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U.S. Department of Agriculture/ARS Children’s Nutrition Research Center and Section of Neonatology, Department of Pediatrics, Baylor College of Medicine and Texas Children’s Hospital, Houston, TX 77030 and * Western Human Nutrition Research Center, University of California at Davis, Davis, CA 95616
2To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSKinetic modelingRESULTSDISCUSSIONREFERENCES |
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2.5%. We conclude that
compartmental modeling can be used to describe zinc kinetics in
children, and that the body weight–corrected zinc pool masses are
significantly greater in children than in adults.
KEY WORDS: • children • compartmental model • stable isotope • zinc metabolism
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSKinetic modelingRESULTSDISCUSSIONREFERENCES |
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). Compartmental models have advanced the
understanding of mineral metabolism by allowing mathematical estimation
of the masses of, and exchanges between kinetically distinct body
compartments. Radioisotope-based zinc compartmental models have
been used to examine the physiologic responses to high zinc intakes in
healthy adults and those with smell or taste dysfunction, as well as
the effect of aging on zinc metabolism (Foster et al. 1979
, Wastney et al. 1986
and 1992
).
Radioisotopes cannot be used safely in healthy children, and
radioisotope-based models from animal or adult studies cannot be
employed in children without extrapolation of the data. Recently, a
stable isotope–based model of zinc kinetics was reported in adults
(Lowe et al. 1997
); however, in contrast to earlier
radioisotope models (Foster et al. 1979
, Wastney et al. 1986
and 1992
), it does not include any compartments
representing red blood cell zinc. This model and others (Lowe et al. 1997
, Miller et al. 1998
) have allowed zinc
metabolism in adults to be studied using stable isotopes rather than
radioisotopes. Comparable data have not been available for children due
to the technical difficulties involved in performing such studies. The
aims of this study were to use stable isotope–based multicompartmental
modeling techniques to describe zinc metabolism in children; to extend
a current stable isotope model (Lowe et al. 1997
) to
include red blood cell data; and to compare kinetic parameters in
children with those previously reported in adults. |
SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSKinetic modelingRESULTSDISCUSSIONREFERENCES |
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). Study diet.
After the subjects were recruited, their usual zinc intake was
estimated using a 24-h food recall conducted by a registered dietician.
Subjects received advice on how to increase their current zinc intake
to 12 mg/d, the current recommended dietary allowance for girls aged
11–14 y (NRC 1989
), by increasing their intake of meat, chicken or
zinc-fortified breakfast cereals. They consumed this diet at home
for 21 d before being admitted to the Metabolic Research Unit of
the USDA/ARS Children’s Nutrition Research Center in Houston, Texas,
for a 6-d zinc metabolic study. Subjects were provided with kitchen
scales, and they and their parents were instructed on the proper
technique of keeping a weighed food record for 3 d before
admission. These records, and those of the foods consumed during the
6-d admission period of the metabolic studies, were used to calculate
the subjects’ zinc intake using the Minnesota Nutrition Data System
(University of Minnesota, version 2.91, Food Database 12A, Nutrition
Database 27).
Isotope and sample preparation.
67Zinc (74% enrichment by mass) and 70zinc (90% enrichment by mass) were produced in the former Soviet Union and obtained as the oxide from Tracer Sciences (Toronto, Canada). Aqueous solutions of the tracers, prepared by the Investigational Drug Service of Texas Children’s Hospital, Houston, Texas, were tested for pyrogenicity and sterility before use.
After 21 d of dietary adaptation, followed by an overnight fast, subjects were admitted to the Metabolic Research Unit. An intravenous catheter was inserted in one arm; each subject drank 1.1 mg of the 67zinc-enriched tracer that had been mixed with milk 18–24 h earlier; 0.5 mg of the 70zinc-enriched tracer was infused intravenously over 60 s by venipuncture in the other arm. Blood samples were drawn at 5, 10, 15, 20 and 30 min, and at 1, 2, 3, 4, and 8 h from the intravenous catheter; and at 24, 48, 72, 96, 120 and 144 h by venipuncture. A complete 6-d urine and stool collection was started immediately after tracer administration. Urine samples were collected, stored and analyzed in 8-h pools. Stool samples were collected, stored and analyzed individually. Blood samples were collected in zinc-free tubes (Monovette AH, Sarstedt, Newton, NC), and plasma was separated by centrifugation (1000 x g for 10 min). An equal volume of 9 g/L sodium chloride was added to the red blood cell pellet and mixed gently. The resulting suspension was centrifuged and the supernatant discarded. This process was repeated three times to remove any residual plasma from the red blood cells. Plasma and red blood cell samples were stored at -80°C pending analysis.
