biochemistry 11, 467–471.CrossRefGoogle ScholarPubMed