Skip to main content
Top
Published in: European Journal of Nutrition 1/2016

Open Access 01-02-2016 | Original Contribution

Increased iron bioavailability from lactic-fermented vegetables is likely an effect of promoting the formation of ferric iron (Fe3+)

Authors: Nathalie Scheers, Lena Rossander-Hulthen, Inga Torsdottir, Ann-Sofie Sandberg

Published in: European Journal of Nutrition | Issue 1/2016

Login to get access

Abstract

Background

Lactic fermentation of foods increases the availability of iron as shown in a number of studies throughout the years. Several explanations have been provided such as decreased content of inhibitory phytate, increased solubility of iron, and increased content of lactic acid in the fermented product. However, to our knowledge, there are no data to support that the bioavailability of iron is affected by lactic fermentation.

Objectives

The objective of the present study was to investigate whether the bioavailability of iron from a vegetable mix was affected by lactic fermentation and to propose a mechanism for such an event, by conducting human and cell (Caco-2, HepG2) studies and iron speciation measurements (voltammetry). We also investigated whether the absorption of zinc was affected by the lactic fermentation.

Results

In human subjects, we observed that lactic-fermented vegetables served with both a high-phytate and low-phytate meal increased the absorption of iron, but not zinc. In vitro digested fermented vegetables were able to provoke a greater hepcidin response per ng Fe than fresh vegetables, indicating that Fe in the fermented mixes was more bioavailable, independent on the soluble Fe content. We measured that hydrated Fe3+ species were increased after the lactic fermentation, while there was no significant change in hydrated Fe2+. Furthermore, lactate addition to Caco-2 cells did not affect ferritin formation in response to Fe nor did lactate affect the hepcidin response in the Caco-2/HepG2 cell system.

