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Original Article
Calcium Supplementation with Calcium-Rich Mineral Waters: A
Systematic Review and Meta-analysis of its Bioavailability
H. BoÈhmer, H. Mu
È
ller and K.-L. Resch
Saxon Balneology and Rehabilitation Medicine Research Institute, Bad Elster, Germany
Abstract. The relevance of calcium (Ca
2+
), an essential
bone mineral, to the prevention and treatment of
osteoporosis is well established. However, a good deal
of evidence casts doubt on the validity of current RDAs
(recommended daily allowance), i.e., 800±1000 mg/day.
New guidelines consistently advocate higher daily
intakes (up to 1500 mg/day), a goal that may be dif®cult
to achieve for many patients. Environmental as well as
individual behavioral factors may limit the consumption
of dairy products, whereas calcium supplements require
a high level of compliance and cause additional costs.
Calcium-rich mineral waters may offer a promising
alternative. A systematic literature search was performed
(Medline, years 1966±1998) to identify experimental
studies on the bioavailability of calcium-rich mineral
waters. First, all publications on calcium absorption from
mineral waters were identi®ed, and, in a second step,
studies comparing calcium absorption from mineral
waters with that from dairy products. Four studies
ful®lled all inclusion criteria. A meta-analysis based on
published p values indicated calcium absorption from
mineral waters was signi®cantly higher (p = 0.03) than
that from dairy products. Although only few studies with
a relatively small number of subjects are available to
date, the bioavailability of calcium from calcium-rich
mineral waters thus seems to be at least comparable to,
and possibly better than, that from dairy products. These
results are in keeping with the assumption that calcium-
rich mineral water is a useful calcium source to achieve
new, higher recommended daily allowances of calcium.
Keywords: Bioavailability; Calcium; Mineral water;
Osteoporosis; Recommended daily allowance
Background
Calcium plays an important role in the human body as an
essential bone mineral [1] as well as a messenger in
signal transduction [2±6]. Its concentration is regulated
by a variety of hormones [7±11]. In principle, the
healthy body is able to eliminate excess calcium, but is
unable to cope with low calcium intake for a extended
period of time [1,12,13].
Current RDAs (recommended daily allowance) have
increasingly been put in question [14], and new
guidelines consistently advocate higher daily intakes
[15±18]. This goal may be dif®cult to achieve for many
patients [19±24]. Supplementation with dairy products is
commonly suggested [25,26], although environmental as
well as individual behavioral factors may limit the
consumption of dairy products. Pharmaceutical prepara-
tions require a high level of compliance and cause
additional costs.
Calcium-rich mineral water, popular beverages free of
calories, may offer an interesting alternative, provided
they have an adequate calcium bioavailability. There-
fore, a systematic analysis of the literature on
bioavailability of calcium from calcium-rich mineral
waters should be performed.
Methods
First a systematic review on the topic should be
performed and, in a second step, published data should
Osteoporos Int (2000) 11:938±943
ß 2000 International Osteoporosis Foundation and National Osteoporosis Foundation
Osteoporosis
International
Correspondence and offprint requests to: Karl-Ludwig Resch, Saxon
Balneology and Rehabilitation Medicine Research Institute, Linden-
strasse 5, D-08645 Bad Elster, Germany. Tel: +49 37437 5570. Fax:
+49 37437 55777. e-mail: fbk@medkur.de
be summarized in a meta-analysis, if possible. We
anticipated only a small number of publications so
decided to tailor details of data processing only after data
selection, but whenever possible in accordance with
commonly accepted standards, such as those of the
Cochrane Collaboration [27].
Study Identi®cation
A systematic electronic literature research was per-
formed to identify experimental studies on the bioavail-
ability of calcium-rich mineral waters. Databases used
were Medline (version Silverplatter 98, years 1966±
1998) and Current Contents. References of identi®ed
publications were checked. The search strategy in
Medline is shown in Table 1.
Study Selection
To be included in the meta-analysis studies had to
compare calcium absorption from mineral water with
that from dairy products in healthy volunteers. Because
of an anticipated increased co-morbidity potentially
in¯uencing absorption rates in the elderly, participants
should not be older than 70 years. Any co-medication
in¯uencing calcium homeostasis had to be excluded.
Participants could be of either gender.
