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U.S. Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, and * Section of Endocrinology, Department of Pediatrics, Baylor College of Medicine and Texas Children's Hospital, Houston, TX 77030
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • human nutrition • calcium metabolism • stable isotopes • bone mineralization • puberty
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Bell et al. 1991 and 1993
, Bell 1997
, Gilsanz et al. 1991
, Fuleihan et al. 1994
, Harris and Dawson-Hughes 1998
, Li et al. 1989
). However,
far fewer data are available comparing Hispanics with other ethnicities
(Ellis et al 1997
, McClure et al 1997
,
Reasner et al 1990
, Sainz et al 1997
,
Villa et al 1995
).
This lack of data regarding Hispanics is due in part to the diversity
of background of Hispanics residing in the United States. For
appropriate comparisons to be made, it is necessary to study Hispanics
of similar background (Villa 1994
). This is feasible in
parts of the southwestern United States, such as southeastern Texas,
where >80% of the Hispanic population is of Mexican heritage.
Lower levels of 25-hydroxyvitamin D
[25(OH)D]6
and greater levels of parathyroid hormone (PTH) in Mexican-American
(MA) adults compared with non-Hispanic Caucasians (CAU) have been
reported by Reasner et al. (1990)
. This pattern is
similar to that reported for African-Americans (Harris and Dawson-Hughes 1998
) and more recently for Asian Indians
(Awumey et al. 1998
). However, unlike African-Americans,
MA adults and children do not demonstrate greater bone mass than CAU,
although they may have a lower risk of osteoporotic fractures
(Ellis et al. 1997
, McClure et al. 1997
,
Villa et al. 1995
).
Our goals in this study were to evaluate the following: 1) whether ethnic differences in 25(OH)D and PTH hormone concentrations identified in adults exist in children and 2) whether these differences are related to measures of bone and mineral metabolism including bone mass, calcium absorption, excretion or bone calcium deposition. We hypothesized that similarities in bone and mineral metabolism would be found between MA and CAU prepubertal girls despite lower levels of 25(OH)D in the MA girls.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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A total of 19 MA and 19 CAU girls participated in the study. Girls were recruited who were 7.0–8.9 y of age and who resided in the greater Houston area. This area has over one-half million people of MA heritage. Girls were chosen according to the criterion that all of the subjects' grandparents were of MA (or CAU) heritage. Of the 19 MA girls, 13 were either born in Mexico or had at least one parent born in Mexico. The other 6 girls had 4 grandparents of Mexican origin.
All girls were healthy and denied substance abuse. None had a history compatible with an eating disorder. None was taking any prescription medications. The protocol was approved by the Institutional Review Board for Human Subject Research at Baylor College of Medicine and Affiliated Hospitals. Informed written consent was obtained from the parents of each subject before the study.
Clinical protocol.
Studies were conducted within the General Clinical Research Center (GCRC) of the Texas Children's Hospital. This report describes initial results from a longitudinal study evaluating the effects on calcium metabolism of diets containing ~1200 mg/d calcium over a period of several years. At study entry (1–2 mo before the initial study), each girl was provided by the research dietitian an individualized dietary plan on the basis of her food preferences to maintain a 1200 mg/d calcium intake. Girls and their families were specifically counseled regarding strategies to increase their usual calcium intake using dietary methods. Follow-up, bimonthly 24-h dietary recalls were done to assure the maximum possible compliance.
At the time of admission, a complete physical examination, including
Tanner staging (Tanner 1962
), was performed by one of
two pediatric endocrinologists. All girls were Tanner 1 on the basis of
this examination.
After an overnight fast (except for water), a heparin lock catheter was inserted and, at 0800 h, 20 mL blood was withdrawn for routine laboratory tests and hormone levels. Subsequently, 2.5 µg/kg (maximum 100 g) of gonadotropin-releasing hormone (GnRH) was administered intravenously. Blood was collected for serum luteinizing hormone/follicle-stimulating hormone (LH/FSH) at 30 and 60 min after the infusion. After the GnRH was infused, each subject was given a breakfast containing ~350 mg of calcium. Toward the end of breakfast, the subjects were given 46Ca (0.4 µg/kg), which had been premixed (and allowed to equilibrate in the refrigerator for 12–24 h) with 120 mL of milk (the calcium in this milk was part of the total 350 mg given with breakfast). One hour after the GnRH infusion, 42Ca (80 µg/kg) was infused over 2 min via the heparin lock catheter. After infusion, the heparin lock was infused with 3 mL saline and the hub of the catheter replaced. Blood (2 mL) was removed for mass spectrometric analysis at 6, 12, 20, 30, 45, 60, 120, 180, 240 and 480 min after completion of the infusion. Beginning with breakfast, a complete 24-h urine collection was obtained in 8-h aliquots.
