Abstract
Speciation is important for good bioavailability of calcium from food and beverages. Effective calcium enrichment of dairy products for prevention of osteoporosis accordingly depends on the calcium compound added. Calcium d-lactobionate (50, 30 or 3 mM) was added to reconstituted skim milk with pH adjusted to 6.6, 6.0, 5.7 and 5.4 at 25 °C in order to investigate the distribution of calcium and phosphorus between micellar and serum phase and the speciation of calcium in the serum phase for enriched milk. The calcium from added calcium d-lactobionate was found to distribute between the micellar and serum phase at pH 6.6–6.0, while at pH 5.7–5.4, the added calcium remained in the serum phase. The concentration of phosphorus after enrichment was increased in the micellar phase and decreased in the serum phase at pH 6.6–6.0, while at pH 5.7–5.4, phosphorus remained constant in both phases. A decrease of total protein content and caseins in milk serum phase was observed after milk enrichment at all pH values as documented by protein determination and sodium dodecyl sulphate polyacrylamide gel electrophoresis (SDS-PAGE). Moreover, concentration of α-lactalbumin remained unchanged, while concentration of β-lactoglobulin decreased after addition of calcium d-lactobionate at all investigated pH values. Bioavailability of calcium from enriched dairy products depends on transfer to the micelles, and pH control is accordingly concluded to be critical for the use of calcium d-lactobionate for enrichment. The pH value needs to be taken into account when new calcium-enriched dairy products are designed to fulfil the primary role of having a product with high nutritional value and good calcium bioavailability.
Similar content being viewed by others
References
Augustin MA, Clarke PT (1990) Effects of added salts on the heat-stability of recombined concentrated milk. J Dairy Res 57:213–226
Bringe NA, Kinsella JE (1991) Effects of cations and anions on the rate of the acidic coagulation of casein micelles: the possible roles of different forces. J Dairy Res 58:195–209
Bugg CE, Cook WJ (1972) Calcium ion binding to uncharged sugars: crystal structures of calcium bromide complexes of lactose, galactose, and inositol. J Chem Soc Chem Commun: 727–729
Canabady-Rochelle LS, Sanchez C, Mellema M, Bot A, Desobry S, Banon S (2007) Influence of calcium salt supplementation on calcium equilibrium in skim milk during pH cycle. J Dairy Sci 90:2155–2162
Corredig M, Dalgleish DG (1996) Effect of temperature and pH on the interactions of whey proteins with casein micelles in skim milk. Food Res Int 29:49–55
Dalgleish DG (1992) In: Fox PF (ed) Advanced dairy chemistry 1: proteins. London, Elsevier
Dalgleish DG, Law AJR (1988) pH-induced dissociation of bovine casein micelles. 1. Analysis of liberated caseins. J Dairy Res 55:529–538
Famelart MH, Le Graet Y, Raulot K (1999) Casein micelle dispersions into water, NaCl and CaCl2: physicochemical characteristics of micelles and rennet coagulation. Int Dairy J 9:293–297
Gaucheron F (2005) The minerals of milk. Reprod Nutr Dev 45:473–483
Gerstner G (2002) Dairy products: the calcium challenge. Int Food Ing 3:45–48
Gueguen L, Pointillart A (2000) The bioavailability of dietary calcium. J Am Coll Nutr 19:119S–136S
Gutierrez LF, Hamoudi S, Belkacemi K (2012) Lactobionic acid: a high value-added lactose derivative for food and pharmaceutical applications. Int Dairy J 26:103–111
Harvey N, Dennison E, Cooper C (2008) In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism, 7th edn. American Society for Bone and Mineral Research, Washington, DC
Heaney RP (2000) Calcium, dairy products, and osteoporosis. J Am Coll Nutr 19(Suppl):83S–99S
Hill AR (1989) The beta-lactoglobulin-kappa-casein complex. Can Inst Food Sci Technol J 22:120–123
Hinz K, Huppertz T, Kelly AL (2012) Susceptibility of the individual caseins in reconstituted skim milk to cross-linking by transglutaminase: influence of temperature, pH and mineral equilibria. J Dairy Res 79:414–421
IDF (2006) Milk. Determination of total phosphorus content. Method using molecular absorption spectroscopy. IDF Standard 42, Brussels, Belgium: Int Dairy Federation
IDF (2007) Milk and milk products. Determination of calcium, sodium, potassium and magnesium contents. Atomic absorption spectrometric method. IDF Standard 119, Brussels, Belgium: Int Dairy Federation
Koutina G, Knudsen JC, Andersen U, Skibsted LH (2014) Temperature effect on calcium and phosphorus equilibria in relation to gel formation during acidification of skim milk. Int Dairy J 36:65–73
