Calcium intake is weakly but consistently negatively associated with iron status in girls and women from six European countries. A cross-sectional study of over 1,000 girls and 500 women found that higher calcium intake was associated with lower levels of serum ferritin, a marker of iron stores, after adjusting for potential confounding factors. A consistent inverse association was seen between calcium intake and serum ferritin in both girls and women, regardless of whether calcium was consumed simultaneously with iron. The study suggests that higher dietary calcium intake is weakly negatively associated with blood iron status in girls and women.
2. 964 VAN DE VIJVER ET AL.
between calcium intake and iron status in the CALEUR study, mean level of 3.3 g/L and for analysis of serum iron the variation
a large cross-sectional study among girls and women in six coefficient was 1.8% at a mean value of 18 mol/L in the quality
European countries. (Kardinaal et al. 1999) control sample.
Blood samples were available for 1,083 girls and 525 women. In a
selection of samples with extremely high or low ferritin levels (ferritin
MATERIALS AND METHODS 3.0 or 10.0 g/L), duplicate measurement was performed. When
the second measurement was comparable to the first measurement,
The CALEUR study was conducted in Denmark, Finland, France, the first value was used. Samples of four subjects (three girls and one
Italy, The Netherlands and Poland, initially to study the association woman) were excluded from statistical analyses because of instability
between calcium intake and peak bone mass (Kardinaal et al. 1999). of the sample, leaving data for 1,080 girls and 524 women for analysis.
In each of the participating countries, girls aged 11–15 y and young Statistical analyses. Mean and SD of serum iron, serum ferritin,
adult women aged 20 –23 y with high and low calcium intake were serum transferrin and transferrin saturation and of dietary intake
selected from random population samples of about 750 girls and 375 levels were calculated. Pearson correlations between potential con-
women. All subjects were of Caucasian origin. In Finland (Oulu), founding factors and calcium intake and parameters for iron status
Denmark (Aarhus), Poland (Warsaw) and The Netherlands (Zeist), were calculated. As potential confounders, age, height, weight, men-
random samples from the local population registries were obtained ses, smoking, tea and coffee consumption, alcohol consumption,
and subjects invited to participate; response rates varied from 25.4 to energy intake, protein intake and vitamin C intake were considered.
51.5% for girls and from 28.6 to 62% for women. In France, girls and Variables associated with calcium intake and serum ferritin levels or
women were recruited via general practitioners and gynecologists in transferrin saturation were included as a covariable in the statistical
two geographical areas, Rhone-Alps and Marseille; in Italy, girls were models with serum ferritin or transferrin saturation as independent
recruited from all eight secondary schools in the town of Rende, and variables. Categorical variables were put into the model as dummy
women from the University of Calabria (response rates were 100%). variables. Though the covariables were not significantly associated
Of those selected, the participation rate varied between 64 and 84% with all the parameters of iron status, we choose to use a fixed set of
for girls and between 52 and 91% for women: data were collected for covariables in the statistical models. With analysis of covariance,
1,116 girls and 526 women. The study was approved by local medical- mean levels of the serum iron parameters were calculated per quartile
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ethical committees, and all participants (and their parents, if re- of calcium intake, adjusted for the covariables. Linear regression
quired) gave their informed consent. Subjects were excluded when analysis was used to calculate the effect of calcium intake on serum
indicating a chronic disease in general, diseases related to bone or levels overall and per country, unadjusted and adjusted for covari-
calcium metabolism in particular, use of corticosteroids, participating ables. The influence of the simultaneous intake of iron and calcium
in sports more than 7 h/wk, current or prior pregnancy, menstruation during a meal was measured by dividing calcium intake into calcium
at irregular intervals (for the women only), vegetarianism or macro- ingested simultaneously with iron and the remaining calcium. Simul-
biotism or a prescribed diet other than an energy-restricted diet. taneous intake of iron and calcium was defined as a moment of the
Dietary intake. To estimate calcium intake in a comparable way day when at least 20% of the total daily iron and at least 20% of the
in the six countries, a 3-d food record method was used. The subjects total daily calcium was consumed. For statistical analysis the BMDP
were asked to record everything they consumed during a consecutive statistical package was used (BMDP version 7.0; BMDP Statistical
Wednesday, Thursday and Friday, the week before their visit to the Software Inc., Los Angeles, CA). P values 0.05 were considered
institute. Time of day, food, quantity and recipes of composite dishes significant.
were recorded. The parent responsible for meal preparation was asked
to assist in completing the food records. At the visit to the institute,
the food records were checked by a dietitian for completeness; house- RESULTS
hold measures were verified by comparison with standard measures.
