Total and soluble contents of calcium, magnesium, phosphorus and zinc in yoghurts

Abstract

This paper examines the content of major minerals (calcium, magnesium, phosphorus and zinc) and its distribution between soluble (non-sedimentable) and micellar fractions of 16 commercial yoghurts from five different branches. These elements were determined by atomic absorption spectrometry after mineralisation by dry ashing. Total mineral contents showed wide intervals of variation (calcium 1090–2050 mg l−1, magnesium 101–177 mg l−1, phosphorus 878–1560 mg l−1 and zinc 4.0–7.3 mg l−1) due to the addition during manufacturing of different dairy products or fractions. Most of the minerals were found in the non-sedimentable fraction. Practically all calcium was measured in the supernatants of ultracentrifugation. Lower proportions of magnesium and zinc were determined in the non-sedimentable fraction (between 87 and 96%) whereas the lowest ones (63–77%) were found for phosphorus.

Full text

Analytical, Nutritional and Clinical Methods
Total and soluble contents of calcium, magnesium, phosphorus and
zinc in yoghurts
Miguel Angel de la Fuente
a
, Fernando Montes
b
, Gonzalo Guerrero
a
, Manuela Jua
´rez
a,
*
a
Instituto del Frı
´o (CSIC), Ciudad Universitaria s/n, 28040 Madrid, Spain
b
Departamento de Ciencias Analı
´ticas, Facultad de Ciencias (UNED), Senda del Rey 9, 28040 Madrid, Spain
Received 23 May 2002; received in revised form 20 October 2002; accepted 20 October 2002
Abstract
This paper examines the content of major minerals (calcium, magnesium, phosphorus and zinc) and its distribution between
soluble (non-sedimentable) and micellar fractions of 16 commercial yoghurts from five different branches. These elements were
determined by atomic absorption spectrometry after mineralisation by dry ashing. Total mineral contents showed wide intervals of
variation (calcium 1090–2050 mg l
1
, magnesium 101–177 mg l
1
, phosphorus 878–1560 mg l
1
and zinc 4.0–7.3 mg l
1
) due to the
addition during manufacturing of different dairy products or fractions. Most of the minerals were found in the non-sedimentable frac-
tion. Practically all calcium was measured in the supernatants of ultracentrifugation. Lower proportions of magnesium and zinc were
determined in the non-sedimentable fraction (between 87 and 96%) whereas the lowest ones (63–77%) were found for phosphorus.
#2002 Elsevier Science Ltd. All rights reserved.
Keywords: Yoghurt; Calcium; Magnesium; Phosphorus; Zinc
1. Introduction
Yoghurts are gaining in popularity due its accept-
ability for the consumers as well as their nutritional
properties and potentially beneficial effects in human
health. There is currently considerable growth in indus-
trialised countries in the economical importance of
yoghurts. In the last few years, this tendency has driven
the manufacturers to develop and produce a wide vari-
ety of these products with different characteristics.
Yoghurt can be a good source of essential nutrients as
minerals in the human diet. It could contribute sig-
nificantly to the recommended daily requirements for
calcium and magnesium to maintain the physiological
processes. Yoghurts are also a good dietary source of
phosphorus (besides calcium, considered the most
important nutrient for bone health) and its contribution
to total phosphorus intake has been reported as
30–45% in western countries (Flynn & Cashman, 1997).
Other key nutrients supplied would include zinc.
Analysis of total content of mineral in yoghurts
have been carried out (Buttriss, 1997; Kim & Choi,
1993) and studies of mineral composition of milk
fruit-added yoghurts (Moreno-Rojas, Sa
´nchez-Segarra,
Garcı
´a-Martı
´nez, Gordillo-Otero, & Amaro-Lo
´pez,
2000; Sa
´nchez-Segarra, Garcı
´a-Martı
´nez, Gordillo-
Otero, Dı
´az-Valverde, Amaro-Lo
´pez, & Moreno-Rojas
2000) and fermented milks fortified with minerals
(Hekmat & McMahon, 1998; Pirkul, Temiz, & Erdem,
1997) can also be found in the literature.