Conclusions

The mechanism for the increased bioavailability of iron from lactic-fermented vegetables is likely an effect of the increase in ferric iron (Fe3+) species caused by the lactic fermentation. No effect on zinc bioavailability was observed.
Literature
1.
go back to reference Lee D, Jang S, Baek E, Kim M, Lee K et al (2009) Lactic acid bacteria affect serum cholesterol levels, harmful fecal enzyme activity, and fecal water content. Lipids Health Dis 8:21CrossRef Lee D, Jang S, Baek E, Kim M, Lee K et al (2009) Lactic acid bacteria affect serum cholesterol levels, harmful fecal enzyme activity, and fecal water content. Lipids Health Dis 8:21CrossRef
2.
go back to reference Martini MC, Lerebours EC, Lin WJ, Harlander SK, Berrada NM et al (1991) Strains and species of lactic acid bacteria in fermented milks (yogurts): effect on in vivo lactose digestion. Am J Clin Nutr 54:1041–1046 Martini MC, Lerebours EC, Lin WJ, Harlander SK, Berrada NM et al (1991) Strains and species of lactic acid bacteria in fermented milks (yogurts): effect on in vivo lactose digestion. Am J Clin Nutr 54:1041–1046
3.
go back to reference Torsdottir I, Blomqvist R, Ekman R, Hagander B, Sandberg A-S (1992) Fermented or fresh vegetables decrease the post-prandial blood glucose and insulin levels in healthy persons. Scand J Nutr 36:4–7 Torsdottir I, Blomqvist R, Ekman R, Hagander B, Sandberg A-S (1992) Fermented or fresh vegetables decrease the post-prandial blood glucose and insulin levels in healthy persons. Scand J Nutr 36:4–7
4.
go back to reference Bering S, Suchdev S, Sjøltov L, Berggren A, Tetens I et al (2006) A lactic acid-fermented oat gruel increases non-haem iron absorption from a phytate-rich meal in healthy women of childbearing age. Br J Nutr 96:80–85 doi:10.1079/BJN20051683 CrossRef Bering S, Suchdev S, Sjøltov L, Berggren A, Tetens I et al (2006) A lactic acid-fermented oat gruel increases non-haem iron absorption from a phytate-rich meal in healthy women of childbearing age. Br J Nutr 96:80–85 doi:10.​1079/​BJN20051683 CrossRef
5.
go back to reference Bergqvist SW, Sandberg A-S, Andlid T, Wessling-Resnick M (2005) Lactic acid decreases Fe(II) and Fe(III) retention but increases Fe(III) transepithelial transfer by Caco-2 cells. J Agric Food Chem 53:6919–6923CrossRef Bergqvist SW, Sandberg A-S, Andlid T, Wessling-Resnick M (2005) Lactic acid decreases Fe(II) and Fe(III) retention but increases Fe(III) transepithelial transfer by Caco-2 cells. J Agric Food Chem 53:6919–6923CrossRef
6.
go back to reference Salovaara S, Sandberg A-S, Andlid T (2002) Organic acids influence iron uptake in the human epithelial cell line Caco-2. J Agricu and Food Chem 50:6233–6238CrossRef Salovaara S, Sandberg A-S, Andlid T (2002) Organic acids influence iron uptake in the human epithelial cell line Caco-2. J Agricu and Food Chem 50:6233–6238CrossRef
7.
go back to reference Proulx AK, Reddy MB (2007) Fermentation and lactic acid addition enhance iron bioavailability of maize. J Agric Food Chem 55:2749–2754CrossRef Proulx AK, Reddy MB (2007) Fermentation and lactic acid addition enhance iron bioavailability of maize. J Agric Food Chem 55:2749–2754CrossRef
8.
go back to reference Hallberg L, Rossander L (1982) Absorption of iron from Western-type lunch and dinner meals. Am J Clin Nutr 35:502–509 Hallberg L, Rossander L (1982) Absorption of iron from Western-type lunch and dinner meals. Am J Clin Nutr 35:502–509
9.
go back to reference Svanberg U, Lorri W, Sandbeag AS (1993) Lactic fermentation of non-tannin and high-tannin cereals: effects on in vitro estimation of iron availability and phytate hydrolysis. J Food Sci 58:408–412CrossRef Svanberg U, Lorri W, Sandbeag AS (1993) Lactic fermentation of non-tannin and high-tannin cereals: effects on in vitro estimation of iron availability and phytate hydrolysis. J Food Sci 58:408–412CrossRef
10.