Zinc concentrations of plasma, red blood cells, urine and feces
were measured by flame atomic absorption spectroscopy. Plasma, red
blood cell, urine and fecal samples were purified using an anion
exchange method (Abrams et al. 1997
). Aliquots of 12 mL
of urine, 0.5 mL of plasma, 0.5 mL of red blood cells and 1 g of
feces were digested with 10 mL of 15 mol/L nitric acid overnight on a
hot plate. The dried sample was dissolved in 1 mL of 6 mol/L
hydrochloric acid and loaded onto an anion exchange resin column (AG
1-X8 resin, Bio-Rad Laboratories, Hercules, CA) that had been
prewashed with 10 mL of double-distilled water and 5 mL of 6 mol/L
hydrochloric acid. The column was washed with serial 5-mL aliquots of 6
mol/L, 3 mol/L, 2 mol/L, 1 mol/L and 0.5 mol/L hydrochloric acid, and
the samples eluted with 6 mL of double-distilled water. Ten
microliters of 0.23 mol/L phosphoric acid was added and the sample
dried on a hot plate overnight before being resuspended in 0.5 mL
double-distilled water. The resulting sample solution (10–20
µL), 2 µL of 0.23 mol/L phosphoric
acid and 6 µL of silica suspension were loaded onto
rhenium filaments. Trace element–free reagents and disposables were
used throughout.
Isotope enrichments were measured by thermal ionization magnetic sector
mass spectrometry (Finnigan MAT 261, Bremen, Germany). Isotope ratios
were expressed with respect to the nonadministered isotope,
66zinc, and corrected for temperature- and
mass-specific differences in fractionation, using the ratio of
64zinc to 66zinc. Ten scans were performed per
block, and replicate blocks repeated until the desired degree of
precision (<0.2%) was obtained. Isotope ratios were converted to
tracer:tracee ratios as described previously (Cobelli et al. 1987
, Lowe et al. 1997
).
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Kinetic modeling |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSKinetic modelingRESULTSDISCUSSIONREFERENCES |
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Figure 1
shows the models used; circles represent kinetically distinct
compartments, and arrows represent the transfers between compartments.
The basic model is based on a stable isotope model described previously
in adults (Lowe et al. 1997
), which in turn was based on
radioisotope models developed by Foster et al. (1979)
and Wastney et al. (1986)
. This model has been shown to
have a priori identifiablity (Lowe et al. 1997
,
Saccomani et al. 1994
) such that, for any given data
set, all of the unknown parameters have one unique solution. The basic
model consists of six compartments, i.e., three gastrointestinal
compartments, a central "plasma" compartment and two kinetically
distinct tissue compartments. Dietary zinc enters the first of a
unidirectional chain of three compartments (#4, 5 and 6). Zinc is lost
from compartment #6 by excretion in the feces. Zinc is absorbed from
the second gastrointestinal compartment (#5) to a central "plasma"
compartment (#1). Zinc from this compartment undergoes bidirectional
transfers with two kinetically distinct compartments (#2 and 3). These
are denoted "fast" and "slow" to reflect their different
turnover rates. In addition, zinc from the central compartment is lost
in urine (urinary excretion) and into the gastrointestinal tract
(endogenous fecal zinc excretion). There is a further loss of zinc from
the central compartment, which represents transfer of tracer to a
large, slowly turning over compartment (Lowe et al. 1997
). This compartment turns over too slowly to be resolved in
short-term tracer studies (Lowe et al. 1997
). Zinc
in this compartment has been estimated to have a half-life of 50
d (Lowe et al. 1997
), and studies of many months
duration are required to identify it (Wastney et al. 1986
). In this study, transfer of zinc to this compartment was
modeled as an irreversible loss from the system.
|
, Wastney et al. 1986
), the basic model was
modified to include a single red blood cell compartment (#10). Previous
studies have identified two red blood cell compartments (Foster et al. 1979
, Wastney et al. 1986
), but the
second of these compartments turns over too slowly to be identified in
our short-term study. Addition of a second red blood cell
compartment did not improve the fit of the red blood cell data. The total amount of tracee excreted in the urine and feces was calculated from the complete urine and fecal collections, averaged over the duration of the study, and entered as data in the tracee model.
