European Journal of Clinical Nutrition (2008) 62, 373–378
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ORIGINAL ARTICLE
Vitamin D status and its association with parathyroid
hormone concentrations in women of child-bearing
age living in Jakarta and Kuala Lumpur
TJ Green1, CM Skeaff1, JEP Rockell1, BJ Venn1, A Lambert2, J Todd2, GL Khor3, SP Loh3,
S Muslimatun4, R Agustina4 and SJ Whiting5
1
Department of Human Nutrition, University of Otago, Dunedin, New Zealand; 2Fonterra Brands Ltd, Auckland, New Zealand;
Department of Nutrition & Health Sciences, Faculty of Medicine & Health Sciences, Universiti Putra, Malaysia; 4SEAMEO TROPMED
Regional Center for Community Nutrition, University of Indonesia, Jakarta and 5College of Pharmacy and Nutrition, University of
Saskatchewan, Saskatoon, Saskatchewan, Canada
3
Objective: To describe the vitamin D status of women living in two Asian cities, – Jakarta (61S) and Kuala-Lumpur (21N), to
examine the association between plasma 25-hydroxyvitamin D and parathyroid hormone (PTH) concentrations, and to
determine a threshold for plasma 25-hydroxyvitamin D above which there is no further suppression of PTH. Also, to determine
whether dietary calcium intake influences the relationship between PTH and 25-hydroxyvitamin D.
Design: Cross-sectional.
Setting: Jakarta, Indonesia and Kuala Lumpur, Malaysia.
Participants: A convenience sample of 504 non-pregnant women 18–40 years.
Main measures: Plasma 25-hydroxyvitamin D and PTH.
Results: The mean 25-hydroxyvitamin D concentration was 48 nmol/l. Less than 1% of women had a 25-hydroxyvitamin D
concentration indicative of vitamin D deficiency (o17.5 nmol/l); whereas, over 60% of women had a 25-hydroxyvitamin D
concentration indicative of insufficiency (o50 nmol/l). We estimate that 52 nmol/l was the threshold concentration for plasma
25-hydroxyvitamin D above which no further suppression of PTH occurred. Below and above this concentration the slopes of the
regression lines were 0.18 (different from 0; P ¼ 0.003) and 0.01 (P ¼ 0.775), respectively. The relation between vitamin D
status and parathyroid hormone concentration did not differ between women with low, medium or high calcium intakes
(P ¼ 0.611); however, even in the highest tertile of calcium intake, mean calcium intake was only 657 mg/d.
Conclusion: On the basis of maximal suppression of PTH we estimate an optimal 25-hydroxyvitamin D concentration of B
50 nmol/l. Many women had a 25-hydroxyvitamin D below this concentration and may benefit from improved vitamin D status.
European Journal of Clinical Nutrition (2008) 62, 373–378; doi:10.1038/sj.ejcn.1602696; published online 7 March 2007
Keywords: vitamin D; parathyroid hormone; women; survey; Jakarta; Kuala Lumpur
Introduction
Vitamin D is essential for bone health, and maintaining
adequate vitamin D status throughout the lifespan may help
reduce the risk of osteoporotic fracture (Dawson-Hughes
Correspondence: Dr CM Skeaff, Department of Human Nutrition, University of
Otago, P.O. Box 56, Dunedin, New Zealand.
E-mail: [email protected]
Guarantor: T Green.
Received 26 October 2006; revised 18 December 2006; accepted 2 January
2007; published online 7 March 2007
et al. , 1997; Chapuy et al., 2002; Holick, 2004). Vitamin D
inadequacy has also been associated with a number of
negative non-skeletal health outcomes such as increased
falls, poor dental health and increased risk of Type 1 diabetes
as well as certain types of cancer (Holick, 2004; BischoffFerrari et al., 2006; Wactawski-Wende et al., 2006). Exposure
to sunlight is the major determinant of vitamin D status
because there are few foods naturally rich in vitamin D.
Consequently, anything that influences the amount of UV
light reaching the skin surface – for example season, time of
day, latitude, clothing and skin color – will affect vitamin D
status (Holick, 1994).
