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2
*
Department of Pediatrics, Washington University School of Medicine, St. Louis, Missouri, 63110;
Department of Paediatrics, College of Medicine, University of Malawi, Blantyre, Malawi;
**
Department of Human Nutrition, University of Otago, Dunedin, New Zealand and
Section of Nutrition, Department of Pediatrics, University of Colorado School of Medicine, Denver, Colorado 80262
2To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • zinc • stable isotopes • phytate • zinc homeostasis • Africa • children
|
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Due to the high content of
phytic acid (myoinositol hexaphosphate) in corn, the bioavailability of
zinc is thought to be restricted. Phytic acid is the most potent
inhibitor of zinc absorption in animal and human studies, particularly
when the molar ratio of phytate to zinc is >15, because it can form
insoluble complexes with zinc in the gastrointestinal tract
(Bindra et al. 1986
, Sandstrom and Lönnerdal 1989
). In addition, substantial quantities of
endogenous zinc enter the lumen of the small intestine postprandially;
the reabsorption of this secreted zinc is necessary to maintain
homeostasis (Wastney et al. 1986
). Dietary phytate may
also form complexes with this endogenous secreted zinc and inhibit its
reabsorption (Lönnerdal et al. 1989
).
In rural Malawi, the high phytate diet is associated with compromised
zinc status (Ferguson et al. 1989
, Huddle et al. 1998
). This is unfortunate because zinc deficiency during
childhood contributes to impaired growth, immunity and cognitive
function and increased severity and incidence of diarrheal, malarial
and respiratory infections (Black 1998
, Zinc Investigators’ Collaborative Group 1999
).
The development of analytical techniques for measuring stable isotope
ratios of zinc in biological samples allows the processes of zinc
absorption and conservation by the intestine to be examined
individually and quantitatively (Jackson et al. 1988
,
Krebs et al. 1995
). These techniques can provide
measurements of the impact of high dietary phytate on the absorption of
exogenous dietary zinc and on the intestinal conservation of endogenous
zinc. This study tested the hypothesis that children who consume a
phytate-reduced corn-plus-soy diet will have greater absorption of
zinc and greater intestinal conservation of endogenous zinc than
children who consume a standard high phytate diet.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Children aged 3–13 y who were hospitalized for tuberculosis treatment
or due to minor trauma or were awaiting an elective orthopedic
procedure or healthy siblings of inpatients at the Queen Elizabeth
Central Hospital in Blantyre, Malawi, were eligible for this study. The
rationale for choosing these children was that they were all relatively
healthy, and thus their zinc homeostasis would probably represent that
of normal Malawian children. Conducting the study in the hospital
allowed for strict dietary control and complete specimen collection. In
Malawi, children are hospitalized for the treatment of tuberculosis for
many weeks; the regimen used at the time of this study was inpatient
treatment for 60 d with streptomycin, rifampicin, pyrazinamide and
isoniazid. During the latter part of their hospitalization, these
children were active and rapidly gaining weight. Other well children,
with either congenital deformities or minor injuries, were waiting in
the hospital many days for an orthopedic consultation. These children
were ambulatory and had no acute disability. The principal
investigator, who was a pediatrician, enrolled only children with a
normal upper respiratory, chest, abdominal and dermatologic physical
examination. All children who were enrolled met the criteria listed in
Table 1
.
|
Children were weighed regularly with an electronic scale accurate to the nearest 200 g, and their height was measured with a stadiometer accurate to the nearest 2 mm.
A blood sample was obtained at the time of isotope administration and
used to measure the concentrations of plasma zinc (Smith et al. 1979
), serum C-reactive protein and
1-antitrypsin (Rose et al. 1986
). The acute-phase proteins were used to assess the
status of inflammatory processes in the children. Care was taken to use
standard trace element–free materials and methods for the measurement
of plasma zinc.
Diets.
