Calcium low-fiber

Tamsin Gerard
ABSTRACT in inhibiting mal, elderly achlorhydria, meal (0.5 fiber calcium 4.0% high-fiber (i meal

absorption in elderly subjects on high- and diets: effect of gastric acidity14

Zohrab Sanjeev Kassarjian, Arora, and
suggest is pH and eight

A Knox, E Dallal,

Bess Robert
that the dependent. elderly

Dawson-Hughes, M Russell
effect In

Barbara

B Golner,

In vitro studies calcium absorption control 47Ca g dietary with retention, SD) meal (P
<

of fiber fiber nine nor-fiber

because complexes

bacterial and gastric pH acid fiber (16).

action releases buffers production Reduced in subjects is pH

in the calcium gastric gastric on dependent

colon for acid acid

breaks absorption and may vitro 6, 70%

down (8, raises adversely diet in elderly

calcium13, 14). people postpranaffect cal-

subjects

subjects

with Reduced gastric

is prevalent

was ingested with fiber), a high-fiber 120 mL measured of 0.1 mol

three test meals: a low-fiber (15). meal (10.5 g), and a high-dial HC/L. In control subjects calcium was counter,

Furthermore, absorption binding

a high-fiber in

because

Downloaded from www.ajcn.org by guest on September 16, 2011

in a whole-body

25.7cium-fiber

with of

increased calcium This the reis

with the low-fiber meal, 19. 1 1.9% with the binding at a higher pH (9). Calcium-phytate 0.002 vs low fiber), and 18.9 3.3% with to precipitate at pH 4-5 (17, 18). At pH

complexesegin b

the high-fiber-plus-acid meal (P < 0.002 vs low fiber, NS vs high bound to phytate, and at pH < 7, 10% ofcalcium is in a soluble state required for absorption by the small intestine (18). fiber). Calcium absorption in achlorhydric subjects was not different from control subjects: 26.2 8.0% with low fiber, 19.6 suggests that the presence of achlorhydria, which promotes 4.1% with high fiber (P < 0.04 vs low fiber), and 21.0 5.8% formation ofinsoluble calcium-fiber complexes, may further with high fiber plus acid(P < 0.04 vs low fiber, NS vs high fiber). duce calcium absorption from a diet high in fiber. However, We conclude with that, high in fiber humans, intake the is reduction unaffected in by calcium gastric sorption abinfluence has not pH. ofgastric previously pH on the fiber-calcium been studied. interaction,

the in vivo,

Am

J C/in

Nutr 199 1 ;53: 1480-6.

Our
cium

objective
absorption

was
from

to determine
a high-fiber

whether
diet

the
was

reduction
affected by

in calgastric

KEY WORDS calcium absorption,

Achlorhydria, whole-body

atrophic counter,

gastritis, fiber

gastric

pH,

pH.
fiber, subjects

We
high

compared
fiber, with and and

the
without

retention
high fiber

of calcium
with exogenous

from

meals
acid in

of low
elderly

achlorhydria.

Introduction
The absorption responsible multifactorial calcium creased metabolite absorption production that elderly and, for population consequently, decreased and include when is at high risk of inadequate calcium

Methods Study We
hydria are Baseline osteoporosis ( 1 , 2). calcium absorption the there inability is low to calcium D, Mechanisms with aging increase intake the vitamin of calcium fractional and D (1, 3, 4).

design recruited
but with were given

17 elderly
otherwise performed. a standard

volunteers
normal

with

and

without function,
occasions

achlorfunction.

gastrointestinal

tests

ofnutritional

status,
On test

gastrointestinal
three meal separate that varied

and
volcon-

bone density deunteers were

in fiber

of 1,25-dihydroxyvitamin stimulates active transport

I From the US Department of Agriculture Human Nutrition Research Center on Aging at Tufts University and the Division of Gastroenterology, Diets high in fiber are commonly promoted in elderly people New England Medical Center, Boston. of this publication do not necessarily reflect the views for their putative preventive and therapeutic properties. The 2 The contents or of the US Department of Agriculture, nor does mention of mechanism by which diets high in fiber decrease intestinal cal- policies commercial products, or organizations imply endorsement cium absorption is unknown (5, 8, 9). Calcium may bind directly trade names, to uronic acid components of fiber and to phytic acid, a com-by the US government. 3 Supported by a contract 53-3K06-5-10 from the US Department of pound commonly found in high-fiber foods (8, 10, 1 1). These Agriculture and National Institute of Health training grant DK07024calcium-fiber and calcium-phytate complexes reduce the bio13. availability ofcalcium for absorption by the small intestine. Ab4 Address reprint requests to TA Knox, Division of Gastroenterology, sorption of calcium also occurs in the colon, and the fraction Box 103, New England Medical Center, 750 Washington Street, Boston, of total calcium absorbed in the colon is increased in subjects MA 02 11 1. with reduced small-intestinal calcium absorption (12). Colonic Received July 23, 1990. for publication October 31, 1990. absorption may be especially important when the diet is high in Accepted

High

fiber

intake

(5)

and

high

gastric

pH 7)(6, may

further

reduce

calcium

absorption

in elderly

people.