A complete dietary food record was maintained during the 24-h period
when the subjects were in the GCRC. As part of the record, individual
food portions were weighed before being given to the subjects; any
uneaten food remaining after the meal was weighed as well. At the end
of the 24-h period, the subjects were discharged and instructed to
collect three urine samples each day for five additional days. Subjects
and their parents were instructed to record all foods ingested during
the 48 h after discharge. Nutrient intakes were calculated using
the Minnesota Nutrition Data System (1993)
as the mean daily intake
from these records (one inpatient and two post-discharge days).
Body composition.
Body composition measurements were performed using a Hologic QDR-2000
dual-energy X-ray (DXA) absorptiometer (Hologic, Waltham, MA). The
whole body was scanned in the single-beam mode. Total body bone mineral
content (BMC) and percentage of body fat (g/100 g) were determined from
the DXA measurements as described by Ellis et al. (1997)
.
Analytical methods: stable isotope studies.
Urine and serum samples were prepared for mass spectrometric analysis
as previously described (Abrams et al. 1995
) with the
use of an oxalate precipitation technique. Samples were analyzed for
isotopic enrichment with a Finnigan MAT 261 (Bremen, Germany) magnetic
sector thermal ionization mass spectrometer. Each sample was analyzed
for the ratio of 42Ca/43Ca and
46Ca/43Ca with correction for fractionation to
the reference 44Ca/43Ca ratio. Accuracy of this
technique for natural abundance samples compared with standard data is
0.1%. Precision, including sequential measurement of the same sample
(on different filaments) over a period of time, is 
0.15%.
Analytical methods: hormonal and biochemical studies.
Serum bone-specific alkaline phosphatase activity was measured with an
immunoradiometric assay (Tandem-R Ostase, Hybritech, San Diego, CA).
Serum intact PTH was measured by using an immunoradiometric assay kit
by Diagnostic Systems Laboratories (Webster, TX). Both serum 25(OH)D
and 1,25-dihydroxyvitamin D concentrations were measured by using an
RIA kit by Incstar (Stillwater, MN). Intact osteocalcin was measured by
RIA as described by Gundberg et al. (1998)
. LH and FSH
were measured with the use of time-resolved fluoroimmunoassay kits by
Wallac (Gaithersburg, MD). Serum phosphorus, calcium and total alkaline
phosphatase activity were measured using standard clinical laboratory
techniques. Urinary calcium was measured using atomic absorption
spectrophotometry.
Calculations and modeling.
The compartmental model used for calcium kinetics is similar to that
described by Neer et al. (1967)
, which we have adapted
for studies in children and adolescents (Abrams et al. 1996
). Our model is based on three sequential pools before
calcium deposition in the "deep" bone calcium pool. The mass of the
third compartment is referred to as the exchangeable pool of bone
(Bronner and Abrams 1998
). Bone calcium deposition rate
(Vo+) is the rate of flow of Ca to the final
pool. Compartmental modeling of the data was performed with the aid of
the SAAM (Simulation, Analysis and Modeling) program (Berman and Weiss 1978
). The ratio of Vo+ and the
exchangeable pool can be determined (ko+) as a
rate constant to evaluate the activity of the exchangeable calcium
pools (Bronner and Abrams 1998
).
Endogenous fecal excretion of calcium was estimated as 1.5
mg/(kg · d) (Abrams et al. 1991
, Heaney and Recker 1994
). Errors in kinetic rates related to this estimate
are likely to be minimal because even an improbably large error in this
estimate [i.e., 0.5 mg/(kg · d)] would have at most a 2–3% net
effect on the calculated kinetic parameters in the older adolescents in
this study (Abrams et al. 1996
).
Statistical methods.