Tracer model.
Oral tracer was introduced into compartment #4, and intravenous
tracer into compartment #1. Plasma data were expressed as tracer:tracee
ratio, urine and fecal data as cumulative losses, and red blood cell
zinc as total red blood cell tracer (assuming a plasma volume of 70
mL/kg and a hematocrit of 0.38) (Lenter 1984
). Each
study, therefore, had six sets of tracer data, i.e., the plasma
tracer:tracee ratio of the orally administered tracer, the plasma
tracer:tracee ratio of the intravenously administered tracer, the
cumulative fecal excretion of the orally administered tracer, the
cumulative fecal excretion of the intravenously administered tracer,
the cumulative urinary excretion of the orally administered tracer and
the cumulative urinary excretion of the intravenously administered
tracer. These data sets were used simultaneously to solve the model.
The complete seven-compartment model had two additional tracer data
sets, namely, the total amount of orally administered tracer in the red
blood cells and the total amount of intravenously administered tracer
in the red cells
Modeling.
Kinetic data were modeled using SAAM II, which uses a weighed,
nonlinear least squares iteration algorithm (SAAM Institute, Seattle,
WA). Measurement errors were assumed to be normally distributed about a
mean of zero, and to have a fractional standard deviation of either 0.1
(for tracer data) or 0.05 (for tracee data). SAAM II was used to
estimate the mass of each compartment (where
Mj denotes the mass of compartment
j) and the fractional transfer coefficient between
compartments [where
k(i,j) represents the
fraction of compartment j entering compartment
i per unit time]. These can be used to calculate the
flux between compartments, where
Flux(i,j) represents the mass of
compartment j entering compartment i per
unit time from the following equation:
 |
The fractional transfer coefficient representing loss of zinc to the large slowly exchanging compartment was denoted k(7,1) to distinguish it from the loss of zinc into the urine, k(0,1), and to indicate that it was entering a large unresolved compartment (#7). Masses are given as mg, fractional transfer coefficients as d-1 and fluxes as mg/d.
The primary kinetic parameters derived from the model were
M1 and the 13 fractional transfer
coefficients. Other compartmental masses and intracompartmental fluxes
can be derived from these. In addition, the following could be
calculated (Lowe et al. 1997
):
 |
 |
Statistical analyses.
Statistical analyses were carried out using StatView version 4.51
(Abacus Concepts, Berkeley, CA) for Macintosh. Normally
distributed variables were compared using paired or two-sample
t tests, as appropriate. All values are given as means
± SD, unless otherwise stated. Differences were
considered significant at P < 0.05. The precision
of kinetic parameters from the compartmental models was assessed using
the standard deviation and CV estimated from the model by SAAM II from
the covariance matrix at the least squares fit. Differences between
compartmental masses and previously published estimates for adults
(Lowe et al. 1997
) were assessed using two-sample
t tests. Compartmental masses from the
six-compartment model (excluding the red blood cell compartment)
and the seven-compartment model (including the red blood cell
compartment) were compared using paired t test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSKinetic modelingRESULTSDISCUSSIONREFERENCES |
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.
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The kinetic parameters for each subject determined using the complete
model are shown in Table 1
. The primary kinetic parameters
(M1 and the 13 fractional transfer
coefficients) were all estimated with a CV < 20%. The masses of
the seven compartments were estimated with precisions (CV) of 6.9
± 1.6% (M1), 16.2 ± 8.0%
(M2), 4.8 ± 1.4%
(M3), 10.9 ± 4.6%
(M4), 16.1 ± 5.1%
(M5), 9.5 ± 1.8%
(M6) and 5.7 ± 1.4%
(M10). Figure 2
shows fits for the eight tracer data sets for a representative subject.
|
Omission of the red blood cell compartment significantly increased the mass of the central plasma compartment (2.4 ± 0.9 vs. 2.5 ± 0.9 mg, P = 0.05) and the "fast" compartment (15.6 ± 8.9 vs. 17.0 ± 8.8 mg, P = 0.007). The mass of the "slow" compartment also tended to increase (78 ± 20 vs. 80 ± 22 mg, P = 0.12). Overall, however, the omission of red blood cell data decreased the total mass of the identifiable nongastrointestinal compartments by 2.5 ± 3.0% (96 ± 28 vs. 99 ± 30 mg, P = 0.02). The masses of the three gastrointestinal compartments did not change significantly when the red blood cell compartment was omitted.