An estimation of effect size can only produce valid
®gures if the within-study comparison between mineral
water and dairy products was appropriate. Since calcium
load and absorption fraction are inversely correlated
[28], it is necessary to include data in the meta-analysis
only if calcium load sizes have been adjusted for, e.g.,
with the same calcium load from mineral water and dairy
products.
The question of whether calcium sources were taken
with meal or by fasting volunteers seems to be of similar
importance, because absorption of calcium increases
when it is taken with a meal [29]. Therefore, evidence
was required that both groups in a study were
comparable in that respect, enabling us to calculate
valid effect sizes from p values.
Data Synthesis
The data in publications comparing calcium absorption
fractions from mineral water with that from dairy
products were quantitatively summarized in a meta-
analysis and respective bioavailabilities were compared.
Statistics
The comparison of calcium absorption fractions from
dairy products with those from mineral waters was based
on a meta-analysis of published or calculated p values
[30], since the necessary information to compute d
values for each study (e.g., mean values and standard
deviations) or t values were not consistently available.
The meta-analysis included the p value for the one-sided
hypothesis that dairy products show an equal or better
calcium absorption than mineral waters. For meta-
analyses it is necessary to use one-sided hypotheses
and p values [30].
A p value was explicitly published in only one study;
all other p values had to be estimated applying different
procedures. The p value of the study by Halpern et al.
[31] was estimated using the binomial test of the given
frequencies. For the studies by Couzy et al. [32] and van
Dokkum et al. [33] the p values were calculated using
the published means and standard deviations and
applying the more conservative Student's t-test for
independent samples (although these data were indeed
dependent in nature). There was no methodologic
alternative to this procedure, which produces a relatively
conservative p value. Thus underestimation of the
resulting p value is quite likely. In consequence, this
estimate is in favor of the assumption that the calcium
absorption fraction is higher for dairy products than for
mineral waters. The meta-analysis of p values gives a
correlation coef®cient r as effect size parameter, which
was transformed to a more convenient d value by a
formula suggested by Rosenthal [34].
Subgroup analysis seemed inappropriate due to the
small number of studies available.
Results
We identi®ed six publications [31±37] with experimental
data on calcium absorption from mineral waters (Table
2). All six publications were identi®ed through the
Medline search. Neither the search in Current Contents
nor the check of references produced additional results.
All ®ve studies with published absorption fractions
used the tracer technique, with either stable [32,33] or
unstable isotopes [31,35,37]. From different measure-
Table 1. Medline search strategy to identify publications on calcium
absorption from mineral water
#1 ``MINERAL-WATERS''/ all subheadings
#2 explode ``BALNEOLOGY''/ all subheadings
#3 ``HEALTH-RESORTS''/ all subheadings
#4 MINERALWATER*
#5 MINERAL
#6 WATER
#7 MINERAL near3 WATER
#8 ``CALCIUM''/ all subheadings
#9 CALCIUM*
#10 ``BIOLOGICAL-AVAILABILITY''
#11 CALCIUM-CHANNEL-BLOCKERS
#12 #8 or #9
#13 #12 not #11
#14 #1 or #2 or #3 or #4 or #7 or #10
#15 #14 and #13
*Indicates truncation of the search term allowing for anything as
second part of the word
Calcium Supplementation with Calcium-Rich Mineral Waters 939
ment technologies this isotopic tracer technique cur-
rently provides the most precise method for determining
calcium absorption from different sources [38±40].
Four studies compared absorption fractions from dairy
products and mineral waters. These studies were
included in the meta-analysis [31±35], as they ful®lled
all inclusion criteria.
The other two studies were not included. Guillemant
et al. [36] used a different type of outcome parameter,
i.e., measurement of the parathyroid hormone concen-
tration. Wynkel et al. [37] compared absorption fractions
of different mineral waters, but did not compare them
with those of dairy products.
Table 2. Publications on calcium absorption from mineral waters
Publication Year n Subjects Results AR
a
D/M
b
Halpern et al. [31] 1991 15 Lactose-intolerant adults Calcium bioavailability from mineral water at
least comparable to dairy products. Mineral
water is a useful calcium source for lactose-
intolerant adults
No Yes
Heaney and Dowell [35] 1994 18 Healthy women Calcium bioavailability from mineral water at
least comparable to dairy products
Yes Yes
Couzy et al. [32] 1995 9 Healthy women Calcium bioavailability from mineral water
comparable to dairy products
Yes Yes
Van Dokkum et al. [33] 1996 12 Healthy young adult women Calcium bioavailability from mineral water
(37.0%) comparable with dairy products
(37.7±42.2%). Combined with a spaghetti
meal, calcium bioavailability from mineral
water increases signi®cantly (46.1%)
Yes Yes
Guillemant et al. [36] 1997 12 Healthy young adult men Inhibition of PTH-secretion induced by mineral
water
No No
Wynckel et al. [37] 1997 12 Students (8 men, 4 women) The intestinal calcium absorption from mineral
waters with three different concentrations
(10.4, 78 and 467 mg/l) is comparable.
