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DOI 10.1007/s00198-004-1679-1
O R I GI N A L A R T IC L E
Received: 19 January 2004 / Accepted: 17 May 2004 / Published online: 10 September 2004
International Osteoporosis Foundation and National Osteoporosis Foundation 2004
Introduction
Calcium is an important nutrient for skeletal health
throughout the lifespan, and assumes a critical role in
the pathogenesis of osteoporosis [1]. In recent years,
considerable evidence has emerged with respect to the
eects of dietary calcium on bone health in all age
groups [2], and osteoporosis is no longer considered ageor gender-dependent [3]. These lines of reasoning
emphasise the need for lifelong adequate calcium intake
in both males and females [4]. Optimal calcium intake
refers to the levels of consumption that are necessary for
maximization of peak bone mass during childhood and
adolescence, maintenance of bone mass during adult
years, and minimization of bone loss later in life [5].
From the several macro- and micronutrients postulated
as putative determinants of bone mass and osteoporosis
risk, however, calcium is probably the most likely to be
inadequate in terms of dietary intake [6]. Assessing
dietary calcium intake could therefore be useful in both
clinical practice and research, and the need for developing cost-eective methods for identifying individuals
at all ages with insucient calcium intakes from food
has been highlighted [5].
There is a wide range of methods that could be used
for the dietary assessment of individuals or groups of
people, and each one has advantages and disadvantages
that make it suitable for use in dierent settings and for
specic purposes [7]. In general, the choice of method
depends on the objectives of the study, the foods or
nutrients of primary interest, the need for group versus
individual data, the need for absolute versus relative
305
Sample
A total of 1060 individuals were randomly selected from
a larger cohort of subjects participating in a nationwide
survey of osteoporosis risk factors in Greece [26].
Apparently healthy children (1015 years old, n=360),
adults (2633 years old, n=300), and elderly people (60
75 years old, n=400) were recruited. Among those asked
to participate, 37 declined the invitation, while 22 collected questionnaires were characterized as incomplete,
unreadable or misreported, and were excluded from the
analysis (overall participation rate was 94.4%). The nal
sample (n=1001), therefore, consisted of 351 children
(189 girls and 162 boys, aged 11.91.2 years), 260
adults (192 women and 68 men, aged 29.62.7 years),
and 390 elderly individuals (317 women and 73 men,
aged 68.64.6 years). All subjects were healthy, did not
use any medications or dietary supplements (including
calcium), and had maintained stable body weights and
dietary habits for the previous 6 months (the stable body
weight criterion was not applied for children). Prior to
306
MeanSD
95% CI
728361*
861415
133333
284219
5.447.6
36.930.5
705, 750
835, 887
154, 112
271, 298
8.4, 2.5
35.1, 38.8
Results
Calcium intakes by both the FFQ and the 24-h
recall were normally distributed, as revealed by the
Kolmogorov-Smirnov test. The FFQ signicantly
underestimated mean calcium intake compared to the
24-h recall by approximately 133 mg/day or 5.4%
(P<0.001; Table 1). This apparent discrepancy (i.e.
307
Fig. 2 The at-slope syndrome of the FFQ. Calcium dierence (y-axis) is the dierence in calcium intake by the FFQ minus
that by the 24-h recall, while calcium by 24-h recall (x-axis) is the
calcium intake by the 24-h recall. The linear regression line (solid
line) and the zero line (broken line) are shown. The zero intercept is
at approximately 561 mg/day
Hence at low true intakes, e.g. 100 mg/day, overestimation was approximately +175% (corresponding to
+175 mg/day), whereas at high intakes, e.g. 1000 mg/
day, underestimation was only 17.7% (corresponding
to 177 mg/day). While absolute dierences would
more or less cancel out (+175177=2 mg/day),
relative dierences would certainly not (+175
17.7=+157.3%). Overall, this is why the ratio of the
means (i.e. 133/861=15.4%) was so much dierent
from the mean of ratios (i.e. 5.4%). Because the mean
of a distribution that spans zero substantially underestimates the absolute error (i.e. regardless of sign), which
is important when dealing with individuals, mean
absolute dierences between the FFQ and the 24-h recall
are also shown in Table 1. Whether expressed in mg/day
or as percentages of true intake, absolute dierences
between the two methods were signicantly dierent
from zero (P<0.001), indicating the inability of the
FFQ to accurately estimate individual calcium intakes.