Daily consumption of food products in grams were converted to The study sample included girls with a mean age of 13.5
nutrient intake using local food composition tables. Mean intakes of 1.5 y (37.8% were premenarcheal) and women with a mean
calcium, iron and energy were calculated as the average over 3 d. age of 22.0 1.1 y. Use of oral contraceptives was reported by
Height and weight were measured with the subjects wearing light 1.0% of the girls and 48.1% of the women. Smoking was
clothing and no shoes. Subjects completed a self-administered ques-
tionnaire on menstrual function and use of oral contraceptives, smok-
reported by 7.0% of the girls and 29.4% of the women.
ing habits, alcohol use, time spent outdoors, height, weight and The ranges for (serum iron, serum ferritin, serum transferrin
education of parents and physical activity. Physical activity was and the transferrin saturation) the different countries were
determined for the previous month and covered activities at school, comparable (Table 1). For the pooled data, serum iron ranged
at work and in leisure time (sports and household activities). For the from 2.9 to 46.8 mmol/L for girls and from 2.1 to 45.1 mmol/L
girls, the questionnaire comprised 58 items, and for the women 88. for women. Ranges for serum ferritin and serum transferrin
The questionnaire was checked in an interview setting. were 2.3–161.1 g/L and 2.0 –5.3 g/L, respectively, for girls
A 10-mL blood sample was drawn from nonfasting subjects in a and 1.1–191.6 g/L and 2.1–5.5 g/L, respectively, for women.
10-mL tube with clot activator and cooled to 4°C. Serum was Transferrin saturation ranged from 3.4 to 60.3% for girls and
prepared within 2 h by centrifugation at 3000 g for 10 min. Serum from 3.0 to 63.3% for women, with the lowest levels in Italy
was stored at 20°C. Serum ferritin was measured as the main marker
for iron status. Serum ferritin levels reflect stored iron. Serum iron
and the highest in Denmark. The lowest levels of serum iron
and the main iron-binding protein, transferrin, reflect the iron in and serum ferritin were seen in Finland, both for girls and
transit and were used to calculate the transferrin saturation {(trans- women. Low-serum iron and ferritin levels were also seen in
ferrin saturation (%) iron (g/L)/[transferrin (g/L) 1.41)]} (Wick Italian women. Latent iron deficiency (ferritin 12 g/L) was
1996). Transferrin saturation can be used as a short-term marker of found in 4.3% of the girls and 7.4% of the women (Fig. 1).
iron concentration (Wick 1996). Serum iron, transferrin and ferritin Calcium intakes of both girls and women were lowest in
were measured with the Hitachi 911 (Boehringer Mannheim, Mann- Italy and highest in Finland (Table 2). Intakes in The Neth-
heim, Germany). Ferritin and transferrin were analyzed immunotur- erlands, Finland and Denmark were all relatively high. The
bidimetrically with a ferritin test kit (No. 1661400; Boehringer lowest iron intakes were in Italy, whereas girls and women in
Mannheim) and a transferrin test kit (No. 1360752; Boehringer Poland had the highest iron intakes.
Mannheim). Serum iron was analyzed after separation of Fe3 from
transferrin. After reduction, Fe2 forms colored complexes with To assess the association between calcium intake and serum
FerroZine™ (Hach Chemical Co., Ames, IA). The coefficient of iron levels, the potential confounders age, height, weight,
variation for the analysis of serum ferritin was 8.1 and 3.9% at mean menses, smoking, tea and coffee consumption, alcohol con-
values of 30 and 60 g/L in the quality control samples, respectively. sumption, energy intake, protein intake and vitamin C intake
The variation coefficient for analysis of transferrin was 2.5% at a were first considered. Inverse associations between serum fer-
3. CALCIUM INTAKE AND IRON STATUS 965
TABLE 1
Serum iron, ferritin and transferrin concentrations and transferrin saturation of girls and women from several European countries1
