Calcium absorption in elderly subjects on high- and low-fiber diets: effect of gastric acidity14 Tamsin Gerard
A Knox, E Dallal,
Zohrab Sanjeev
Kassarjian, Arora, and
ABSTRACT in inhibiting
In vitro studies calcium absorption
mal,
control
elderly
subjects
Bess Dawson-Hughes, Robert M Russell
suggest that the is pH dependent. and
eight
Barbara
effect of fiber In nine nor-
elderly
subjects
fiber
because
fiber
complexes
with
Reduced
achlorhydria, 47Ca was ingested with meal (0.5 g dietary fiber), a high-fiber
three test meals: a low-fiber meal (10.5 g), and a high-
(15).
fiber
HC/L.
calcium
meal
calcium
with
120
retention,
mL
of 0.1
measured
mol
in a whole-body
± 4.0% (i ± SD) with the low-fiber high-fiber meal (P < 0.002 vs low
meal, fiber),
In control
subjects
counter,
was 25.7
dial
We
conclude
sorption
Am
that,
with
in
humans,
the
high fiber intake 199 1 ;53: 1480-6.
J C/in Nutr
in calcium
is unaffected
by
suggests formation
atrophic counter,
gastritis, fiber
pH.
gastric
absorption responsible
population and, for
multifactorial
is at high
consequently, decreased and
absorption
risk
pH.
pH,
fiber
intake
calcium
Diets
high
for their
include
the
inability
when
there
is low
(5) and
with
in fiber
calcium
acid
sorption
components
high
and of calcium
1480
may
pH
be especially
intake
dependent (17,
in
18). 7,
60 y and in good health, based physical exam, and laboratory indices. surgery; calcium,
A 72-h
after
24-h
alkalinc-picrate)
calcium
by using
(Beckman CA)
and
(kinetic,
urinary
spectroscopy
(MAO)
control enrolled
colorimetry;
a colorimetric
Pentagastrin-stimulation
we exam-
(n
1481
specimen
La Jolla,
population
were
by
an acidified
of estimating
retention,
of47Ca.
whole-body-counter
of exogenous
Study
for
test in a
as an estimate
method calcium
of volunteers
ofthe
the
subgroup effect
whole-body-counter
FIBER
o-cresolphthalein
excretion
d was
absorption
AND
Twenty-four-hour
absorption.
calcium med
by the method
with
of exogenous
fiber,
ACID,
meals
con-
15 g grape
jelly,
ogen I and II by a double-antibody radioimmunoassay (RIA) described by Samloffet al (20); serum gastrin by RIA (Cambridge Medical Diagnostics, Billerica, MA); serum 25-hydroxyand
and 20 g enriched farina (dry weight), but the high-fiber meal also contained 1 5 g honey and 23.7 g raw wheat bran. Radiolabeled tracers were administered in 90 mL whole milk with
1,25-dihydroxyvitamin ing vitamin D-deficient
each test meal. (0.035 g phytate)
(22), respectively; petitive protein
D by competitive rat serum (21)
and binding
lowing
assays
(Roche
bumin
by
were
protein binding by uscalf-thymus receptor
serum folate and vitamin by using milk-folate-binding
and purified hog gastric phase, Corning Medical
alyzer
and
intrinsic Diagnostics,
performed
Diagnostic
bromcresol-green-dye
factor, respectively Medfield, MA).
on a Cobas
Systems,
B-12
Fara
10.5 g dietary mg Ca. With
(IMMO
which
The
fol-
radiolabeled
An-
acid
Centrifugal
Montclair, binding;
by comproteins
calcium
NJ):
serum by
al-
reaction
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water with
included test
fiber (2.22 g crude fiber, 0.35 g phytate) and 275 the low- and high-fiber test meals, 160 mL water, the water calcium,
meal
to total the
The low-fiber meal contained 0.5 g dietary fiber and 245 mg Ca. The high-fiber meal contained
meals.
was
used also
to rinse consumed.
the milk The
glass
containing
high-fiber-plus-
had 120 mL 0.1 mol HC1/L and 40 mL rinse 160 mL. No other food or drink was consumed
KNOX
1482 Calcium
retention
Calcium
retention
a whole-body were
counter
mixed
overnight
after
in 90 before
an oral
the
whole
being
was drunk
cup
milk
with
each
meal.
