INTAKE AND EXCRETION OF CALCIUM AND PHOSPHORUS BY INFANTS; CALCIUM RETENTION AND MODEL

Full text

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PART 2

668

INTAKE

AND

EXCRETION

OF

CALCIUM

AND

PHOSPHORUS

BY

INFANTS;

CALCIUM

RETENTION

AND

MODEL

INTRODUCTION

T

HE metabolism of radiostrontium is

cus-tomarily described in relation to

cal-cium. This study of the retention of

envi-ronmental strontium-90 in infants therefore

includes measurements of calcium intake

and excretion, estimates of calcium

accu-mulation, and the construction of a simple

model of calcium movement in the infant.

Phosphorus intake and retention were

mea-sured because the phosphorus/calcium

ra-tio in the diet affects the relative retention

of strontium and calcium.’ Surprisingly, in

view of the importance of calcium to the

in-fant, accurate intake data are meager,2

ac-cumulation values are contradictory,3 and

no model has been proposed. The situation

is no better for phosphorus.

The many excellent discussions of

cal-cium and phosphorus requirements and

metabolism in man, especially during

in-fancy,3h7 provide the following

informa-tion:

1.The calcium content of the 3.3- to

3.5-kg infant at full term is 0.8% of his body

weight, and reaches 1.7% in the 70 kg

man.4’10’13 No direct measurement is

avail-able of the calcium content of infants after

birth. Two calculations based on weight’4

and weight gain’3 suggest calcium contents

of 100 and 84 gm, respectively, in the 1

year old; a number of computed higher

values are considered to be based on

erroneous assumptions.’4 The ratio of

phos-phorus to calcium in the entire body is

1/1.7 or 1/1.8 at full term, and between

1/1.8 and 1/2.0 in the adult.’5

2. Most of the body calcium is in the

skeleton and teeth. Estimates include over

91)%,6 95% ‘ 98%, over 98%,’ and over

99%810 The normal ratio of phosphorus to

calcium in bone is approximately 1/2.2 at

all ages.

3. Calcium metabolism in humans seems

to adapt readily to intakes between 200 and

1,500 mg per day.6”#{176}Populations that

con-sume amounts of calcium near the extremes

of this range do not appear to suffer from

diseases connected with these intakes. The

statures and skeletal weights of groups with

low calcium intakes may be smaller than

those of groups with higher intakes, but not

in proportion to their calcium intakes.10 The

body appears to adjust to lower intakes by

higher fractional retention, and to

compen-sate by continued higher retention during

subsequent periods of higher intakes.’0,’6

4. Because of the adaptation of calcium

retention to bodily requirements, short-term

metabolic balance studies can be

mislead-ing unless the subjects’ diets have been

maintained at a reasonably constant

cal-cium level for a long period. The extremely

high calcium retention in balance studies of

infants, summarized by Holmes, may have

resulted from very low intakes prior to the

studies. Calcium and phosphorus data from

several carefully controlled metabolic

bal-ance studies of infants on all-milk or

all-for-mula diets are available.19,20

5. Discussions of calcium metabolism

frequently include the effects on retention

of such dietary components as vitamin D,

phosphorus, phytic acid, and oxalic acid.

The relative availability of calcium in

var-ious foods is mentioned”2’ and is related to

the presence of substances that form

com-plexed or insoluble calcium compounds. In

the range of normal intakes, and with the

vitamin D supplements now fed to infants,

it is doubtful that calcium needs are

seri-ously influenced by these components over

long periods.’#{176}

6. The Food and Nutrition Board,

Na-tional Academy of Science-National

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1gef (da)

No. of

Infant Periods

in .1rerage

Fruits,

.Juzces and 1)esserts

(ing)

Vege-tables (mg)

Mixed Meat rind

Vege-tables

(mg)

Meat

and Eggs (mg)

Cereals

(ing)

Milk (ing)

Water

(ing)

Total

(rng)

31-60 H 2 1 1 0 4 448 17 47

61-90 4 5 4 1 0 6 454 18 489

91-HO 31 9 8 3 7 418 14 461

Ul-150 33 16 9 3 7 7 440 14 496

151-180 32 18 9 6 9 8 436 14 505

181-l10 25 4 9 6 11 7 48 13 511

111-40 9 6 11 7 14 7 453 14 553

41-70 18 8 H 9 16 7 446 15 543

71-3O0 10 35 10 13 15 6 4l4 16 5

* See Tables I, II, and III for kinds of foods.

t At midpoint of Q8-day period.

669

Mostly dilution water used for formula; only a small fraction was drinking water.

dietary calcium allowance of 700 mg;11 an

expert group of the Food and Agriculture

Organization/World Health Organization

suggested a practical allowance of 500 to

600 mg per day for infants.10 An earlier

re-port of the Food and Nutrition Board is

cited by Hegsted8 as suggesting that

phos-phorus allowances in the diets of children

should be at least equal to those of calcium.

RESULTS

All daily intake and excretion values are

listed in Appendix A. Gross retentions-the

difference between intake and excretion,

uncorrected for other pathways or

system-atic losses-are listed in Appendix B,

to-gether with the retention of phosphorus

relative to calcium. Values considered

un-reliable for the reasons discussed in Part

I-Intake and Excretion Results, although

reported, were not used in analyzing the

data. Infants that were unusual with regard

to size, diet, and so forth are discussed in

Appendix D.

Average daily intakes of calcium and

phosphorus are itemized by type of food

and infants’ ages in Tables VI and VII. One

set of values below age 31 days and seven

sets above 300 days were omitted because

the values were too few in number for their

averages to be significant. Total values

slightly exceed the sums of the components

because of contributions from the “others”

category in Table III.

Excretion values are presented as a

func-tion of age in Table VIII, and the averages

of all intake and excretion values are

sum-marized in Table IX. Averages for separate

urine and feces values are also given in

both tables, and computed retention values

in Table IX. Individual values of intake,

fecal excretion, and total excretion showed

approximately arithmetic normal

distribu-tions about these averages. Urine values,

however, showed a log-normal distribution,

and the averages of logarithmic urine

values are therefore presented in both

ta-bles. These averages of logarithmic values

were in every case lower than arithmetic

averages. It is only for this reason that

ex-cretion totals exceed the sums of urinary

and fecal averages in Tables VIII and IX.