n Ferritin Iron Transferrin Transferrin saturation
g/L mol/L g/L %
Girls
The Netherlands 165 35.2 16.3 16.5 5.3 3.45 0.45 19.4 7.1
Finland 190 28.3 16.1 13.7 5.7 3.38 0.43 16.6 7.9
Denmark 165 38.2 21.3 17.6 6.3 3.31 0.40 21.5 8.2
Italy 197 33.4 21.4 15.2 6.1 3.78 0.51 16.4 7.1
France 167 36.4 19.6 15.4 5.7 3.36 0.43 18.6 7.5
Poland 196 36.1 17.9 16.6 6.4 3.51 0.43 19.1 7.8
Overall 1080 34.5 19.1 15.8 6.1 3.47 0.47 18.5 7.8
Women
The Netherlands 96 47.0 38.1 17.9 7.7 3.93 0.59 18.5 8.2
Finland 82 29.7 25.3 14.4 8.7 3.39 0.62 17.6 11.4
Denmark 77 50.2 36.4 19.4 7.8 3.67 0.66 21.5 9.2
Italy 99 33.1 19.2 14.4 5.8 3.47 0.51 16.9 7.1
France 74 39.6 30.2 17.3 7.7 3.69 0.53 19.1 8.5
Poland 96 42.2 26.9 18.0 6.4 3.43 0.49 21.1 7.5
Overall 524 40.2 30.5 16.9 7.5 3.59 0.60 19.1 8.8
1 Values are means SD.
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ritin and age and between serum transferrin and vitamin C women, respectively, P 0.05). After adjustment was made
intake were observed. Age, weight, height, protein intake and for the set of covariables, the adjusted linear regression coef-
energy intake were positively associated with serum trans- ficient for the pooled data was 0.57 0.20 for girls. This
ferrin. Calcium intake was positively associated with age, means that for every 100-mg/d increase of calcium intake the
height, energy intake, protein intake and vitamin C intake. ferritin level is reduced by 0.57 g/L. For an average ferritin
In Table 3 the mean levels of serum iron, ferritin, trans- level of 34.5 g/L, this means a reduction in ferritin level of
ferrin and transferrin saturation per quartile of calcium intake 1.6%. For women a linear regression coefficient of 1.37
are presented. The means were adjusted for a fixed set of 0.46 was found, i.e., a reduction in ferritin concentration of
covariables, age, country, tea, protein, vitamin C and iron 3.3% for every 100-mg/d increase in calcium intake at an
consumption and for menses (in girls only). Adjusted means average ferritin level of 40.2 g/L. Calculation of the associ-
differed significantly between quartiles of calcium intake for ation for each country separately revealed a consistent inverse
transferrin levels in girls and serum iron and transferrin satu- association between calcium intake and serum ferritin, even
ration in women. though in none of the countries this association reached
Linear regression modeling was used to assess the contribu- significance. When transferrin saturation as a measure of
tion of various independent variables of influence to serum short-term iron concentration was put in the model as the
iron status. Calcium intake was not associated with serum dependent variable, we found a significant adjusted inverse
levels of iron or transferrin. For the main indicator of iron regression coefficient for the girls of 0.18 0.08 per 100-
status, serum ferritin, the linear regression coefficients are mg/d increase of calcium. The regression coefficient calculated
presented for the separate countries and for all countries for the separate countries showed only a significant inverse
pooled (Table 4). Both for girls and for women a significant association in Denmark. For women, no association was ob-
inverse association was found between calcium intake and served between calcium intake and transferrin saturation.
serum ferritin level (r 0.09 and 0.07 for girls and Several studies suggest that only the simultaneous intake of
calcium and iron leads to an inhibitory effect (Gleerup et al.
1993). Our linear regression model, adjusted for iron intake,
age, menarche, country, protein intake and vitamin C intake,
did not reveal a difference in inhibition between calcium
taken simultaneously with iron and the remaining calcium.
The two linear models in which the calcium variables were
separated neither revealed a significant association with cal-
cium taken with iron nor with the remaining calcium. The
contribution of the two calcium sources independent of the
other source was assessed by putting both calcium variables in
one regression model. In the adjusted model with serum fer-
ritin as the dependent variable, the linear regression coeffi-
cients for calcium-consumed simultaneously with iron and for
the remaining calcium were 0.56 0.25 and 0.58 0.22,
respectively, in girls and 1.34 0.56 and 1.37 0.50,
respectively, in women (P 0.05 for all values).
The dose dependence of the association between calcium
FIG. 1. Percentage of women and girls in each country with latent intake and serum ferritin levels was checked over strata of
iron deficiency (ferritin 12 g/L). calcium intake levels. A division was made between intake
4. 966 VAN DE VIJVER ET AL.