Passage
an intestinal
transit
but
elimination
before
with
with milk
three
time
(1-h
calcium
of 5’Cr
had
point,
been
when
in the
counts)
were
pressed
as a percentage
recorded.
7 and 8) had absolute and
5.8, respectively.
72-h
fecal
and vitamin D conin both groups. Bone urea nitrogen, serum normal.
fiber
Dietary
were
and achlorhydric
in-
similar.
subjects Achlorhydric subjects (n=8)
pH
values
values
remained
relatively
constant
were averaged.
3:6
Age (y) Pepsinogen Pepsinogen
and stored by using Cambridge, MA). NC)
were
used
for
Clinfo C/info data
(BBN and
analysis.
Software SAS (SAS Baseline
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69.1 1 14.2 8.7
I (zg/L) I-Il ratio
MAO (mmol/h) Gastrin(ng/L) Calcium (mmol/L) 25-hydroxyvitamin D (nmol/L) l,25-dihydroxyvitamin D (pmol/L) Radius (% age-matched) Spine (% age-matched) Urine calcium (mmol/d) Urine creatinine (mmol/d) Dietary calcium (mg/d) Crude fiber intake (g/d) Dietary vitamin D (mg/d)
basal
SD. Results
tfII =
acid output;
77
values
maximal
Significantly different from §P = 0.015, lIP = 0.0035.
0.0003,
74.6 ± 8.6 37.0 ± 25.9t 1.8 ± 0.8 0.005 ± 0.0l3 0. 15 ± 0.32 459 ±472 2.27 ± 0.05
±
±
72
22
94 ± 26 97 ± 9 99 ± 10 3.2 ± 1.3 10.6 ± 3.5 857 ± 162 4.6 ± 1 . 1 5.35 ± 2.53
are serum
MAO,
2:6
44 ± 66.8 ± 3.6 0.41 ± 0.39 7.53 ± 5.43 130± 11 2.34 ± 0.10
BAO (mmol/h)
S
Products
of
excretion.
I-Il ratio, and in pentagastrin stimulation results, BAO and MAO. The gastrin values for the two groups were not significantly dif-
Statistics Data
was Linear-
the association
calcium
Control subjects (n=9)
a high-fiber meal and of exogenous control subjects and 5 achlorhydric
pH was recorded
fasting including
differences
Results
as a percentage
participated in a substudy to monitor postprandial gasAfter an overnight fast a nasogastric pH probe was placed
Baseline
by rediffer-
pH
in the stomach and nectics Digitrapper meal,
indepen-
± 1 SD.
Sex(M:F) To document acid on gastric
for
measurement.
to measure
urinary
dose.
gastric
tests
t
intrasubject
for
used
24-h
as mean
centrations,
tion.
Whole-body
by Student’s
retention values were analyzed of variance. Because significant
found between the groups, Student’s t tests for paired were used to carry out individual comparisons between The variability ofthc whole-body-counter method was
calculated
are
compared
were
samples groups.
of0.0
for radioactive decay, background counts, radiation exposure was small: 47Ca ingestion and 0.014 mSv per 51Cr inges-
per
Calcium analysis
subjects
(%)
container
were
dent samples. peated-measures
Measure-
1-h 51Cr counts.
retained
characteristics
Subjects
the test meal
for 47Ca and then counted
2% of the
Whole-body
marker was
dose).
chromium
stools, of the
stool of 47Ca,
47Ca counts:
whole-body
and
reached
unabsorbed
excreted
given
tracer
until At this
160 mL liquid
1 h after
at the 209.6 fJ photopeak for 5’Cr. Subjects were
activity
per-
water
administered
=
This
the wash
to that
ments were made 5 1.2 fJ photopeak the
and
counter
counts
meal.
AL
ences
calcium in the milk After the milk was
a nonabsorbable
of unabsorbed
in
to equilibrate
test
times
similar
in the whole-body voiding
the
measured
51Cr ( 1 85 kBq)
and
as part ofthe
of 51Cr,
was
allowed
the stable proteins.
was washed
with
to signal
and
consumed
with the test meal
were counted
of47Ca
(1 9). 47Ca (37 kBq)
mL
mitted the 47Ca to exchange and the 5’Cr to bind with consumed,
dose
ET
unless
1
± 22
98 ± 14 92 ± 8 102 ± 7 2.7 ± 2.0 8.0 ± 2.7 697 ± 233 3.8 ± 1.3 5.43 ± 3.05 stated
otherwise.