Comparison with adult data.
The masses of the nongastrointestinal zinc compartments (compartments
#1, 2 and 3) derived from the basic model were significantly greater
than those determined in adults using the same model (Table 2
) (Lowe et al. 1997
), when corrected for body weight. The
weight-specific masses of two of the gastrointestinal compartments
(#4 and 6) also exceeded those reported for adults (Lowe et al. 1997
). The fractional transfer coefficients between the plasma
and the tissue compartments were similar in adults and children except
for k(2,1), which was significantly higher in children
(Table 2)
. The fractional transfer coefficient k(5,1),
representing loss of zinc into the gastrointestinal tract, was
significantly lower in children than that previously reported in adults
(Table 2)
. Significant differences in the fractional transfer
coefficients between the gastrointestinal compartments were also noted;
k(5,4) and k(0,6) were significantly lower in
children than adults, and k(6,5) was significantly higher
(Table 2)
.
|
. Fecal zinc excretion
was 1.66 ± 0.07 mg/d in our subjects compared with 2.79 ± 1.70 mg/d in adults (P = 0.055). No difference was seen
when fecal excretion was corrected for body mass (Table 2)
. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSKinetic modelingRESULTSDISCUSSIONREFERENCES |
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Limited data are available on the total body zinc content of children,
but a value of 22.3 mg/kg fat-free mass, or 17 mg/kg, has been
suggested (De Kok et al. 1993
). The total zinc mass
resolvable by the seven-compartment model was therefore only
15% of the estimated total body zinc mass. This was not unexpected
because previous radioisotope studies found that 90% of body zinc
in adults was located in very slowly turning over body pools, largely
in bone and muscle (Wastney et al. 1986
). These pools
are not resolvable in short-term studies (i.e., <14 d), but can be
detected only in studies lasting many months (Wastney et al. 1986
). We contend that this should not limit the value of such
short-term models in studying the physiologic adaptations to zinc
deficiency. The clinical and biochemical effects of established zinc
deficiency correct very rapidly after zinc supplementation, suggesting
that these features are associated with depletion of rapidly turning
over tissue compartments. If the symptoms of zinc deficiency were due
to depletion of slowly turning over tissue compartments, then prolonged
zinc supplementation would be required to replete these compartments,
and resolution of symptoms would be much slower.
In this study, the mass of the central compartment was 0.60 mg/kg. This
is higher than we would have expected on the basis of measurements of
plasma zinc and estimates of plasma volume. Assuming a plasma zinc
concentration of 15 µmol/L (1 mg/dL), a blood volume
of 70 mL/kg and a hematocrit of 0.38 (Lenter 1984
), the
plasma zinc mass would be expected to be 0.43 mg/kg. The central
"plasma" compartment identified in our study may therefore include
other physiologic spaces in addition to the plasma. The difference may
be related to zinc in rapidly equilibrating extravascular compartments,
or zinc bound to cellular elements in the blood. Equilibration must
occur so rapidly that zinc in these compartments is not distinguishable
kinetically from that in plasma.
We identified one red blood cell compartment; the inclusion of
additional red blood cell compartments did not improve the fit of the
model. Previous radioisotope studies in adults have identified two red
blood cell compartments (Wastney et al. 1986
). The
second of these red blood cell compartments, however, turns over too
slowly to be resolved in this 6-d study.
Whether these red blood cell zinc pools are useful measures of zinc
status is unclear. There is, however, preliminary in vitro evidence
that uptake of zinc into red blood cells is affected by zinc status
(De Kok et al. 1993
) and that zinc uptake into the red
blood cells changes during periods of zinc loading (Wastney et al. 1986
). Although the inclusion of the red blood cell
compartment involves additional effort and cost, it allows a more
complete understanding of zinc metabolism. Furthermore, inclusion of
the red blood cell pools may be particularly useful when studying
subjects with concurrent infective or inflammatory processes such as
Crohn’s disease or infective diarrhea. In these conditions, plasma
zinc may decrease due to sequestration into the liver (Brown 1998
) such that the mass of the plasma compartment may fall,
whereas the mass of the nongastrointestinal compartments may increase.
