Advertisement

Analytical and Bioanalytical Chemistry

, Volume 409, Issue 27, pp 6475–6484 | Cite as

Assessment of bioavailable B vitamin content in food using in vitro digestibility assay and LC-MS SIDA

  • Toomas Paalme
  • Allan Vilbaste
  • Kaspar Kevvai
  • Ildar Nisamedtinov
  • Kristel Hälvin-Tanilas
Research Paper

Abstract

Standardized analytical methods, where each B vitamin is extracted from a given sample individually using separate procedures, typically ensure that the extraction conditions provide the maximum recovery of each vitamin. However, in the human gastrointestinal tract (GIT), the extraction conditions are the same for all vitamins. Here, we present an analytically feasible extraction protocol that simulates conditions in the GIT and provides a measure of the content of bioavailable vitamins using LC-MS stable isotope dilution assay. The results show that the activities of both human gastric and duodenal juices were insufficient to liberate absorbable vitamers (AV) from pure cofactors. The use of an intestinal brush border membrane (IBBM) fraction derived from the mucosal tissue of porcine small intestine ensured at least 70% AV recovery. The rate of AV liberation, however, was strongly dependent on the cofactor, e.g., in the case of NADH, it was magnitudes higher than in the case of thiamine diphosphate. For some vitamins in some food matrices, the use of the IBBM fraction assay resulted in lower values for the content of AV than conventional vitamin determination methods. Conventional methods likely overestimate the actual bioavailability of some vitamins in these cases.

Graphical abstract

Assessment of bioavailable B vitamin content in food

Keywords

B vitamins Bioavailability Absorbable vitamers LC-MS Stable isotope dilution assay 

Notes

Funding

Financial support for this research was provided by the European Regional Development Fund (project EU48667) and Estonian Ministry of Education (institutional research funding IUT19-27).

