New data on the bioavailability of bread magnesium

Magnesium Research. Volume 17, Numéro 4, 335-40, December 2004, Original article

Auteur(s) : Hubert Walter Lopez, Fanny Leenhardt, Christian Remesy , ULICE, Limagrain Céréales Ingrédients, avenue George Gershwin, BP 173, 63204 Riom Cedex, France, U3M, INRA Theix, F-63122 Theix, France.

Illustrations

ARTICLE

Auteur(s) :, Hubert Walter Lopez^1,*, Fanny Leenhardt², Christian Remesy²

¹ULICE, Limagrain Céréales Ingrédients, avenue George Gershwin, BP 173, 63204 Riom Cedex, France
²U3M, INRA Theix, F-63122 Theix, France

Introduction

More than 50 % of the world’s total food energy is supplied by grain species. They are the major source of starch and fibre, and they also contain significant amounts of proteins, vitamins and minerals. Many studies have shown that efforts should be made to replace refined-grain with whole-grain foods. Indeed, increased intake of whole grains may reduce disease risk by means of favourable effects on metabolic risk factors [1, 2]. Magnesium intake may partially explain these beneficial effects [3, 4] and it seems to be of interest to increase Mg bioavailability in whole cereal products. Since Mg, the second most abundant intracellular cation, plays an essential role in a wide range of fundamental reactions, it is not surprising that its deficiency in the organism may lead to severe biochemical and physiological perturbations. In many countries, cereal products are the main source of magnesium in human nutrition [5]. Table 1( Table 1 ) shows that whole grains, wheat bran or maize germ are extremely rich in Mg. Nevertheless, mineral subdeficiencies occur in developed countries. In France, the SU-VI-MAX study showed that 72 % of men and 77 % of women had Mg intakes lower than the French recommended dietary allowances [6]. One of the causes of this low Mg intake in developed countries is the increase of refined products available on the market (white flour, white sugar, etc.). Food processing can negatively affect the nutritional quality of food. Milling is a process that consists of separating bran and germ from the starchy endosperm in order to produce white flour, and it leads to the loss of vitamins and minerals. Even if whole grain products and wheat bran are important sources of Mg [7], they contain considerable amounts of phytic acid (PA). PA or myo-inositol hexakisphosphate has been found to lower the absorption of trace elements such as Fe or Zn, as well as macrominerals Ca or Mg, in cereal products by chelating multivalent cations with its six anionic phosphate groups to form phytate complexes that are insoluble at physiological pH [8].
Table 1 Magnesium content and density in different foods. From [36]

	Content mg/100 g	Density mg/100 kcal
Wheat
White bread	24	10
Wholemeal bread	60	30
Germ	285	95
Bran	490	285
Rice
Polished	32	9
Unpolished	119	34
Corn
Unsweetened corn flakes	14	4
Whole grain	91	28
Germ	500	167
Seeds
Sesame	347	61
Soya beans	220	67
Nuts
Hazelnut	156	24
Peanut	182	31
Cashew nut	267	47
Vegetables
Lettuce	9	82
Spinach	60	375
Purslane	151	1372
Cocoa products
Cocoa powder	414	120
Milk chocolate	71	13
Animal Products
Whole cow milk	12	18
Beef sirloin	23	17
Mussel	32	47

Mg bioavailability is different between wheat varieties

As bread is a staple food in many countries and whole wheat bread ranks within the highest foods for its Mg contribution, increasing bread Mg contribution by using wholemeal flour and lowering PA content to levels that do not affect the mineral bioavailability would be necessary to prevent metabolic disorders associated with Mg deficiency. Wheat is the main ingredient of bread and Mg bioavailability from wheat flour is different between varieties. Recent unpublished work on 230 wheat varieties from 50 different countries confirmed a large difference in Mg composition (between 997 and 2048 mg/kg) within varieties of wheat. Good correlations were found between minerals, especially between Mg and Zn. However, many of the varieties with a higher Mg content are poor yielding genotypes. Indeed strong negative correlations were observed between most of the minerals and production yield. Nevertheless, the positive consequence of this observation is that nutrient contents were significantly correlated to protein contents and with technological value. Moreover, for a same agronomic yield, different Mg accumulation potential could be found. This variation in mineral levels could be attributed to genetic and environmental effects and their interaction. Multi-site experiments investigated the relative influence of each of these effects. Accumulation of minerals in wheat grain seems to be subject to rather different determining factors. Breeding for higher grain Mg content could easily succeed, due to the wide biodiversity observed for this criterion and the small genetic x environmental interaction effect measured. In contrast, traditional breeding for iron seed content would be almost impossible, due to the strong Genetic x Environmental interaction and consequently the low genotype effects of this criterion. Multi-local trials confirm the strong environmental impact on Mg seed contents. Soil mineral composition and pH are especially influential. Agronomic growing conditions also influence the mineral content of cereals. El-Gindy et al. [9] reported a correlation between fertiliser treatment and total ash of three hard red winter wheat grains grown in 13 locations, utilising seven different fertilisers. They also concluded that concentration of minerals depends on the varieties tested. In the same way, Peterson et al. [10] investigating mineral composition of bran originating from 27 varieties of durum wheat, found significant influences of variety and region of cultivation on this composition. Farming practices can also influence the Mg density of a wheat variety. Organic crops contain significantly more magnesium than conventional crops. These differences could be explained by the presence of a greater population of microorganisms in organically managed soils. These micro-organisms produce many compounds that help plants, including substances such as citrate or lactate that combine with mineral soil and make them more available to plant roots. Furthermore, potassium fertiliser can reduce the Mg content and indirectly the phosphorus content of some plants [11]. Thus, Mg bioavailability would be different between organic and conventional crops. In contrast, nitrogen fertilisation plays a role in nutrient accumulation by the spikes.