go back to reference Bergqvist S, Sandberg A-S, Carlsson N-G, Andlid T (2005) Improved iron solubility in carrot juice fermented by homo-and hetero-fermentative lactic acid bacteria. Food Microbiol 22:53–61CrossRef Bergqvist S, Sandberg A-S, Carlsson N-G, Andlid T (2005) Improved iron solubility in carrot juice fermented by homo-and hetero-fermentative lactic acid bacteria. Food Microbiol 22:53–61CrossRef
11.
go back to reference Eakins JD, Brown DA (1966) An improved method for the simultaneous determination of iron-55 and iron-59 in blood by liquid scintillation counting. Int J Appl Radiat Isot 17:391–397CrossRef Eakins JD, Brown DA (1966) An improved method for the simultaneous determination of iron-55 and iron-59 in blood by liquid scintillation counting. Int J Appl Radiat Isot 17:391–397CrossRef
12.
go back to reference Björn-Rasmussen E, Halberg L, Magnusson B, Rossander L, Svanberg B et al (1976) Measurement of iron absorption from compositite meals. Am J Clin Nutr 29:772–778 Björn-Rasmussen E, Halberg L, Magnusson B, Rossander L, Svanberg B et al (1976) Measurement of iron absorption from compositite meals. Am J Clin Nutr 29:772–778
13.
go back to reference Arvidsson B, Cederblad A, Bjoern-Rasmussen E, Sandstroem B (1978) A radionuclide technique for studies of zinc absorption in man. Int J Nucl Med Biol 5:104–109CrossRef Arvidsson B, Cederblad A, Bjoern-Rasmussen E, Sandstroem B (1978) A radionuclide technique for studies of zinc absorption in man. Int J Nucl Med Biol 5:104–109CrossRef
14.
go back to reference Harland BF, Oberleas D (1986) Anion-exchange method for determination of phytate in foods: collaborative study. J Assoc Off Anal Chem 69:667–669 Harland BF, Oberleas D (1986) Anion-exchange method for determination of phytate in foods: collaborative study. J Assoc Off Anal Chem 69:667–669
15.
go back to reference Sandberg AS, Carlsson NG, Svanberg U (1989) Effects of inositol Tri-, Tetra-, Penta-, and hexaphosphates on in vitro estimation of iron availability. J Food Sci 54:159–161CrossRef Sandberg AS, Carlsson NG, Svanberg U (1989) Effects of inositol Tri-, Tetra-, Penta-, and hexaphosphates on in vitro estimation of iron availability. J Food Sci 54:159–161CrossRef
16.
go back to reference Sandberg AS, Ahderinne R (1986) HPLC method for determination of inositol Tri-, Tetra-, Penta-, and hexaphosphates in foods and intestinal contents. J Food Sci 51:547–550CrossRef Sandberg AS, Ahderinne R (1986) HPLC method for determination of inositol Tri-, Tetra-, Penta-, and hexaphosphates in foods and intestinal contents. J Food Sci 51:547–550CrossRef
17.
go back to reference Ashoor SH, Knox MJ (1987) Determination of vitamin A derivatives in fortified foods and commercial vitamin supplements by high-performance liquid chromatography. J Chromatogr 409:419–425CrossRef Ashoor SH, Knox MJ (1987) Determination of vitamin A derivatives in fortified foods and commercial vitamin supplements by high-performance liquid chromatography. J Chromatogr 409:419–425CrossRef
18.
go back to reference Scheers NM, Almgren AB, Sandberg A-S (2014) Proposing a Caco-2/HepG2 cell model for in vitro iron absorption studies. J Nutr Biochem 25:710–715CrossRef Scheers NM, Almgren AB, Sandberg A-S (2014) Proposing a Caco-2/HepG2 cell model for in vitro iron absorption studies. J Nutr Biochem 25:710–715CrossRef
19.
go back to reference Allen A, Flemström G (2005) Gastroduodenal mucus bicarbonate barrier: protection against acid and pepsin. Am J Physiol Cell Physiol 288:1–19CrossRef Allen A, Flemström G (2005) Gastroduodenal mucus bicarbonate barrier: protection against acid and pepsin. Am J Physiol Cell Physiol 288:1–19CrossRef
20.
go back to reference Scheers N, Andlid T, Alminger M, Sandberg A-S (2010) Determination of Fe2+ and Fe3+ in aqueous solutions containing food chelators by differential pulse anodic stripping voltammetry. Electroanalysis 22:1090–1096CrossRef Scheers N, Andlid T, Alminger M, Sandberg A-S (2010) Determination of Fe2+ and Fe3+ in aqueous solutions containing food chelators by differential pulse anodic stripping voltammetry. Electroanalysis 22:1090–1096CrossRef
