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Public Health Nutrition: 17(2), 383–389 doi:10.1017/S1368980012005307
Calcium intake and osteoporosis: the influence of calcium
intake from dairy products on hip bone mineral density and
fracture incidence – a population-based study in women over
55 years of age
Dariusz W"odarek
1,
*, Dominika G"a˛bska
1
, Aleksandra Ko"ota
2
, Piotr Adamczyk
3
,
Aleksandra Czekaj"o
4
,W"adys"aw Grzeszczak
5
, Bogna Drozdzowska
6
and
Wojciech Pluskiewicz
7
1
Department of Dietetics, Faculty of Human Nutrition and Consumer Sciences, Warsaw University of Life
Sciences–SGGW, 159c Nowoursynowska Street, 02-776 Warsaw, Poland:
2
Chair of Nutritional Physiology,
Department of Dietetics, Faculty of Human Nutrition and Consumer Sciences, Warsaw University of Life
Sciences, Warsaw, Poland:
3
Department and Clinic of Pediatrics, Medical University of Silesia, Katowice,
Poland:
4
Department of Nephrology, Regional Hospital in Racibo
´rz, Racibo
´rz, Poland:
5
Department and Clinic
of Internal Diseases, Diabetology and Nephrology, Medical University of Silesia, Katowice, Poland:
6
Department of Pathomorphology, Medical University of Silesia, Katowice, Poland:
7
Metabolic Bone
Diseases Unit, Department and Clinic of Internal Diseases, Diabetology and Nephrology, Medical
University of Silesia, Katowice, Poland
Submitted 19 June 2012: Final revision received 30 October 2012: Accepted 12 November 2012: First published online 10 December 2012
Abstract
Objective: The incidence of osteoporosis increases with age and is most frequently
observed in postmenopausal women. The objective of the present population-
based cohort study was to assess the influence of Ca intake from dairy sources on
hip bone mineral density and hip fracture incidence in a group of Polish women
over 55 years of age.
Design: The main outcome measures included: bone mineral density, the number
of previous fractures and the reported Ca intake from dairy sources, assessed by a
diet questionnaire.
Setting: The RAC-OST-POL Study was conducted in the District of Raciborz in the
south of Poland.
Subjects: The study was carried out in a group of 625 women, randomly recruited
from the general population of women aged .55 years.
Results: Median Ca intake from dairy products was lower in the group of women
with femoral neck T-score #–2?5thaninthegroupwithT-score.–2?5(275v.
383 mg/d; P50?0019). For total hip score, the difference was close to borderline
significance (P50?0698). Median Ca intake from dairy products was lower in
the group of women with previous fractures than in those without fracture history
(336 v. 395 mg/d; P50?0254). The main dairy source of Ca in the analysed group
included milk drinks, rennet cheese and milk.
Conclusions: Higher dairy Ca intake is recommended, since a number of the
women analysed were unable to satisfy their Ca requirement exclusively from
their diet.
Keywords
Osteoporosis
Women
Calcium
Dairy products
Osteoporosis is a skeletal disease associated with low
bone mass, microarchitectural deterioration of bone
tissue and, as a consequence, increased bone fragility and
susceptibility to fracture
(1)
. The incidence of osteoporosis
increases with age and is most frequently observed in
postmenopausal women, as bone tissue loss and remo-
delling are accelerated by decreased ovarian oestrogen
levels associated with menopause
(2)
. Osteoporotic bone
fractures may be particularly devastating in the case of
elderly women. Fracture prevention is one of the key
goals of osteoporosis therapy in postmenopausal women,
with targets to inhibit bone loss processes, maintain
proper bone strength, and minimise or eliminate the
factors contributing to slips or falls
(3)
.
The relationship between Ca intake and bone mineral
density (BMD) is a widely analysed issue; higher Ca intake
is associated with increased bone density in children
(4)
,as
well as higher bone mass
(5)
, reduced risk of osteoporosis
(6)
*Corresponding author: Email dariusz_wlodarek@sggw.pl rThe Authors 2012
and lower fracture risks
(7)
in adults and the elderly.