Calcium-rich mineral water is a useful calcium
source for the elderly and patients with lactose
intolerance
Yes No
a
.Absorption fractions published.
b
.Comparison of dairy (D) and mineral water (M).
Table 3. Calcium absorption from mineral water and calcium load
Study n Mean
(%)
Calcium
load
(mg)
Standard
deviation
Heany and Dowell [35] 18 47.5 100 No data
Couzy et al. [32] 9 23.8 248 4.8
van Dockum et al. [33] 12 37.0 150 9.8
Wynckel et al. I
a
[37] 12 34.1 200 15.4
Wynckel et al. II
a
[37] 12 37.0 200 8.3
Wynckel et al. III
a
[37] 12 36.1 200 13.0
a
.Calcium absorption fractions of three different mineral waters ( I, II
and III).
Fig. 1. Mean absorption fraction versus calcium load.
Table 4. Four studies comparing calcium absorption from mineral
water and dairy products
Study np
a
Remarks
Halpern et al. [31] 15 0.0547 Minieral water vs milk; 8
subjects with a higher
calcium absorption from
mineral water, 2 subjects
with a higher absorption
from milk, p value
calculated from binomial
test
Heany and Dowell [35] 18 0.0175 Mineral water vs milk
Couzy et al. [32] 9 0.668 Mineral water vs milk; p
value conservatively
estimated from Student's t-
test for independent
samples
van Dokkum et al. [33] 12 0.568 Mineral water vs cheese; p
value conservatively
estimated from Student's t-
test for independent
samples
a
.p value for the one-sided hypothesis that calcium bioavailability
from dairy products to equal to or higher than that from mineral water.
940 H. BoÈhmer et al.
The mean absorption fractions of all included studies
are shown in Table 3. Figure 1 plots the mean absorption
fractions versus calcium load, and shows the known
inverse correlation between the two [27], with a range
from 23.8% (248 mg calcium load) to 47.5% (100 mg
calcium load).
Studies including a comparison of calcium absorption
from mineral waters with that from milk or dairy
products are shown in Table 4. The meta-analysis of p
values indicated a signi®cantly higher calcium absorp-
tion from mineral waters than from dairy products
(p = 0.03). The observed effect size was r = 0.27,
corresponding to a d value of 0.56, which indicates a
moderate effect size. The 95% con®dence interval of the
d value was 70.02 to 1.19 and a chi-square test of
homogeneity among studies revealed no signi®cant
differences (w
2
= 4.8, d.f. = 3, p = 0.19).
Discussion
An adequate calcium alimentation of the population is an
increasingly important target. Because of demographic
changes due to increasing life expectancy, osteoporosis
is about to become a major problem for Western health
care systems [41] with enormous economic conse-
quences [42]. Main preventive strategies aim at raising
peak bone mass [43] and at a reduction of age-related
bone loss [44] in order to delay for as long as possible a
drop in bone mineral content below the fracture
threshold.
The relevance of adequate calcium intake seems to be
well established. Recommended daily intakes are
dependent on age and sex [45]. According to studies
from the last decade children and adolescents, perime-
nopausal women and the elderly have a particular high
demand for calcium, of up to 1000±1500 mg per day
[15±18,46,47]. It was demonstrated that these groups do
not reliably achieve desirable intakes through their
normal diet: dietary calcium intake assessed with food-
frequency questionnaires normally reaches 600±800 mg
calcium per day [19,21±24], rarely higher [48].
It seems necessary, therefore, to facilitate daily
calcium intake as much as possible. This means that
preference should be given to adequate dietary intake
over substitution of calcium salts. A choice of different
options of intake might positively affect compliance and
effectiveness. In this respect calcium-rich mineral waters
may offer an alternative to the `standard' recommenda-
tion of milk and dairy products, or complement this
suggestion. Between 1 and 2 l of a typical calcium-rich
mineral water with a concentration of about 500 mg
calcium/l can help satisfy even an increased demand
(Table 5). This recommendation is based on the
assumption of an adequate bioavailability of the ingested
calcium. The bioavailability depends on the absorption
fraction, i.e., the proportion of absorbed calcium and
dietary calcium intake.