Vitamin D & PTH in Southeast Asian Women
TJ Green et al
374
Suboptimal vitamin D status, – based on low circulating
25-hydroxyvitamin D concentrations, has been described in
many populations (Looker et al., 2002; Zittermann, 2003;
Ruston et al., 2004; Rockell et al., 2005, 2006). Recently,
vitamin D insufficiency has been described not only in
populations living at higher latitudes but also in sun-rich
environments such as the Southern United States (Looker
et al., 2002), Saudi Arabia (Fonseca et al., 1984) and Australia
(McGrath et al., 2001). Vitamin D deficiency is common in
northern parts of Asia such as China (Du et al., 2001) and
Mongolia (Fraser, 2004), but has also been described in
people living in the Indian subcontinent such as Bangladesh
(Islam et al., 2006), India (Harinarayan, 2005) and Pakistan
(Atiq et al., 1998). However, less is known about the vitamin
D status of southeast Asian people living near the equator.
Women in some of these countries may be at risk of
inadequacy because the custom of dress leaves very little
skin exposed; as well, heat avoidance and shift work may
keep many indoors much of the day (Kung and Lee, 2006).
There is a lack of consensus on the concentration of
circulating 25-hydroxyvitamin D required for optimal health
(Dawson-Hughes et al., 2005; Bischoff-Ferrari et al., 2006).
Poor calcium absorption owing to vitamin D insufficiency
results in a compensatory rise in parathyroid hormone
leading to accelerated bone loss (Aloia et al., 2006;
Bischoff-Ferrari et al., 2006). Cutoffs that define vitamin D
insufficiency are based primarily on the concentration of
25-hydroxyvitamin D above which there is no further suppression of parathyroid hormone (PTH), somewhere between 25
and 122 nmol/l (Aloia et al., 2006). However, these cutoffs
have been based largely on studies in older Europeans and
only one was carried out in women of child-bearing age
(Aloia et al., 2006). Furthermore, in these studies the PTH
suppressing effect of 25-hydroxyvitamin D has been found
to differ with calcium intake (Aloia et al., 2006). Generally, at
lower calcium intakes a higher concentration of 25-hydroxyvitamin D was required to cause maximal suppression of
PTH. The effect of calcium intake on the vitamin D has not
been examined in South-East Asian populations.
Here we describe the vitamin D status of young women
living in two Asian cities, Jakarta (61S) and Kuala-Lumpur
(21N), and explore the relation between plasma 25-hydroxyvitamin D and parathyroid hormone concentrations.
Methods
Subjects
Non-pregnant women, 18–40 years (n ¼ 504), were recruited
using convenience sampling from the cities of Jakarta (61S)
and Kuala-Lumpur (21N). Recruitment was through letters,
the posting of flyers, the internet and word of mouth.
Women were excluded if they were breastfeeding, had
breastfed within 12 months, or had a serious or chronic
illness. A total of 378 women, 18–40 years, comprising
roughly equal proportions of Malay, Chinese and Indian
European Journal of Clinical Nutrition
ethnicities were recruited in Kuala Lumpur, between January
and March 2005. In Jakarta, 126 women 18–40 years, were
recruited in late 2004. Demographic details of the women
were collected using questionnaires. Approval to conduct the
studies was obtained from the Ethics Committee of the
Faculty of Medicine and Health Sciences, Universiti Putra,
Malaysia and the Ethical Committee Faculty of Medicine,
University of Indonesia, Jakarta.
Dietary
Dietary data were collected from each participant using a
single 24-h recall. Calcium intake was calculated based on
local (Gizi, 1990; Tee et al., 1997) and United States food
composition data (US Department of Agriculture, 2006).