BAO,
acid output. control
subjects:
tP
=
0.0081,
P
CALCIUM Table
2 and Figure
subjects
and
retention
1 show
achlorhydric
was
25.7
percent
subjects.
± 4.0%
from
47Ca retention In control
the
high-fiber
meal
(18.9
NS vs high-fiber meal achlorhydric subjects ucs in control jects
47Ca
meal,
after
retention
the same was
p
E
low-fiber
in 6 d in 7 studies, in 8 d in 33 studies, in 10 d in 12 d in 47 studies, in 14 d in 50 studies, and
18 d in all 5 1 studies.
after
meal).
0.002
=
with 8.8 ± 1 .2 d for achlorhydric (3 studies of 17 subjects), the 5Cr
d in 4 studies, in 40 studies, in
not
P
(2 1 .0 ± 5.8%;
subjects high-fiber but the addition
subjects
d compared 5 1 studies
meal
I)
in val-
meal, dropped to 19.6 ± 4. 1% with the high-fiber meal (P = 0.037 vs low-fiber meal), and was not affected by addition of exogenous acid
NS
0.0002 vs low-fiber of exogenous acid to
meal.
26.2
1483
FIBER
=
0.002
=
AND
calcium
without acid). Mean calcium retention did not differ significantly from mean
subjects
mean
P
± 3.3%;
ACID,
in control
subjects
low-fiber
19. 1 ± I .9% with the high-fiber meal (P meal); and was not affected by addition the
ABSORPTION,
the meal fasting
except
and
for ach-
lorhydric subjects, in whom postprandial pH after the meal with acid was significantly lower than that after the meal with water (P = 0.04). There were significant, (P < 0.0001 by repeated
KNOX
1484 TABLE 3 Urinary excretion of 47Ca tracer during the study period from ingestion of 47Ca in the test meal until passage ofthe 51Cr stool marker in seven control subjects and four achlorhydric subjects
ET
AL Previous
isotope
High fiber plus acid
Urinary calciumt
.
mmo//d
agreement
2.18 1.27
0.83 1.09 0.26
-
9 1±SD Achlorhydric subjects 2 4 6
-
-
-
3.42
0.79
0.92
4.44
1.39 0.98 0.19 1.08 1.26
1.47 1.11 0.23 1.08 3.42 0.99
2.2 2.9 2.0 2.6 4.7 2.0
2.87
3.65
2.6
-
-
1.71
0.37
0.64
0.60
0.66 0.69 1.08
-
0.54
are expressed
whole-body
as a percentage
counts
of the administered
dose (ie,
100%).
=
t Urinary 47Ca excretion r = 0.55; P = 0.078.
t Not significantly
1.9
2.4 1.9 0.5
0.71 1.77
-0.063
=
+
0.621
x (24-h
urinary
from
control
P
subjects,
calcium).
intestinal
tract
complex and calcium-fiber
hydric 4.9 ± ± 0.6),
between
control
subjects in gastric pH while fasting after the meal with water (pH and after the meal with acid (pH Exogenous the gastric
no
different
acid.
This
from
that
substudy
ences in achlorhydric gastric
acid administered pH well below
postprandial subjects
pHs
of control
confirmed
subjects
were
achlor-
appears
differ-
high-fiber
calcium
acid
is not
whether
the
may
source
with
be the
salt
in
for calcium
calcium
taken
complex
carbonate required
is from
meals.
most
important
de-
depending
shown
the
nature
(12). In dependent,
of the vitro with
calcium in the
calcium-food
studies insoluble
show that calcium-
formed at gastric pHs found in individuals pH 5) (9, 17, 18). We measured intestinal
absorption effect
on
and colon. Thus, at many locations
over
the
range
on calcium-fiber that
high
gastric
from
fiber
in vivo.
to remain
stable
of gastric solubility
pH
through
does
Thus,
pHs
that
in vitro. not
the
the range
with cal-
have
the
However,
reduce
calcium
calcium-fiber
ofgastric
we bio-
complex
pHs found the stability be irrelevant
6
6
D study
of eight
calcium from meal.