The diet was corn-plus-soy porridge served five times each day. The
porridge was prepared from a mixture of 80% unrefined white corn flour
and 20% soybean flour, with vegetable oil and sugar added. Water was
added to form a 20% slurry. In addition to the porridge, a
sugar-based drink and a fruit or nut snack were provided once
daily. For the phytate-reduced diet, the phytate content was
reduced by the addition of commercial phytase enzyme (5000
U/g; BASF, Mount Olive, NJ), 1 g of flour/kg was added
to cooled porridge. Children received a zinc-free multivitamin
supplement daily. The menus were identical for both diets, except for
the phytate reduction of the porridge. The nutrient and antinutrient
contents of the diets are shown in Table 2
.
|
, Scythes et al. 1982
), and the phytate
content was determined according to a modified method of
Lehrfeld (1989)
. The dietary zinc intake on the day of
isotope administration was used to calculate total absorbed zinc
(TAZ).3
. If the dietary zinc intake on the day of isotope administration was
<80% of the mean daily zinc intake for the 3-d period proximate to
this day, then the 3-d zinc intake was used to calculate TAZ. Metabolic study.
Stable isotopes 67Zn and 70Zn (Martin Marietta
Energy Systems, Oak Ridge, TN) were prepared for human administration
according to standard sterile techniques (Krebs et al. 1996
). On d 1 of the metabolic zinc study, children received a
precisely measured intravenous dose of 
750 µg of 70Zn.
During the five meals on d 1, an oral dose of 67Zn was
consumed with the food. The total dose of 67Zn was 20% of
the total zinc intake estimated from the weighed dietary records of the
previous 48 h (1.5–2.5 mg 67Zn; Sian et al. 1996
).
A brilliant blue fecal marker was administered 72 h after administration of the 70Zn and again precisely 4 d later. All stools between markers were collected. Children defecated into zinc-free plastic bags. Three times daily on d 3–8, a clean-void midstream urine sample was collected into a zinc-free plastic container. Specimens were frozen and transported unprocessed to the laboratories in Denver, CO, for analyses.
A 24-h urine collection was completed for most of the children, beginning 48 h after the administration of isotopes. The specimens were analyzed for total urinary zinc losses.
Sample analyses.
The zinc concentration and ratio of zinc isotopes were measured for
each individual fecal and urine sample as described by Peirce et al. (1987)
and Friel et al. (1992)
. Briefly,
samples were reduced to ash, and total zinc was determined with
flame atomic absorption spectrometry. Zinc was separated from other
inorganic constituents with ion-exchange chromatography
(Turnland et al. 1982
). Zinc isotopic ratios were
determined with fast atom bombardment–induced secondary ion-mass
spectrometry on a double focusing mass spectrometer equipped with an
Ion Tech atom gun (Peirce et al. 1987
).
Isotopic enrichments were calculated from measured isotopic ratios using curves determined from the measurement of standard zinc isotope solutions. Adjustments were made to isotopic enrichment data to correct for the presence of the other zinc isotopes. For each isotope used, enrichment was defined as the total zinc in the sample from an isotopically enriched source divided by the total amount of zinc in the sample.
Calculations.
For the determinations of fractional absorption (FAZ), the ratio of the
urinary isotopic enrichment of the intravenously administered
70Zn to the orally administered 67Zn was used
in the following equation (Friel et al. 1992
):
 |
Ten urine specimens that were obtained during study d 3–8 were analyzed, and the calculated FAZ values for specimen were averaged to determine the FAZ for each subject.
Endogenous fecal zinc (EFZ) excretion was measured according to an
isotopic dilution technique in which urine enrichment was substituted
for enrichment in solid tissue or plasma (Sian et al. 1996
).
 |
where Fi is total zinc in each sample (mg), fi is intravenous
isotope enrichment in each sample, ua is average IV isotope enrichment
in urine during collection, d is duration of collection (i.e., 4 d).
 |
 |
The size of the combined pools of zinc that intermixed with
plasma within a 2-d period (EZP, in mg) was estimated by dividing the
mass of 70Zn administered intravenously by the
enrichment value at the y intercept of the linear regression
of a semilog plot of urine enrichment data between d 3 and 9
(Miller et al. 1994
).