1480

Am J C/in Nuir l991;53:1480-6.

Printed

in USA.

1991

American

Society

for Clinical

Nutrition

CALCIUM
tent acid. plus
(0.5

ABSORPTION,
of exogenous with

ACID,

AND

FIBER
colorimetry; colorimetric urinary calcium (kinetic, excretion and 24-h urinary was

1481
creatinine assay. on

or

10.5 test The

g) and meals meal

in the were order

presence low was

or absence

o-cresolphthalein a

The acid.

fiber, high fiber, and assigned in a random

excretion by high fiber manner. Twenty-four-hour

alkalinc-picrate)

measured

An oral dose of 47Ca in milk was meal. The volunteers were measured whole-body counter by the method

an specimen by using direct-current plasma-emission administered with each test acidified daily for 47Ca activity in spectroscopy a (Beckman Spectraspan VI, Beckman Instruments, ofShipp et al (19). Fractional La Jolla, CA) after dilution with lithium in 50 g nitric acid/L.

47Ca
calcium To calcium med daily tention culated. study subgroup effect

retention

from

the

test

meal

was

used

as an
of retention, Urine

estimate

A of 72-h
d was

stool
assayed fast. collected

collection
by The the stomach during

for fat after

method tests was a 30-mm Peptavlon, of were van

a diet
de performed

with 100
Kamer and period.

g fat/d (23). after gastric an

for

3 over-

absorption. validate the absorption the from Five of the of magnitude a subgroup (retained ofthe volunteers

whole-body-counter by measuring losses volunteers (n in body subjects

=

method calcium of47Ca.

=

estimating we was calcium losses) A measure high-fiber collected rewas second the

Pentagastrin-stimulation exam- night were tg/kg

intubated baseline

secretions (6

ofurinary of control (n acid counts

Pentagastrin Philadelphia)

1 1). Net urinary reported (19). to the after

subcutaneously,

Wyeth-Ayerst,

plus were method was

was calume meal. the

administered
were and basal pH pooled were acid

and
in

gastric
15-mm and

secretions
collection these (BAO) values and by using

were
a Beckman were

collected
Altex used

for
Sample pH acid

I h.
volmeter output

in a validation

Samples (Beckman

intervals.

whole-body-counter 1 2) gastric on

recorded output

studied pH

Instruments)

to calculate

of exogenous

maximal

Study
Nine were

population
control enrolled subjects in this study. and eight Volunteers subjects were with recruited achlorhydria through

(MAO) Bone
Bone

(24). densiometry
density by of the the nondominant radius absorptiometry (#{188} distal method site) of was

Downloaded from www.ajcn.org by guest on September 16, 2011

the US Research

Department of Agriculture Center on Aging at Tufts

(USDA) University.

Human Nutrition measured Volunteers were

history, exclusion Cameron Madison, termined

single-photon

aged > 60 y and in physical exam, and from the study were

good health, based laboratory indices. peptic-ulcer disease;

on screening Reasons for previous

et al (25) (SP-2 model, Lunar Radiation WI). Lumbar-vertebral bone mineral density by the dual-photon absorptiometry method

Corporation, was deof Peppler Corporation). sex-matched obtained exposure the spine from was and

gastrointestinal

and Mazess (26) (DP-3 model, Lunar Radiation surgery; malabsorption; renal insufficiency; abnormal baseline Values were expressed as a percentage ofan age- and calcium, phosphorus, alkaline phosphatase, or creatinine; dcpopulation. Data on the reference population were vated 24-h urinary calcium; low 25-hydroxyvitamin D concenLunar Radiation Corporation software. Radiation trations; or recent use ofglucocorticoids, estrogens, fluoride, di0. 10 mSv to the pelvis from measurements of uretics, or anticonvulsants. Volunteers were instructed not to 0.15 mSv to the radius.

take

vitamins,

mineral

supplements,
1 mo

antacids,

or histaminc-2The presence

receptor achlorhydria

antagonists was

for initially (< 20 g/L) were

before

the

study.

I concentrations II (< 2.9) and

(20). for The

determined and a low

by low serum pepsinogen ratio of pepsinogen I to

Study
Dietary

of

diet

and
intakes

test

meals
were determined by a 7-d food and 867, record analyzed USDAthat

was confirmed

volunteers

pentagastrin-stimulation

density measurement, a whole-body counter. after passage of unabsorbed

and Subsequent

testing was administered and reviewed by a nutritionist admitted to a metabolic study unit with the use ofthe Grand Nutrient Database (release testing, fecal-fat analysis, boneARS Grand Forks, Human Nutrition Research measurement of 47Ca retention with Forks, ND). A3-d cycle menu was prepared on
test in the meals stool were was administered confirmed 47Ca ward that by calcium, matched phosphorus, calculated were for on 2 wk this test the mean self-selected and daily fiber. magnesium, through then placed before supplement

by pentagastrin-stimulation

Center, Grand the metabolic

intake Vitamin of protein, D conquestionof 0.0 1 mg metabolic the an study. order. Each interval of meals 15 g jelly, grape conward

measurement was approved

Human and was the New

Cr stool marker ( I 9). This research protocol by both the Radiation Safety Committee and
Review Medical each and volunteer. gast were rointestinal determined function as follows: serum Committees Center Hospital. at Tufts Written University England from status values

sumption was thenaire. Volunteers

a food-frequency on a supplement to the throughout in random fast, with and high-fiber