However, it is now generally recognised that mineral
absorption does not depend solely on the amount of the
element present in the dairy product but also on other
factors such as solubility (Delisle, Amiot, & Dore
´,
1995). Mineral availability in dairy products is affected
by the nature of the complex. The chemical form of the
nutrient may influence bioavailability: free or soluble
form are well absorbed, whereas those that are bound
could be poorly. Technological treatments used in the
processing of dairy products are known to modify the
proportions of its various chemical forms (De la Fuente,
1998). Bacterial production of lactic acid from lactose of
milk is an essential step in yoghurt manufacture. Low-
ering pH causes important alterations in the composi-
tion, structure and reactivity of casein micelles and
0308-8146/03/$ - see front matter #2002 Elsevier Science Ltd. All rights reserved.
PII: S0308-8146(02)00505-8
Food Chemistry 80 (2003) 573–578
www.elsevier.com/locate/foodchem
* Corresponding author. Tel.: +34-91-544-5607; fax: +34-91-549-
3627.
E-mail address: mjuarez@if.csic.es (M. Jua
´rez).

modifying the mineral equilibrium. The acid nature of
yoghurt would also have positive effects on the gastro-
intestinal absorption of calcium from milk.
Yoghurt manufacture may result in the redistribution
of nutrients as mineral, mainly those associated with
caseins. Changes in this distribution may have effects on
nutritional properties. Therefore, their occurrence in
yoghurts is of particular concern in view of the
demanding quality standard that this product must
meet with respect to nutrition. However, no studies
have been carried out to evaluate the extent and nature
of mineral redistribution arising from yoghurt proces-
sing. This paper was undertaken to determine the parti-
tion of calcium, magnesium, phosphorus and zinc
between micellar and non-sedimentable phases in a wide
spectrum of yoghurts commercialised in the market as a
contribution to improve the knowledge and the nutri-
tional characteristics of these of dairy products.
2. Materials and methods
2.1. Samples and reagents
Sixteen yoghurts made of milk with different fat con-
tent (0.1–5.5%), belong to five different brands were
purchased in local markets. One of them (sample 16)
was manufactured from goat’s milk. In all cases sodium
azide was added as preservative (0.1 g l
1
). High purity
water with a resistance of 18cm was used to prepare
all samples and standards. All reagents used were of the
highest purity available and at least of analytical grade.
2.2. Apparatus
The determination of potassium and sodium was car-
ried out by atomic emission spectrometry using a model
5100PC atomic absorption spectrometer (Perkin-Elmer,
Norwalk, CT, USA) in an air–acetylene flame. Calcium,
magnesium and zinc were determined by atomic
absorption spectrometry with the same instrument using
a multi-element (Ca–Mg–Zn) hollow-cathode lamp.
Phosphorus was measured using an UV–visible
spectrophotometer, model Lambda 15 (Perkin-Elmer,
Norwalk, CT, USA).
2.3. Methods of analysis
Total solids were determined according to FIL-IDF
(1991). The non-sedimentable or soluble fraction was
separated by high speed centrifugation. Thirty grams of
yoghurt was centrifuged at 100,000 gusing a 50-RT-1250
rotor at 20 C in an ultracentrifuge (Sorvall Combi Plus,
Wilmington, DE, USA). The supernatant fluid was care-
fully removed and filtered through Whatman 40 paper. It
was then stored for analysis at 5 C before digestion.
Samples (yoghurts and its supernatants) were miner-
alised by dry ashing in a muffle furnace. Five gram
samples were weighed into a porcelain crucible and
dried on a hot plate. After charring, samples were
incinerated in a muffle furnace at 450 C for 24 h. If
necessary, the ash was bleached by treatment with
HNO
3
and heating in the muffle furnace for 1 h. Finally,
the ashes were diluted with concentrated nitric acid and
distilled water and measured by atomic absorption.
Calcium, magnesium, sodium, potassium and zinc
were measured in the digested samples by flame atomic
absorption in the conditions specified by De la Fuente
and Jua
´rez (1995a). Phosphorus was determined by
visible spectrophotometry at 750 nm by the molybde-
num blue method according to De la Fuente and Jua
´rez
(1995b). All analysis were performed in triplicate.