The averages of intake, total excretion,

and gross retention for the entire group and

for the subgroup whose urinary and fecal

excretion was measured separately are

al-most identical, as shown in Table X. In the

absence of noticeable differences between

the subgroup and the entire group with

re-gard to calcium and phosphorus

metabo-TABLE VI

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.‘lgtt (da) Number of Infant Periods lfl A verage Fruits, Juwes and Th seerts (mg) Vege-tables (mg) Mixed Meat and Vegetables (mg) Meal and eggs (ing) 31-60 61-90 91-120 19 1-150 151-180 181-210 211-240 241-270 971-300 13 24 Si 33 32 25 29 18 10 ‘2 6 12 18 21 27 29 32 38 6 10 11 13 19 14 15 12 2 5 10 18 17 ‘22 29 49 Cereals Mi!k (ing) (ing)

0 22 363

‘2 31 365

10 36 339

24 38 348

33 40 351

42 34 339

52 35 369

63 33 369

56 33 335

Total (ing) 39! 413 408 453 477 479 524 544 519

* See Tables I, II and III for kinds of foods.

t At midpoint of 28-day period.

lism, average values for separated urinary

and fecal excretions were applied to the

entire group.

DISCUSSION

Intake

The average intakes of calcium and

phosphorus gradually increased with age,

as shown in Tables VI and VII. The

contri-bution from milk (fresh or evaporated) and

formulas decreased slightly, and that from

other foods increased rapidly, as seen in

Figure 5. Note also the consistently lower

average intakes by the infants who

con-sumed prepared formulas. Only two of the

heavier infants (2 and 17) in this group

took in as much calcium as the infants (1,

4, 13, 14, 15, and 24) who drank

evapo-rated milk.

Many of the daily intakes by infants in

this study (Appendix A) are appreciably

lower than intake values obtained through

surveys and are also lower than

recom-mended dietary allowances. In upper

mid-dle-income families in Denver, infants who

consumed cows’ milk were reported in 1954

TABLE VIII

670 STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

* First number refers to total excretions, second number refers to separated urine and feces.

f Averages of log values.

‘I’ABLE VII

A-I:uAo1: I)iiy INTAKE OF PHOSI,III)II1S*

AVERAGE DAILY EXCRETION OF CALCIUM AND PHOSPHORUS

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TABLE IX

AVERAGE 1)AILY CALCIUM AND Puoseiiouus BALAN(ES

J)ata

(‘alciuin

(mg)

‘214 96

118

141

78

63

141

78

63

214 96 118

x

All ‘26±1.07t

x

Boys 22±1.10

x

Girls 32#{247}1.10

Urinary excretion plus

fecal excretion

All 325± 8

Boys 325± 10

Girls 325±11

Gross retention

All 214 180± 4

Boys 96 198± 7

Girls 118 166± 5

* Standard deviation of average.

t Averages of log values, and geometric standard deviation of average.

More values exist for urinary plus fecal excretion than for separated urine and feces.

§(;ross retention= intake- (urinary excretion +feeal excretion).

x 147±1.04

x

161± 1.04

x 132 #{247}1.08

334± 8

357 ± 19 ‘315±10

132± 3

144± 5

123± 4 Intake

All

Boys Girls

Ftual Excretion All Boys Girls

Urinary Excretion

Number of

Values

505± 8*

523 ± 10

491± 12

290± 9

282 ± 10

300±15

Phosphorus

(mg)

466± 9

501 ± 13

438 ± 11

175± 6

175± 7 175± 9

to consume 810 mg calcium daily at age 1

to 2 months, and 1,050 mg at 6 to 9 months;

respective phosphorus intakes were 660 and

950 mg. In a nationwide survey reported

in 1964, average calcium and phosphorus

consumptions at average age 6.8 months

were 1,103 and 961 mg, respectively.23

In-takes in the present study were lower for

the following reasons:

1. Solid foods were fed early in life.

These foods partially replace milk or

for-mula, hut have lower calcium and

phospho-rus concentrations.

2. Most of the infants were fed

premodi-fled milk formulas, which contain calcium

and phosphorus concentrations nearer to

human milk than to cows’ milk (Tables I

and II).

3. Commercial ready-to-eat cereals,

which contain less calcium, were fed

in-stead of the more commonly used dry

ce-reals to which milk is added in the home.

Their use reduced daily milk consumption

by approximately 80 ml.

4. The infants drank approximately 123

ml less milk or formula per day than the

av-erage indicated in an extensive survey,2

even after taking into account points 1

and 3.

The first two practices appear to be

com-mon in the United States at this time, hence

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TABLE X

COMPARISON OF BALANCE AVERAGES FOR ALL PERIODS AND FOR PERIODS IN WHICH URINE AND

FECES WERE COLLECTED SEPARATELY

700

-600

-500

-400

-300

-200

-10< -0 E 4

I-2

>--J

4

Ui

4

Ui > 4

I I I I I

0 0 Co

#{163}#{149}.P

NUMBER OF PERIODS

GIVEN WITH SYMBOL

52202L2

22I2II2e

I,33l32Ill

}

C0WS MILK *

}

FORMULAS A&B*

FOODS OTHER

THAN MILK

672 STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

Data

All #{163}14 Periods (‘mg/day)

141 Periods in

Which Urine and Feces Were Separated

(mg/day)

Ca P Ca P

Intake Total excretion Gross retention

505±8* 325±8 180±4

466±9

334 ± 8 132±3

511±8

324 ± 9

186±4

472±9

836 ± 9

185±4

* Standard deviation of average.

is recommended may be a frequent

occur-rence. Usually, however, cows’ milk would

replace formula during the second quarter

year and lead to a higher average intake of

calcium and phosphorus.24 Nevertheless,

average intakes in this study were above

re-cently published advisable daily intakes

(set at twice the estimated requirements)

of 500 mg calcium and 220 mg phosphorus.24

Adverse effects on the infants’ growth and

health resulting from these practices were

not observed during this study and do not

seem to have come to the attention of

pedi-atricians in general.bo

Infants who drink mothers’ milk, with

re-spective calcium and phosphorus

concentra-tions of 0.3 and 0.1 gm/i, take in even

lesser amounts of these minerals. In a

bal-ance study in which human milk, without

any other food, was fed ad libitum, daily

calcium and phosphorus intakes were 320

mg and 110 mg, respectively.19 The Food

OWS S5-3-I

0 30 60 90 I0 IbO 60 IU e.U o iou iio jbV AGE, days

FIG. 5. Daily intake of calcium and phosphorus with cows’ milk. #{176}Soybean

formulas included with cows’ milk for calcium and with formulas for

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600

-I I I I I I I I

500

-400 -E

(I)

UI U

UI IL. z z

0

I-UI U

x

UI

U -J

4

U

4

ID

00

300

-0

200

-100 y:0.907X_

S

#{149}MALE

o FEMALE

0-100

-I I

700 800 900 000

and Nutrition Board stated,1’ “Although the

infant fed at the breast has less calcium

available and retains less, it must be

pre-sumed that calcium needs are fully met by

breast feeding.” Moreover, “Because.. . the

nutrient allowances are intended to meet

the needs of essentially all individuals in

the population, it is self-evident that they

are in excess of need for the majority of the

individuals in such a population.”