However, zinc influx into red blood cells appears to be unaffected by
inflammation (Naber et al. 1994
), and the red blood cell
compartment may therefore provide important information concerning zinc
status that is not confounded by a concurrent inflammatory process.
A simplified version of the model that excluded the red blood cell compartment also fit the observed data well. The mass of the central plasma pool increased significantly when the red blood cell data were omitted, but the absolute change was small (0.003 ± 0.003 mg/kg). Similarly, the total mass of the identifiable nongastrointestinal zinc compartments decreased by only 2.5% after omission of the red blood cell data. The masses of the three gastrointestinal compartments were not affected significantly by omission of red blood cell data.
This six-compartment model is comparable to one previously
described in adults (Lowe et al. 1997
) but the
compartmental masses in our subjects, corrected for body weight,
significantly exceeded those reported previously (Lowe et al. 1997
). The greater size of the nongastrointestinal compartments
may be explained by the fact that the adolescent growth spurt begins at
about the age at which our subjects were studied (Marshall and Tanner 1986
). This period is associated with a significant
increase in lean body mass. Approximately 60% of body zinc is in
skeletal muscle (Cousins 1996
); thus it is possible that
increased amounts of kinetically labile zinc are present to support the
rapid growth in lean tissue mass. This difference in zinc pool masses
at different ages is also compatible with studies of calcium
metabolism, which have shown larger compartmental masses in children
than in young women (Wastney et al. 1996
).
Two of the three gastrointestinal compartments, corrected for body
mass, were larger in children than those previously reported in adults.
This may reflect a difference in gastrointestinal transit or may be
explained by the higher dietary zinc intakes in our study than that of
Lowe et al. (1997)
.
The fractional transfer coefficients between tissue zinc compartments
did not differ significantly from those described in adults
(Lowe et al. 1997
), except for k(2,1), which
was significantly higher in children. The reason for this difference is
unclear. The fractional transfer coefficients between the three
gastrointestinal compartments were significantly different than those
previously described in adults (Lowe et al. 1997
);
k(5,4) and k(0,6) were significantly lower in
children and k(6,5) was significantly higher. These
differences may relate to subtle differences in the manner in which the
oral tracer was administered. In the previous adult study, the oral
tracer was given 15 min after a low zinc breakfast (Lowe et al. 1997
). In our study, the oral tracer was given at the same time
as a breakfast that included zinc-fortified breakfast cereal. The
observed differences in fractional transfer coefficients would be
compatible with a difference in the time course of zinc absorption when
zinc is given in these different ways, with absorption occurring more
rapidly when given 15 min after a low zinc breakfast than with a meal
containing higher zinc.
It is unclear whether fecal excretion should be compared in
absolute terms (mg/d) or on a body weight-specific basis
[mg/(kg·d)]. Because the recommended dietary allowance for zinc is
expressed as mg/d and does not change in females between the ages of 11
and 51 y (NRC 1989
), the former method may be preferable because
it relates more intuitively to net zinc balance. Using this method,
endogenous fecal zinc excretion tended to be lower in children than
that reported in adults (P = 0.02). This is consistent
with our finding that the fractional transfer coefficient
k(5,1), representing loss of zinc into the gastrointestinal
tract, was significantly lower in children than that reported
previously in adults. Endogenous fecal zinc excretion is a major site
of regulation of zinc homeostasis (Cousins 1996
,
Wastney et al. 1986
), and the lower value in children
may be a compensatory mechanism to meet the high zinc requirements that
are likely during the adolescent growth spurt. No difference in
endogenous fecal zinc excretion was seen, however, after correction for
differences in body mass. Urinary zinc excretion was significantly
higher in children than in adults, although the absolute difference was
small.
We have described the use of two related compartmental models to study zinc kinetics in children and demonstrated the suitability of stable isotope–based models to study zinc metabolism in this population. The current study demonstrates significant differences in zinc metabolism between children and adults, with children having greater weight-specific zinc compartmental masses, higher urinary zinc excretion and possibly lower endogenous fecal zinc excretion. We believe that the further use of such compartmental models offers a novel approach to the study of zinc metabolism in health and disease, and will provide insights that could not otherwise be obtained.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Manuscript received January 18, 2000. Initial review completed February 29, 2000. Revision accepted May 16, 2000.
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