3. Results and discussion
3.1. Total content of minerals
Total and non-sedimentable calcium, magnesium,
phosphorus and zinc contents in yoghurts can be seen in
Table 1. Total mineral content showed wide intervals of
variation (calcium 1090–2050 mg l
1
, magnesium
101–177 mg l
1
, phosphorus 878–1560 mg l
1
and zinc
4.0–7.3 mg l
1
). There are numerous factors which
affect yoghurts chemical composition, mainly the methods
of fortification used to increase the solid content. This is
a common practice during yoghurt manufacture. A
wide range of total solids and other minerals (sodium
and potassium) was also found in the yoghurts studied
(Table 2) indicating the possible addition of different
dairy fractions or products. Although, whey protein
concentrates, milk protein concentrate or caseinates
have been successfully assayed (Guzma
´n-Gonza
´lez,
Morais, & Amigo, 2000; Guzma
´n-Gonza
´lez, Morais,
Ramos, & Amigo, 1999) the most common approach in
the industry is the utilisation of milk modified by the
addition of skim milk powder. Yoghurt 4 had the high-
est content in calcium, magnesium, phosphorus and
zinc. At the same time it showed very high levels in
sodium and potassium either. This would indicate the
enrichment of the raw milk with dairy additives abun-
dant in these minerals as milk powders.
Although other samples (1, 5, 11 and 15) have mineral
concentrations similar to the generally reported for raw
milk, most of the yoghurts showed higher contents in
these nutrients, suggesting the possible addition of
dairy ingredients. This supply can represent an advan-
tage from a nutritional point of view as a source of
essential nutrients in diet in comparison with other
dairy products. Moreover yoghurt could act as an
alternative source of mineral for sufferers of lactose
intolerance.
574 M.A. de la Fuente et al. / Food Chemistry 80 (2003) 573–578

The mean concentrations of the minerals studied in
this work were not affected by the different fat content
(Table 2). Although a very important fraction of other
minerals (copper and iron) is linked to fat globule, any
of the elements studied in the present work has been
reported in high percentage bound to dairy lipids (Flynn
& Cashman, 1997).
3.2. Percentage of non-sedimentable minerals
The physico-chemical changes of the casein micelles
brought about by acidification due to biotransfor-
mation of lactose to lactic acid are reflected in changes
in the salt balance.
3.2.1. Calcium and phosphorus
The percentage of non-sedimentable calcium ranged
from 96.7 to 99.1% whereas the levels of phosphorus
detected in the supernatants were within the interval of
63.2–77.5% (Fig. 1).
Table 1
Total and non-sedimentable contents (meanstandard deviation) of calcium, magnesium, phosphorus and zinc in commercial yoghurts
a
Sample mg l
1
Ca Mg P Zn
Total Soluble Total Soluble Total Soluble Total Soluble
1 11705 1147 10 115 3 101 3 899 10 697 7 4.70.1 4.4 0.1
2 152238 1472 7 144 7 128 1 1178 15 825 8 5.30.1 5.0 0.1
3 147449 1454 48 131 1 127 1 1140 3 801 2 4.60.1 4.3 0.1
4 205037 2003 7 177 1 167 1 1560 14 1089 10 7.3 0.3 6.9 0.1
5 10888 1068 18 101 1951 87815 6139 4.80.4 4.5 0.1
6 131434 1274 17 129 2 124 2 1157 26 822 12 5.40.2 5.1 0.2
7 180763 1780 8 136 3 126 2 1391 16 987 1 5.90.1 5.1 0.2
8 15606 1530 5 141 2 134 1 1283 61 952 8 5.90.1 5.5 0.4
9 154040 1520 10 137 3 133 1 1328 17 911 11 5.20.1 4.9 0.3
10 15347 1513 11 132 2 127 2 1326 20 927 10 5.20.1 5.0 0.1
11 10908 1080 2 112 3 101 1 1006 1 675 10 4.50.1 4.2 0.1
12 14004 1380 5 118 2 114 1 1058 10 792 11 4.80.1 4.6 0.1
13 166020 1640 40 124 1 109 1 1222 2 793 8 5.90.1 5.5 0.3
14 148028 1459 12 114 1 105 1 1181 32 746 40 4.60.1 4.4 0.2
15 113020 1110 10 123 2 108 1 901 23 603 8 4.30.5 4.0 0.3
16 131030 1290 3 123 2 108 1 952 6 665 17 4.00.1 3.7 0.1
a
Each value is the average of three analysis and triplicate determinations.