Excretion

Fecal excretion of calcium and

phospho-rus was proportional to intake over the

range observed in this study. Straight lines

of best fit relate excretion to intake in

Fig-ures 6 and 7 according to the equations:

(Equation 2-i)

Cafm,l = 0.907Ca - 173, and

(Equation 2-2)

PfocaI 0.477 Pin- 50

in units of milligrams per day. The squared

linear correlation coefficients (R2) for these

relations are 0.73 for calcium and 0.52 for

phosphorus, and respective standard

devia-tions are 55 and 46 mg/day. Neither sex

nor age significantly affected these

rela-tions. The average fecal excretion of

cal-cium was slightly higher for boys than girls.

No difference between sexes occurred for

fecal excretion of phosphorus, despite

higher intakes by boys.

Net absorption-absorption exclusive of

reabsorbed endogenous secretions-from

the gastrointestinal tract into blood can be

related to intake through Equations 2-1 and

2-2:

(Equation 2-3)

Caaboorption = Cain - Cafal

= 0.O93Cajn + 173, and

See note below Table XX

and application of R’.

for definition of R

OWl 15.5.5

200 300 400 500 600

DAILY CALCIUM INTAKE, mg

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674 STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

E 500

In

Ui UI IL

I I I I I

OWl 65.5.3

0

S

0

So

0.0 5

0

0

5

0 0

S S

OS

#{149}MALE FEMALE

y=0 477

0 00 200 300 400 500 600

DAILY PHOSPHORUS INTAKE,mg

Fic. 7. Phosphorus fecal excretion versus intake.

700 800 900

z - 4OO-z

0

UI U

X

300-UI

In

D

cr

9

200H

iOO=-a

(Equation 2-4)

1) . -P. _P

absorption - in fecal

= 0.523Pin + 50.

According to Equation 2-3, calcium

absorp-tion increases from 199 to 251 mg per day

within the entire range of calcium

intake-280 to 840 mg per day-in this study.

Phos-phorus absorption is much more responsive

to intake: extreme intakes of 240 and 840

mg per day correspond respectively to

ab-sorptions of 175 and 490 mg per day by

Equation 2-4.

Phosphorus in urine increased with

phos-phorus intake. The line of best fit has the

equation:

(Equation 2-5)

Purine = 0.430Pjn - 42

in units of milligrams per day; R2 is 0.48,

and the standard deviation is 46 mg per

day. Calcium in urine was not related

lin-early to intake. Probably for these reasons,

phosphorus excretion in urine increased

with age, whereas calcium excretion in

urine varied randomly with age (see Table

VIII). The log-normal distribution of daily

calcium and phosphorus excretion in urine

can be attributed to the multiplication of

independent factors25 in the transfer from

the gastrointestinal tract to blood,

be-tween blood and bone, and from blood to

urine.

Approximately 80% of the calcium values

lie within Knapp’s26 maximum and minimum

normal values for adults in terms of percent

of calcium intake in urine versus daily

cal-cium intake per body weight (Figure 8).

There is, however, no correlation between

the two variables in the infants; rather, the

percent calcium values form a band

be-tween intakes of 40 and 130 mg calcium per

kilogram body weight.

Gross Retention

Gross retention, defined as the difference

between intake and fecal plus urinary

ex-cretion, increased only slightly with intake.

Linear relationships between gross

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DWG 65-5-4

0 20 30 405060 80 100 200 300400 6008001000

DAILY CALCIUM INTAKE PER BODY WEIGHT, mg/kg

(Equation 2-6)

Caretention = 0.l90Ca0 + 84, and

(Equation 2-7)

‘retention = 0.lI j+ 59.

Respective standard deviations about these

lines are 58 and 45 mg per day, and R2

values are 0.13 and 0.16. Calcium and

phos-phorus retentions are unquestionably too

complex to be described as simple linear

functions of intake; Equations 2-6 and 2-7

are intended only to indicate the gradual

increase in retention with daily intake

values between 300 and 800 mg. At higher

intakes, retention would be expected to

ap-proach an upper limit. Near zero intake,

re-tention cannot exceed intake, and the

con-stant term vanishes, or becomes negative in

cases of endogenous excretion.13

Gross retention was almost constant

be-tween ages 60 and 300 days, as shown in

Figure 9. Retention at age 30 to 60 days

was somewhat lower, and agreed with

re-ported values.hu An almost constant value is

predicted by Equation 2-6. For example,

the increase of daily calcium intake from

483 mg in the second to 520 mg in the

tenth month only increases predicted gross

retention from 175 to 182 mg per day.

Be-cause retention was constant in this age

range, the common practice of reporting

re-tention in milligrams per kilogram body

weight (Figure 10) resulted in a

decreas-ing function with age.

Equation 2-6 is compared in Figure 11

with the average gross calcium retention

computed as a function of intake from the

results of Fomon, et ai.19 (dotted line). The

latter is based on values for infants who

consumed between 300 and 800 mg of

cal-cium in either human milk or formula A.

Gross retention in our study was 7% lower

at daily intakes of 300 mg, and 14% lower

at 800 mg. The line based on Fomon’s data,

however, lies within the standard deviation

of 59 mg per day of the curve for this

p-I

Li

Fic. 8. Relation between calcium in urine and in diet. Points are from this

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I I I I I 1 1 1 I I I

I I I I I I I I I I I

0

0

I I

I I I I I I I I I I

STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

Fic. 10. Average daily calcium retention per body weight as function of age.