Compliance with ethical standards

Human and animal rights

This article does not contain any studies with animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Said HM. Intestinal absorption of water-soluble vitamins in health and disease. Biochem J. 2011;437:357–72.CrossRefGoogle Scholar
  2. 2.
    Sklan D, Trostler N. Site and extent of thiamin absorption in the rat. J Nutr. 1977;107:353–6.Google Scholar
  3. 3.
    Middleton HM. Intestinal absorption of pyridoxal-5′ phosphate disappearance from perfused segments of rat jejunum in vivo. J Nutr. 1979;109:975–81.Google Scholar
  4. 4.
    Daniel H, Binninger E, Rehner G. Hydrolysis of FMN and FAD by alkaline phosphatase of the intestinal brush border membrane. Int J Vitam Nutr Res. 1983;53:109–14.Google Scholar
  5. 5.
    Gross CJ, Henderson LM. Digestion and absorption of NAD by the small intestine of the rat. J Nutr. 1983;113:412–20.Google Scholar
  6. 6.
    Shibata K, Gross CJ, Henderson LM. Hydrolysis and absorption of pantothenate and its coenzymes in the rat small intestine. J Nutr. 1983;113:2107–15.Google Scholar
  7. 7.
    Nabokina SM, Said HM. A high affinity and specific carrier-mediated mechanism for uptake of thiamine pyrophosphate by human colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2012;303:389–95.CrossRefGoogle Scholar
  8. 8.
    White HB, Merril AH. Riboflavin-binding proteins. Annu Rev Nutr. 1988;8:279–99.CrossRefGoogle Scholar
  9. 9.
    Combs GF Jr. The vitamins: fundamental aspects in nutrition and health. London: Academic press; 2012.Google Scholar
  10. 10.
    Akiyama T, Selhub J, Rosenberg IH. FMN phosphatase and FAD pyrophosphatase in rat intestinal brush borders: role in intestinal absorption of dietary riboflavin. J Nutr. 1982;112:263–8.Google Scholar
  11. 11.
    Ball GFM. Niacin: nicotinic acid and nicotinamide. In: Vitamins. Their role in the human body. Oxford: Blackwell Publishing; 2004. p. 301–9.Google Scholar
  12. 12.
    Subramanian VS, Ghosal A, Subramanya SB, Lytle C, Said HM. Differentiation-dependent regulation of intestinal vitamin B(2) uptake: studies utilizing human-derived intestinal epithelial Caco-2 cells and native rat intestine. Am J Physiol Gastrointest Liver Physiol. 2013;304:741–8.CrossRefGoogle Scholar
  13. 13.
    Baum CL, Selhub J, Rosenberg IH. The hydrolysis of nicotinamide adenine dinucleotide by brush border membranes of rat intestine. Biochem J. 1982;204:203–7.CrossRefGoogle Scholar
  14. 14.
    Trammell SAJ, Schmidt MS, Weidemann BJ, Redpath P, Jaksch F, Dellinger RW, et al. Nicotinamide riboside is uniquely and orally bioavailable in mice and humans. Nat Commun. 2016;7:12948.CrossRefGoogle Scholar
  15. 15.
    Henderson LM, Gross CJ. Metabolism of niacin and niacinamide in perfused rat intestine. J Nutr. 1979;109:654–62.Google Scholar
  16. 16.
    Kumar JS, Subramanian VS, Kapadia R, Kashyap ML, Said HM. Mammalian colonocytes possess a carrier-mediated mechanism for uptake of vitamin B3 (niacin): studies utilizing human and mouse colonic preparations. Am J Physiol Gastrointest Liver Physiol. 2013;305:207–13.CrossRefGoogle Scholar
  17. 17.
    Said HM. Recent advances in transport of water-soluble vitamins in organs of the digestive system: a focus on the colon and the pancreas. Am J Physiol Gastrointest Liver Physiol. 2013;305:G601–10.CrossRefGoogle Scholar
  18. 18.
    Elbert J, Daniel H, Rehner G. Intestinal uptake of nicotinic acid as a function of microclimate-pH. Int J Vitam Nutr Res. 1986;56:85–93.Google Scholar
  19. 19.
    Nabokina SM, Kashyap ML, Said HM. Mechanism and regulation of human intestinal niacin uptake. Am J Phys Cell Phys. 2005;289:97–103.CrossRefGoogle Scholar
  20. 20.
    Eto M, Nakagawa A. Identification of a growth factor in tomato juice for a newly isolated strain of Pediococcus cerevisiae. J Inst Brew. 1975;81:232–6.CrossRefGoogle Scholar
  21. 21.
    Prasad PD, Wang H, Huang W, Fei YJ, Leibach FH, Devoe LD, et al. Molecular and functional characterization of the intestinal Na+-dependent multivitamin transporter. Arch Biochem Biophys. 1999;366:95–106.CrossRefGoogle Scholar
  22. 22.
    Chen Y, Zhao S, Zhao Y. Efficacy and tolerability of coenzyme A vs pantethine for the treatment of patients with hyperlipidemia: a randomized, double-blind, multicenter study. J Clin Lipidol. 2015;9:692–7.CrossRefGoogle Scholar
  23. 23.
    Gregory JF 3rd, Ink SL. Identification and quantification of pyridoxine-β-glucoside as a major form of vitamin B6 in plant-derived foods. J Agric Food Chem. 1987;35:76–82.CrossRefGoogle Scholar