Fig. 1. Intervals of variation of non-sedimentable calcium, magne-
sium, phosphorus and zinc in commercial yoghurts.
Table 2
Total solids, fat, sodium and potassium (mean standard deviation) in
commercial yoghurts
Sample Total solids
(%)
Fat labelled
(%)
K
a
(mg l
1
)
Na
a
(mg l
1
)
1 10.1 3.1 16416 476 14
2 9.9 0.1 199012 637 14
3 13.0 3.9 199029 652 36
4 12.8 0.1 263019 766 7
5 11.0 3.9 154710 591 9
6 7.8 0.1 23258 766 2
7 11.4 0.1 202810 658 2
8 12.5 2.0 227537 716 19
9 12.6 2.1 233854 777 3
10 10.6 0.1 223025 768 5
11 11.3 2.2 181220 752 12
12 10.3 0.1 207439 746 9
13 16.9 3.8 16963 605 11
14 12.6 3.4 207125 654 14
15 11.6 3.1 158237 604 14
16 12.2 5.5 162838 558 2
a
Each value is the average of three analysis and triplicate
determinations.
M.A. de la Fuente et al. / Food Chemistry 80 (2003) 573–578 575

At pH 6.7, in raw milk, approximately two thirds of
the calcium are associated with casein micelles and
being sedimentable after centrifugation. However, dur-
ing bacterial acidification changes in micellar calcium
and phosphorus take place. As the milk pH decreased
from pH 6.7 to 4.0 the amount of calcium and phos-
phorus associated with the micellar proteins decreases
while an increase of calcium and phosphorus in the
serum milk can be observed (Dalgleish & Law, 1989;
Gastaldi, Lagaude, & Tarodo de la Fuente, 1996; Le
Graet & Brule
´, 1993; Van Hooydonk, Hagedoorn, &
Boerrigter, 1986). Previous studies (Dalgleish & Law,
1989; Le Graet & Brule
´, 1993) have shown that the dis-
sociation of calcium and phosphate from the casein
micelles is sigmoidal in shape as the milk is acidified.
This decrease is relatively slow until about pH 6.0–5.8
and then became faster. At pH 5.1 most of the micellar
inorganic phosphorus was solubilised, whereas about
17% of the calcium was still present in the casein
micelles (Gastaldi et al., 1996). Dalgleish and Law
(1989) even at pH 4.9 estimated that 1 mM calcium was
sedimentable while Hekmat and McMahon (1998)
found at pH 4.5 small amounts of calcium remaining in
the pellet after ultracentrifugation. Le Graet and Brule
´
(1993) also observed solubilisation of calcium remaining
amounts (245 mg l
1
) within the region at pH 5.2–3.5.
The remaining sedimentable calcium levels at pH
below 5.0 have been attributed to the adsorption of
calcium directly to the casein molecules (Dalgleish &
Law, 1989; Le Graet & Brule
´, 1993). Decreasing of pH
below 5.0 causes the calcium phosphate to dissolve but
also removing the calcium directly bind to casein which
is not bound to phosphate. Most of the remaining sedi-
mentable calcium levels calculated in the present study
for yoghurts therefore they could be ascribed to calcium
bound to casein without being involved in calcium
phosphate formation.
Phosphorus had the lowest percentages of non-sedi-
mentable minerals in yoghurts (Fig. 1). Micellar phos-
phorus calculated represents the covalently bound
phosphate of the phosphoserine groups of caseins. In
cow’s milk, about 25% of phosphorus in milk is asso-
ciated with caseins in the micelles as calcium phosphate,
whereas 25% occurs as organic phosphate esterified to
casein. The another half is soluble mainly as free phos-
phate ions. The organic phosphate esterified to casein
would not removal when pH is decreased during
yoghurt manufacture and would stay in the pellet after
ultracentrifugation.