Investigation obtained

vitamin D/d consent and continued

admission

Three different meal was consumed

meals were given after an overnight

Nutritional Laboratory

1 wk between meals. The low-fiber pepsin- sisted of2l g white bread, 4.5 g corn

margarine,

ogen I and II by a double-antibody radioimmunoassay (RIA) and 20 g enriched farina (dry weight), but the high-fiber meal described by Samloffet al (20); serum gastrin by RIA (Cambridge also contained 1 5 g honey and 23.7 g raw wheat bran. RadioMedical Diagnostics, Billerica, MA); serum 25-hydroxyandlabeled tracers were administered in 90 mL whole milk with 1,25-dihydroxyvitamin D by competitive protein binding by us- each test meal. The low-fiber meal contained 0.5 g dietary fiber ing vitamin D-deficient rat serum (21) and calf-thymus receptor (0.035 g phytate) and 245 mg Ca. The high-fiber meal contained (22), respectively; and serum folate and vitamin B-12 by com- 10.5 g dietary fiber (2.22 g crude fiber, 0.35 g phytate) and 275 petitive protein hog binding gastric Medical performed by using milk-folate-binding proteins and purified phase, Corning lowing assays intrinsic Diagnostics, on factor, respectively Medfield, MA). The a Cobas Fara calcium Centrifugal mg Ca. With (IMMO which included the the calcium, meal had meals. lowwater was and high-fiber used also to rinse consumed. test the meals, milk The 160 glass mL water, containing

folserum

were

radiolabeled An-acid test

high-fiber-plus-

alyzer
bumin

(Roche
by

Diagnostic

Systems,
binding;

Montclair,

NJ):
by

alwater
with

to total
the

120 mL 0.1 mol HC1/L 160 mL. No otherood or drink f

and was

40 mL consumed

rinse

bromcresol-green-dye

reaction

1482 Calcium
Calcium

KNOX retention
retention after mL an whole consumed with milk oral milk dose of47Ca was measured to meal. equilibrate This

ET

AL
were compared by Students t tests for indepenby rediffer-

characteristics dent samples. in peated-measures ences were

a whole-body
were overnight mixed in before

counter
90 being

(1 9). 47Ca

(37
with

kBq)
and the

and
allowed test

( 1 85 kBq) 51Cr

Calcium analysis

retention of variance.

values were analyzed Because significant

mitted the 47Ca to exchange and the 5Cr to bind with consumed, the cup was washed

the stable proteins. three times

calcium After and the

in the the milk wash

samples permilkgroups.
water calculated was divided

found between the groups, Studentst tests for paired were used to carry out individual comparisons between The variability ofthc whole-body-counter method was as follows: by 2#{176} give to The the SD SD ofthe for urinary intrasubject each measurement. differences Linearwas

was drunk
with with each an

with
meal. intestinal elimination

the

test
transit

meal
time

as part
similar

ofthe
to calcium

160 mL
that

liquid

given regression

techniques
losses as mean

were
and 24-h

used

to measure
calcium

the

association
excretion.

of
Data

Passage

of 51Cr,

a nonabsorbable

47Ca stool marker urinary are expressed of 47Ca, was used tracer (19). Subjects

values 1 SD.

to signal

of unabsorbed

were
but ments 5 1.2

counted
before fJ

in the
voiding

whole-body
(1-h counts
=

counter
administered

1 h after
dose). for then 1-h and

the

test

meal Results
at the jects daily

Measure47Ca and counted

were made photopeak

at the 209.6 fJ photopeak for 5Cr. Subjects were

<

Table
and

1 shows
eight

the baseline
achlorhydric and

data
subjects.

obtained
Ages

on nine
ranged

control
from 62

subto 93 sig-

until the activity of 5Cr reached At this point, when unabsorbed had counts) pressed whole-body calcium All data were been as excreted were a recorded. percentage in the stools, Whole-body of the

2% of the chromium the retained calcium administered

y. The 51Cr counts. nificantly calcium tracers 47Ca retention dose, ie, counts

control subjects in concentrations

achlorhydric subjects differed ofserum pepsinogen I, in pepsinogen

(finalI-Il ratio, and in pentagastrin The gastrin values for the two was cxthe ferent, 1-h enced although by two the values mean of had and

stimulation results, groups were not

in the achlorhydric 1000 gastrin>

BAO

and MAO. significantly dif-

Downloaded from www.ajcn.org by guest on September 16, 2011

group tg/L.