Blood collection and laboratory analysis
Blood samples were taken by venipuncture into tubes
containing ethylenediaminetetraacetic acid following an
overnight fast. Plasma was obtained by centrifuging the
whole blood at 1650 g for 15 min. Blood samples were stored
at 801C until analyzed. Plasma 25-hydroxyvitamin D and
intact PTH were determined using radioimmunoassay kits
(DiaSorin Stillwater, MN, USA). Two levels of controls
provided by the manufacturer were run in each assay. Interand intra-assay coefficient of variations based on repeated
analysis of a pooled control for vitamin D were 13 and 9%,
respectively. We defined vitamin D deficiency as a 25hydroxyvitamin D less than 17.5 nmol/l and vitamin D
insufficiency as a 25-hydroxyvitamin D less than 50 nmol/l.
Inter- and intra-assay coefficient of variations based on a
pooled control for PTH were 11 and 5%, respectively.
Analysis
Differences between Jakarta and Kuala-Lumpur were determined using a Fisher’s Exact Test for categorical variables and
a Student’s t-test for continuous variables. Analysis of
variances, with a Bonferroni correction and a w2 test were
used to test for differences between the three Malay ethnic
(Malay, Chinese and Indian) groups. Results were considered
significant at Po0.05. To examine the relation between
plasma 25-hydroxyvitamin D and PTH we used the
MKSPLINE function of STATA (Stata Corp, TX, USA). Moving
the cutoff point for 25-hydroxyvitamin D concentration
from 30 to 80 nmol/l, in single unit increments, we
compared the slope of the regression line for data below
the cutoff to that of the slope of the line for data above the
cutoff. We determined the 25-hydroxyvitamin D concentration at which the difference in slopes of the two lines was
largest and the slope of the line for data above the cutoff was
not different from 0.
To examine the effect of calcium intake on the relationship between PTH and 25-hydroxyvitamin D, participants
were divided into tertiles according to calcium intake (low,
Vitamin D & PTH in Southeast Asian Women
TJ Green et al
375
o207 mg/day; medium, 207–385 mg/day; and high,
4385 mg/d), and plasma 25-hydroxyvitamin D concentration (low, o39 nmol/l; medium, 39–52 nmol/l; and high,
X53 nmol/l). We used multiple regression analysis with PTH
as the dependent variable and calcium intake and plasma
25-hydroxyvitamin D concentration as the independent
variables, with and without an interaction term in the model.
(P ¼ 0.014). Over two thirds of women in both countries were
single and the majority of women had received secondary
education or higher.
Mean plasma 25-hydroxyvitamin D concentration and
plasma PTH concentrations as well as the percentage of
women below 17.5 and 50 nmol/l are shown in Table 2. The
mean plasma 25-hydroxyvitamin D concentration of all
women was 48 nmol/l. Less than 1% of women had a plasma
25-hydroxyvitamin D concentration indicative of vitamin D
deficiency (o17.5 nmol/l), whereas over 60% of women had
a 25-hydroxyvitamin D concentration indicative of insufficiency (o50 nmol/l). There were no differences between
women in Jakarta and Kuala Lumpur with respect to mean
25-hydroxyvitamin D concentration or the proportion of
women deficient or insufficient. Within the ethnicities in
Kuala Lumpur, Indian (45 nmol/l) and Malay (43 nmol/l)
women had a lower mean plasma 25-hydroxyvitamin D
concentration than Chinese (58 nmol/l; Po0.001) women
Results
Select characteristics of the participants are given in Table 1.
Women surveyed in Jakarta were older than women in Kuala
Lumpur (30.0 cf 25.2 years; Po0.001).