The mean absorption fractions from the ®ve studies
where absorption fractions were available, are similar to
that of dairy products in other studies. Heaney et al.
reported a calcium absorption fraction for milk of 31.7%
[49] in one study and 26.7% in a second [50]. Studies
analyzing calcium absorption from pharmaceutical
preparations report rates of about 25±35% [51±56].
Although only a few studies with a relatively small
number of subjects are available, the bioavailability of
calcium from calcium-rich mineral waters seems to be at
least comparable to, and possibly better than, that from
dairy products or pharmaceutical preparations.
Mineral waters are not monosubstances. Often
different minerals are leached in relevant concentrations.
Available study results indicate that calcium absorption
is not substantially in¯uenced by other accompanying
ion species, e.g., Wynkel et al. [37] observed no
signi®cant difference in absorption fractions of different
calcium-rich mineral waters (Table 6).
It should be mentioned, however, that accompanying
ion species could in¯uence urinary calcium excretion. In
particular, sodium may increase urinary calcium [57±
60]. Clinical studies indicate a correlation between levels
of urinary sodium and calcium. This correlation is in the
®rst place sodium-driven, i.e., the sodium load in¯uences
the urinary calcium level. One hundred millimoles
sodium may take out approximately 1 mmol of calcium
Table 5. Some mineral waters with their calcium contents
Brand name Calcium (mg/l) Country
Contrex 486 France
Adelborner 569 Switzerland
Eptinger 555 Switzerland
St. Augustinus 585 Germany
Schillerquelle Ensingen 585 Germany
St Margareten 566 Germany
Ferrarelle 368 Italy
Table 6. Ion concentration of tested mineral waters (mg/l)
Study Brand name Na
+
K
+
Ca
2+
Mg
2+
Cl
7
Sulphates HCO
7
3
Na
3
Silicate
Heany and Dowell [35] Sangemini 16.50 3.20 318.00 14.60 15.00 42.00 1000.00 23.30
Van Dokkum et al. [33] Ferrarelle 47.00 45.00 368.00 17.00 22.00 5.00 1385.00
Halpern et al. [31] Vittel Grande 3.80 2.00 202.00 36.00 7.20 306.00 402.00 6.00
Couzy et al. [32] Contrex 10.00 3.00 466.00 83.00 8.00 1160.00 403.00
Wynckel et al. [37] Mineral water I 8.0 5.4 10.4 6.0 7.5 6.7 64.0 4.0 30.5
Mineral water II 5.0 1.0 78.0 24.0 4.5 10.0 387.0 3.8 13.5
Mineral water III 7.0 3.0 467.0 84.0 7.0 1192.0 377.0 3.2 8.0
Calcium Supplementation with Calcium-Rich Mineral Waters 941
[61,62], according to a report on higher calcium loss
[63]. Consumers should therefore consider the level of
sodium when choosing a mineral water, not because of
its bioavailability but because of its biological activity.
Guillemant et al. [36] showed that the body reacts to
calcium supplemented from mineral water. The observed
reduction in the parathyroid hormone level could be
considered an indicator of the biological activity of the
ingested calcium.
Epidemiologic data support the assumption that
chronic low dietary calcium intake promotes osteoporo-
sis [64,65]. An inverse correlation between calcium
intake and osteoporotic fracture rates has been demon-
strated in several studies [66±69]. Osteoporotic bone loss
was reduced by 25% through adequate calcium
supplementation, especially in high-risk groups such as
women over 65 years of age [44]. Even a signi®cant
reduction in the rate of dangerous hip fractures due to
calcium supplementation has been demonstrated in a
clinical trial [68]. Clinical evidence of such biological
effects was shown by Cepollaro et al. [70] for calcium-
rich mineral waters. In a controlled clinical trial they
observed a signi®cant reduction in postmenopausal bone
loss with calcium supplementation.
Conclusion
Although data are available from only a few studies with
a relatively small number of subjects, calcium-rich
mineral waters seem to offer an interesting, effective
alternative to calcium supplementation from milk and
dairy products because of their comparable or possibly
even better bioavailability of calcium.
References
1. Dambacher MA. Calciumhormone, Skelett und Mineralstoff-
wechsel. In: Siegenthaler W, editor. Klinische Pathophysiologie.
