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Bile composition, plasma lipids and oxidative hepatic damage induced by calcium supplementation; effects of goat or cow milk consumption

Published online by Cambridge University Press:  07 March 2013

Javier Díaz-Castro*
Affiliation:
Department of Physiology, Faculty of Pharmacy and Institute of Nutrition and Food Technology ‘José Mataix’, University of Granada, 18071 Granada, Spain
María JM Alférez
Affiliation:
Department of Physiology, Faculty of Pharmacy and Institute of Nutrition and Food Technology ‘José Mataix’, University of Granada, 18071 Granada, Spain
Inmaculada López-Aliaga
Affiliation:
Department of Physiology, Faculty of Pharmacy and Institute of Nutrition and Food Technology ‘José Mataix’, University of Granada, 18071 Granada, Spain
Teresa Nestares
Affiliation:
Department of Physiology, Faculty of Pharmacy and Institute of Nutrition and Food Technology ‘José Mataix’, University of Granada, 18071 Granada, Spain
Ana Sánchez-Alcover
Affiliation:
Department of Physiology, Faculty of Pharmacy and Institute of Nutrition and Food Technology ‘José Mataix’, University of Granada, 18071 Granada, Spain
Margarita S Campos
Affiliation:
Department of Physiology, Faculty of Pharmacy and Institute of Nutrition and Food Technology ‘José Mataix’, University of Granada, 18071 Granada, Spain
*
*For correspondence; e-mail: javierdc@ugr.es

Abstract

Calcium-fortified foods, especially milk and dairy products are recommended to be consumed daily for groups in risk of nutritional deficiency, including children, young adults, menopausal women, pregnant women and the elderly, however Ca-supplementation promotes gallstone formation because Ca is a nucleating factor. The objective of the current study was to assess the influence of cow or goat milk-based diets, either normal or Ca-supplemented, on bile composition, biochemical parameters and hepatic antioxidant status. Weanling male rats were randomly divided into six groups, fed standard, goat or cow milk-based diets, either with normal Ca content (5·0 g/kg), or Ca-supplemented (10·0 g/kg), for 2 weeks. Bile cholesterol concentration and output was higher in rats fed goat milk in comparison with those fed with standard and cow-milk-based diet. Ca-supplementation increased lithogenic index with the standard and cow-milk based diets, this change was not observed with the goat milk diet. Activities of plasma transaminases were also lower in the animals fed Ca-supplemented goat milk, in comparison with the other diets assayed. In general, Ca-supplement in the diet led to an increase in the hepatic oxidative damage, with an increase in the activities of all the antioxidant enzymes studied in the standard and cow milk diet, but not with goat milk. The habitual consumption of goat milk has positive effects on the plasma lipid profile, biliary composition and hepatic antioxidant defence. In addition, under our experimental conditions, Ca-supplementation of this type of milk does not increase the lithogenic index, or hepatic oxidative damage.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2013