Sample size was chosen to provide an 80% chance (power) of
detecting a 12% difference in fractional absorption between racial
groups (P < 0.05). This is comparable to the magnitude
of the difference in calcium absorption between Caucasian and
African-American girls found in our previous study (Abrams et al. 1995
). Data were compared between MA and CAU for unadjusted
variables using ANOVA. Seasonal effects on vitamin D status were
evaluated by using ANOVA after separating studies into those done
during "summer" (middle of May through early October) and
"winter" (late November–early April) months. Data were also
compared between MA and CAU by using analysis of covariance (ANCOVA) to
determine whether calcium absorption and vitamin D levels were
different among ethnic groups after adjusting for the season during
which the study was performed. All data are presented as means ±
SEM.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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).However, only 2 of the 19 MA girls were obese, with body mass index
(BMI) of 25.1 and 27.0 kg/m2 and a Z-score for
body weight >2.0. All other girls had BMI < 22
kg/m2. Whole-body bone mineral content (g) and bone mineral
density (g/cm2) (data not shown) also did not differ
between groups. This lack of difference persisted when height and
weight were included as covariates in the analysis.
|
).Serum phosphorus in the MA girls was not related to dietary calcium
(Table 3
)or phosphorus intake. Phosphorus intake averaged 1253 ± 65 mg/d
in the MA girls and 1315 ± 64 mg/d in the CAU girls
(P = 0.50). Serum total alkaline phosphatase activity
and bone-specific alkaline phosphatase values were greater in the MA
girls, although serum osteocalcin concentrations were not significantly
different.
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. The ratio of the bone calcium deposition rate
(Vo+) to the exchangeable pool mass also did not
differ between MA and CAU girls (0.69 ± 0.03 vs. 0.66 ±
0.05, respectively, P = 0.63). Neither
Vo+ nor ko+ was
significantly correlated with serum PTH levels.
Fractional calcium absorption and urinary calcium excretion in this
study are similar to those we reported previously for premenarcheal CAU
girls who were ~9 y old (Abrams et al. 1995
). Dietary vitamin D
intake did not differ between MA and CAU girls (7.8 ± 2.9 vs.
7.1 ± 2.2 µg/d, respectively, P = 0.40). There
were no significant correlations between body weight, body mass index,
or percentage of body fat and serum PTH levels for either the entire
group of girls or for girls of either ethnic group considered
separately (P > 0.3 for each comparison).
The peak stimulated serum LH values did not differ between groups
(Table 4
).Oerter et al. (1990)
evaluated the GnRH-stimulated serum
LH/FSH ratio and proposed that a serum LH/FSH ratio of <0.6 is
consistent with a prepubertal status. In this study, the mean serum
LH/FSH ratio was 0.3 and was <0.6 in all girls.
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; Fig. 1
).These persisted when the two MA girls with BMI > 25
kg/m2 were excluded from the analysis (values for PTH for
these two girls were 5.05 and 3.76 pmol/L). Two MA subjects studied
during the winter had 25(OH)D values <40 nmol/L (values were 34.7 and
35.3 nmol/L). However, there were no significant ethnic differences in
1,25-dihydroxyvitamin D concentration.
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).Differences in 25(OH)D values between MA and CAU girls were significant
during both summer (P = 0.04) and winter
(P = 0.007).
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However, 25(OH)D and PTH concentrations were not closely correlated (r = 0.14, P = 0.44). This lack of correlation persisted when data were evaluated on the basis of season or ethnicity. Similarly, there was no close correlation between 25(OH)D values and serum P or PTH values and serum P in study subjects considered together or separately by ethnicity.
To evaluate whether the small number of girls with low 25(OH)D values was responsible for the ethnic differences in PTH, we excluded nine girls with 25(OH)D <50 nmol/L. In this analysis, we found that ethnic differences in PTH (1.89 ± 0.56 pmol/L for 14 CAU girls vs. 4.31 ± 0.66 pmol/L for 12 MA girls, P = 0.01) were similar to those seen when comparing all of the study subjects.
There were no significant correlations between 25(OH)D levels,
1,25-dihyroxyvitamin D concentration or PTH levels and fractional
absorption of calcium, urinary Ca excretion or Ca kinetic values. We
previously were unable to identify a correlation between 25(OH)D
concentration and fractional calcium absorption in a group of 71 CAU
and African-American girls aged 5–16 y (Abrams et al. 1995
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). These similarities in calcium metabolism and bone
mass are present despite significant ethnic differences in serum
25(OH)D and PTH concentrations.
The ethnic differences in 25(OH)D and PTH found in this study are
similar to those reported by Reasner et al. (1990)
for
MA and CAU adults. They are also similar to ethnic differences in
25(OH)D and PTH between CAU and both African-Americans and Asian
Indians (Awumey et al. 1998
, Bell 1997
).