Mean dietary calcium intakes were higher in Kuala
Lumpur than Jakarta (386 cf 270 mg/day; P ¼ 0.001) with
higher intakes in Indian women (457 mg/day) compared
with Malay (369 mg/day) or Chinese (338 mg/day) women
Table 1 Participant characteristics
Descriptive
Jakarta
Kuala Lumpur
All
Malay
Chinese
Indian
126
378
133
123
122
30.070.6
22.570.4
9 (7)
20 (16)
25.270.3
22.570.2
5 (1)
69 (18)
26.070.5
24.070.4
1 (1)
26 (20)
23.070.3
21.370.3
2 (2)
29 (24)
26.7 70.6
22.370.5
2 (2)
14 (10)
Marital status n (%)
Single
Married
Widowed/divorced
94 (75)
29 (23)
3 (2)
287 (76)
86 (22)
5 (1)
81 (61)
48 (36)
3 (2)
118 (96)
5 (4)
0
84 (69)
36 (30)
2 (2)
Highest education n (%)
Primary
Secondary
Matriculation
Polytechnic/University
26
19
60
21
10
61
49
258
3
35
23
72
0
3 (2)
14 (11)
106 (86)
7
24
12
77
Number of women
Age (years)
BMI (kg/m2)
Smokers n (%)
Multivitamin users n (%)
(20)
(15)
(47)
(16)
(3)
(16)
(13)
(68)
(2)
(26)
(18)
(54)
(6)
(20)
(11)
(63)
Abbreviation: BMI, body mass index.
a
Values are means 7s.e.m. unless otherwise indicated.
Table 2 Mean plasma 25-hydroxyvitamin D and PTH concentrations, dietary calcium intake, and prevalence of vitamin D deficiency (o17.5 nmol/l) and
insufficiency (o50 nmol/l) by city and by ethnic group
N
Plasma 25-hydroxyvitamin D (nmol/l)
Mean (95% CI)
All
Jakarta
Kuala Lumpur
Malay
Chinese
Indian
504
126
378
133
123
122
48
46
49
43
58
45
(46,
(43,
(47,
(40,
(55,
(43,
49)
48)
50)
46)
61)b
48)
%o17.5 (95% CI)
0.8 (0.0, 1.5)
1.6 (0.2, 5.7)
0.3 (0.0, 1.4)
0
0
1.0 (0.8, 4.6)
PTH (ng/l) Mean (95% CI)
Dietary Calcium (mg/d) Mean (95% CI)
%o50 (95% C I)
61
63
60
74
38
68
(57,
(55,
(55,
(66,
(30,
(60,
65)
72)
65)
81)
47)b
76)
21.6
25.6
20.2
19.4
17.7
23.8
(2
(2
(1
(1
(1
(2
0.7,
4.0,
9.2,
7.9,
6.2,
1.8,
22.4)
27.2)
21.2)a
20.9)
19.2)
25.8)b
357
270
386
369
338
457
(331,
(239,
(353,
(322,
(286,
(384,
384)
302)
420)a
415)
389)
531)b
Abbreviations: CI, confidence interval; PTH, parathyroid hormone.
a
Significantly different from Jakarta, Po0.01.
b
Significantly different from other two ethnic groups, Po0.01.
European Journal of Clinical Nutrition
Vitamin D & PTH in Southeast Asian Women
TJ Green et al
376
Plasma parathyroid hormone (ng/L)
30
Figure 1 Plasma parathyroid hormone by 25-hydroxyvitamin D
concentration in 504 females (18–40 years). The figure depicts the
slopes of the fitted regression lines (solid) with 95% CI (shaded area).
The regression predicts an inflection point at 52 nmol/l plasma 25hydroxyvitamin D.
and higher rates of insufficiency (68% and 74% cf 38%,
respectively; Po0.001). The mean PTH hormone concentration was 21.6 pg/ml. Women in Jakarta had higher mean
PTH concentrations than women in Kuala Lumpur (Po0.01).
Within the Kuala Lumpur ethnic groups, Indian (23.8 pg/ml)
women had higher PTH concentrations than Malay (19.4 pg/ml)
or Chinese (17.7 pg/ml) women (Po0.01).