was

influ-

47Ca counts:
retention corrected (%)= 100
X

serum

subjects
(final counts)/(1-h counts) of0.0

(subjects
mmol/h

7 and
and

8) had
minimum

absolute

These two achlorhydria with MAOS

gastric including pHs 72-h of 6.2 fecal

stimulated

and
tion.

container
per

size ( 19).
47Ca

,.#0. 1 12 mSv

for radioactive The radiation ingestion and

decay, background counts, absorptive exposure was small: fat, folate, 0.014 mSv per 51Cr ingescentrations,

and

5.8,

respectively.
function

All B-l2,
within

other
nutritional

assessments
status,

of gastrointestinal

vitamin
were

albumin,
normal function clearance) D, and

Whole-body
calcium absorption

fractional
because the in

47Ca

retention
47Ca

underestimates
is excreted

absorbed

and stool. To measure studies were performed and four measured achlorhydric for 47Ca

extent of urinary 47Ca losses, a subgroup of seven control was collected net calcium

density and tests of renal true creatinine, and creatinine in urine takes of calcium, vitamin further subjects daily and TABLE retention Baseline I characteristics

calcium, and vitamin D conrangesn both i groups. Bone (blood urea nitrogen, serum
were crude fiber normal. were Dietary similar. in-

subjects. All urine activity. In these subjects

was
losses of the

calculated
ofradiolabeled administered

as whole-body
calcium dose. pH

calcium
and was

retention
expressed

plus

urinary

of control

and

achlorhydric

subjects Achlorhydric subjects (n=8)

as a percentage

Control subjects (n=9)

Postprandial To document acid on gastric subjects thc pH. in the nectics

gastric the pH,

Sex(M:F)
effect seven a high-fiber meal control subjects to monitor fast a nasogastric pH and of exogenous and 5 achlorhydric postprandial Age (y) Pepsinogen gasPepsinogen

3:6 I (zg/L)
I-Il ratio 69.1 1 14.2 8.7 44 66.8 3.6 0.41 0.39 7.53 5.43 130 11 2.34 0.10

2:6
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

participated After stomach and Digitrapper

in a substudy connected MKII,

an overnight

probe was placed

pH monitor

BAO (mmol/h)

MAO (mmol/h) (SyGastrin(ng/L) (mmol/L) Baseline fasting pH was recorded for 30 mm. test Calcium 25-hydroxyvitamin D meal, including 90 mL whole milk without radiolabeled calcium, (nmol/L) was consumed over 15-20 mm. Either 120 mL water or 120 l,25-dihydroxyvitamin D mL 0. 1 mol HC1/L solution was taken with the meal. The meals (pmol/L) with water or acid were consumed on consecutive days in random Radius (% age-matched) order. Postprandial gastric pH was monitored for 60 mm. Spine (% age-matched) A computer program (Gatrosofi, STA TpHAC, Synectics Medical Urine calcium (mmol/d) Urine creatinine (mmol/d) Inc) was used to calculate mean pH values over 1 5-30-mm incalcium (mg/d) tervals. Because these pH values remained relatively constant Dietary Crude fiber intake (g/d) over 1 h, the interval values were averaged. Dietary vitamin D (mg/d) to a continuous Synectics Medicalmc,

Milwaukee). The high-fiber

77

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 unless acid control output. subjects: stated

98 14 92 8 102 7 2.7 2.0 8.0 2.7 697 233 3.8 1.3 5.43 3.05 otherwise.
=tP

Statistics
S

SD. Results
acid output;

are serum values

MAO, maximal

BAO, P

Data
Products Institute

were collected Corporation,

Inc, Cary,

and stored Cambridge,

NC) were

by using Clinfo MA).C/info

used for data

(BBN
and

Software SAS (SAS

Baseline

basal
tfII
=

analysis.

0.0003,

Significantly different from P = 0.015, lIP = 0.0035.

0.0081,

CALCIUM Table
subjects retention

ABSORPTION, in control
calcium dropped to to
I)

ACID,

AND

FIBER p<0.0002 NS

1483

2 and
and was

Figure
achlorhydric 25.7

1 show
4.0%

percent
In the

47Ca retention
control subjects meal, low-fiber

subjects. from

19. 1 I .9% with the high-fiber meal); and was not affected by the NS high-fiber vs high-fiber meal meal subjects (18.9 did not the was 3.3%; P differ without

meal = 0.0002 (P addition of

=

vs low-fiber exogenous acid meal; retention from mean

0.002 Mean

vs low-fiber calcium

acid). same 26.2

in val-

achlorhydric

significantly

ucs in control subjects after jects mean 47Ca retention meal, dropped to vs low-fiber meal), acid fiber to the meal; high-fiber NS vs AC

meal. In achlorhydric 8.0% from the

sub-E low-fiber U

19.6 4. 1% with the and was not affected meal subjects but the (2 1 .0 high-fiber addition modify 98% high-fiber meal).