  24. 24.
    Gregory JF 3rd, Sartain DB. Improved chromatographic determination of free and glycosylated forms of vitamin B6 in foods. J Agric Food Chem. 1991;39:899–905.CrossRefGoogle Scholar
  25. 25.
    Albersen M, Bosma M, Knoers NVVAM, de Ruiter BHB, Diekman EF, de Ruijter J, et al. The intestine plays a substantial role in human vitamin B6 metabolism: a Caco-2 cell model. PLoS One. 2013;8:e54113.CrossRefGoogle Scholar
  26. 26.
    Gregory JF 3rd, Trumbo PR, Bailey LB, Toth JP, Baumgartner TG, Cerda JJ. Bioavailability of pyridoxine-5′-beta-D-glucoside determined in humans by stable-isotopic methods. J Nutr. 1991;121:177–86.Google Scholar
  27. 27.
    Tsuge H, Maeno M, Hayakawa T, Suzuki Y. Comparative study of pyridoxine- α,β-glucosides, and phosphopyridoxyl-lysine as a vitamin B6 nutrient. J Nutr Sci Vitaminol. 1996;42:377–86.CrossRefGoogle Scholar
  28. 28.
    Ndaw S, Bergaentzle M, Aoude-Werner D, Hasselmann C. Extraction procedures for the liquid chromatographic determination of thiamin, riboflavin and vitamin B6 in foodstuffs. Food Chem. 2000;71:129–38.CrossRefGoogle Scholar
  29. 29.
    Rychlik M. Quantification of free and bound pantothenic acid in foods and blood plasma by a stable isotope dilution assay. J Agric Food Chem. 2000;48:1175–81.CrossRefGoogle Scholar
  30. 30.
    Hälvin K, Paalme T, Nisamedtinov I. Comparison of different extraction methods for simultaneous determination of B complex vitamins in nutritional yeast using LC-MS-TOF and stable isotope dilution assay. Anal Bioanal Chem. 2013;406:7355–66.CrossRefGoogle Scholar
  31. 31.
    Salvati LM, McClure SC, Reddy TM, Cellar NA. Simultaneous determination of total vitamins B1, B2, B3, and B6 in infant formula and related nutritionals by enzymatic digestion and LC-MS/MS: single-laboratory validation, first action 2015.14. J AOAC Int. 2016;99:776–85.CrossRefGoogle Scholar
  32. 32.
    EVS-EN 15652:2009 Foodstuffs – Determination of niacin by HPLC. Tallinn: Estonian Centre for Standardisation; 2009.Google Scholar
  33. 33.
    Holm H, Hanssen L, Krogdahfl A. High and low inhibitor soybean meals affect human duodenal proteinase activity differently: in vivo comparison with bovine serum albumin. J Nutr. 1988;118:515–20.Google Scholar
  34. 34.
    Gregory JF, Ink SL, Cerda JJ. Comparison of pteroylpolyglutamate hydrolase (folate conjugase) from porcine and human intestinal brush border membrane. Comp Biochem Physiol B. 1987;88:1135–41.CrossRefGoogle Scholar
  35. 35.
    Aller K, Adamberg K, Timarova V, Seiman A, Feštšenko D, Vilu R. Nutritional requirements and media development for Lactococcus lactis IL1403. Appl Microbiol Biotechnol. 2014;98:5871–81.CrossRefGoogle Scholar
  36. 36.
    Almaas H, Cases AL, Devold TG, Holm H, Langsrud T, Aabakken L, et al. In vitro digestion of bovine and caprine milk by human gastric and duodenal enzymes. Int Dairy J. 2006;16:961–8.CrossRefGoogle Scholar
  37. 37.
    Sumeri I, Arike L, Adamberg K, Paalme T. Single bioreactor gastrointestinal tract simulator for study of survival of probiotic bacteria. Appl Microbiol Biotechnol. 2008;80:317–24.CrossRefGoogle Scholar
  38. 38.
    EVS-EN 14122:2003 Foodstuffs – Determination of vitamin B1 (thiamin) by HPLC. Tallinn: Estonian Centre for Standardisation; 2003.Google Scholar
  39. 39.
    EVS-EN 14152:2003 Foodstuffs – Determination of vitamin B2 by HPLC. Tallinn: Estonian Centre for Standardisation; 2003.Google Scholar
  40. 40.
    EVS-EN 14663:2006 Foodstuffs – Determination of vitamin B6 (including its glycosylated forms) by HPLC. Tallinn: Estonian Centre for Standardisation; 2006.Google Scholar
  41. 41.
    Hälvin K, Paalme T, Vilbaste A, Nisamedtinov I. LC-MS quantification of B-group vitamins in yeast. In: Advances in Science and Industrial Production of Baker’s Yeast. Proceedings of the 27th VH Yeast Conference. 2014. p. 71–81.Google Scholar
  42. 42.
    Henthorn PS, Raducha M, Kadesch T, Weiss MJ, Harris H. Sequence and characterization of the human intestinal alkaline phosphatase gene. J Biol Chem. 1988;263:12011–9.Google Scholar
  43. 43.
    Yedlin ST, Young GP, Seetharam B, Seetharam S, Alpers DH. Characterization and comparison of soluble and membraneous forms of intestinal alkaline phosphatase from the suckling rat. J Biol Chem. 1981;256:442–52.Google Scholar
  44. 44.
    Sandhu M, Mahmood A. Kinetic characteristics of soluble and brush border alkaline phosphatase and sucrase activities in developing rat intestine: effect of hormones Indian. J Biochem Biophys. 1990;27:88–92.Google Scholar