Tabular and text results are expressed as mean ± SD, and the results in figures are expressed as mean ± SEM. Anthropometric Z-scores were calculated using Epi Info Version 6 (World Health Organization/Centers for Disease Control and Prevention, Atlanta, GA). An ANOVA model was used to determine if group (recovering from tuberculosis or other well children) was an important determinate of zinc absorption. Multiple stepwise regression was used to develop a predictive model for the dependent variables (FAZ, TAZ, EFZ) for each group (recovering from tuberculosis or well children), using diet, age, sex and anthropometric indices as independent variables. The regression model identified which independent variables affected zinc absorption and retention. Differences in the means between different groups of children were compared using ANOVA. Pearson’s correlation coefficient was used to test for associations between variables. Statistical analyses were conducted with SPSS 9.0 (SPSS, Chicago, IL). Differences of P < 0.05 were considered to be significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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were
enrolled in October/November 1997 and May 1998. Eight other children
completed the zinc stable isotope study but were excluded from the
analyses because they had a markedly elevated C-reactive protein
concentration (>80 mg/L), indicating coincident systemic infection, or
were not fully ambulatory. The children were compliant with the diet;
weighed records of all meals were kept. There was no difference in
dietary zinc intake between the children receiving the high or
reduced-phytate diet. One child lost stool samples, and thus her
stool data were omitted. Two children missed meals on the day of
isotope administration, and thus 3-d dietary intakes were used to
calculate TAZ. Children receiving a reduced-phytate diet had a
greater FAZ (0.35 ± 0.14 versus 0.24 ± 0.07, P
< 0.05) and TAZ [148 ± 61 versus 100 ± 41 µg/
(kg · d), P < 0.05].
All of the FAZ values of >0.29 were found in children recovering from
tuberculosis. The group effect (recovering from tuberculosis or other
well children) was as important as the phytate content of the diet
(Table 3
). Because of the dichotomy between the two groups of children, the data
are presented separately for both diet and group. The demographic
characteristics of the children recovering from tuberculosis (hereafter
referred to as recovering children) and the other children (hereafter
referred to as well children) are presented in Table 4
. For TAZ, FAZ and EFZ, only diet was found to be predictive in the
multiple stepwise regression model for the recovering children.
Inclusion of the anthropometric indices only improved the model from
r2 = 0.30 to
r2 = 0.38. Although diet was
significant (P < 0.05) in the model, weight-for-age
Z-score (WAZ), height-for-age Z-score (HAZ) and
weight-for-height Z-score (WHZ) were not (P
> 0.3). The correlation coefficients between WAZ, HAZ or WHZ and
FAZ or TAZ were not significant.
|
|
, Figs. 1
,
2). FAZ was greater among boys than among girls regardless of diet (0.43
± 0.13 versus 0.27 ± 0.12, P < 0.05).
Recovering children gained 0.77 kg, a 4% increase in body mass, during
the 7-d metabolic study.
|
|
, Figs. 1
, 2
). Although the statistical power of the
comparisons between these small groups of well children is too low to
say they are truly the same, there was only a 5% chance that FAZ
varied by 
0.03 between the high and reduced-phytate diets. Well
children gained 0.18 kg during the 7 d of metabolic collections, a
change in body mass of <1%, and significantly less than gained by the
recovering children (P = 0.01). No child lost weight
during the 7-d period.
|
Seven recovering and seven well children completed 24-h urine collections. The urinary zinc excretion in the well children was almost twice that of the recovering children, but this difference was not significant (234 ± 149 versus 128 ± 63, P = 0.10). Plasma zinc was lower among recovering children than among well children (10.9 versus 13.7 µmol/L, P = 0.04).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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By distinguishing between well and recovering children, the sample size
of each group was reduced, which limited the strength of the
statistical comparisons between groups and introduced uncertainty as to
whether anthropometric indices could also be related to zinc
absorption. Because of the short period of time the children consumed
the monotonous, low phytate diet and the rapid growth of the recovering
children, caution should be exercised in extrapolating the findings to
normal children on a reduced-phytate diet for a prolonged period of
time. The recovering children received medications for the treatment of
tuberculosis. Streptomycin, rifampicin and isoniazid have been
investigated for their ability to chelate zinc and their effect on
plasma zinc concentration, and no significant interactions were found
(Cole et al. 1983
, Elo and Uksila 1970
).
Any changes in zinc absorption produced by tuberculosis or its
treatment would be seen in the recovering children receiving both low
and high phytate diets, and comparisons between these two dietary
groups are likely to remain valid. Stable isotope studies with 4-d
stool collections require highly motivated, cooperative subjects and
unfortunately can be conducted only with small groups of individuals.