high-fiber meal= 0.037 (P by addition of exogenous vs AC control lowsubjects In both

5.8%; = 0.002 P

and achlorhydric calcium retention fiber meal did subjects not Control d compared 5 1 studies

intake significantly ofexogenous acid calcium retention. tracer 5Cr

reduced to the high 3.6 Of

Low

Fiber

High

Fiber

High

Acid

further passed

Meal
in 8.7

of the

with 8.8 1 .2 d for (3 studies of 17 subjects), in 6 d in 7 studies, in 12 d in 47 studies, all 5 1 studies. test Stool meals.

achlorhydric 5Cr tracer the in

subjects.

passed

in 4

d in 4 studies, in 40 studies, in after 18 d in the

8 d in 33 studies, in in 14 d in 50 studies, time did not

FIG 1 . the (hatched fiber (0.5 10 d (120 mL and

Percent whole-body calcium bars) and nine achiorhydric g dietary fiber), a high-fiber 0.1 mol HC1/L) test meal.

retention in nine control subjects subjects (solid bars) after a low(10.5 g), and a high-fiber-plus-acid

Downloaded from www.ajcn.org by guest on September 16, 2011

passage

decrease Because on calcium the exogenous retention meal high-fiber acid with administration the with high-fiber and An test were without had meal, no we acid apparent used to subjects treated the estimate effect results the results as repe-

high-fiber

TABLE 2 Percent calcium retention in control and achlorhydric subjects given oral 47Ca with three test meals: low fiber (0.5 g dietary fiber), high fiber (10.5 g), and high fiber plus acid (1 20 mL 0. 1 mol HC1/L)* High fiber plus acid

of

reproducibility with each titions surements dose in Expressed from the 18.4% be (ic, lorhydric and may ment of the

of this method. of the two high-fiber measurement. retention and the (19% variability

individual meals were The variability 2.4% ofthe

of the same ofcalcium

of the meaadministered of 20.3% subjects. calcium in achsubjects measurein five

Low Control subjects

1 31.1 21.3

fiber

High

fiber

control subjects in terms of high-fiber subjects), exaggerated the test meal the

3.7% in mean retained in control subjects. the The conditions not identical.

achlorhydric fraction subjects, estimates for in control each (19).

20.9
18.0

25.1
22.2

is 12.6%

2 3
4

in achlorhydric because meals) was whose radioactivity.

of variability

20.8
26.4

19.1
19.0

19.6
16.7 15.3 17.4

were

Variability

5 6 7
8

29.2
27.9

22.2
17.7

control

subjects subjects

reported

previously

Table
achlorhydric measured

3 shows
for 47Ca

a subgroup

of seven
urine The

control
samples urinary

subjects
were 47Ca losses

and
for

four
and each dose. loss

24.3
29. 1

17.1
20.7

18.5
20.4

collected

9 iSD Achlorhydrics subjects

1

20.9 25.74.0

16.5 19.1
l.9t

15.3
18.93.3

subject were expressed as a percentage ofthe administered The losses ranged from 0.23% to 3.65%. The 47Ca urinary for the control was subjects 0.83
=

was

1.71

1.31% means

and

for were

the not

achlorhydric significantly with meanet adminisin-

30.5

23.6

25.7

subjects different measured surements testinal tered gastric

5.811

0.40%.

These

2
3

20.8
27.1

21.0
19.8

16.4
18.9

(P

0. 14). 24-h urinary ofwhole-body

Urinary 47Ca excretion calcium (r = 0.55, P = 0.08). 47Ca by mean 60 retention a mean retained mm) and after five subjects, of 1.4% fraction.

correlated Thus, of the

4
5

28.3
42.3

20.8
19.5

20.5
32.5

underestimated

6
7 8

16.3 23.8
20.8

10.2 23.1
19.1

13.6 20.9
19.6 4.1

calcium absorption dose or 6.5% of the

Figure
pH subgroup both

2 shows
(monitored ofsevcn control

the
control and

effect
over achlorhydric

of exogenous
subjects

acid

on

postprandial
meal subjects. gastric in a

a high-fiber achlorhydric postprandial

I
*

SD were no

26.2

8.0

19.6

21.0 control

There

significant the

differences same test

between meal.

and

achlor- In

hydric

subjects

consuming

pH
was

was
taken

increased
with pH subjects,

over
water

the baseline
or with acid.

fasting

pH

whether

the
fasting

meal
and achwith water

different from low fiber, = 0.0002, tP f#{231}P0.0021, = lip = 0.037, #{182}P = 0.00 19. Subjects with absolute achlorhydria defined by BAO 0.0 mEq/h, = MAO = 0.0 mEq/h, and stimulated gastric pH after pentagastrin
>
5.8.