The above-mentioned association is very complex and
some authors emphasise the role of other factors, such as
environmental factors for example, while doubting any
strong correlation with Ca
(8,9)
. Simultaneously, besides
gender and age, body mass is the third important element
which influences the risk of osteoporosis
(10)
, while being
also associated with Ca intake
(11,12)
.
The most important sources of Ca are dairy products,
providing over 60 % of daily Ca intake in women’s
diets
(13,14)
and even 74 % in some Polish studies
(15)
.Simul-
taneously, they are at least as efficacious as Ca supplements
in osteoporosis prevention
(16)
.
It was hypothesised that Ca intake from dairy sources
will be associated with BMD in women over 55 years of
age. The objective of the present population-based cohort
study was to assess the influence of Ca intake from dairy
sources on hip BMD and hip fracture incidence in a group
of Polish women aged .55 years.
Methods
The RAC-OST-POL study was carried out in a group of
Polish women aged .55 years, randomly recruited from
the general population of women over 55 years of age in
the District of Raciborz in the south of Poland. The total
number of eligible women inhabiting the region at the
time of enrolment was 17 500, from whom 1750 were
randomly selected and invited by regular mail to partici-
pate in the study. A blind list of women, selected for the
study, was provided by the local government and each
woman was assigned a number without showing her
name. A group of 625 women responded positively to
the invitation and declared their intention to take part in
the study, which was performed in May 2010. Among
these women, six were still menstruating. All 625 partici-
pants were submitted to the study protocol, including
BMD measurements and an FFQ to assess Ca intake.
Body weight and height were measured with a standard
medical balance and used to calculate BMI (kg/m
2
).
The study complied with the guidelines of the Declara-
tion of Helsinki and all procedures involving human
subjects were approved by the Ethics Committee of the
Medical University of Silesia, Katowice, Poland. A written
informed consent was obtained from all participants.
The study group was described in a previous paper
(17)
.
Osteoporosis has been operationally defined on the
basis of BMD assessment. According to the WHO criteria,
osteoporosis is defined as a BMD level that lies 2?5SD or
more below the average value for young healthy women
(T-score of #–2?5)
(18)
. The skeletal status was assessed
by a Lunar DPX bone densitometer (GE Healthcare,
Waukesha, WI, USA), assessing femoral neck and total
hip bone density. Densitometric variables are presented
as BMD (g/cm
2
) and T-score. All measurements were
performed by one operator. The CV for measurements
(calculated on the basis of fifty measurements – two
for each participant with reposition) was 1?6 % for
femoral neck and 0?82 % for total hip. Participants were
queried about previous fractures of non-traumatic origin,
e.g. caused by a fall from standing height or less; since no
radiograms were obtained, some spine fractures might
have been missed.
Participants were asked questions from the applied
FFQ to assess their Ca intake from dairy products;
they were asked by a dietitian about the frequency of
consumption of forty-nine dairy products most common
in Poland (e.g. milk, yoghurt, other milk beverages,
rennet cheese, cottage cheese) and of meals containing
dairy products, as well as typical portion sizes. Ca intake
from a particular product was estimated by the following
formula: Ca intake (mg) 5typical portion size (g) 3Ca
content (mg/g). The FFQ results were analysed using the
Dietetyk 2 software package (the Polish dietetic software)
and the Polish database of nutritional values of food
products
(19)
. The use of an FFQ to assess Ca intake is a
commonly accepted and widely applied method, taking
into account specified sources of Ca in the diet, mainly
dairy products
(13,20–23)
. The standard error of the Ca
estimate for the FFQ administered (calculated on the basis
of two measurements for fifty participants with repetition
during the period of 6 weeks) was 180 mg, while the
median difference for the two estimations of daily Ca
intake was 12 %. A similar questionnaire, taking into
account similar groups of products and applied to assess
Ca intake in the Polish population, was also characterised
by high sensitivity
(24)
.