TABLE 2
Daily intake of calcium, iron and energy among girls and women in the pooled data and per country1
Calcium Iron Energy intake
Girls Women Girls Women Girls Women
mg MJ
The Netherlands 1083 379 1139 458 10.9 4.4 10.5 3.5 9.5 2.1 9.4 2.0
Finland 1227 512 1265 545 11.3 9.6 10.3 5.7 7.8 2.0 7.6 2.0
Denmark 1133 499 1263 596 10.7 11.1 10.3 6.8 8.0 2.1 8.1 1.9
Italy 680 302 609 279 8.2 2.6 8.0 2.9 7.8 1.9 8.2 1.9
France 950 381 887 335 10.9 4.3 10.4 2.7 8.6 2.2 8.8 1.9
Poland 937 400 829 364 13.0 6.5 12.4 5.6 8.8 2.3 9.8 2.3
Overall 992 449 988 504 10.8 7.0 10.3 5.0 8.4 2.2 8.7 2.2
1 Values are means SD.
levels of 300, 300 – 600, 600 –900, 900 –1200, and 1200 prudence is called for when using these data as a measure of
mg/d. No indication of a threshold effect was seen. None of intake for a specific country. Also, blood was collected accord-
the linear regression coefficients in the strata showed a signif- ing to the same protocol, and all blood samples were analyzed
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icant association between calcium intake and serum ferritin centrally in one laboratory.
levels. In all strata an inverse association was observed except Dietary assessment took place on three consecutive days.
for a positive linear regression coefficient in women with a From the Dutch National Food Consumption Survey, it was
calcium intake lower than 300 mg. No trend could be de- calculated that the day-to-day variation in calcium intake in
tected. The Netherlands was small (Van Erp-Baart 1996). A 3-d
dietary record could thus give a representative estimate of
DISCUSSION usual calcium intake. Day-to-day variation in iron is expected
In this cross-sectional study, performed in six European to be more pronounced and consequently the 3-d record is not
countries, a weak but consistent inverse association was seen likely to accurately reflect habitual individual intake. On the
between calcium intake and serum ferritin status, irrespective other hand, measurement of serum iron parameters variable is
of whether calcium was ingested simultaneously with iron. also exposed to biological and analytical variances. The con-
Further, no dose-response relationship between calcium intake sequence of these factors is that whenever an association really
and serum ferritin was detected. exists, the association is either not found, or it seems to be
The study was conducted in six countries throughout Eu- weaker than in reality.
rope, which contributed to a wide variety in intakes of both In this study dietary information was collected at differ-
calcium and iron. In each country, two groups of subjects were ent periods over the year for the separate countries. There-
recruited, a group of girls and a group of young women. To fore, comparison of intakes between countries can give a
ensure comparability of the data between groups and among biased view. Blood collection took place in the same pe-
countries, all procedures were similar. Because the study pop- riod as the dietary assessment was made. Because blood
ulations are not necessarily representative for the countries, levels reflect intake, seasonality plays only a minor role in
TABLE 3
Serum iron, ferritin and transferrin concentrations and transferrin saturation of girls and women per quartile of calcium intake1