Stuttgart: Thieme, 1994:279±301.
2. Bushinsky DA, Monk RD. Electrolyte quintet: calcium. Lancet
1998;352:306±11.
3. Rasmussen H. The calcium messenger system. N Engl J Med
1986;314:1094±100, 1164±70.
4. Putney JW. Calcium signaling: up, down, up, down ..... What`s
the point? Science 1998;279:191-2.
5. Laniado ME, Abel PD. Ion channels: new explanations for old
diseases. BMJ 1997;315:1171±2.
6. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y,
Shibasaki F, McKeon F, et al. Ca
2+
-induced apoptosis through
calcineurin dephosphorylation of BAD. Science 1999;284:339±
43.
7. Wimalawansa SJ. Calcitonin: molecular biology, physiology,
pathophysiology and its therapeutic uses. In: Pecile A, Bernard B,
editors. Advances in bone regulatory factors: morphology,
biochemistry, physiology and pharmacology. New York:
Plenum Press, 1999:121.
8. Anon. PTHrP: endocrine and autocrine regulator of calcium
[editorial]. Lancet 1991;337:146.
9. Audran M, Kumar R. The physiology and pathophysiology of
vitamin D. Mayo Clin Proc 1985;60:851±66.
10. Ringe JD. Vitamin D. Regulation des Vitamin-D-Stoffwechsels
und Therapie mit D-Metaboliten. Med Mod Pharm 1983;6:263.
11. Wassermann RH, Fullmer CS. Vitamin D and intestinal calcium
transport: facts, speculations and hypothesis. J Nutr
1995;5:S1971±9.
12. Resch KL, Waldow R, BoÈ hmer H. Osteoporose und Kalzium. J
Pharmakol Ther 1998;4:99-106.
13. Heaney RP, Recker RR, Saville PD. Calcium balance and
calcium requirements in middle-aged woman. Am J Clin Nutr
1977;30:2698.
14. Deutsche Gesellschaft fu
È
r ErnaÈhrung. Empfehlungen fu
È
r die
NaÈhrstoffzufuhr, 5. U
È
berarbeitung. Frankfurt: Umschau Verlag,
1991.
15. Masi L, Bilezikian JP. Osteoporosis: new hope for the future. Int J
Fertil Womens Med 1997;42:245±54.
16. Murray TM. Calcium nutrition and osteoporosis. Can Med Assoc
J 1996;155:935-9.
17. NIH consensus conference. Optimal calcium intake. JAMA
1994;272:342±51.
18. Reid IR. The management of osteoporosis. Baillieres Clin
Endocrinol Metab 1997;11:63±81.
19. Devine A, Prince RL, Bell R. Nutritional effect of calcium
supplementation by skim milk powder or calcium tablets on total
nutrient intake in postmenopausal woman. Am J Clin Nutr
1996;64:731±7.
20. Alaimo K, McDowell MA, Briefel RR, et al. Dietary intake of
vitamins, minerals, and ®ber of persons ages 2 months and over in
the United states: Third National Health and Nutrition Examina-
tion Survey, phase 1 1988±91. Hyattsville, MD: National Center
for Health Statistics, 1994.
21. Stone J, Doube A, Dudson D, Wallace J. Inadequate calcium,
folic acid, vitamin E, zinc, and selenium intake in rheumatoid
arthritis patients: results of a dietary study. Semin Arthritis
Rheum 1997;27:180±5.
22. Bergmann R, Huch R, Bergmann KE, Dudenhausen JW.
ErnaÈhrungspraÈvention in der Schwangerschaft. Dtsch A
È
rztebl
1997;94:A2411-5.
23. Michaelsson K, BergstroÈm R, Holmberg L, Mallmin H, Wolk A,
Ljunghall S. Calcium intake among woman aged 46±70 in
Sweden. J Epidemiol Community Health 1996;50:577±8.
24. US Department of Agriculture. Nationwide Food Consumption
Survey: continuing survey of food intakes by individual. USDA
NFCS, CFS 2 report no. 86-93. 1988.
25. Riggs BL, Melton LJ. Involutional osteoporosis. N Engl J Med
1986;314:1676±86.
26. Stracke H, Renner E, Knie G, Leidig G, Minne H, Federlin K.
Osteoporosis and bone metabolic parameters in dependence upon
calcium intake through milk and milk products. Eur J Clin Nutr
1993;47:617±22.