0 Fomon, et al.” (formula A)

676

E 300

z

0

I-z

UI

200 Ix

UI

4

Ix

100 4

OWl 15.5.1

0 30 60 90 I20 50 I80 210 240 270 300

AGE, days

330 360

Fic. 9. Average daily retention as function of age. 0, Ca.; S P; fl and

#{149}

are Ca and P from Fomon, et al.’

study. Although retention by the youngest

infants in our study was similar to that

ob-served by Fomon, et al.1 with formula A,

our older infants retained less calcium.

Corrected Values

Average balance values corrected

ac-cording to Appendix C are listed in Table

XI. Forty-one percent of ingested calcium

was absorbed in the gastrointestinal tract,

32% of ingested calcium was retained, and

6% was excreted in urine. Average percent

phosphorus absorption was greater (64%),

but retention was less (21%); urinary

ex-cretion was 40%. Similar percent calcium

absorption has been reported for infants

(average, 34%)3 and adults (approximately

40%) 6 The average urinary excretion of

calcium was almost identical with Knapp’s

value of 5.7% of intake26 at the average

calcium intake of 63 mg per kilogram

body weight; the much higher phosphorus

I-I

I

z 20

0

I-z

Li

I-.

Li

Ix

Li

4

30

-10

0 30 60 90 120 150 80 210 240

AG E, days

(10)

I I I I I I I I I I I I I

I I I I I I

E

Ix

300

H

z

UI ...

F- ...

200-THIS STUDY, GR0SS(EQu...-’

<ZOO - THIS STUDY CORRECTED

I I I I

I

I

I

I

I

I

I

I

0 100 200 300 400 500 600 700 800 900

DAILY CALCIUM INTAKE (I), mg

Ftc. 11. Relation between intake and retention of calcium in infants.

based on Fomon, et a!.”

P/ins phorus

(mg)

461

292, 301*

160 175

21

96

SUPPLEMENT

OWO 15-5.6

values agreed with the observation that the

infant’s kidney is the chief organ for

ex-creting phosphorus.7

The dependence of retention on intake

within the range of this study is shown by

Equations 2-8 and 2-9, which are corrected

versions (see Appendix C) of Equations

2-6 and 2-7:

(Equation 2-8)

Caretention = 0.182Ca1, + 66 [correctedj, and

(Equation 2-9)

‘retention = 0. 149Pm + 25 [corrected].

The equations qualitatively support earlier

reports that calcium and phosphorus

reten-tions increase with intake, and that the

per-cent retention is larger at lower intake

rates.6’19 According to Equation 2-8, for

ex-ample, retention is 26% at an intake of 800

mg per day, and 42% at 300 mg per day of

calcium.

The average corrected calcium and

phos-phorus retentions in Table XI are only

slightly higher than respective daily tissue

increments of 148 and 89 mg estimated by

Fomon in 1967 for the male infant from

birth to age 12 months.24 Balance studies

performed before 1945 showed appreciably

higher values: daily calcium retention

be-tween 100 and 600 mg, with most values

clustered near 300 mg.3 A careful study of

infants between the ages of 52 and 325 days

who consumed cows’ milk, reported by

Nel-son in 1931,20 showed average daily calcium

and phosphorus retentions of 430 and 270

mg, respectively. The study by Fomon19

re-sulted in the calcium retention indicated in

Figure 11; over the same range of intake,

calcium and phosphorus retention were

both approximately 20% higher than the

corrected retentions in the present study.

Calcium accumulation to age 1 year

com-puted from the lower retention values in this

TABLE XI

COIIRErED AVERAGE DAILY CALcIU%1 AND PHOSPHORUS BALANCES

Calcium Data

(nig)

Intake 500

Net absorption 202, 210*

Fecal excretion 290

Urinary excretion 31

Sweat and saliva loss 13

Retention 158

* First value: net absorption = urinary excretion

+sweat and saliva loss+retention. Second value: net

absorption = intake- fecal excretion. The difference

occurs because intake and retention values are based

on 214 values, fecal and urinary excretion on only 141

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parable to the infants in this study, but on a

diet restricted to milk formula.

Phosphorus retention is highly correlated

with calcium retention. The line of best fit

for uncorrected retention, shown in Figure

12, has the equation, in units of milligram

per day,

(Equation 2-10)

Pretent jon = O.S7Caretent +30 [uiicorrectedl.

The standard deviation about the line is ±

34 mg per day, and R’ is 0.52. The mean

value of the ratio of phosphorus to calcium

for 214 values is 0.73.

Corrected according to Appendix C,

Equation 2-10 becomes:

(Equation 2-1 1)

Pretention = O.57Cart.Ieflt Oh + 7 [corrected].

0 50 100 150 200 250 300 350 400 450 500

DAILY CALCIUM RETENTION, mq

678 STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

study agrees with predicted values (see Part

2-Calcium Retained by Infants During the

First Year). In contrast, the very high

re-tention values reported in many of the early

studies lead to an impossibly high calcium

content in the body.3 The higher retention

values can be attributed to one or more of

four causes: (1) the possible effect, in early

studies, of a sudden increase in calcium

in-take over prebalance diets; (2) higher

cal-cium intake on diets of cows’ milk,

com-pared to the relatively-low-calcium diet in

this study; (3) lack of correction for

sys-tematic losses in feeding and collecting

ex-creta, and in other paths of excretion, such

as perspiration (see Part 1-Accuracy); or

(4) the possibly greater availability for

absorption of calcium from milk than from

many other foods.17’2’ The infants in the

study by Fomon, et al.’9 from whose

bal-ance values the line in Figure 11 was

con-structed, ingested amounts of calcium

com-Phosphorus Retention Versus

Calcium Retention

Fic. 12. Relation between calcium and phosphorus retention. Not shown are two negative values

(In-fant 9, Period 9-61, and Infant 24, Period 10-62, see Appendix B) and nine extreme values (see Part

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(‘aictuin Gain in Period

(‘orrected

(mg/day) (ing/day) (gm/perwd) Age (da) () 8-30 31-6() 61-9() 91-120 121-150 151-18() 181-21() ‘211-241) 241-271) 271-300 Number ci Infants 30 6 13(11) ‘25 (22) 31(29) 33 32 25 29 (28) 18 (6) 10 Calcium at End of Period (gm) Body Weight at End of

Period (kg) 3.4 5.3 6.1 6.8 7.3 7.8 8.3 8.7 8.9 9.1 -- ‘28.’2t

144 123 ‘2.7 30.9

140 119 3.6 34.5

190 167 5.0 39.5

169 146 4.4 43.9

179 157 4.7 48.6

177 155 4.6 53.2

194 171 5.1 58.3

176 154 4.6 62.9

190 169 5.0 67.9

187 165 4.9 72.8

(‘dcii, rn/Body Weight (%) 0.82 0.65 0.65 0.65 0.67 0.69 0.7(1 0.72 0.76 0.80

* Intake-excretion for indicated number of (lays in age group. f From References 4, 7, and 13, Part 2.