The relationship between plasma 25-hydroxyvitamin D
concentration and PTH is depicted in Figure 1. We
determined that 52 nmol/l was the cutoff concentration of
plasma 25-hydroxyvitamin D at which the difference in
slopes of the regression lines below and above this point, was
maximum, and above which there was no increase in
parathyroid hormone concentration (i.e. slope of line not
different from 0). Below and above a 25-hydroxyvitamin D
concentration of 52 nmol/l the slopes were 0.18 (different
from 0; P ¼ 0.003) and -0.01 (P ¼ 0.775), respectively. The
difference between the slopes of the two lines was 0.17
(P ¼ 0.053). At a cutoff of 52 nmol/l for 25-hydroxyvitamin D
the R2 for the model was 3% (P ¼ 0.002) higher than that for
any other model. Figure 2 gives the mean plasma PTH for
each tertile of plasma 25-hydroxyvitamin D by tertile of
dietary calcium. In the regression model, tertile of 25hydroxyvitamin D (P ¼ 0.003) concentration but not tertile
of calcium intake (P ¼ 0.531) was associated with PTH
concentration. There was no significant interaction between
tertile of calcium intake and 25-hydroxyvitamin D concentration with plasma PTH (P ¼ 0.611).
Discussion
Less than 1% of women had plasma 25-hydroxyvitamin D
concentrations indicative of deficiency (o17.5 nmol/l) sugEuropean Journal of Clinical Nutrition
< 207
207-385
> 385
25
20
15
10
5
0
<39
39-52
.53
Plasma 25-Hydroxyvitamin D (nmol/L)
Figure 2 Mean (95% CI) plasma parathyroid hormone concentration by tertile of plasma 25-hydroxyvitamin D values and tertile of
calcium intake.
gesting that the risk of osteomalacia is probably low in this
population. However, over 60% of women had concentrations indicative of vitamin D insufficiency (o50 nmol/l),
which may have a detrimental effect on bone health and
increase the risk of osteoporotic fracture later in life
(Dawson-Hughes et al., 1997; Chapuy et al., 2002; Holick,
2004). Moreover, for women who become pregnant low
maternal vitamin D status increases the risk of vitamin D
deficiency in their infants (Hollis and Wagner, 2004).
Maternal and cord blood 25-hydroxyvitamin D are correlated and supplementation with vitamin D during pregnancy improves infant vitamin D status and may improve
birth and infant health outcomes (Brooke et al., 1980).
It was somewhat unexpected that despite living in cities
near the equator, many young women in Jakarta (61S) and
Kuala Lumpur (21N) had suboptimal vitamin D status.
Nevetheless, their mean plasma 25-hydroxvitamin D concentrations are higher than those reported in Beijing (391N)
and Ulaanbaatar, Mongolia (491N), where rickets and
osteomalacia are not uncommon (Du et al., 2001; Fraser,
2004). For example, in a Beijing survey of adolescent girls in
the winter the mean 25-hydroxyvitamin D concentration
was only 20 nmol/l with 40% of girls classified as deficient
(25-hydroxyvitamin D o12.5 nmol/l) (Du et al., 2001).
We found that Chinese women in Kuala Lumpur had
B14 nmol/l higher 25-hydroxyvitamin D concentrations
and lower rates of insufficiency than Indian and Malay
women. These findings by ethnic group are similar to those
reported in older women of postmenopausal age living in
Kuala Lumpur, where mean 25-hydroxyvitamin D concentrations were substantially lower in Malay (44 nmol/l) than
in Chinese women (68 nmol/l) (Rahman et al., 2004).
Vitamin D & PTH in Southeast Asian Women
TJ Green et al
377
Although our study was not designed to assess the reasons
for the high rate of vitamin D insufficiency in women living
in Jakarta and Kuala Lumpur there are a number of possible
explanations. These explanations are somewhat speculative
because we did not specifically assess in our survey the
factors that determine vitamin D synthesis in the skin. The
darker skin of Asian women, caused by greater amounts of
skin melanin – which acts as a natural sunscreen – is one
explanation. Indeed the finding that Malay and Indian
women have lower vitamin D status than Chinese women
would seem to support this explanation. Another possibility
is that women may follow a cultural or religious dress custom
that leaves little skin exposed; indeed, this may explain why
Malay women, who are predominantly Muslim and the most
covered, have lower vitamin D status. Finally, women may
be avoiding the sun to get away from the heat, or for
cosmetic reason. In a recent survey in Hong Kong of women
(n ¼ 547), 62.3% indicated that they did not like going in the
sun (Kung and Lee, 2006).