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References

Aebi, H 1984 Catalase in vitro. Methods in Enzymology 150 121127CrossRefGoogle Scholar
Alférez, MJM, Barrionuevo, M, López-Aliaga, I, Sanz-Sampelayo, MR, Lisbona, F, Robles, JC & Campos, MS 2001 Digestive utilization of goat and cow milk fat in malabsorption syndrome. Journal of Dairy Research 68 451461Google Scholar
Alférez, MJM, López-Aliaga, I, Barrionuevo, M & Campos, MS 2003 Effect of dietary inclusion of goat milk on the bioavailability of zinc and selenium in rats. Journal of Dairy Research 70 181187Google Scholar
Alférez, MJM, López-Aliaga, I, Nestares, T, Díaz-Castro, J, Barrionuevo, M, Ros, PB & Campos, MS 2006 Dietary goat milk improves iron bioavailability in rats with induced nutritional ferropenic anaemia in comparison with cow milk. International Dairy Journal 16 813821Google Scholar
Bergmeyer, HU 1974 Cholesterol and esterified cholesterol. In Methods of Enzymatic Analysis, 2nd edition, pp. 18901893 (Ed Bergmeyer, HU). Weinheim, Basel: Verlag ChemieGoogle Scholar
Bergmeyer, HU, Scheibe, P & Wahlefeld, AW 1978 Optimization of methods for aspartate aminotransferase and alanine aminotransferase. Clinical Chemistry 24 5873CrossRefGoogle ScholarPubMed
Braun, M & Weaver, CM 2006 A call to evaluate the impact of calcium-fortified foods and beverages. Nutrition Today 41 4047CrossRefGoogle Scholar
Bravo, E, Flora, L, Cantafora, A, De Luca, V, Tripodi, M, Avella, M & Botham, KM 1998 The influence of dietary saturated and unsaturated fat on hepatic cholesterol metabolism and the biliary excretion of chylomicron cholesterol in the rat. Biochimica et Biophysica Acta 1390 134148CrossRefGoogle ScholarPubMed
Campos, MS, López-Aliaga, I, Alférez, MJM, Nestares, T & Barrionuevo, M 2003 Effects of goats´ or cows´ milks on nutritive utilization of calcium and phosphorus in rats with intestinal resection. British Journal of Nutrition 90 6167CrossRefGoogle ScholarPubMed
Crapo, JD, McCord, JM & Fridovich, I 1978 Preparation and assay of superoxide dismutases. Methods in Enzymology 53 382393Google Scholar
Deeg, R & Ziegenhorn, J 1983 Kinetic enzymic method for automated determination of total cholesterol in serum. Clinical Chemistry 10 17981802Google Scholar
DeSandro, V, Chevrier, M, Boddaert, A, Melcion, C, Cordier, A & Richiert, L 1991 Comparison of the effects of propylthiouracil, diphenyl hydantoin, phenobarbital and 3 methylcholanthrene on hepatic and renal T4 metabolism and thyroid gland function in rats. Toxicology and Applied Pharmacology 111 263278Google Scholar
Díaz-Castro, J, Alférez, MJM, López-Aliaga, I, Nestares, T & Campos, MS 2009 Effect of calcium-supplemented goat or cow milk on zinc status in rats with nutritional ferropenic anaemia. International Dairy Journal 19 116121CrossRefGoogle Scholar
Díaz-Castro, J, Ramírez, López-Frías, M, Campos, MS, López-Frías, M, Alférez, MJM, Nestares, T, Ortega, E & López-Aliaga, I 2011a Goat milk during iron repletion improves bone turnover impaired by severe iron deficiency. Journal of Dairy Science 94 27522761CrossRefGoogle ScholarPubMed
Díaz-Castro, J, Pérez-Sánchez, LJ, Ramírez, López-Frías, M, López-Aliaga, I, Nestares, T, Alférez, MJ, Ojeda, ML & Campos, MS 2011b Influence of cow or goat milk consumption on antioxidant defence and lipid peroxidation during chronic iron repletion. British Journal of Nutrition 108 18Google Scholar
Ferreira, M, Coxito, PM, Sardao, VA, Palmeira, CM & Oliveira, PJ 2005 Bile acids are toxic for isolated cardiac mitochondria: a possible cause for hepatic-derived cardiomyopathies? Cardiovascular Toxicology 5 6373CrossRefGoogle ScholarPubMed
Flohé, L & Günzler, WA 1984 Assays of glutathione peroxidase. Methods in Enzymology 105 114121Google Scholar
García Unciti, MS 1996 Utilidad terapéutica de los triglicéridos de cadena media (MCT). Dietas cetogénicas en la epilepsia infantil. Nutrición Clínica 16 735Google Scholar
Ghone, RA, Kumbar, KM, Suryakar, AN, Katkam, RV & Joshi, NG 2008 Oxidative stress and disturbance in antioxidant balance in beta thalassemia major. Indian Journal of Clinical Biochemistry 23 337340Google Scholar
Gorinstein, S, Leontowicz, H, Lojek, A, Leontowicz, M, Ciz, M, Krzeminski, R, Gralak, M, Czerwinski, J, Jastrzebski, Z, Trakhtenberg, S, Grigelmo-Miguel, N, Soliva-Fortuny, R & Martin-Belloso, O 2002 Olive oils improve lipid metabolism and increase antioxidant potential in rats fed diets containing cholesterol. Journal of Agricultural and Food Chemistry 50 61026108Google Scholar
Haenlein, GFW 2001 Past, present and future perspectives of small ruminant dairy research. Journal of Dairy Science 84 20972115.CrossRefGoogle ScholarPubMed
Hofmeyr, GJ, Lawrie, TA, Atallah, AN & Duley, L 2011 Calcium supplementation during pregnancy for preventing hypertensive disorders and related problems. Review of fortified food and beverage products. Cochrane Database of Systematic Reviews 2 162Google Scholar
Kabrnová-Hlavatá, K, Hainer, V, Gojová, M, Hlavatý, P, Kopský, V, Nedvídková, J, Kunesová, M, Parízková, J, Wagenknecht, M, Hill, M & Drbohlav, J 2008 Calcium intake and the outcome of short-term weight management. Physiological Research 57 237245Google Scholar