Although milk calcium absorption in vivo is con-
trolled by complex homeostatic mechanisms and this
matter is still subjected to controversy, different studies
have suggested that calcium in a soluble form would be
a prerequisite for its better absorption in the gastro-
intestinal tract. Delisle, St-Amand, Gosselin, Pichette,
and Amiot (1993) postulated that the high content in
ionic calcium generated in yoghurts during simulated
gastro-intestinal digestion could be an index of high
bioavailability of this dairy product. In that case, the
high content of non-sedimentable calcium in yoghurts
may represent an advantage from a nutritional point of
view.
On the other hand, calcium phosphate can form
insoluble precipitates from which calcium can not be
absorbed. Casein phosphopeptides, formed during the
digestion of caseins, have a positive effect on calcium
absorption because of their ability to bind calcium and
maintain it in a soluble form in the intestinal lumen, and
therefore available for absorption. Although infor-
mation available from human is still scarce, numerous
animal studies have shown that phosphopetides enhance
the absorption of calcium in the intestine (FitzGerald,
1998; Jovanı
´, Barbera
´, & Farre
´, 2001). The use of milk
powders as enrichment vehicles in yoghurt manufacture
could increase such phosphopeptides to enhance cal-
cium absorption.
The real significance that any of the above would have
on calcium absorption and human nutrition is still a
matter of study. However, it would seem evident that
the choice of fortifier agent could have consequences on
calcium bioavailability and, therefore, on the yoghurt
nutritional quality.
3.2.2. Magnesium
Between 88 and 97% of total magnesium in yoghurt
was non-sedimentable (Fig. 1). In cow’s milk 65% of
magnesium is in a soluble form while the remainder is
colloidal associated with the casein micelles (about half
associated with colloidal calcium phoshate and half
bound directly to phosphoserine residues in caseins)
(Flynn & Cashman, 1997).
This micellar magnesium is progressively released as
the pH was decreased from 6.7 to 4.9 (Dalgleish & Law,
1989). At pH 4.9, the lowest pH which was used by
those authors, there was still some magnesium remain-
ing on the casein. It appeared from Dalgleish and Law
(1989) results that the behaviour of the small amount of
micellar magnesium paralleled that of the calcium. Le
Graet and Brule
´(1993) also remarked the similarity of the
magnesium solubilisation with the calcium and deter-
mined that the remaining micellar magnesium (around
1/3) was only solubilised at pH between 5.2 and 3.5.
As for calcium, magnesium may bind to the non-
phosphorylated binding sites in the caseins. However it
has been suggested that magnesium occur in combination
with casein rather that with micellar inorganic phos-
phate (Van Hooydonk et al., 1986). This could help to
explain why lower percentages of magnesium than cal-
cium were found in the non-sedimentable yoghurt frac-
tion (Fig. 1). These percentages would correspond to
magnesium linked to non-phosphorylated binding sites
in the caseins.
576 M.A. de la Fuente et al. / Food Chemistry 80 (2003) 573–578

There is little information on the bioavailability of
magnesium from dairy products in humans. Apparent
absorption of magnesium in rats fed with different dairy
products varied widely (Deslisle et al., 1995). In skim
milk, milk powders and yoghurt magnesium absorption
was high (40–45%) whereas the lowest levels were found
in cheese (15%). A previous work (Pantako, Passos,
Desrosiers, & Amiot, 1992) showed that the onset of
magnesium absorption was faster with diets based on
caseins, mainly b-casein, compared to those based on
lactoserum proteins demonstrating the importance of
dairy additives in the magnesium bioavailability.
According to this, commercial yoghurts manufactured
with dairy ingredients enriched in caseins as fortifiers,
could potentially enhance magnesium absorption. How-
ever more studies should be carried out to confirm it.