27. Mulrow C, Oxman AD, editors. Cochrane Collaboration hand-
book [updated 1 March 1997]. In: The Cochrane Library
[database on disk and CD-ROM]. Oxford: Update Software,
1996± [Updated quarterly].
28. Heaney RP, Weaver CM, Fitzsimmons ML. In¯uence of calcium
load on absorption fraction. J Bone Miner Res 1990;4:1135±8.
29. Heaney RP, Smith KT, Recker RR, Hinders SM. Meal effects on
calcium absorption. Am J Clin Nutr 1989;49:707±9.
30. Becker BJ. Combining signi®cance levels. In: Cooper H, Hedges
LV, editors. The handbook of research synthesis. New York:
Russel Sage Foundation, 1994:215±30.
31. Halpern GM, Van de Water J, Delabroise AM, Keen CL,
Gershwin ME. Comparative uptake of calcium from milk and a
calcium-rich mineral water in lactose intolerant adults: implica-
tions for treatment of osteoporosis. Am J Prev Med 1991;7:379±
83.
32. Couzy F, Kastenmayer P, Vigo M, Clough J, Munos-Box R,
Barclay DV. Calcium bioavailability from a calcium- and sulfate-
rich mineral water, compared with milk, in young adult woman.
Am J Clin Nutr 1995;62:1239±44.
33. Van Dokkum W, De la Gueronniere V, Schaafsma G, Bouley C,
Luten J, Latge C. Bioavailability of calcium of fresh cheeses,
enteral food and mineral water: a study with stable calcium
isotopes in young adult women. Br J Nutr 1996;75:893±903.
942 H. BoÈhmer et al.
34. Rosenthal R. Parametric measures of effect size. In: Cooper H,
Hedges LV, editors. The handbook of research synthesis. New
York: Russel Sage Foundation, 1994:231±44.
35. Heaney RP, Dowell MS. Absorbability of the calcium in a high-
calcium mineral water. Osteoporos Int 1994;4:323±4.
36. Guillemant J, Le HT, Guillemant S, Delabroise AM, Arnaud MJ.
Acute effects induced by a calcium-rich mineral water on calcium
metabolism and on parathyroid function [letter]. Osteoporos Int
1997;7:85±6.
37. Wynckel A, Hanrotel C, Wuillai A, Charnard J. Intestinal calcium
absorption from mineral water. Miner Electrolyte Metab 1997;
23:88±92.
38. DeGarzia JA, Ivanovich P, Fellows H, Rich C. A double isotope
method for measurement of intestinal absorption of calcium in
man. J Lab Clin Med 1965;66:822±9.
39. Eastell R, Vieira NE, Yergey AL, Riggs BL. One-day test using
stable isotopes to measure true fractional calcium absorption. J
Bone Miner Res 1989;4:463±8.
40. Heaney RP, Recker RR. Estimating true fractional calcium
absorption. Ann Intern Med 1988;103:905±6.
41. Kanis JA, McCloskey EV. Epidemiology of osteoporosis. Bone
1992;13:S1±10.
42. Rungby J, Hermann AP, Mosekilde L. Epidemiology of
osteoporosis: implications for drug therapy. Drugs Aging
1995;6:470±8.
43. Matkovic V. Calcium and peak bone mass. Int J Med 1992;
231:151±60.
44. Dawsen-Hughes B, Dallal GE, Krall EA, Sadowski L, Sahyoun
N, Tannenbaum S. A controlled trial of the effect of calcium
supplementation on bone density in postmenopausal woman. N
Engl J Med 1990; 27:878±83.
45. Yates AA, Schlicker SA, Suitor CW. Dietary reference intakes:
the new basis for recommendations for calcium and related
nutrients, B vitamins, and choline. J Am Diet Assoc 1998;98:699-
706.
46. Oster P, Mu
È
ller T, Schmidt-Gayk H, Schlierf G. Parathyroid
hormone, 25-hydroxyvitamin D and 1,25-dihydroxyvitamin D
concentration in elderly patients. Klin Wochenschr 1990;68:421±
6.
47. Scott PJ. Consensus viewpoint on the treatment of postmenopau-
sal osteoporosis. N Z Med J 1997;110:397±9.
48. Welten DC, Kemper HCG, Post GB, van Staveren WA, Twisk
JWR. Longitudinal development and tracking of calcium and
dairy intake from teenager to adult. Eur J Clin Nutr 1997;51:612±
8.