tIt11 Significantly

Within-group

postprandial lorhydric ofacid

differences in whom

were not postprandial that

significant except for pH after the meal

<

(P

was significantly 0.04). There

lower than were significant,

(P

after the 0.0001

meal with by repeated

1484 TABLE Urinary ingestion marker

KNOX
3 excretion of 47Ca tracer during the study period from of 47Ca in the test meal until passage ofthe 51Cr stool in seven control subjects and four achlorhydric subjects Urin ary 47Ca excre tion Low fiber High fiber High plus % fiber acid Urinary calciumt mmo//d

ET

AL
Previous studies absorption method, carbonate compared absorption with food subjects gastric pH calcium or by gastric were and our from pH. fed ofthe provided and taken by using by showed tablets with control results, calcium Review or effect ofgastric conflicting Recker without subjects. an they found decreased calcium food Bo-Linn intestinal-washout that given studies the absorption. carbonate ifthe calcium that gastric calcium is not the taken may be the calcium with most required meals. important deacid results (6), which absorption in achlorhydric et al(27) method. calcium with in terms conflicting In Reckers increased carbonate acid may salt for source calcium is from food measured In absorption was not of whether results (6) to be in alone (6, on 7, 27). used intestinal Studies a doublefrom calsub-

calcium by cium jects calcium agreement from affected the on isotope

Ivanovich

et al (7)

carbonate ofprior calcium from calcium subjects postulate insoluble acid whether fasting resolves

Control subjects 1 2 4 5 6
7

intestinal in achlorhydric a meal. We the that fed state complex but

2.18 1.27
-

0.83 1.09 0.26

-

1.39 0.98 0.19 1.08

-

3.42

0.79

0.92
-

1.26
2.87

1.47 1.11 0.23 1.08 3.42 0.99

3.65

2.2 2.9 2.0 2.6 4.7 2.0

2.6

study,

absorption

control amounts was taken with necessary the food The terminate plexed fasting or from absorption to state in the

solubilize

carbonate

gastric supplements

9 1SD Achlorhydric subjects 2 4 6

7

4.44

1.71

1.31

calcium

calcium-food of calcium with dietary

Downloaded from www.ajcn.org by guest on September 16, 2011

0.37
-

0.64

0.60
-

0.54

1.9

absorption in the fed proteins, sugars, phytate,

state. Calcium comor fiber is liberated Thus, locations the studies insoluble calcium in the show that calciumwith calhave the we bio-

0.66 0.69 1.08

0.71 1.77

SD
*

0.66 0.70 1.43 0.83 0.40 of the administered x (24-h subjects, P urinary
=

2.4 1.9 0.5

as food is digested in the small intestine may be in a soluble and ionized form intestinal dose complex (ie,calcium-fiber tract and depending its degradation binding is pH ( on that from on the (12). dependent, In

and colon. at many of vitro with

nature

calcium-food

Results whole-body
=

are expressed counts

0.078. =

as a percentage
100%).
=

-h

t Urinary r = 0.55; P

47Ca excretion

-0.063 from

0.621 control

calcium).

fiber complexes achlorhydria cium absorption effect shown greatest have availability

formed at gastric pHs found in individuals pH 5) (9, 17, 18). We measured intestinal over high fiber the gastric in vivo. range pH Thus, of solubility does the not gastric pHs in vitro. reduce calcium-fiber that calcium-fiber However, calcium

t Not significantly

different

0.14.

complex

analysis hydric 4.9 0.6), 0.6). lowered no acid. This

2.3),

of

variance)

differences

between

subjects in gastric pH while fasting after the meal with water (pH and after the meal with acid (pH Exogenous the gastric from substudy postprandial subjects in acid pH that administered well below of control that pH there

to remain stable through the achlor- appears in control and achlorhydric subjects. (pH 2.0 1.6 vs pH ofthe calcium-fiber complexes in the 3.4 1 .8 vs pH 6.1 2.7 0.9 vs pH 4.9
control and subjects a pH range exogenous differand 6 meal
.U

range

ofgastric

pHs

found

Alternatively, stomach may

the stability be irrelevant

to achlorhydric 6.0 and into without were

different

subjects

8
7

confirmed

significant

ences in achlorhydric gastric pHs

gastric pH and documents subjects

between our control the range of postprandial with the high-fiber

achlorhydric

(pH

5.6-6.8).

6
I,

4
3

Discussion
In subjects, differ fiber high-fiber from meal. this study calcium control meal did of eight absorption subjects not with the affect achlorhydric in either addition calcium and achlorhydric the of nine low-fiber exogenous absorption. control subjects or the acid We elderly did

D not highto found a a

Furthermore,

0
Control AC

mean postprandial gastric pHs of 2.7, 3.5, high-fiber meal with and without exogenous groups (Fig 2). At all gastric pHs studied remained that calcium by gastric not have constant absorption pH and, an additive from a high-fiber from meal. a high-fiber

4.9, and 6. 1 after acid in our subject calcium absorption This meal demonstrates is not

Group

thus, that the presence of achlorhydria effect in reducing calcium absorption

a high-fiber

meal.