Data are presented as means and standard deviations,
along with minimum, maximum and median values. The
distribution of the analysed factors was verified using
the Shapiro–Wilk test, while the Spearman correlation
coefficient was used to characterise relationships among
the analysed factors and the Mann–Whitney Utest was
used to analyse differences between groups.
An additional statistical analysis was performed in order
to confirm that the analysed population might be treated as
a representative sub-sample. It was verified whether the
mean age in the analysed sub-population matched the
mean age in the general population. The two-sided level of
significance P#0?05 was accepted to define the signifi-
cance of correlations. Statistical analysis was carried out
using the Statistica software version 8?0.
Results
Table 1 presents the characteristic features of the partici-
pants: age, body weight, body height and BMI. According
to the 2010 Statistical Yearbook, the general population
of women over 55 years of age in Poland comprises the
following age subgroups: 29?8 % aged 55–59 years, 14?3%
384 DW"odarek et al.
aged 60–64 years and 55?9 % aged 65 years and older
(25)
.
These age subgroups accounted for respectively 27?0%,
19?8 % and 53?2 % of the women in the present study.
The x
2
test performed for the subgroup aged 60–64 years
revealed a significant difference between typical and
observed numerical strength in the analysed group.
A significant correlation was found between age and BMI
values (P50?0017; r50?12).
Dairy Ca intakes of the women, grouped according to
femoral neck and total hip T-scores .–2?5or#–2?5, are
presented in Table 2. Ca intake from dairy products
was lower in the group of women with femoral neck
T-scores #–2?5 than in the group with T-scores .–2?5
(P50?0019). For the total hip scores, the difference was
borderline significant (P50?0698).
Table 3 presents the associations between dairy Ca
intake and fractures. Ca intake from dairy products was
lower in the group of women with previous fractures than
in those without fracture history (P50?0254).
Ca intake from various dairy sources is presented in
Table 4. The median Ca intake from total dairy products
was 373?2 mg/d in the analysed group; however with a
considerable variability among particular individuals,
ranging from 3?6 mg/d to 1922?9 mg/d. Other milk drinks
(i.e. drinks other than milk, such as yoghurt, kefir,
buttermilk) were the main dairy source of Ca, providing a
Table 1 Characteristic features of the participants: Polish women (n625) aged .55 years, RAC-OST-POL Study,
May 2010
Mean SD Median Minimum Maximum
Age (years) 66?47?865?7* 55?092?2
Body height (cm) 155?46?0 156?0* 136?0 175?0
Body weight (kg) 75?514?275?0* 39?0 125?0
BMI (kg/m
2
)31?25?530?8* 15?453?1
*Variable was not normally distributed (verified by the Shapiro–Wilk test; P#0?05).
Table 3 Dairy calcium intake (mg/d) according to fracture status: Polish women (n625) aged .55 years, RAC-OST-
POL Study, May 2010
Dairy Ca intake (mg/d)
Fracture status nMean SD Median Minimum Maximum Pvalue*
Fractures 176 390?5 256?5 336?4-3?6 1922?90?0254
No fractures 450 438?1 273?6 395?4-15?5 1915?1
*Differences assessed by the Mann–Whitney Utest.
-Variable was not normally distributed (verified by the Shapiro–Wilk test; P#0?05).
Table 2 Dairy calcium intake (mg/d) according to femoral neck and total hip bone mineral density T-scores: Polish
women (n625) aged .55 years, RAC-OST-POL Study, May 2010
Dairy Ca intake (mg/d)
T-score nMean SD Median Minimum Maximum Pvalue*
Femoral neck #22?5 59 360?4 226?1 274?9-3?6 1915?10?0019
.22?5 559 431?1 263?1 383?0-15?5 1922?9
Total hip #22?5 23 311?1 202?2 239?2-99?0 770?30?0698
.22?5 595 428?0 271?8 374?0-3?6 1922?9
*Differences assessed by the Mann–Whitney Utest.