3.2.3. Zinc
About 95% of the zinc in yoghurts was found in the
supernatants after ultracentrifugation (Fig. 1). This is in
contrast with the low level of this mineral in the soluble
phase in raw milk. Zinc in cow’s milk is primarily bound
to casein (90–95%), and only small amounts are
linked to whey proteins and low molecular weight
ligands in the serum (De la Fuente, Fontecha, & Jua
´rez,
1996; Shen, Robberecht, Van Dael, & Deelstra, 1995;
Singh, Flynn, & Fox, 1989).
Singh et al., (1989) documented that non-micellar zinc
levels increased when the pH of milk was reduced before
ultracentrifugation so that 95% of the zinc was non-
sedimentable at pH 4.6. Within the casein micelles, one-
third of the zinc is loosely bound to casein phosphoserine
residues, whereas two-thirds are more tightly bound to
colloidal calcium phosphate. Most of the zinc directly
bound to casein is readily removed when pH decrease to
low values. It was inferred that the more tightly bound
zinc fraction in skim milk was largely that associated
with colloidal calcium phosphate. Nevertheless at pH
4.5, as we mentioned above, virtually all calcium phos-
phate has been solubilised. Consequently the remaining
sedimentable zinc calculated in yoghurts should be
attributed to the fraction bound directly to casein
phosphoserine residues.
It is well known that binding of a significant fraction
of the zinc in human milk to a low molecular weight
zinc-binding ligand may enhance zinc absorption either
by facilitating zinc transport across the gastrointestinal
tract wall or by preventing the sequestration of zinc
by other substances in the gastrointestinal tract that
reduces its availability for absorption. On the contrary,
the binding of a large fraction of zinc in cow’s milk
to casein may result in the entrapment in casein
curds formed in the stomach which may be incom-
pletely digested in the small intestine, thus rendering a
significant proportion of the zinc unavailable for
absorption.
Nowadays, it is not well clarified if the chemical form
of zinc in dairy products can represent an advantage
from a nutritional point of view. Few studies have been
specifically devoted to the estimation of the bioavail-
ability of zinc in different dairy products. However, it
does not seem likely that zinc absorption from yoghurt
were reduced in comparison to raw milk. Fermentation
of milk with Staphylococcus thermophilus or Lacto-
bacillus bulgaricus to yield yoghurt significantly
increased zinc availability (12.5%) compared with raw
milk (Van Dael, Shen, & Deelstra, 1993). Bobilya,
Ellersieck, Gordon, and Veum (1991) showed that zinc
was absorbed and retained as well from nonfat dry milk
as lowfat plain yoghurts in diets fed to neonatal pigs.
The low pH of yoghurt would facilitate the high levels
of soluble zinc bound to low-molecular weight ligands.
Such ligands may enhance zinc absorption either by
facilitating zinc transport across the gastrointestinal
tract wall or by preventing the chelation of zinc by other
substances in the gastrointestinal tract, which would
lower its availability for absorption (Shen et al., 1995).
Moreover, milk acidified to pH 4.6 and then readjusted
to pH 6.7, simulating conditional of gastrointestinal
tract, contained significantly more non-sedimentable
zinc than untreated skim milk (50%) (Singh et al.,
1989). Although a positive correlation between high
content in soluble form and absorption is far to be
completely demonstrated and more research is required,
the consumption of yoghurt as a potential source of zinc
more easily available in the diet should not be left aside.
4. Conclusions
High concentrations of minerals detected in the pre-
sent study in most of the samples confirmed the role of
yoghurts as source of essential nutrients in comparison
with raw milk. Moreover, this food could represent an
excellent alternative to milk for lactose intolerant
population. The distribution of minerals (calcium,
magnesium, phosphorus and zinc) in yoghurts differed
dramatically from those of milk showing that elements
associated with casein were redistributed during manu-
facturing. The noticeable increase in the levels of non-
sedimentable minerals could favour the absorption of
these nutrients in the gastrointestinal tract. However the
implications of these findings for nutritional properties
should be investigated further.
Acknowledgements
The authors acknowledge the financial support for
this research project (AGL2000-0727-C03-02) furnished
by the Comisio
´n Interministerial de Ciencia y Tecnologı´a
(CICyT).
M.A. de la Fuente et al. / Food Chemistry 80 (2003) 573–578 577

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