FIG 2. Gastric pH in seven control subjects and five achlorhydric subjects (AC) measured for 30 mm while fasting (solid bars) and for 60 affected mm after a high-fiber test meal given with water (hatched bars) or with does acid (white bars). I SD. Letters above bars denote statistically significant fromdifferences between groups sharing the same letter as follows:P a, = 0.004; b, P = 0.007; c, P = 0.0003; , P = 0.04.

CALCIUM
to pH plexes soluble absorption absorption, concentrating (28, 29). increased ofgastric The acid the may intestinal be from calcium of the food of possibly unabsorbed presence in solubilizing absorption major because complexes. the meal through of may have and enhancing calcium sugars and within in our influenced glucose water the mixed influence high of calcium. on pH Rather, formation promotes

ABSORPTION,
high of calcium formation the increase movement intestinal meal intestinal of intestinal calcium

ACID,
presence in- the in

AND
ofachlorhydria does of

FIBER
in elderly not fiber. Shipp HNRC. for assistance with the whole-body affect calcium people, absorption whether from

1485 endogenous food, even

corn-or iatrogenic, presence

U
counter,

Components

calcium.

Lactose

and

We thank Clanton the staff of the

and lumen References may have effect

1.

Gallagher JC, Riggs BL, Eisman J, Hamstra A, Arnaud SB, DeLuca HF. Intestinal calcium absorption and serum vitamin 0 metabolites in normal subjects and osteoporotic patients: effect ofage and dietary our goal was to measure calcium absorption in a normal diet calcium. J Clin Invest 1979;64:729-36. that contains carbohydrate sources. We cannot determine 2. Bullamore JR. Wilkinson R, Gallagher JC. Nordin BEC. Effect of whether the decrease in calcium absorption with the high-fiber age on calcium absorption. Lancet l970;2:535-7. diet was due to the fiber components, the phytate, or both, be3. Ireland P, Fordtran JS. Effect ofdietary calcium and age on jejunal cause there was a 20-fold increase in fiber content and a 10-fold calcium absorption in humans studied by intestinal perfusion. J Clin increase in phytate content between the low- and high-fiber diets. Invest 1973;52:2672-8 1. Cereals and legumes, which are the major dietary source of fiber, 4. Silverberg Si, Shane E, de Ia Cruz L. Segre GV, Clemens TL, Bilcontain both fiber and phytates. ezikian JP. Abnormalities in parathyroid hormone secretion and Although most calcium is actively absorbed by the proximal 1,25-dihydroxyvitamin D-3 formation in women with osteoporosis. small intestine, passive absorption also occurs in the ileum and N EngI J Med 1989;320:277-81. 5. R, Johnson EJ, Marlett JA. Effect of wheat bran colon, where food residue is in contact with the mucosa for Balasubramanian on bowel function and fecal calcium in older adults. J Am CoIl Nutr longer periods of time (1 2). The whole-body-counter method calcium-fiber complexes. However, of assessing fractional calcium absorption colon, and absorption throughout because ofits retained was selected because 6.
7.

calcium

absorption

overwhelmed

a small

Downloaded from www.ajcn.org by guest on September 16, 2011

1987;6: 199-208.

it estimates calcium tract, including the of administered

Ivanovich P. Fellows H, Rich C. The absorption of calcium carbonate. Ann Intern Med l967;66:9l7-23. diation exposure allowed repeated measures in a group of subjects 8. James WPT, Branch WJ, Southgate DAT. Calcium binding by diwho served as their own controls. etary fibre. Lancet l978;l:638-9. Intestinal calcium absorption was decreased 20% by a high 9. Champagne ET. Effects ofpH on mineral-phytate, protein-mineralfiber intake. Differences in calcium absorption between low- and phytate, and mineral-fiber interactions. Possible consequences of atrophic gastritis on mineral bioavailability from high-fiber foods. J high-fiber meals could not be explained by differences in stool Am Coll Nutr 1988;7:499-508. passage times or in urinary calcium losses, because these were JG, Lahimgarzadeh A, Nasr K, Hedayati H. Effects of the same with both low- and high-fiber meals. Further, the slight 10. Reinhold purified phytate and phytate-rich bread upon metabolism of zinc, difference in calcium content of the low-fiber (245 mg) and highcalcium, phosphorus, and nitrogen in man. Lancet l973;1:283-7. fiber (275 mg) test meals could not explain a 20% decrease in 1 1 . GrafE. Calcium binding to phytic acid. J Agric Food Chem l93;3 1: calcium absorption between the low-fiber and the high-fiber 5 1-5. meals. The vitamin D status, subject age, and usual dietary cal1 2. Barger-Lux Mi, Heaney RP, Recker RR. Time course of calcium cium intake arc other important determinants of intestinal calabsorption in humans: evidence for a colonic component. Calcif cium absorption that were carefully controlled in our subjects. Tissue Int 1989;44:308-l 1. dose, 1 5% of fraction). The low raFractional true for intestinal calcium period, in the Because of the of47Ca same whole-body calcium losses which control losses underestimated dose fraction in urine retention absorption or of calcium underestimates it does not account during secretions
13.

the gastrointestinal reproducibility (3%

Recker
l985;3

RR.
13:70-3.