-Variable was not normally distributed (verified by the Shapiro–Wilk test; P#0?05).
Table 4 Calcium intake (mg/d) from dairy sources: Polish women (n625) aged .55 years, RAC-OST-POL Study, May
2010
Ca intake (mg/d)
Mean SD Median Minimum Maximum
Total dairy products 424?7 269?6 373?2* 3?6 1922?9
Milk 95?7 138?170?8* 0?0 1300?0
Other milk drinks 134?3 138?999?1* 0?0 1377?4
Rennet cheese 117?5 139?772?6* 0?0 1091?1
Cottage cheese 34?134?525?5* 0?0 274?6
Dairy dishes 31?135?620?5* 0?0 252?2
*Variable was not normally distributed (verified by the Shapiro–Wilk test; P#0?05).
Calcium intake and osteoporosis 385
median of 99?1 mg Ca/d. Important sources of Ca
included rennet cheese (median 72?6 mg/d) and milk
(median 70?8 mg/d). The other analysed sources of Ca
included cottage cheese, dairy dishes and other products.
The correlations of age and BMI with Ca intake from
various dairy sources are presented in Table 5. In the case
of older individuals, a lower intake of Ca was observed,
both from total dairy products and particular dairy products
groups (including milk, other milk drinks, cottage and
rennet cheese), while a higher intake of Ca from dairy
dishes was confirmed. BMI values were inversely cor-
related with Ca intake levels from cottage cheese only.
Table 6 presents correlations between Ca intake from
various dairy sources and measured BMD values. Positive
correlations between femoral neck and total hip BMD
were observed for total dairy Ca intake as well as Ca
intake from milk and other milk drinks, while a negative
correlation was found between total hip BMD values and
Ca intake from dairy dishes.
Discussion
The present data were obtained from research carried out
in a group of Polish women aged .55 years, analysing
their dietary Ca intake from dairy products and its
association with osteoporosis. The correlation between
dietary Ca intake and osteoporosis development arouses
a great deal of controversy, as Ca intake is not the only
factor affecting BMD
(9)
, but remains a vital issue that is
evaluated intensively in various countries
(26–30)
.
The group of women analysed in the present study was
characterised by excessive body mass, with a median BMI
of 30?84 kg/m
2
. The high BMI values in these women
are congruent with BMI levels observed in osteoporosis
studies conducted in Europe
(26,27)
. Increased BMI may
be associated with bone mineral loss
(31)
and during
weight reduction overweight postmenopausal women are
also more susceptible to bone loss, even if they are
characterised by daily Ca intake of 1000 mg
(32)
.
Femoral neck T-score is the main indicator of osteo-
porosis in BMD assessment
(18)
, with fractures being the
most adverse effect of the disease
(33)
. In the present study,
womenwitheitherlowerfemoralneckT-scoresor
previous fractures were characterised by lower dairy Ca
intake. Other reports indicate that postmenopausal women
with higher intakes of dairy products are also characterised
by higher lumbar BMD values
(10)
. Some researchers have
emphasised a strong negative correlation between Ca
intake and hip fracture incidence among women
(34)
,as
well as a correlation between Ca intake and broadband
ultrasound attenuation Z-score in elderly women
(35)
.
However, other studies of Ca intake and osteoporosis
indicated associations between Ca intake and BMD to be
rather contradictory. Some researchers claim that, even if a
certain influence of Ca intake on bone mass improvement
is observed, neither Ca nor vitamin D supplementation
demonstrates any short-term effect on fracture risk
(6)
; thus
coming to the conclusion that no correlation exists between
Ca intake and fracture incidence
(28)
.