Recently, Harris and Dawson-Hughes (1998)
reported
seasonal variability in 25(OH)D concentrations in young adult women
living in the northern part of the United States. Bell et al. (1985)
reported increased PTH in obese subjects, but this was
not the case in our study subjects because only two of the MA girls
were obese, and omitting their data from analyses did not alter the
significant differences found between MA and CAU girls.
It has been hypothesized that increased skin pigmentation is
responsible for the lower 25(OH)D seen in non-CAU relative to CAU
populations. Lower vitamin D stores may place children at risk for
rickets. This is a well-characterized problem, especially for children
with dark skin pigmentation and limited sun exposure or those with very
low dietary vitamin D and calcium intakes. However, in the subjects in
our study, similar to those African-Americans studied by Harris and Dawson-Hughes (1998)
, there were no ethnic differences in
1,25-dihydroxyvitamin D concentrations. Nonetheless, the greater PTH
levels may represent a risk factor for accelerated bone loss.
We found that in a southern climate, 25(OH)D levels in MA children were all >30 nmol/L and most were >40 nmol/L. These values indicate that most MA girls in the study maintained adequate vitamin D stores during the winter. However, our findings may not be universally applicable because we counseled the subjects extensively to increase their calcium intake using milk and other dairy products. These products are largely fortified with vitamin D, and therefore vitamin D intakes might have been higher than those achieved by MA children who have lower calcium intakes.
A correlation between 25(OH)D and PTH concentrations was not identified in our population. In general, however, such a correlation is related to increases in PTH that occur with 25(OH)D levels below those of our study subjects. Although it has been hypothesized that elevated PTH in non-CAU populations is related to a deficiency of 25(OH)D in these groups, our data suggest that increases in PTH in MA children do not require an overt vitamin D deficiency. Exclusion of subjects with 25(OH)D values <50 nmol/L had no effect on the ethnic differences in PTH. This conclusion is supported by the lack of ethnic differences in 1,25-dihydroxyvitamin D concentration between subject groups.
The similarity in calcium absorption and urinary calcium excretion in
MA and CAU girls is in contrast to the greater calcium absorption and
lower urinary Ca excretion reported for African-American relative to
CAU girls (Abrams 1995
, Bell et al. 1993
,
Bell 1997
). It has been suggested that relative PTH
resistance in African-Americans leads to decreased bone turnover and
greater bone mass in African-Americans relative to CAU (Fuleihan et al. 1994
). Although this mechanism may not exist for other
non-CAU ethnic groups, our finding of greater serum phosphorus in the
MA girls despite elevated PTH levels may indicate some degree of PTH
resistance in these girls (Food and Nutrition Board
1997
). However, only one of the MA girls ( a non-obese girl
with a BMI of 15.0 kg/m2) had a PTH level above the usually
identified upper limit of normal for this age group of 80 ng/L (8.51
pmol/L) (Kruse 1992
), suggesting that this effect does
not generally lead to hyperparathyroidism.
Although we did not find a relationship between 25(OH)D concentration and calcium absorption, it is possible that supplementation of vitamin D would enhance bone mass or increase calcium absorption in MA girls. At the present time, however, our results provide no evidence for adjusting dietary recommendations for mineral or vitamin D intake by MA girls.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 This work is a publication of the U.S.
Department of Agriculture (USDA)/Agricultural Research Service (ARS)
Children's Nutrition Research Center, Department of Pediatrics, Baylor
College of Medicine and Texas Children's Hospital, Houston, TX.
2 Supported in part with federal funds from
the USDA/ARS under Cooperative Agreement number 58–6250–6-001, the
National Institutes of Health, NCRR General Clinical Research for
Children grant number RR00188 and National Institutes of Health
AR43740.
3 Contents of this publication do not necessarily
reflect the views or policies of the USDA, nor does mention of trade
names, commercial products, or organizations imply endorsement by the
U.S. Government.
4 The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 USC section 1734 solely to indicate this fact.
6 Abbreviations used: BMC, bone mineral content;
BMI, body mass index; CAU, Caucasian; DXA dual-energy X-ray
absorptiometry; FSH, follicle-stimulating hormone; GnRH,
gonadotropin-releasing hormone; ko+, ratio of
bone calcium deposition rate to the mass of the exchangeable pool in
bone; LH, luteinizing hormone; MA, Mexican-American; 25(OH)D,
25-hydroxyvitamin D concentration; PTH, parathyroid hoormone;
Vo+, bone calcium deposition rate.
Manuscript received September 24, 1998. Initial review completed November 6, 1998. Revision accepted December 2, 1998.
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