Calcium

absorption

and

achlorhydria.

N EngI

J Med

because gastrointestinal

the test similar 1.4% tion). are tion

averaged 8 d. Urinary losses of47Ca were 14. and achlorhydric groups and represented dose ofcalcium true (6.5% from as urinary calcium ofthe losses, mean retained secretions retenby ---2.8% 16. 1 3% of cal-1 7. used, 18. frac15.

ofthe

administered magnitude

gastrointestinal whole-body absorption

of the administered the mean retained cium with calcium study, related absorption

(ic, 2 X urinary (30). Measurements depending subjects fell within retention method (19).

losses) or by offractional on the method (6, 7, 27). Fractional this range.

absorption vary widely a range of 3-35% 1 in control retention whole-body with the (r
=

in our

study

In a separate highly corcalcium 19. with suggest a

20.

fractional excreta-recovery 0.84,

of

47Ca was of measuring

<

0.0001)

In summary, high-fiber diet that dietary individuals

the reduction is independent

in calcium bioavailability ofgastric pH. These results may diet. be increased However,

Cummings JH, Southgate DAT, Branch WJ, Wiggins HS. The digestion of pectin in the human gut and its effect on calcium absorption and large bowel function. Br J Nutr 1979;4l:447-85. Salyers AA, West SEH, Vercellotti JR. Wilkins TD. Fermentation ofmucins and plant polysaccharides by anaerobic bacteria from the human colon. AppI Environ Microbiol l977;34:529-33. Krasinski SD, Russell RM, SamlofflM, et al. Fundic atrophic gastritis in an elderly population: effect on hemoglobin and several serum nutritional indicators. J Am Geriatr Soc l986;34:800-6. Tadesse K. The effect of dietary fibre isolates on gastric secretion, acidity and emptying. Br J Nutr 1986;55:507-23. Martin Ci, Evans WJ. Phytic acid-metal ion ionteractions. II. The effect ofpH on Ca(II) binding. J Inorg Biochem l986;27:l7-30. Champagne ET, Rao RM, Liuzzo JA, Robinson JW, Gale Ri, Miller F. Solubility behaviors ofthe minerals, proteins, and phytic acid in rice bran with time, temperature, and pH. Cereal Chem 1985;62: 2 18-22. Shipp CC, Maletskos Ci, Dawson-Hughes B. Measurement of calcium-47 retention with a whole body counter. Calcif Tissue Int
1987;41:307-l2.

calcium consuming

requirements a high-fiber

in elderly the frequent

Samloff IM, Secrist DM, Passaro E. A study tween serum group I pepsinogen levels and Gastroenterology I 975:69: 1 196-200.

of the gastric

relationship beacid secretion.

1486
21. Adams JS, Clemens TL, Parrish and metabolism after ultraviolet JA, Holick irradiation MR. Vitamin of normal

KNOX

ET

AL

D synthesis 26. Peppler WW, Mazess RB. Total body mineral and lean body mass and vitamin by dual photon absorptiometry. CalcifTissue Int 198 1;33:353-9. D deficient subjects. New Engl J Med l982;306:722-5. 27. Bo-Linn GW, Davis OR, Buddrus DJ, Morawski SO, Santa Ana C, 22. Reinhardt TA, Horst RL, Orf JW, Hollis BW. A microassay for Fordtran JS. An evaluation ofthe importance ofgastric cid secretion a l,25.dihydroxyvitamin D not requiring high performance liquid in the absorption ofdietary calcium. J Gin Invest 1984;73:640-7. chromatography: application to clinical studies. Gin Endocrinol J 28. Norman DA, Morawski SO, Fordtran JS. Influence ofglucose, frucMetab 1984;5:9l-8. tose, and water movement on calcium absorption in the jejumum. 23. van de Kamer JH, ten Bkel Huinnink H, Weijers HA. Rapid method Gastroenterology l980;78:22-5. for determination of fat in feces. Biol Chem J l949;177:347-55. 29. Kobayashi A, Kawai 5, Ohbe Y, Nagashima Y. Effects dietary of 24. Powell DW, Drossman DA. Gastric analysis. In: Drossman DA, ed. lactose and a lactase preparation on the intestinal absorption of calcium and magnesium in normal infants. Am J Clin Nutr 1975;28: Manual of gastroenterologic procedures. New York: Raven Press, 1982:53-60. 681-3. 25. Cameron JR. Mazess RB, Sorenson JA. Precision and accuracy of 30. Heaney RP, Recker RR, Saville PD. Calcium balance and calcium bone mineral determination by direct photon absorptiometry. Invest requirements in middle-aged women. Am Gin J Nutr 1977;30: Radiol 1968;3: 14 1-50. 160-1.

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