Infants tonsuining Formula A only, from Reference 19, Part ‘2.

§First number applier to body weight, number in parentheses to calcium gain. Number iIItIy exceed 30 becaIlse two 28-day periods for tile same infant solnetimes fall into tile same 30-day age group.

‘FABLE XII

AvEIt.GF: CALCIUII CONTENT OF INFANTS

Thus, the phosphorus/calcium ratio is

al-most independent of the amount of

re-tained calcium, and has a value slightly

above 0.57. At average daily retentions of

96 mg phosphorus and 158 mg calcium, the

ratio is 0.61.

Earlier balance studies provide similar

values. The average ratio for infants

be-tween ages 52 and 325 days who consumed

only cows’ milk was 1/1.75 = Q572o In a

study with infants aged 11 to 182 days who

consumed only formula A, the average ratio

was 0.65.’

Measurements of the body content of

calcium and phosphorus in infants

through-out their first year are not available for

checking these ratios computed from

bal-ance studies. From the few whole-body

analyses available in newborns and adults,

the average phosphorus/calcium ratio is

16.2 gm per 28.2 gm = 0.58 in the 3.5 kg

in-fant, and 740 gm per 1,320 gm = 0.56 in the

70 kg adult.4 Changes in calcium and

nitro-gen composition of the body are very

simi-lar for the same dietary regimens, and

changes in phosphorus content follow these

two elements.7 In the absence of any

infor-mation on possible extremes in the

phosphorus/calcium ratio between birth

and maturity, the ratio in retained material

would therefore be expected to be near 0.56.

Calcium Retained by Infants During

the First Year

The retention of calcium in infants

dur-ing their first year is computed in Table XII

by adding the average corrected retained

calcium for each consecutive 30-day age

group to the amount initially present. The

average amount of calcium at birth is

usu-ally taken to be 28.2 gm,4 or 0.82% of body

weight for infants weighing approximately

3.4 kg.13 For the calcium accumulation to

age 30 days, the average obtained by

Fomon, et a!. for infants fed only formula A

was used;19 subsequent average body

weights and calcium retentions are from

the present study.

The calcium content of infants,

com-puted in Table XII, is shown as a function

of age in Figure 13. After a slight initial

curve, calcium increases linearly from age

60 to 300 days. Extrapolation yields 83 gm

(13)

>. 0

0 z

0

4

IIII’II’I’T#T

calcium content at age 1 year, based on

body weight, are 82 to 85 gm by Leitch and

Aitken,13 approximately 84 gm by Beninson,

et al.,27’28 100 gm by Mitchell, et a!. for

boys,14 and 81 gm by Fomon for boys.24

Stearns pointed out the effect of calcium

intake on calcium retention and computed

the body content relative to body weight

DWG 65-5-i

2 0.4 -U -J

(-3

0.2

-I I I 1 1 1 I I

0 30 60 90 120 150 180 210 240 270 300 330 360 390

AGE, days

Fic. 14. Calcium per body weight during first year. Curves for intake of

cows’ milk and human milk from Steams.’ [J Mitchell, et al.;”

[J

Leitch and

Aitken.’

680 STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

30 60 90 120 50 80 210 240 270 300

AGE, doys

Fic. 13. Calcium content of infants.

ws ss.s for consumption of equal amounts of either

cows’ milk or human milk.7 The curves,

re-produced in Figure 14, predict a much

higher calcium content in infants who drink

relatively-high-calcium cows’ milk. They

also show a minimum percent calcium in

the body early in the first year. The

per-centages of calcium per body weights of

0.90 to 0.93 by Leitch and Aitken13

(rectan-gle) and 0.94 by Mitchell, et al.’ (square)

at age 1 year are more consistent with the

lower curve. The values from Table XII

(circles in Figure 14) also show a

mini-mum and fall between the two curves by

Stearns, as is appropriate to calcium intakes

that were between mothers’ and cows’ milk

in magnitude.

Corrected retention thus agrees with

pre-dicted accumulation values, especially those

of Leitch and Aitken,3 Fomon,24 and

Be-ninson, et al.27,2s The uncorrected calcium

content at age 300 days was 79 gm and

0.87% per body weight, and extrapolates to

(14)

respec-DWG 655IO

023 g/doy

ABSORPTION

EXCHANGEABLE POOL

33g

(RETENTION -.O.OO8g/day)

Fic. 15. Compartment model for calcium metabolism in infants (age 164

days, weight 7.4 kg).

681

0 50 g/day

I NTAKE

O 03 g/day

ENDOGENOUS FECAL EXCRE TA

0 30 g/day

FECAL

E XC RE TA

I

I

0.03 Ig/doy 0.OI3g/doy

URINE SWEAT AND

SALIVA LOSS

tively, at age 1 year. These values are 10%

higher than corrected values of

approxi-mately 83 gm and 0.89%, but are still

rea-sonably similar to the predicted values

cited above.

Calcium Model

To provide the basis for computing

strontium-90 retention, a model for calcium

metabolism in the infant was constructed

(Figure 15) that is analogous to the model

for adults by Dolphin and Eve.’5 It uses the

definitions of accretion, resorption, and so

forth, by Bauer, et al.29 The exchangeable

pool as defined to contain the calcium that

exchanges with calcium in plasma at a half

time of several hours or less. It is believed

to consist of calcium in extracellular fluid,

soft tissue, and a small fraction of the

skele-ton. Gross absorption is taken to be the net

absorption computed from the balance

study, plus an amount equal to the

endoge-nous fecal excretion. Reabsorption of

en-dogenous calcium is not considered in the

model, although it is taken into account in

computing fractional transfers by Equations

2-14 and 2-15. It is assumed that

endoge-nous calcium enters the gastrointestinal tract

in digestive juice.13

Average intake, excretion, and retention

values in Figure 15 are from this study

073g/doy

EEiTIO”1EXCH&NGEABLEI

I BONE I

I 47g I

O 58g/day J(RETENTION

I

PTIOdJ

(Table XI). The size of the exchangeable

pool, the accretion rate, and the rate of

en-dogenous fecal excretion are from tracer

studies with radiocalcium. All other values

are derived from these combined data, as

indicated in Table XIII. Average values for

all periods, and for periods classified by

age, are given in Appendix E, Table

XXXVI. The values in Figure 15 are

rounded off to one or two significant figures

in the direction required for a balance of

in- and out-flow.