The most surprising fact is that varieties with the same PA content do not have the same bioavailability of Mg. It could mainly be explained by variability in the vegetal phytase activities and by the mineral/PA ratio. Thus, the total mineral content in whole cereals plays a predominant role in bioavailability. In seeds, PA accumulation is correlated to phosphorus accumulation but not to total mineral content. Thus, if PA content was relatively constant in the wheat tested, varieties with higher Mg bioavailability had greater Mg stores and higher activity of vegetal phytase [12]. Indeed, by comparing mineral bioavailability of four soft wheat varieties in rats ( (figure 1) ), Mg absorption and accumulation in bone were stimulated by the ingestion of KON and BNC varieties. Mineral bioavailabilities from KON or BNC varieties were higher than those observed with Soissons or Hardi varieties. Thus, genetic origin plays a major role in determining mineral bioavailability in whole wheat.

In order to optimise animal growth with reducing mineral accumulation in the soil, nutritional availability of P is most commonly improved by supplying animal fodder with microbial phytases. Other strategies, however, aim at overexpression of phytases in transgenic cereals and on mutational breeding of low-phytate mutants [13]. Low phytate crops such as corn or barley, represent a strategy to improve P-utilisation and to reduce the environmental impact of phytate-rich manure. It must be noted that Mg contents are not severely affected by low-phytate mutations [14, 15].

Food processes and Mg bioavailability

Wheat is rarely consumed as a whole grain product and most of the time goes through a fractionation step (milling) and transformation processes (bread making, extrusion).

The major part of Mg, as well as B-group vitamins, is located in the aleurone layer. Its strong adhesion to the pericarp explains why it is usually lost with the milling by-products. This predominant mineral localisation in the aleurone cells also plays an important and negative role in their bioaccessibility. Indeed, the cations are enclosed within thick cell walls and are chelated with PA. Increasing the bioaccessibility of Mg requires both its permeation through the aleurone cell walls and its solubilisation out of the phytic acid complex. Decreasing the size of aleurone containing cell particles (usually bran) promotes Mg availability. Decreasing the dough pH, as it is the case with the sourdough process, on the other hand, allows the Mg solubilisation in the media. This phenomenon is largely due to the activation of endogenous phytases (optimum pH = 5.5), also located in the aleurone layer. Indeed, moderate acidification of the dough in the absence of leaven, and therefore of microbial phytases, allows the same level of phytate degradation as in the case of sourdough fermentation.

In whole cereal products, dietary fibre (cellulose, hemicellulose, resistant starch) and phytic acid occur together in fibre-rich diets and, thus, it is difficult to separate the effects of fiber and phytate in the utilization of Mg. Nevertheless, the recommendation for increasing dietary fibre in Western communities would not be expected to have any adverse effect on mineral absorption if we increase not only the intake of fibre, but also the dietary intake of other food components such as protein (both vegetable and animal protein) and ascorbic, citric, and oxalic acids (in fruits and vegetables) [16].

Manufacturing processes (kneading, soaking, fermentation, baking, toasting, extrusion, cooking) play a key role in the PA content of the final cereal product and thus in the mineral bioavailability. Varying losses of PA occur during the manufacturing process. For instance, all the PA from the ingredients is found in whole wheat biscuits, because there is no destruction of PA in a whole wheat pastry. The PA reduction in extrusion cooking products is still discussed: a 25 % decrease was found by Le Francois [17] whereas Sandberg et al. [18] observed no change in the PA content in extruded products. Moreover, it must be underlined that extrusion cooking may lead to a considerable impairment in the digestion of PA, due to a loss of intrinsic cereal phytase activity [19]. The plant phytase, PA-degrading enzyme that is deactivated during extrusion cooking, is of significance for phytate hydrolysis in the stomach and small intestine. Thus a possible impairment of mineral absorption mediated by the resistance of PA to digestion in the human gut must be considered [20].

Another way to reduce phytate and to improve the availability of Mg in foods is the addition of exogenous phytase in whole-wheat products [21]. Recent publications described the development of new microbial phytases with improved thermostability and optimum pH much closer to the pH range obtained during yeast fermentation [22]. However, this microbial phytase supplementation is not permitted for human food in many countries and it seems easier and more natural to use sourdough fermentation in order to stimulate Mg availability in bread.