We caution that we cannot generalize these results to all
women living in Indonesia and Malaysia or even to all
women living in Jakarta and Kuala Lumpur because
convenience samples of women were recruited and they
may not be representative of the population. Further, based
on their high educational attainment, it is likely that women
in our study were of above average socio-economic status.
Whether the women in our study have higher or lower
plasma 25-hydroxyvitamin D concentrations than other
urban-dwelling or rural women is not known. It is possible
that rural women might spend more time outdoors. At high
latitudes there is significant seasonal variation in plasma 25hydroxyvitamin D concentrations (Rockell et al., 2006)
therefore, vitamin D status must be assessed over a full year.
Women in our study were recruited over part of year;
however, the seasonal variation in UV light at the equatorial
latitudes of Kuala Lumpur and Jakarta is small, suggesting
that our results should reflect vitamin D status over the
whole year.
Based on the data, we predict that a plasma 25-hydroxyvitamin D concentration of 52 nmol/l is needed to
maximally suppress PTH in our population. The difference
in the slopes of the lines of regression above and below this
point does not quite reach the conventional 0.05 standard of
statistical significance (P ¼ 0.053). However, the slope of the
regression line between plasma PTH and 25-hydroxyvitamin
D below 52 nmol/l is significantly different from zero
(Po0.003), whereas, above this concentration the slope of
regression line does not differ from zero (P ¼ 0.775). Further,
our estimate is similar to estimates obtained in other
populations and the same as the global estimate for the
optimal 25-hydroxyvitamin D concentration of 450 nmol/l
suggested by Lips, (2004). Aloia et al., (2006) recently
conducted a systematic review that included 31 studies that
reported a 25-hydroxyvitamin D threshold for PTH suppression. There was a wide range of thresholds for 25-hydroxyvitamin D of 25 to 122 nmol/l with those using the
radio-immuno assay for vitamin D analysis clustered around
40–50 nmol/l. Only one of these studies was in women of
childbearing age; in that study Lamberg-Allardt et al. (2001)
reported a threshold of 80 nmol/l in Finish women. More
studies are required in non-European populations to determine the threshold for other ethnicities.
In our study, parathyroid hormone concentrations decreased across the categories (low, medium, high) of plasma
25-hydroxyvitamin D but within each category of vitamin D
status, calcium intake had no effect on PTH concentrations
(Figure 2). This result differs from that of Steingrimsdotter
(2005), who reported, in an Icelandic population, the effect
of calcium intake on PTH was more pronounced in those
with low than high serum 25-hydroxyvitamin D. It may be
that calcium intakes amongst women in our study were not
high enough to suppress PTH. Women in the highest
category of calcium intake in our population had a mean
calcium intake of 657 mg/day, whereas the lowest tertile of
calcium intake in the Icelandic study was defined as less than
800 mg/day; the highest tertile was defined as greater than
1200 mg/day. We acknowledge that the imprecision of
categorizing women into tertiles of calcium intake based
on a single 24-h recall may severely attenuate our ability to
detect the interaction between calcium, PTH and 25hydroxyvitamin D if one exists. Further, there may be
cultural practices that dictate seasonal variation in the
consumption pattern of calcium containing food sources.
In conclusion, based on maximal suppression of PTH we
estimate an optimal 25-hydroxyvitamin D concentration of
50 nmol/l in these women of child-bearing women living in
Jakarta and Kuala Lumpur. Vitamin D has many different
roles, and cutoffs for 25-hydroxyvitamin D up to 100 nmol/l
have been proposed for some non-skeletal outcomes
(Dawson-Hughes et al., 2005; Bischoff-Ferrari et al., 2006). Nevertheless, even using a conservative cutoff of 50 nmol/l many
of the women in our study had suboptimal vitamin D status.
Strategies to improve the vitamin D status of Indonesian and
Malaysian women may be required, such as taking supplements or consuming vitamin D fortified foods.
Acknowledgements
This work was supported by a research grant from Fonterra
Brands Limited.
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