  45. 45.
    Fan MZ, Adeola O, Asem E. Characterization of brush border membrane-bound alkaline phosphatase activity in different segments of the porcine small intestine. J Nutr Biochem. 1999;10:299–305.CrossRefGoogle Scholar
  46. 46.
    Almo SC, Smith DL, Danishefsky AT, Ringe D. The structural basis for the altered substrate specificity of the R292D active site mutant of aspartate aminotransferase from E. coli. Protein Eng. 1994;7:405–12.CrossRefGoogle Scholar
  47. 47.
    Miller ER, Ullrey DE. The pig as a model for human nutrition. Annu Rev Nutr. 1987;7:361–82.CrossRefGoogle Scholar
  48. 48.
    Zhang Q, Widmer G, Tzipori S. A pig model of the human gastrointestinal tract. Gut Microbes. 2013;4:193–200.CrossRefGoogle Scholar
  49. 49.
    Piao JH, Goding JW, Nakamura H, Sano K. Molecular cloning and chromosomal localization of PD-Ibeta (PDNP3), a new member of the human phosphodiesterase I genes. Genomics. 1997;45:412–5.CrossRefGoogle Scholar
  50. 50.
    Vovk AI, Babiĭ LV, Murav'eva IV. [Relative reactivity of thiamine monophosphate and thiamine diphosphate upon interaction with alkaline phosphatase]. Ukr Biokhim Zh (1999). 2002;74:93–6. [Article in Russian]Google Scholar
  51. 51.
    Paalme T, Kevvai K, Vilbaste A, Hälvin K, Nisamedtinov I. Uptake and accumulation of B-group vitamers in Saccharomyces cerevisiae in ethanol-stat fed-batch culture. World J Microbiol Biotechnol. 2014;30:2351–9.CrossRefGoogle Scholar
  52. 52.
    Kodicek E, Ashby DR, Muller M, Carpenter KJ. The conversion of bound nicotinic acid to free nicotinamide on roasting sweet corn. Proc Nutr Soc. 1974;33:105A–6A.Google Scholar
  53. 53.
    Nakano K, Sugawara Y, Ohashi M, Harigaya S. Glucoside formation as a novel metabolic pathway of pantothenic acid in the dog. Biochem Pharmacol. 1986;35:3745–52.CrossRefGoogle Scholar
  54. 54.
    Gregory JF 3rd. Chemical changes in vitamins during food processing. In: Richardson T, Finley JW, editors. Chemical changes in food during processing. Boston, MA: Springer US; 1985. p. 373–402.Google Scholar
  55. 55.
    Gregory JF 3rd, Kirk JR. Interaction of pyridoxal and pyridoxal phosphate with peptides in a model food system during thermal processing. J Food Sci. 1977;42:1554–7.CrossRefGoogle Scholar
  56. 56.
    Mihhalevski A, Nisamedtinov I, Hälvin K, Ošeka A, Paalme T. Stability of B-complex vitamins and dietary fiber during rye sourdough bread production. J Cereal Sci. 2013;57:30–8.CrossRefGoogle Scholar
  57. 57.
    Ashihara H, Stasolla C, Yin Y, Loukanina N, Thorpe TA. De novo and salvage biosynthetic pathways of pyridine nucleotides and nicotinic acid conjugates in cultured plant cells. Plant Sci. 2005;169:107–14.CrossRefGoogle Scholar
  58. 58.
    Ashihara H, Yin Y, Watanabe S. Nicotinamide metabolism in ferns: formation of nicotinic acid glucoside. Plant Physiol Biochem. 2011;49:275–9.CrossRefGoogle Scholar
  59. 59.
    Eitenmiller RR, Landen WO Jr, Ye L. Vitamin analysis for the health and food science. Boca Raton, FL: CRC Press; 2016.Google Scholar
  60. 60.
    Tadera K, Oda K, Nakahara C. Occurrence in soybeans of a novel vitamin B6 conjugate that liberates pyridoxine by β-glucosidase action after alkali treatment. Biosci Biotechnol Biochem. 1999;63:213–5.CrossRefGoogle Scholar
  61. 61.
    Armada LJ, Mackey AD, Gregory JF 3rd. Intestinal brush border membrane catalyzes hydrolysis of pyridoxine-5′-β-D glucoside and exhibits parallel developmental changes of hydrolytic activities toward pyridoxine-5′-β-D-glucoside and lactose in rats. J Nutr. 2002;132:2695–9.Google Scholar
  62. 62.
    Gregory JF 3rd. Nutritional properties and significance of vitamin glycosides. Annu Rev Nutr. 1998;18:277–96.CrossRefGoogle Scholar
  63. 63.
    Nakano H, McMahon LG, Gregory JF 3rd. Pyridoxine-5′-β-glucoside exhibits incomplete bioavailability as a source of vitamin B6 and partially inhibits the utilization of co-ingested pyridoxine in humans. J Nutr. 1997;127:1508–13.Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Toomas Paalme
    • 1
  • Allan Vilbaste
    • 2
  • Kaspar Kevvai
    • 2
  • Ildar Nisamedtinov
    • 1
    • 2
    • 3
  • Kristel Hälvin-Tanilas
    • 2
  1. 1.Department of Chemistry and BiotechnologyTallinn University of TechnologyTallinnEstonia
  2. 2.Center of Food and Fermentation TechnologiesTallinnEstonia
  3. 3.Lallemand, Inc.MontrealCanada

Personalised recommendations