Quartile 1 2 3 4
Girls2
n 268 271 268 271
Calcium intake, mg 462.0 7.5 766.0 4.2 1031.9 6.2 1686.9 24.9
Iron, mol/L 15.5 0.6 15.2 0.4 16.0 0.4 16.5 0.7
Ferritin, g/L 34.0 1.8 32.0 1.3 34.0 1.2 37.8 2.1
Transferrin,* g/L 3.55 0.04 3.54 0.03 3.45 0.03 3.35 0.05
Transferrin saturation, % 17.8 0.7 17.4 0.5 18.9 0.5 19.9 0.9
Women3
n 129 130 130 131
Calcium intake, mg 482.9 10.8 798.2 6.9 1081.6 9.3 1597.9 27.8
Iron,* mol/L 15.4 1.1 17.9 0.7 15.8 0.7 18.4 1.2
Ferritin, g/L 41.2 4.5 40.8 3.0 42.9 2.7 36.4 5.1
Transferrin, g/L 3.57 0.09 3.56 0.06 3.59 0.05 3.67 0.10
Transferrin saturation,* % 17.3 1.3 20.1 0.9 18.0 0.8 21.0 1.5
1 Values are means SEM.
2 Adjusted for age, menses, country, protein, vitamin C, tea, iron.
3 Adjusted for age, country, protein vitamin C, tea, iron. * Significant difference among the means, P 0.05.
5. CALCIUM INTAKE AND IRON STATUS 967
TABLE 4
Linear regression coefficients for calcium intake (per 100 mg) as predictor of serum ferritin level
Crude Adjusted1 Multivariate adjusted2
( SD)
Girls
The Netherlands 0.37 0.28 0.46 0.29 0.88 0.46
Finland 0.06 0.22 0.20 0.23 0.44 0.42
Denmark 0.28 0.28 0.32 0.29 1.94 0.53**
Italy 0.30 0.55 0.53 0.58 0.49 0.79
France 0.01 0.46 0.08 0.48 0.43 0.58
Poland 0.62 0.35 0.72 0.36 0.58 0.50
Overall 0.25 0.12* 0.34 0.12** 0.57 0.20**
Women
The Netherlands 0.46 1.03 0.32 1.09 0.49 1.94
Finland 1.77 0.52 1.83 0.51 1.37 0.87
Denmark 0.55 0.85 0.59 0.85 1.87 1.37
Italy 0.29 0.65 0.15 0.69 0.43 1.05
France 0.82 0.93 0.66 0.99 1.99 1.22
Poland 1.03 0.68 0.85 0.74 1.33 0.94
Overall 0.60 0.30* 0.62 0.30* 1.37 0.46**
1 Adjusted for iron intake.
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2 Adjusted for iron intake, age, menarche (in girls only), protein, tea, vitamin C and country. * P 0.05, ** P 0.01.
the association between calcium intake levels and iron iron absorption is inhibited, Hallberg and colleagues (1992a)
status. argued that the mechanism must involve inhibition of iron
Several studies show an inhibitory effect of calcium intake extrusion from the enterocyte. Recent studies suggest that
on iron absorption (Deehr et al. 1990, Cook et al. 1991, Galan calcium competes for iron-binding sites on the intestinal iron-
et al. 1991, Hallberg et al. 1992a). In these intervention binding protein mobilferrin.
studies, calcium was provided via a supplement or added to the It can be argued whether the finding that higher calcium
meal (Hallberg et al. 1991, 1992a, 1992b). Some studies pro- intake is associated with reduced serum ferritin levels is of
vide extra yogurt or milk during the meal (Gleerup et al. 1993, biological relevance. The normal absorption of iron from the
1995). An effect of calcium on iron absorption was reported to diet is estimated to be 10% (about 1 mg/d). To maintain the
be most pronounced when calcium was provided during the iron balance, several mechanisms are involved. In case of an
same meal in which iron was consumed. Gleerup et al. (1993) iron deficiency, the uptake of iron may be increased by up to
showed that calcium given 2 or 4 h before a meal had no 20 –30% (Wick et al. 1996). Several studies showed that iron
inhibitory effect on iron absorption. Some studies, however, absorption is strongly and inversely associated with serum
did not find an inhibitory effect of milk on iron absorption ferritin level (Hulten et al. 1995). Therefore, reducing calcium
´
(Turnlund et al. 1990, Tidehag et al. 1995), and in a study intake does not necessarily lead to increased serum ferritin
among lactating Gambian women, no effect of calcium sup- levels. Because inadequate calcium intake may lead to other
plementation on serum ferritin level was observed (Yan et al. serious health problems such as osteoporosis (Heaney 1993), it
1996). seems inappropriate to advise strongly against the consump-
A far as we know, our study is the first to look at normal tion of calcium to prevent iron deficiency.
dietary intake levels instead of supplementation with calcium. From our results we conclude that dietary calcium intake is
Contrary to most studies which evaluate iron absorption, our weakly, inversely associated with the iron status of blood in
interest was the influence of calcium intake on iron status. girls and young women, irrespective of whether calcium was
This study, therefore, may yield a better assessment of the ingested simultaneously with iron.
long-term effect of calcium on iron absorption. Our study did
not reveal an effect of time of calcium consumption on iron ACKNOWLEDGMENTS
status. It may well be that the effect of simultaneous consump-
tion of calcium and iron is readily reflected in iron absorption, We thank all those who have contributed to data collection,
whereas the iron status of blood is a more long-term variable questionnaire development, data management, biochemical analysis
on which this effect is less clear. In our study we did not and technical and administrative support.
distinguish between heme and nonheme iron. However, be-
cause the inhibitory effect of calcium was observed in both LITERATURE CITED
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women. Am. J. Clin. Nutr. 44: 83– 88.
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