Dairy Ca intake may be perceived as a strong predictor
of total Ca intake, as Ca intake from products other than
dairy products is fairly constant. The results of other
authors indicate that dairy products provide over 60 % of
daily Ca intake in women’s diets; in a group characterised
by Ca intake of about 800 mg/d the contribution from dairy
products was about 62 %, while in group characterised by
Ca intake of about 900 mg/d the contribution amounted to
about 84 %
(13)
. As the daily Ca intake from non-dairy
products remains at a fairly stable level, a higher total daily
Ca intake suggests a higher contribution of Ca from dairy
products in the diet. The total Ca intake of the women in
the present study may be estimated as the sum of Ca
intakes from all products in the FFQ and about 250mg
Ca from products other than dairy products. Thus, in
the present group of Polish women, Ca intake can be
estimated at the level of about 675 mg/d. In other research
conducted in postmenopausal women in Poland, the
total Ca intake was similar – over 600 mg daily
(36)
.
The latter study, performed in nine European countries,
indicated that Polish women are characterised by low Ca
intake compared with women in the other countries
evaluated
(36)
. Ca intake in non-European populations
was lower than in Poland – below 600 mg/d
(37–39)
.The
recommended daily Ca intake for postmenopausal women
Table 6 Correlations between calcium intake from dairy sources
and femoral neck and total hip bone mineral density (BMD): Polish
women (n625) aged .55 years, RAC-OST-POL Study, May 2010
BMD – femoral neck BMD – total hip
Pvalue rPvalue r
Total dairy products 0?0048* 0?11 0?0198* 0?09
Milk 0?0039* 0?12 0?0361* 0?08
Other milk drinks 0?0001* 0?15 0?0001* 0?15
Rennet cheese 0?2799 0?04 0?2870 0?04
Cottage cheese 0?1203 0?06 0?5519 0?02
Dairy dishes 0?1470 20?06 0?0057* 20?11
*Significant correlations (assessed by the Spearman correlation coefficient;
P#0?05).
Table 5 Correlations of age and BMI with calcium intake from dairy
sources: Polish women (n625) aged .55 years, RAC-OST-POL
Study, May 2010
Age BMI
Pvalue rPvalue r
Total dairy products 0?0000* 20?19 0?4192 20?03
Milk 0?1980 20?05 0?2066 0?05
Other milk drinks 0?0002* 20?15 0?5740 0?02
Rennet cheese 0?0001* 20?16 0?7871 20?01
Cottage cheese 0?0000* 20?19 0?0115* 20?10
Dairy dishes 0?0008* 0?13 0?3257 0?04
*Significant correlations (assessed by the Spearman correlation coefficient;
P#0?05).
386 DW"odarek et al.
is 1000–1500 mg, depending on age and recommending
institution
(40)
. As a result, a number of women in the
present study were unable to satisfy their Ca requirement
exclusively from their diet.
The present women had lower intakes of Ca from milk
and milk drinks, as well as from cheeses and other products,
as compared with the results of other studies
(13)
. The pro-
portion of dairy products as sources of Ca was also different.
In the study by Poliquin et al.
(14)
the proportion of Ca from
milk to Ca from other dairy products was about 3?2:4 and in
the study by Fardellone et al.
(26)
it was about 1?8:4, whereas
the proportion was 0?7:4 in the present study. Simulta-
neously, Gonelli et al.
(13)
found the proportion of Ca from
milkandmilkdrinkstoCafromcheesesandotherdairy
products to be about 3:4, while this proportion was 5?5:4
in our study. Therefore it may be concluded that while
milk consumption was low in the present study group,
the consumption of other milk drinks was fairly high in
comparison with the results from other research.
ThestrongeffectofageonCaintakeweobservedisalso
reported by other researchers
(26,37,39)
.Accordingtoother
authors, the daily Ca intake of postmenopausal women is
significantly lower than that of premenopausal women
(39)
and the proportion of women with low Ca intake rises with
age
(26,37)
. However, the character of the relationship is not
obvious, as other authors report lower Ca inadequacy in
women above 75 years of age
(36)
, probably associated with
higher intake of Ca supplements
(14)
.