Breadmaking using sourdough increases Mg bioavailability

Bread has the advantage of conjugating the vegetal (from cereals) and microorganism (yeast or/and lactic acid bacteria) phytate-degrading enzymes. Leavening of bread reduces PA and improves mineral absorption. Thus, in Iran and Turkey, Ca, Zn and Mg deficiencies have been observed when people consume non fermented whole cereal products, whereas mineral status has been reported to be normal in people consuming leavened bread [23]. A lactic acid fermentation of PA-rich foods (bread, etc.) allows the release of Mg from vegetal matrix and leads to a better Mg solubility [24]. In parallel, it must be underlined that lactic acid bacteria isolated from sourdough have the ability to degrade PA [25] and thus the destruction of PA by micro organisms occurs during sourdough bread making [26]. Bread making using baker’s yeast contributes to PA degradation. Although a PA decrease was detected during bread making assigned to yeast phytase activity, the main degradation of PA seems to be the result of activity by endogenous plant phytases present in the flour [27]. It must be noted that PA breakdown was less pronounced in yeast bread than sourdough bread. As the PA content in bread affects mineral assimilation, it appears coherent that Mg was less absorbed from yeast-fermented bread than from sourdough bread. Increased whole bread consumption should raise the intake of essential elements, as high mineral contents are found in wholewheat breads, particularly Mg [28].

Various physical and chemical factors affect mineral absorption, including particle size, water content, pH, temperature, and fermentation time. Flour granulometry is essential for mineral bioavailability: a reconstituted wholewheat flour (white flour + bran) reduces Mg absorption in rats whereas the grain from the same variety that is ground in order to obtain a particle size between white flour and bran did not alter Mg absorption in rats. Thus, the particle size of flour may play a role in Mg assimilation in experimental animals [29]. Furthermore, soaking is important during bread making, because it activates endogenous vegetal phytase. Thus, a high water content of dough increases PA hydrolysis, and phytate reduction in doughs made of coarse meal from wheat and rye is lower than that made of the corresponding flours [30]. To increase PA destruction and mineral bioavailability in whole bread, dough pH has been suggested as the main determining factor [31]. Solubilities of the phytic acid chelates with cations depend on the pH and the amounts and type of cations. The limiting factor for phytate destruction in whole-wheat dough above pH 6 is the insolubility of its Mg salt, whereas at pH 5 the limiting factor appears to be the activity of phytase [32]. Moreover, in some circumstances, calcium ions can play a role in preventing PA disappearance during baking and it has been shown that the addition of milk-derived calcium inhibits phytate hydrolysis [33]. On the other hand, it has been found that fermented milk did not inhibit phytate degradation to the same extent [34] . Possible explanations are that lactic acid present in fermented milk increased the solubility of Ca phytate, or that the lower pH in dough containing fermented milk was close to the optimum pH of phytase compared to that in the dough made with regular milk. The optimum pH for PA hydrolysis of wheat is 4.5 - 5.0 and the optimum temperature is 55 °C. Thus, the acidification of dough by lactic acid bacteria associated with a long fermentation time significantly enhances the phytate hydrolysis. PA breakdown during bread making by rapid processes is indeed less extensive than after a long fermentation process. If bread has a high phytate or a low Mg content, increasing the rising time may result in a considerable improvement in mineral availability [35]. If all these parameters are optimised to increase PA breakdown, increased consumption of whole products may contribute to increase mineral intake, without compromising their bioavailability.

Conclusion

Significant Mg bioavailability improvement in bread could be supplied by a choice of technologically and nutritionally suitable cereal raw materials, if this potential is preserved or enhanced by the milling and baking processes. Improvement of Mg content of wheat grain was proven possible by traditional plant selection. Today, the potential Mg content of white bread could be improved by 10 fold and its total bio-accessibility increased by adapted baking practices. Sourdough fermentation was more efficient than yeast fermentation in reducing PA content in bread and only sourdough fermentation reduces the pH of the dough. The lower pH, due to organic acid production by the sourdough microflora, may be optimal for the endogenous phytase activity present in whole-grain flour and PA destruction in sourdough bread may be the resulting effect of both vegetal and microbial phytase activities.

As Mg absorption is mainly influenced by Mg solubility [35], it can be concluded that sourdough fermentation improves Mg bioavaibility and that the overall effect includes the effect of pH on wheat phytase and on solubility of cation complexes. However, PA may be desirable for its potential ability to prevent or delay various health disorders. Many studies designed to completely hydrolyse phytates by means of more acidic conditions of fermentation do not take into consideration the potential health benefits of PA in the diet. Furthermore, most consumers dislike the acidic taste of sourdough breads. It must be noted that a slight acidification does not affect the sensory properties of the bread (pH 5) and effectively reduces the PA content. As mixed starters with both lactic acid bacteria and yeast are recommended, an aromatic proportion of sourdough with baker’s yeast could be a good compromise to achieve breads with high mineral bioavailability.

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