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

Calcium absorption in elderly subjects on high- and low-fiber diets: effect of gastric acidity.

In vitro studies suggest that the effect of fiber in inhibiting calcium absorption is pH dependent. In nine normal, elderly control subjects and eight...
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