meal
achlorhydric
absorption
control subjects Furthermore,
high-fiber
did
not
and
remained
constant
calcium
from
absorption
pH and, an additive
nine
in achlorhydric with either the addition affect
calcium
a high-fiber from
control
absorption.
meal.
a high-fiber
elderly
subjects
the low-fiber of exogenous
mean postprandial gastric pHs of 2.7, 3.5, high-fiber meal with and without exogenous groups (Fig 2). At all gastric pHs studied
a high-fiber
insoluble
4
I,
In this
by gastric not have
to
.U
Discussion
that
(6)
increased
carbonate
7
-
differ fiber
results
In Recker’s
meal
5.6-6.8).
subjects,
not
8
exogenous
significant
the
was
of whether
conflicting
in control and achlorhydric subjects. Alternatively, ofthe calcium-fiber complexes in the stomach may
between our control and the range of postprandial with
food
subjects a pH range
without
there
gastric pH and documents
in achlorhydric
to achlorhydric 6.0 and into
pH
subjects
that
and
(pH 2.0 ± 1.6 vs pH 3.4 ± 1 .8 vs pH 6.1 2.7 ± 0.9 vs pH 4.9
2.3),
± 0.6). lowered
(pH
differences
with
the
In
absorption
in terms
absorption.
supplements
its degradation binding is pH
fiber complexes achlorhydria (
availability of variance)
measured
subjects ifthe calcium carbonate postulate that gastric acid may be
gastric
fed state
calcium
given
calcium
calsub-
method.
calcium
studies
as food is digested in the small intestine may be in a soluble and ionized form
have analysis
the
calcium-food
greatest
0.14.
=
in the
or from
that
resolves
from
that
et al(27)
calcium
in achlorhydric a meal. We but
from
Bo-Linn
ofprior
fasting
absorption
state
absorption
cium
different
or
absorption in achlorhydric
found
Studies
a double-
food
carbonate
intestinal
to solubilize
fasting
used
terminate of calcium absorption in the fed state. Calcium complexed with dietary proteins, sugars, phytate, or fiber is liberated
0.66 0.70 1.43 0.83 ±0.40
-
±SD Results
necessary
(6), which calcium
they
Review
fed
control amounts was taken with
The
7
*
calcium
food
1.31
±
study,
were pH and
on intestinal
(6, 7, 27).
an intestinal-washout
calcium pH.
alone
results
without subjects.
results,
or from
subjects
the
control
our
by gastric
on gastric
7
-h
food
taken
by using
with
affected the
Control subjects 1 2 4 5 6
with
absorption
acid
by Recker
decreased
tablets
compared
from %
showed
ofgastric conflicting
et al (7) and
carbonate
calcium
effect
provided
method,
cium jects
High fiber
ofthe
absorption
by Ivanovich
Urin ary 47Ca excre tion Low fiber
studies
calcium
did
not
meal
2
or the highacid to a We
found
4.9, and 6. 1 after a acid in our subject calcium absorption This
3
demonstrates is not
thus, that the presence of achlorhydria effect in reducing calcium absorption
affected does from
meal.
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0 Control
AC
Group FIG 2. Gastric pH in seven control subjects and five achlorhydric subjects (AC) measured for 30 mm while fasting (solid bars) and for 60 mm after a high-fiber test meal given with water (hatched bars) or with acid (white bars). I ± SD. Letters above bars denote statistically significant differences between groups sharing the same letter as follows: a, P = 0.004; b, P = 0.007; c, P = 0.0003; , P = 0.04.
CALCIUM to the pH
intestinal
may
absorption
be the
plexes
from
soluble
major
food
because
calcium
high
of the
meal
of calcium.
absorption, concentrating (28, 29). The
calcium
in solubilizing
our
was
to measure
was
cause
due
to the was
and
contain
both
colon,
where
longer
periods
and
residue
in calcium
fiber
mg)
intake
cium
absorption
the test period, similar in the 1.4%
ofthe
tion).
Because same
(r
presence
in elderly not affect
people,
calcium
whether
absorption
endogenous from
food,
even
U
of fiber.
decreased
(245
low
determinants
high-
decrease
in
cal-
in our
of calcium
underestimates not
(6.5%
ofthe
from as urinary true
losses,
calcium
during
study