Kenar, L, Karayilanoglu, T, Aydin, A, Serdar, M & Kose Erbil, MK 2008 Protective effects of diets supplemented with omega-3 polyunsaturated fatty acids and calcium against colorectal tumor formation. Digestive Diseases and Sciences 53 21772182CrossRefGoogle ScholarPubMed
Kris-Etherton, PM & Yu, S 1997 Individual fatty acid effects on plasma lipids and lipoproteins: human studies. American Journal of Clinical Nutrition 65 16281644Google Scholar
Kristian, T & Siesjö, KB 1998 Calcium in ischemic cell death. Stroke 29 705718CrossRefGoogle ScholarPubMed
Lafont, H, Lairon, D, Vigne, JL, Chanussot, F, Chabert, C, Portugal, H, Pauli, AM, Crotte, C & Hauton, JC 1985 Effect of wheat bran, pectin and cellulose on the secretion of bile in rats. Journal of Nutrition 115 849855CrossRefGoogle ScholarPubMed
López-Aliaga, I, Alférez, MJM, Nestares, MT, Ros, PB, Barrionuevo, M & Campos, MS 2005 Goat milk feeding causes an increase in biliary secretion of cholesterol and a decrease in plasma cholesterol levels in rats. Journal of Dairy Science 88 10241030CrossRefGoogle Scholar
López-Aliaga, I, Diaz-Castro, J, Nestares, T, Alférez, MJM & Campos, MS 2009 Calcium-supplemented goat milk does not interfere with iron absorption in rats with anaemia induced by dietary iron depletion. Food Chemistry 113 839841Google Scholar
Lowry, OH, Rosenburgh, NJ, Farr, AL & Randall, RJ 1951 Protein measurement with folin phenol reagent. Journal of Biological Chemistry 193 265270CrossRefGoogle ScholarPubMed
Ma, KY, Liang, YT, Chen, JN, Jiang, Y, Kwan, KM, Peng, C, Jiao, R, Zuo, YY, Huang, Y & Chen, ZY 2012 Dietary calcium decreases plasma cholesterol level only in female but not in male hamster fed a high cholesterol diet. Biomedical and Environmental Sciences 25 392398Google Scholar
Menon, VB, Baxmann, AC, Froeder, L, Martini, LA & Heilberg, IP 2009 Effects of calcium supplementation on body weight reduction in overweight calcium stone formers. Urological Research 37 133139Google Scholar
Muller, E, Grace, PA & Pitt, HA 1986 The effect of parenteral nutrition on biliary calcium and bilirrubin. Journal of Surgery Research 40 5562Google Scholar
Ohkawa, H, Ohishi, N & Yagi, K 1979 Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95 351358CrossRefGoogle ScholarPubMed
Powell, RA 1985 Pure calcium carbonate gallstones in a two year old in association with prenatal calcium supplementation. Journal of Pediatric Surgery 20 143144CrossRefGoogle Scholar
Quiles, JL, Huertas, JR, Battino, M, Ramírez-Tortosa, MC, Casinello, M, Mataix, J, Lopez-Frias, M & Mañas, M 2002 The intake of fried virgin olive or sunflower oils differentially induces oxidative stress in rat liver microsomes. British Journal of Nutrition 88 5765Google Scholar
Reeves, PG, Nielsen, FH & Fahey, GC 1993 AIN-93 Purified diets for laboratory rodents: final report of the American Institute of Nutrition and Ad Hoc Writing Committee on the reformulation of the AIN-76A rodent diet. Journal of Nutrition 123 19391951Google Scholar
Sahin, E & Gümüşlü, S 2007 Stress-dependent induction of protein oxidation, lipid peroxidation and anti-oxidants in peripheral tissues of rats: comparison of three stress models (immobilization, cold and immobilization-cold). Clinical and Experimental Pharmacology and Physiology 34 425431Google Scholar
Schwesinger, WH, Kurtin, WE & Johnson, R 1988 Alcohol protects against cholesterol gallstone formation. Surgery 207 641647Google Scholar
Sokol, RJ, Dahl, R, Devereaux, MW, Yerushalmi, B, Kobak, GE & Gumpricht, E 2005 Human hepatic mitochondria generate reactive oxygen species and undergo the permeability transition in response to hydrophobic bile acids. Journal of Pediatric Gastroenterology and Nutrition 41 235243Google Scholar
Stefan, MI, Edelstein, SJ & Le Novere, N 2008 An allosteric model of calmodulin explains differential activation of PP2B and CaMKII. Proceedings of the National Academy of Sciences USA 105 1076810773Google Scholar
Takeyama, M, Itoh, S, Nayasaki, T & Tanimazu, I 1977 A new enzymatic methods for determination of serum choline-containing phospholipids. Clinical Chemical Acta 79 9398Google Scholar
Talalay, P 1960 Enzymatic analysis of steroid hormones. Methods of Biochemical Analysis 8 119143CrossRefGoogle Scholar
Thomas, PJ & Hofmann, AF 1973 A simple calculation of the lithogenic index of bile: expressing biliary lipid composition on rectangular coordinates. Gastroenterology 65 698700Google Scholar
Tolman, KG & Rej, R 1999 Liver function. In Tietz Textbook of Clinical Chemistry, pp. 11251177 (Eds Burti, CA & ER, Ashwood). Philadelphia, PA: W.B. Saunders CompanyGoogle Scholar
Van Der, MR, Lapre, JA, Govers, MJ & Kleibeuker, JH 1997 Mechanisms of the intestinal effects of dietary fats and milk products on colon carcinogenesis. Cancer Letters 114 7583Google Scholar
Van Erpecum, KJ, Van Berge Henegouwen, GP, Stoelwinder, B, Schmidt, YMG & Willekens, FLH 1990 Bile concentration is a key factor for nucleation of cholesterol crystals and cholesterol saturation index in gallbladder bile of gallstone patients. Hepatology 11 16CrossRefGoogle ScholarPubMed
Weaver, CM 2009 Should dairy be recommended as part of a healthy vegetarian diet? American Journal of Clinical Nutrition 89 1634S1637SGoogle Scholar
Yagi, K 1976 A simple fluorometric assay for lipoperoxide in blood plasma. Biochemical Medicine 15 212216Google Scholar