Actual values for surrogate FFQ quartiles manifested
a progressive increase with signicant dierences
between mean calcium intakes (F=158.9, P=0.001;
Table 2). The latter suggests that the FFQ could reliably
distinguish between categories at any level of intake. It is
worth mentioning that, individuals whose calcium intake was overestimated by the FFQ (due to the at-slope
syndrome referred to above) were more likely to have
been classied into the second quartile, rather than the
rst. When ve surrogate categories were assigned, the
FFQ lost its discriminatory ability between the second
and the third quintile (P=0.142), but it was still highly
discriminative across all the remaining categories
(F=126.8, P<0.001; Table 2). Following a stepwise
increase in the number of surrogate categories, it was
observed that the FFQ could readily distinguish between
308
Table 2 Discriminatory power of the FFQ. For each FFQ quartile or quintile, true values for calcium intake (meanSD) by the 24-h
recall have been calculated. These latter intakes do not represent 24-h recall quartiles or quintiles
FFQ
quartiles
Calcium range
by FFQ (mg/day)
Calcium intake
by 24-h recall
(mg/day)
FFQ
quintiles
Calcium range
by FFQ (mg/day)
Calcium intake
by 24-h recall
(mg/day)
1
2
3
4
250
251
250
250
<473
473676
676951
>951
576292a
760326b
886343c
1223397d
1
2
3
4
5
200
200
201
200
200
<425
425600
600762
7621025
>1025
551283a
733324b
811334b
938348c
1272394d
a,b,c,d
Quartiles or quintiles not sharing the same letter are statistically signicantly dierent from each other at P<0.001 (i.e. they are
discriminated), by one-way ANOVA and Tukeys post hoc tests. Quintiles 2 and 3 share the same letter and are not dierent from each
other (i.e. they cannot be discriminated by the FFQ)
Discussion
Although osteoporosis was once thought to be a natural part of aging among women, it is now widely
accepted that the disease may aect all individuals
regardless of age or gender [3]. Optimization of bone
health by appropriate dietary and lifestyle practices,
therefore, is a process that must occur throughout the
lifespan in both males and females [3]. Dietary calcium
Table 3 Cross-classication
analysis for the FFQ.
Frequencies and marginal
distributions are shown
FFQ quartiles
1
2
3
4
Total
Total
130 (52.0)
73 (29.1)
44 (17.6)
3 (1.2)
250
66 (26.4)
74 (29.5)
75 (30.0)
36 (14.4)
251
40 (16.0)
67 (26.7)
72 (28.8)
71 (28.4)
250
14 (5.6)
37 (14.7)
59 (23.6)
140 (56.0)
250
250
251
250
250
1001
309
accordance with previous observations [14]. These values might be expected keeping in mind the tendency of
the FFQ to underestimate calcium intake in general, and
can be considered moderate at best compared with other
questionnaires [14,17,21,25].
Some discussion on the validation method is also
justied. Virtually all of the available techniques have
been used previously as reference tools against which the
various calcium FFQs have been validated, including
modied diet history interviews [10], 4-day weighed
[11,19] or semi-weighed [22] food records, 3-day [14],
4-day [18,25], 7-day [20,21,23], or 14-day [17] estimated
food records, as well as 24-h diet recalls [15,16] and
full-length FFQs [12,13]. Depending on the more or less
burdensome nature of the reference method, sample
sizes have ranged from approximately 2060
[10,11,15,18,19,23,25] to approximately 100 [13,20,21,22]
subjects, although in some studies greater numbers were
recruited, e.g. more than 200 [14,17] or 500 [12] individuals. Although our choice of the 24-h recall as a
reference tool may not be the best for validation purposes, nevertheless, this method is considered the most
suitable to get population means and distributions for
subjects aged 10 years and over with reasonable accuracy, especially when combined with visual aids for
estimating portion sizes [8]. Thus, the 24-h recall was
preferred over other methods under these circumstances,
as a practical, cost-eective, and fairly accurate technique. Also, because of the large number of subjects
surveyed, inter-individual variability in daily food intake
would be expected to decrease [7].
Another limitation that should be acknowledged is
the lack of information on the reproducibility (reliability) of the FFQ. This is usually assessed by administering the questionnaire at two (or more) points in time to
the same group of people. Generally, however, less than
half of all FFQs being validated are tested for reproducibility [35, 36]. In the case of Ca calcium-specic
questionnaires, we could identify only three studies that
actually did that [12,13,21]. Bearing in mind that the
present FFQ was self-administered, the two major concerns regarding reproducibility, namely, intra- and interrater reliability, would automatically cancel out, as no
interviewer was involved [35]. Therefore, not testing for
reproducibility might not be as much of a problem for
this FFQ as it would, for example, for those questionnaires administered by trained dietitians (e.g. [17]). What
is more, in order to assess reproducibility, one must allow for sucient time before re-administrating the
questionnaire, so as to avoid a possible memory eect on
the respondents behalf. Because the present FFQ was
quite short (30 items), and hence the responses were easy
to remember, the time interval before re-administration
would have to be longer. In this instance, however, true
changes in dietary intake might have occurred (as they
usually do), contributing to falsely low reproducibility
[37]. For all these reasons, we feel that absence of any
information on the reliability of the FFQ is probably not
as critical, though indeed an omission.
310
Fig. 4 The 30-item FFQ developed and used for estimating usual calcium intake in the Greek population
311
Appendix A
Figure 4 shows the 30-item FFQ that was developed and
used for estimating usual calcium intake in the Greek
population. The questionnaire was self-administered by
the subjects and then returned for analysis. The nal two
questions were included for cross-checking purposes (i.e.
subjects who answered yes in either one were excluded
from subsequent analysis; see Materials and methods).
Appendix B
Table 4 lists the calcium content of each FFQ item.
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120
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60
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65
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88
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56
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