21.
go back to reference Brune M, Rossander-Hulten L, Hallberg L, Gleerup A, Sandberg AS (1992) Iron-absorption from bread in humans—inhibiting effects of cereal fiber, phytate and inositol phosphates with different numbers of phosphate groups. J Nutr 122:442–449 Brune M, Rossander-Hulten L, Hallberg L, Gleerup A, Sandberg AS (1992) Iron-absorption from bread in humans—inhibiting effects of cereal fiber, phytate and inositol phosphates with different numbers of phosphate groups. J Nutr 122:442–449
22.
go back to reference Hallberg L, Brune M, Rossander L (1989) Iron absorption in man: ascorbic acid and dose-dependent inhibition by phytate. Am J Clin Nutr 49:140–144 Hallberg L, Brune M, Rossander L (1989) Iron absorption in man: ascorbic acid and dose-dependent inhibition by phytate. Am J Clin Nutr 49:140–144
23.
go back to reference Scheers N (2013) Regulatory effects of Cu, Zn, and Ca on Fe absorption: the intricate play between nutrient transporters. Nutrients 5:957–970CrossRef Scheers N (2013) Regulatory effects of Cu, Zn, and Ca on Fe absorption: the intricate play between nutrient transporters. Nutrients 5:957–970CrossRef
24.
go back to reference Pereira DIA, Mergler BI, Faria N, Bruggraber SFA, Aslam MF et al (2013) Caco-2 cell acquisition of dietary iron(III) invokes a nanoparticulate endocytic pathway. PLoS ONE 8:e81250CrossRef Pereira DIA, Mergler BI, Faria N, Bruggraber SFA, Aslam MF et al (2013) Caco-2 cell acquisition of dietary iron(III) invokes a nanoparticulate endocytic pathway. PLoS ONE 8:e81250CrossRef
25.
go back to reference McKie AT, Barrow D, Latunde-Dada GO, Rolfs A, Sager G, Mudaly E, Mudaly M, Richardson C, Barlow D, Bomford A, Peters TJ, Raja KB, Shirali S, Hediger MA, Farzaneh F, Simpson RJ (2001) An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291:1755–1759CrossRef McKie AT, Barrow D, Latunde-Dada GO, Rolfs A, Sager G, Mudaly E, Mudaly M, Richardson C, Barlow D, Bomford A, Peters TJ, Raja KB, Shirali S, Hediger MA, Farzaneh F, Simpson RJ (2001) An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291:1755–1759CrossRef
26.
go back to reference Conrad ME, Umbreit JN, Moore EG (1994) Iron absorption and cellular uptake of iron. Adv Exp Med Biol 356:69–79CrossRef Conrad ME, Umbreit JN, Moore EG (1994) Iron absorption and cellular uptake of iron. Adv Exp Med Biol 356:69–79CrossRef
27.
go back to reference Conrad ME, Umbreit JN, Moore EG (1993) Regulation of iron-absorption-proteins involved in duodenal mucosal uptake and transport. J Am Coll Nutr 12:720–728CrossRef Conrad ME, Umbreit JN, Moore EG (1993) Regulation of iron-absorption-proteins involved in duodenal mucosal uptake and transport. J Am Coll Nutr 12:720–728CrossRef
28.
go back to reference Han O, Failla M, Hill AD, Morris ER, Smith JCJR (1995) Reduction of Fe(III) is required for uptake of nonheme iron by Caco-2 cells. J Nutr 125:1291–1299 Han O, Failla M, Hill AD, Morris ER, Smith JCJR (1995) Reduction of Fe(III) is required for uptake of nonheme iron by Caco-2 cells. J Nutr 125:1291–1299
29.
go back to reference Baynes RD, Macfarlane BJ, Bothwell TH, Siegenberg D, Bezwoda WR et al (1990) The promotive effect of soy sauce on iron absorption in human subjects. Eur J Clin Nutr 44:419–424 Baynes RD, Macfarlane BJ, Bothwell TH, Siegenberg D, Bezwoda WR et al (1990) The promotive effect of soy sauce on iron absorption in human subjects. Eur J Clin Nutr 44:419–424
Metadata
Title
Increased iron bioavailability from lactic-fermented vegetables is likely an effect of promoting the formation of ferric iron (Fe3+)
Authors
Nathalie Scheers
Lena Rossander-Hulthen
Inga Torsdottir
Ann-Sofie Sandberg
Publication date
01-02-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 1/2016
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-0857-6

Other articles of this Issue 1/2016

European Journal of Nutrition 1/2016 Go to the issue