The exchangeable pool size and internal

transfer rates are based on meager data,

and hence are tentative. The exchangeable

pool size is the average of five values for

“control” infants aged 6 to 9 months.3#{176}

Ear-lier values (312 mg per kilogram) reported

by the same authors3’ for seven normal

in-fants, and values for two infants (169 mg

per kilogram) reported by other authors32

are appreciably lower. The accretion rate

was computed from a linear relation

be-tween accretion rate and exchangeable pool

size; the numerous values-normal and

rachitic, infant and adult-varied

apprecia-bly about the line of best fit.8#{176}The

endoge-nous fecal value was for a single “control”

infant on a low-calcium diet.33 The average

of two other values for endogenous

(15)

(‘ornpartment or Pat/i

.1 mount

(gui) (‘alculation

442 mg/kg body weight

Source

Exchangeable pool 3.3

Non-exchangeable bone 47

l)aily accretion (1.73

I)aily retention in

exchangeable pool 0. 01*

I)aily retention in

non-exchangeable bone 0. 15

I)aily resorption 0.58

l)aily endogenous fecal

excretion 0.03

Daily gross absorption 0.23

Table XI

Reference 31

Table XI

atnciu ut. in compartment

682 STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

TABLE XIII

VALUES FOR COMPARTMENT MODEL OF CALCIUM METABOLISM IN THE INFANT*

* Age= 164 days; weight=7.4 kg.

Referene 30

50.7 gm total calcium-exchangeable pool Table XII

0.25X44’2- 11.7=99 mg per day/kg body weight Reference 80

[(body weight, age 300 days) - (body weight, ago 0 days)] 44’2

1 ,000 X 300 days

Retention - Retention in exchangeable pool

Daily accretion-Daily retention in non-exchangeable bone

Daily net absorption +daiiy endogenous fecal excretion

(reab8orbed endogenous calcium not included)

per day for endogenous fecal excretion if

the urinary excretion was 31 mg per day.

Leitch and Aitken estimated 40 to 60 mg

per day for endogenous excretion in small

children.’3

The two half-lives, T, describing the

re-lease of calcium from the body according to

this model were calculated by analogy to

values for the decrease of calcium tracer

after a single intravenous injection:

(Equation 2-12)

exp ( - 0.693 X time interval/i)

amoiiiit retained in compartment after interval amount illcompartment

(Equation 2-12a)

(‘Xp ( - 0.693 X tinie iiiterval/T)

= 1 uut0”A. from conipartrneiit. in time interval

amount in compartment

When the time interval is one day,

(Equation 2-12h)

(‘Xp (-O.693/T)

= - daily outflow from compartment

The half-life for outflow from the

exchange-able pooi (Tn) is, therefore,

(Equation 2-12c)

exp (-0.693/T0)

=

1---(Equation 2-12d)

0.73 + 0.013 + 0.031 + 0.03

3.3

T1. = 2.5 days.

For non-exchangeable bone, the daily

out-flow at equilibrium is the resorption rate

multiplied by the ratio of total outflow

from the body to the total outflow from the

exchangeable pooi, i.e., 0.58(0.013 +

0.031 + 0.03)/0.80 = 0.054 gm. For this

small daily outflow (relative to the amount

in the compartment), Equation 2-12b can

be simplified to:

(Equation 2-13)

0.693 T

daily outflow from conipaitinent

(16)

f.,’ =

(Equation 2-13a)

(0.693) amount iii compartment

(laity outflow from compartment

The half-life for outflow from

non-exchange-able bone (Tb) is, therefore,

(Equation 2-13b)

(0.693)47

600 days

0.054

Because flows from and to the two

com-partments are related, it is an

oversimplifi-cation to associate these half-lives with the

compartments. Moreover, the two values

are only approximate because recirculation

of tracer has been ignored for the

ex-changeable pool and simplified for

non-ex-changeable bone. The two values apply to

the average coefficients in Figure 15, and

would not necessarily remain constant

throughout the first year, in view of the

in the adult.3 The high replacement rate

agrees with the value by Beninson, et a!.

of 50% in the first year,35 and with Bryant

and Loutit’s estimate of considerable, if

not complete, turnover in the first 2 years

of life. Total accumulation of newly

de-posited calcium during the first year would

be approximately 65 gm: 34% replacement

of the 28 gm at birth plus a net increase

of 55 gm.

The fractional transfer of calcium from

the gastrointestinal tract to blood and

from blood to bone-f, and f2’, respectively,

in ICRP terminology’8-can be computed

from the model if the total endogenous

calcium in the gastrointestinal tract is

known. Accurate values of digestive-juice

calcium in infants are difficult to obtain

and are variable, but the average in a

tracer study of rachitic infants was

ap-proximately 0.1 gm per day. Thus,

(Equation 2-14)

(Equation 2-15)

- absorption + endogeiious re-absorption

intake + endogenous to GI tract

0.23 + 0.07

= --______ = 0.50

0.50 +0.1

accretion

accretion + urine+ sweat & saliva + endogenous to (II tract

0.73

= = 0.84.

0.73 + 0.031 + 0.013 + 0.1

changing coefficients shown in Table

XXXVI.

In two radiocalcium tracer studies with

infants, one showed a half life of

approxi-mately 2 days between the second and fifth

day after tracer injection,3’ and the other

gave an average value of 1.5 days.32 A

shorter-lived component (0.1 to 0.2 day)

that was also reported’ probably refers to

equilibration within the exchangeable pooi.

The replacement rate of calcium in

non-exchangeable bone for a 600-day half life

is 34% per year, compared to 2.0 to 3.5%

Adult values are similar: f, = 0.6 and

f2 = 0.9.”