However, stable isotope techniques currently provide the most reliable
quantitative human data on zinc homeostasis. Because of the limitations
of this study, these data must be considered as preliminary.
Children recovering from tuberculosis are recovering from a wasting
illness and are experiencing rapid catch-up growth. Indeed, the
recovering children gained 6 g/(kg · d) during the metabolic study.
Several investigators have noted that plasma zinc concentrations are
lower in children with tuberculosis, and plasma zinc concentration
increases gradually during treatment (Bogden et al. 1977
, Sharda and Bhandari 1977
, Sinha et al. 1985
). Hair and tissue zinc contents have been found to be
lower in patients with tuberculosis as well (Lysenko et al. 1997
, Zhang 1991
). The plasma zinc concentration
was lower in the recovering children than in the well children.
Together, the rapid catch-up growth and compromised zinc status of
tuberculosis suggest that these recovering children had increased
requirements for zinc, and they improved their zinc absorption with
phytate reduction. Boys are thought to have greater zinc requirements
than girls (Castillo-Duran et al. 1994
), and FAZ was
higher among the boys studied here as well. This also supports the
concept that the absorption efficiency of zinc varies with the
physiologic zinc requirement. During periods of rapid growth, such as
in utero, infancy and adolescence, as well as during pregnancy and
lactation, increased zinc bioavailability may be particularly
important, and phytate reduction may be beneficial.
The mean net zinc absorption among the well children was quite modest:
17 µg/(kg · d), or 375 µg/(child · d). Estimates of
insensible losses from other investigators are 7 µg/(kg · d)
(Johnson et al. 1993
), and the measured urinary zinc
losses were 9 µg/(kg · d) in the well children. Thus, the well
children absorbed sufficient zinc to replace their losses but appeared
to retain no zinc for growth. Why was this so? The well children
consumed 0.41 mg zinc/(kg · d) compared with 0.50 mg/(kg · d), as
found in a home-based dietary survey of 4- to 6-y-old Malawian
children (Ferguson et al. 1989
). It is possible that the
children in the study consumed less food than they would have at home
because the diet was so monotonous. The additional retained zinc
provided by a higher dietary intake might have been sufficient to
facilitate normal growth (World Health Organization 1996
). Alternatively, the lack of zinc retained for growth in
these nine well children could reflect an anomaly of this small sample
size. This discrepancy makes it difficult to assume that these nine
well children represent normal Malawian children. Further studies are
in progress in normal Malawian children to further investigate zinc
homeostasis.
Although EFZ did not decrease with phytate reduction among the recovering children, phytate reduction ameliorated the direct correlation between EFZ and its principal dietary correlate, TAZ, and thus potentiated increased zinc conservation. This indicates that although increased amounts of zinc were absorbed, corresponding amounts of endogenous zinc were not lost through the gastrointestinal tract, and the retained zinc was used for growth and repletion of stores. The well children had substantial EFZ relative to TAZ that was unaffected acutely by phytate reduction. The observation that phytate reduction did not change zinc homeostasis in the well children indicates that zinc was probably not a limiting nutrient at the time of the metabolic study. Increased dietary zinc intake appears to compensate for the reduced bioavailability of the high phytate diet.
EZP is thought to be a measure of zinc status, although an
interpretation of values are not possible because of the paucity of
normative data. Although no other data are available for a comparable
age group, the EZP in this study, considered on a body weight basis,
was certainly not low in comparison with either adults (Miller et al. 1994
) or infants (Krebs et al. 2000
). The
EZP from the Malawian children were measured only a few days after
initiation of the diet and thus reflect their zinc status before
enrollment rather than being an effect of the intervention.
This study provides evidence that dietary phytate reduction may be useful in improving zinc nutriture among populations who consume a cereal-based diet with increased physiologic zinc requirements. Studies that examine the long-term effects of phytate reduction on zinc homeostasis in a variety of nutritional and developmental states are needed to understand what role phytate reduction can play in improving zinc nutriture in the developing world.
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FOOTNOTES |
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3 Abbreviations used: EFZ, endogenous fecal zinc;
EZP, pool of zinc exchangable in 2 d; FAZ, fractional absorption
of zinc; TAZ, total absorbed zinc.
Manuscript received February 2, 2000. Initial review completed March 28, 2000. Revision accepted August 11, 2000.
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