49. Heaney RP, Recker RR, Weaver CM. Absorbility of calcium
sources: the limited role of solubility. Calcif Tissue Int
1990;46:300±4.
50. Heaney RP, Weaver CM, Recker RR. Calcium absorbability from
spinach. Am J Clin Nutr 1988;47:707±9.
51. Hansen C, Werner E, Erbes HJ, Larrat V, Kaltwasser JP.
Intestinal calcium absorption from different calcium preparations:
in¯uence of anion and solubility. Osteoporos Int 1996;6:386±93.
52. Heany RP. Calcium supplements: practical considerations.
Osteoporos Int 1991;1:65±71.
53. Pak CY, Avioli LV. Factors affecting absorbability of calcium
from calcium salts and food. Calcif Tissue Int 1988;43:55±60.
54. Miller ZJ, Smith DL, Flora L, Slemenda C, Jiang X, Johnston CC.
Calcium absorption from calcium carbonate and a new form of
calcium (CCM) in healthy male and female adolescents. Am J
Clin Nutr 1988;48:1291±4.
55. Sheikh MS, Santa Ana CA, Nigar MJ, Schiller LR, Fordtran JS.
Gastrointestinal absorption of calcium from milk and calcium
salts. N Engl J Med 1987;317:532±6.
56. Heaney RP, Smith KT, Recker RR, Hinders SM. Meal effects on
calcium absorption. Am J Clin Nutr 1989;49:372±6.
57. Massey LK, Whiting SJ. Dietary salt, urinary calcium, and bone
loss. J Bone Miner Res 1996;11:731±6.
58. Lijnen P, Petrov V. Blood pressure and cationic transport systems
during combined calcium channel blocker and calcium adminis-
tration in males. Methods Find Exp Clin Pharmacol 1996;18:287±
94.
59. Dawson-Hughes B, Fowler SE, Dalsky G, Gallagher C. Sodium
excretion in¯uences calcium homeostasis in elderly men and
women. J Nutr 1996;126:2107±12.
60. O'Brien KO, Abrams SA, Stuff JE, Liang LK, Welch TR.
Variables related to urinary calcium excretion in young girls. J
Pediatr Gastroenterol Nutr 1996;23:8±12.
61. Itoh R, Suyama Y. Sodium excretion in relation to calcium and
hydroxyproline excretion in a healthy Japanese population. Am J
Clin Nutr 1996;63:735±40.
62. Nordin BE, Need AG, Morris HA, Horowitz M. The nature and
signi®cance of the relationship between urinary sodium and
urinary calcium in women. J Nutr 1993;123:1615±22.
63. Matkovic V, Ilich JZ, Andon MB, Hsieh LC, Tzagournis MA,
Lagger BJ, Goel PK. Urinary calcium, sodium, and bone mass of
young females. Am J Clin Nutr 1995;62:417±25.
64. Macus R. The relationship of dietary calcium to the maintenance
of skeletal integrity: an interface of endocrinology and nutrition.
Metabolism 1982;31:93±102.
65. Matkovic V, Kostial K, Simonovic I, Buzina R, Brodarec A,
Nordin BEC. Bone status and fracture rates in two regions of
Yugoslavia. Am J Clin Nutr 1979;32:540±9.
66. Cumming RG. Calcium intake and bone mass: a quantitative
review of the evidence. Calcif Tissue Int 1990;47:194±201.
67. Dawsen-Hughes B. Calcium supplementation and bone loss: a
review of controlled clinical trials Am J clin Nutr
1991;54(Suppl):S274±280.
68. Holbrook TL, Barrett-Conner E, Wingard DL. Dietary calcium
and risk of hip fracture: 14-year prospective population study.
Lancet 1988 5;2:(8629)1046±9.
69. Nieves JW, Golden AL, Siris E, Kelsey JL, Lindsay R. Teenage
and current calcium intake are related to bone mineral density of
the hip and forearm in women aged 30±39. Am J Epidemiol
1995;141:342±51.
70. Cepollaro C, Orlandi G, Gonelli S, Ferrucci G, Arditti JC,
Boracelli D, et al. Effect of calcium supplementation as a high-
calcium mineral water on bone loss in early postmenopausal
woman. Calcif Tissue Int 1996;59:238±9.
Received for publication 24 August 1999
Accepted in revised form 29 March 2000
Calcium Supplementation with Calcium-Rich Mineral Waters 943