In adults, a simple compartment mode

of the type shown in Figure 15 would be a

gross simplification for at least the

follow-ing reasons:

1. Calcium turnover is more complex,

with replacement rates ranging from 1.2 to

4.0% per year in compact bone and from 8

to 9% in trabecular bone. 4 Rates from a

multiplicity of compartments presumably

combine to yield the power function by

(17)

684 STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

can be described.38’39 Moreover, individual

processes of exchange and accretion are less

distinct than is assumed in the model.4#{176}

2. Old and newly-accreted bone do not

mix instantly and completely, as was

as-sumed for calculating half lives (see

pre-viously given information) and stable

strontium/calcium and strontium-90/stable

strontium ratios in resorbed bone material

(see Part 3-Strontium Model and Part

4-Strontium-90 Balance as Test of

Com-partment Model for Infants 26 to 37).

Ac-tual ratios in resorbed material relative to

the non-exchangeable pooi would fluctuate

between lower values and “hot spots.”

3. Endogenous calcium and strontium

that pass to the gastrointestinal tract and

are reabsorbed signfficantly affect

calcula-tions of percent absorption, discrimination

factors, and so forth.6’38’41

In infants, this model is undoubtedly a

better approximation because the rapid

turnover of skeletal material decreases the

significance of the first two factors, and

endogenous reabsorption-as considered

in Equations 2-14 and 2-15-appears

to have a relatively small effect. For

example, if the estimated amount of

di-gestive-juice calcium were 0.2 instead of

0.1 gm per day as in Equations 2-14 and

2-15, f, would change only to 0.40/0.70 =

0.57, and f,’ to 0.73/0.97 = 0.75.

Never-theless, the model presents only a first

ap-proach, and tracer studies with long-lived

radiocalcium in young animals are needed

to evaluate its applicability.

SUMMARY

Intake, excretion, and retention of

cal-cium and phosphorus were determined for

30 infants by a metabolic balance study in

the home. In addition, the average

accumu-lation of calcium during the first year was

computed, and a simple model of calcium

metabolism was developed from these

values and published tracer data.

The corrected average daily intake was

0.50 gm calcium and 0.46 gm phosphorus.

These values are appreciably lower than

recommended intakes based on cows’ milk,

mainly because the premodified-milk

for-mulas and infant foods in the infants’ diets

contained less calcium and phosphorus than

cows’ milk. Both items are commonly used

in the United States and may result in

cal-cium and phosphorus intakes below

recom-mended levels for many infants; human

milk provides even lesser amounts of these

two minerals.

The respective corrected average daily

fecal excretions of calcium and phosphorus

were 0.29 and 0.16 gm, and urinary

excre-tions were 0.031 and 0.18 gm. The amounts

excreted in feces were related linearly to

the intake. Phosphorus in urine was also

correlated linearly with intake, but calcium

was not.

Corrected average daily retention of

cal-cium and phosphorus was 0.16 and 0.10 gm,

respectively. Calcium and phosphorus

re-tention increased slightly with intake; for

example, changing the daily calcium intake

from 0.40 to 0.80 gm is predicted to

in-crease daily retention from 0.14 to 0.21 gm.

Percent retention, however, decreased with

increasing intake. Calcium and phosphorus

retention did not change between the third

and tenth month of life. The measured

values were 7% higher for calcium and 8%

higher for phosphorus than estimated by

Fomon for boys in their first year.24

Accumulated calcium increased almost

linearly with age. Based on the commonly

cited calcium content at birth of 28 gm and

observed accumulation of 43 gm between

the first and tenth months, the calcium

con-tent at age 1 year was estimated to be 83

gm. Leitch and Aitken13 estimated 82 to 85

gm at this age. Relative to body weight,

based on a value of 8.2 gm per kilogram at

birth, the computed calcium content

reached a minimum of 6.5 gm per kilogram

in the third month and then increased to

8.0 gm per kilogram at the end of the tenth

month.

A calcium model was developed for the

average age and weight of the infants in

the study-164 days and 7.4 kg,

respec-tively. The two compartments consisted of

(18)

SUPPLEMENT

and 3.3 gm in the exchangeable pool

(ex-tracellular fluid, soft tissue, and bone

sur-faces). The half lives for replacing a single

dose of calcium tracer were computed to be

2.5 and 600 days. Transfer fractions from

gastrointestinal tract to blood (f,) and

from blood to bone (f2’) were estimated to

he 0.5 and 0.8, respectively.

REFERENCES

1. Comar, C. L., and Wasserman, R. H.:

Stron-tium. In Comar, C. L., Bronner, F., ed.:

Mineral Metabolism, Vol. II, Part A. New

York: Academic Press, pp. 523-572, 1964.

2. United Nations: Report of the United Nations

Scientific Committee on the Effects of

Atomic Radiation. General Assembly,

Seven-teenth Session, Suppl. No. 16 (A/5216),

pp. 288-305, 1962.

3. Holmes, J. 0.: The requirement for calcium

during growth. Nutr. Abstr. Rev., 14:597,

1945.

4. Widdowson, E. M., and Dickerson, J. W. T.:

Chemical composition of the body. In

Comar, C. L., and Bronner, F., ed: Mineral

Metabolism, Vol. II, Part A. New York:

Aca-demic Press, pp. 1-247, 1964.

5. Irving, J. T.: Dynamics and function of

phos-phorus. In Comar, C. L., and Bronner, F.,

ed.: Mineral Metabolism, Vol. II, Part A.

New York: Academic Press, pp. 249-313,

1964.

6. Bronner, F.: Dynamics and function of

cal-cium. In Comar, C. L., and Bronner, F., ed.:

Mineral Metabolism, Vol. II, Part A. New

York: Academic Press, pp. 341-444, 1964.

7. Stearns, G.: The mineral metabolism of normal

infants. Physiol. Rev., 19:415, 1939.

8. Ilegsted, D. M.: Calcium and phosphorus. In

Wohl, M. C., and Goodhart, B. S., ed.:

Mod-em Nutrition in Health and Disease.

Phila-delphia: Lea and Febiger, pp. 205-219, 1955.

9. White, P. L.: Symposium on human calcium

requirements. J. A. M. A., 185:588, 1963.

10. World Health Organization. Calcium

Require-ments. WHO Tech. Rep. Ser. No. 230,

1962.