Kruger NJ (1991). In: Walker JM (ed) Methods in molecular biology, vol 32. Basic protein and peptide protocols. Humana Press Inc, Totowa, NJ, USA
Le Ray C, Maubois JL, Gaucheron F, Brule G, Pronnier P, Garnier F (1998) Heat stability of reconstituted casein micelle dispersions: changes induced by salt addition. Lait 78:375–390
Lucey JA, Singh H (1997) Formation and physical properties of acid milk gels: a review. Food Res Int 30:529–542
McCarron DA, Heaney RP (2004) Estimated healthcare savings associated with adequate dairy food intake. Am J Hypertens 17:88–97
McMahon DJ, Brown RJ, Richardson GH, Ernstrom CA (1984) Effects of calcium, phosphate, and bulk culture media on milk coagulation properties. J Dairy Sci 67:930–938
Mekmene O, Le Graet Y, Gaucheron F (2010) Theoretical model for calculating ionic equilibria in milk as a function of pH: comparison to experiment. J Agric Food Chem 58:4440–4447
Nieves JW, Golden AL, Siris E, Kelsey JL, Lindsay R (1995) Teenage and current calcium intake are related to bone mineral density of the hip and forearm in women aged 30–39 years. Am J Epidemiol 141:342–351
Omoarukhe ED, On-Nom N, Grandison AS, Lewis MJ (2010) Effects of different calcium salts on properties of milk related to heat stability. Int J Dairy Technol 63:504–511
Pathomrungsiyounggul P, Grandison AS, Lewis MJ (2010) Effect of calcium carbonate, calcium citrate, tricalcium phosphate, calcium gluconate and calcium lactate on some physicochemical properties of soymilk. Int J Food Sci Technol 45:2234–2240
Philippe M, Gaucheron F, Le Graet Y, Michel F, Garem A (2003) Physicochemical characterization of calcium-supplemented skim milk. Lait 83:45–59
Ramasubramanian L, D’Arcy B, Deeth HC (2012) Heat-induced coagulation of whole milk by high levels of calcium chloride. Int J Dairy Technol 65:183–190
Rollema HS, Brinkhuis JA (1989) A 1H-NMR study of bovine casein micelles—influence of pH, temperature and calcium-ions on micellar structure. J Dairy Res 56:417–425
Rowland SJ (1938) The determination of the nitrogen distribution in milk. J Dairy Res 9:42–46
Singh G, Muthukumarappan K (2008) Influence of calcium fortification on sensory, physical and rheological characteristics of fruit yogurt. LWT Food Sci Technol 41:1145–1152
Singh G, Arora S, Sharma GS, Sindhu JS, Kansal VK, Sangwan RB (2007) Heat stability and calcium bioavailability of calcium-fortified milk. LWT Food Sci Technol 40:625–631
Udabage P, McKinnon IR, Augustin MA (2000) Mineral and casein equilibria in milk: effects of added salts and calcium-chelating agents. J Dairy Res 67:361–370
Udabage P, McKinnon IR, Augustin MA (2001) Effects of mineral salts and calcium chelating agents on the gelation of renneted skim milk. J Dairy Sci 84:1569–1575
van Hooydonk ACM, Hagedoorn HG, Boerrigter IJ (1986a) The effect of various cations on the renneting of milk. Neth Milk Dairy J 40:369–390
van Hooydonk ACM, Hagedoorn HG, Boerrigter IJ (1986b) pH-induced physicochemical changes of casein micelles in milk and their effect on renneting. 1. Effect of acidification on physicochemical properties. Neth Milk Dairy J 40:281–296
Vavrusova M, Skibsted LH (2014) Calcium nutrition. Bioavailability and fortification. LWT Food Sci Technol 59:1198–1204
Vavrusova M, Bøgelund Munk M, Skibsted LH (2013) Aqueous solubility of calcium L-lactate, calcium D-gluconate, and calcium D-lactobionate: importance of complex formation for solubility increase by hydroxycarboxylate mixtures. J Agric Food Chem 61:8207–8214
Volatier JL, Maffre J, Couvreur A (2000) Enquête INCA individuelle et nationale sur les consommations alimentaires. CRÉDOC - AFSSA - Ministère de l’agriculture et de la pêche. TEC & DOC, Paris, France
Wosje KS, Specker BL (2000) Role of calcium in bone health during childhood. Nutr Rev 58:253–268
Acknowledgments
This work was supported by Arla Foods amba. We thank Charlotte Louise Sparre for technical support during the SDS-PAGE and protein determination process.
Author information
Authors and Affiliations
Corresponding author
Additional information
This paper is part of the special issue dedicated to the 2nd International Symposium on Minerals & Dairy Products (MADP2014) held on 26-28th February in Auckland, New Zealand.
About this article
Cite this article
Koutina, G., Knudsen, J.C. & Skibsted, L.H. The effect of pH on calcium and phosphorus distribution between micellar and serum phase after enrichment of skim milk with calcium d-lactobionate. Dairy Sci. & Technol. 95, 63–74 (2015). https://doi.org/10.1007/s13594-014-0196-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13594-014-0196-z