In the present study it can be concluded that the lower
Ca intake observed in the case of older women
can be attributed to lower consumption of dairy products,
probably as a result of changing nutritional habits.
Simultaneously, milk consumption remains stable, inde-
pendently of age, while the consumption of dairy dishes
is higher, without any major impact on the total dairy Ca
intake. With age, everyday activities such as preparing
meals become more difficult
(41)
and chewing ability also
decreases
(42)
. So, the above-mentioned higher consump-
tion of dairy dishes may probably result from the fact that
dairy dishes are easy to prepare and eat.
In the research of Zhong et al.
(28)
, a close to significant
association was observed between Ca intake and BMI:
postmenopausal women with higher BMI values reported
lower Ca intake. No such correlation was observed in our
study group. The only correlation we observed, that
between cottage cheese consumption and BMI, could have
been attributed to the general observation that individuals
with lower BMI consume more cottage cheese, also con-
firmed by other researchers
(43)
.
In the present group of females, correlations were
observed between Ca intake from various dairy sources
and BMD that corresponded to the results of other
authors, claiming similar correlations between Ca intake
and BMD
(39,44,45)
.
In contrast, the observed negative correlation between
Ca intake from dairy dishes and total hip BMD score is
rather difficult to explain. Only the fact indicated
previously, that dairy dishes are generally easier to pre-
pare and to eat and may be more often chosen by elderly
people, may provide an explanation. The positive corre-
lation between dairy Ca intake and BMD in the case of Ca
from milk and other milk drinks, but not for Ca from
rennet cheese and cottage cheese, may be associated with
lactose. Lactose is contained in milk and other milk
drinks, being a factor promoting Ca absorption
(46)
.
The content of lactose in milk and other milk drinks
is significantly higher than in either rennet cheese or
cottage cheese; according to the Polish food composition
database, the lactose content is 4?6–4?9 g/100 g and
4?1–5?0 g/100 g for cow’s milk and other milk drinks, as
opposed to 0?1–1?0 g/100 g and 1?0–3?3 g/100 g for rennet
cheese and cottage cheese, respectively
(19)
. So, it may be
concluded that BMD is correlated not only with Ca from
dairy products but with Ca intake from lactose-containing
dairy products, where lactose improves Ca absorption.
One of the factors that influences Ca metabolism in the
human body, and as a consequence reduces the risk of
osteoporosis, is vitamin D
3
. In the present study, neither
vitamin D intake nor its serum level was assessed.
This may be a limitation of the study, but nevertheless the
proper intake of Ca is the main dietary factor influencing
bone density, and in the research of other authors a
similar attitude is chosen
(10,47)
. Other potential limitations
of our study may be associated with the fact that only
36 % of invited women participated and that BMD was
measured at the hip only and spine radiograms were not
available, thus some spine fractures might not have been
taken into account.
Conclusions
In the present group of Polish women above 55 years of
age, it may be concluded that lower BMD (femoral neck
T-score #–2?5) and previous fractures were associated
with lower reported dairy Ca intake. Due to the insuffi-
cient consumption of dairy products, a number of women
were unable to satisfy their Ca requirement exclusively
from their diet. The main dairy sources of Ca in the
analysed group included milk, other milk drinks and
rennet cheese. It is therefore important to recommend
the consumption of dairy products with lactose, a Ca-
absorption improving factor, such as milk and milk
drinks, to improve BMD and reduce fracture risks in the
population of postmenopausal women with osteoporosis.
Acknowledgements
Sources of funding: This research received no specific grant
from any funding agency in the public, commercial or non-
for-profit sectors. Conflicts of interest: The authors have no
conflicts of interest to declare. Authors’ contributions: D.W.
and W.P. designed study; D.W., D.G., A.K., P.A., A.C., W.G.,
Calcium intake and osteoporosis 387
B.D. and W.P. conducted the research; D.W., D.G. and A.K.
analysed the data and performed the statistical analysis;
D.W. and D.G. wrote the paper; D.W. had primary
responsibility for final content.
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