11. National Academy of Science-National

Re-search Council: Dietary Allowances, ed. 6,

revised. Publication 1146. Washington, D.C.:

NAS-NRC, 1964.

12. Nicolaysen, R., Eeg-Larsen, N., and Maim,

0. J.: Physiology of calcium metabolism.

Physiol. Rev., 33:424, 1953.

13. Leitch, I., and Aitken, F. C.: The estimation of

calcium requirement: A re-examination.

Nutr. Abst. Rev., 29: 393, 1959.

14. Mitchell, H. H., Hamilton, T. S., Steggerda,

F. R., and Bean, H. W. : The chemical

com-position of the adult human body and its

bearing on the biochemistry of growth. J.

Biol. Chem., 158:625, 1945.

15. Dolphin, C. W., and Eve, I. S. : The

metabo-tism of strontium in adult humans. Phys.

Med. Biol., 8:193, 1963.

16. MaIm, 0. J.: Calcium Requirement and

Adap-tation in Adult Men. Oslo, Norway: Oslo

University Press, 1958.

17. Sherman, H. C. : Calcium and Phosphorus in

Foods and Nutrition. New York: Columbia

University Press, 1947.

18. International Commission on Radiological

Pro-tection: Report of ICRP Committee II on

permissible dose for internal radiation

(1959), with bibliography for biological,

mathematical and physical data. Health

Phys., 3:1, 1960.

19. Fomon, S. J., Owen, C. M., Jensen, R. L., and

Thomas, L. N.: Calcium and phosphorus

balance studies with normal full term infants

fed pooled human milk or various formulas.

Amer. J. Clin. Nutr., 12:346, 1963.

20. Nelson, M. V. K.: Calcium and phosphorus

metabolism of infants receiving undiluted

milk. Amer. J. Dis. Child., 42:1090, 1931.

21. Lengemann, F. W., Comar, C. L., and

Wasser-man, B. H.: Absorption of calcium and

strontium from milk and nonmilk diets. J.

Nutr., 61 :571, 1957.

22. Beal, V. A.: Nutritional intake of children. J.

Nutr., 53-54:499, 1954.

23. Filer, L. J., and Martinez, C. A.: Intake of

se-lected nutrients by infants in the United

States. Clin. Pediat., 3:633, 1964.

24. Fomon, S. J.: Infant Nutrition. Philadelphia:

W. B. Saunders Co., pp. 142 and 163, 1967.

25. Koch, A. L.: The logarithm in biology 1.

Mechanisms generating the log-normal

dis-tribution exactly. J. Theoret. Biol., 12:276,

1966.

26. Knapp, E. L.: Factors influencing the urinary

excretion of calcium. I. In normal persons. J.

Clin. Invest., 26:182, 1947.

27. Beninson, D., Migliori, H., and Ramos, E.:

Strontium-90 levels in the diets and bones

of children, Progress Report-1962-63. In

Fallout Program Quarterly Summary Report,

Atomic Energy Commission Report

HASL-149, pp. 105-118, October 1, 1964.

28. Beninson, D., Ramos, E., and Touzet, R.:

Strontium in children. In Fallout Program

Quarterly Summary Report, Atomic Energy

Commission Report HASL-165, pp. 289-300,

January 1, 1966.

29. Bauer, C. C. H., Carlsson, A., and Lindquist,

B.: Evaluation of Accretion, Resorption, and

(19)

686 STRONTIUM, CALCIUM, AND PHOSPHORUS RETENTION

Fysiografiska Sallskapets I Lund

Forhandlin-gar, BD 25. NR1., 1955.

30. Harris, F., Hoffenberg, R. and Black, E.:

Cal-cium kinetics in vitamin D deficiency

rick-ets. I. Plasma kinetic studies after

intrave-nous and oral Ca”. Metabolism, 14:1101,

1965.

31. Hoffenberg, R., Harris, F., and Black, E.; Ca”

in the investigation of rickets. In Medical

Uses of Ca”: Second Panel Report,

Techni-cal Report Series No. 32. Vienna:

Interna-tional Atomic Energy Agency, p. 61, 1964.

32. Bauer, C. C. H., Cartsson, A., and Lindquist,

B.: Bone salt metabolism in humans studied

by means of radiocalcium. Acta Med.

Scand., 158:143, 1957.

33. Hoffenberg, B., Harris, F., and Black, E.:

En-dogenous faecat calcium, total digestive

juice calcium and utilization of intestinal

calcium. in Medical Uses of Ca47: Second

Panel Report, Technical Report Series No.

32. Vienna: International Atomic Energy

Agency, p. 131, 1964.

34. United Nations: Report of the United Nations

Scientific Committee on the Effects of

Atomic Radiation. General Assembly,

Nine-teenth Session, Suppl. No. 14 (A/5814), p.

32, 1964.

35. Beninson, D., Ramos, E., Abramides, and

Men-ossi, C.: Strontium-90 levels in the diets

and bones of children, Progress

Report-1966. In Fallout Program Quarterly

Sum-mary Report, Atomic Energy Commission

Report HASL-173, pp. 1-31 to 1-57, October

1, 1966.

36. Bryant, F. J., and Loutit, J. F.: Human Bone

Metabolism Deduced from Strontium

As-says. United Kingdom Atomic Energy

Au-thority Report AERE-R 3718, 1961.

37. Cohn, S. H., Bozzo, S. R., Jesseph, J. E.,

Con-stantinides, C., Huene, D. B. and Cusmano,

E. A.: Formulation and testing of a

com-partmental model for calcium metabolism in

man. Radiat. Res., 26:319, 1965.

38. Dolphin, C. W., and Eve, I. S.: Some aspects

of radiostrontium dosimetry. Phys. Med.

Biol., 8:205, 1963.

39. Marshall, J. H.: Theory of alkaline earth

me-tabolism. J. Theoret. Biol., 6:386, 1964.

40. Heaney, B. P.: Evaluation and interpretation

of calcium-kinetic data in man. Clin.

Or-thop., 31:153, 1964.

41. Cran, F. C., and Nicolaysen, R.: A theoretical

analysis of radiostrontium metabolism and

deposition in humans. Acta Physiol. Scand.,

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1969;43;668

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INTAKE AND EXCRETION OF CALCIUM AND PHOSPHORUS BY INFANTS;

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