Dietary protein intake and urinary excretion of calcium: a
cross-sectional study in a healthy Japanese population1–3
Roichi Itoh, Noriko Nishiyama, and Yasuo Suyama
ABSTRACT To evaluate whether habitual excess protein
intake is a significant risk factor for calcium loss, we studied the
relation between urinary excretion of calcium and protein intakes,
in 349 male and 406 female Japanese aged 20–79 y. The subjects
were apparently healthy, free-living, and consuming diets of their
own choosing. We divided the subjects into two groups: those
aged 20–49 y and those aged 50–79 y. In each group, we observed
a significant positive correlation between daily urinary excretion
of calcium and protein intake. Calcium excretion also correlated
positively with daily urinary excretion of urea. Multivariate
analyses revealed that in each age group the relation between cal-
cium excretion and urea excretion remained significant even after
sex, age, body weight, urinary sodium excretion, and calcium
intake were adjusted for. The correlation of calcium excretion
with animal protein intake was significantly positive in both sexes
and in each age group whereas that with plant protein was not. We
observed a significant positive correlation between daily calcium
excretion and daily urinary excretion of sulfate. The correlation in
50–79-y old subjects remained significant even after sex, age,
body weight, sodium excretion, and calcium intake were adjusted
for. Our findings suggest that excess protein, especially that rich
in sulfur-containing amino acids, in habitual diets may augment
calcium excretion in the urine, at least in the elderly. Am J
Clin Nutr 1998;67:438–44.
KEY WORDS Urine, calcium, urea, protein, sulfate, plant
protein, animal protein, humans, Japan
INTRODUCTION
A high-protein diet has been shown in experimental human
and animal studies to increase calcium excretion (1). It has been
hypothesized that this is due to the increase in glomerular filtra-
tion rate and the decrease in renal reabsorption of calcium (1).
Because intestinal calcium absorption is not increased simulta-
neously with a high-protein diet (2), urinary calcium loss often
leads to adverse calcium balance (3). A diet rich in protein may
lead to bone resorption, resulting in osteoporosis.
To evaluate habitual excess protein intake as a significant risk
factor for calcium loss, it is essential to conduct epidemiologic
studies on the relation between these factors in free-living popu-
lations consuming diets of their own choosing.
Metz et al (4) observed, in 38 white women aged 24–28 y, that
protein intake was negatively associated with radial bone min-
eral content and bone density. To elucidate the major dietary
determinants of the calcium loss induced by elevated intakes of
438 Am J Clin Nutr 1998;67:438–44. Printed in USA. © 1998 American Society for Clinical Nutrition
protein, Hu et al (5) examined the relation between dietary intake
and calcium in overnight urine samples obtained in a cross-sec-
tional survey of 764 middle-aged and elderly women living in
five districts in China, where the residents had markedly differ-
ent dietary patterns and lifestyles. They found that urinary cal-
cium correlated positively with urinary acid excretion as well as
with animal protein intake, but correlated negatively with plant
protein intake. They concluded that under free-living conditions,
urinary calcium excretion is likely determined by the acid-base
status of the total diet, and pointed out the importance of animal
protein in endogenous acid production.
In 1994, we conducted a cross-sectional survey on sodium
intake and calcium loss in a culturally homogeneous population
of 886 healthy free-living males and females of a wide age range
(6). Besides a positive correlation of sodium intake with calcium
excretion, we also found that protein intake correlated positively
with calcium excretion in this population. The correlation
remained even after sex, age, body weight, sodium excretion,
and calcium intake were adjusted for.
This prompted us to examine whether the effect of dietary
protein sources on calcium excretion could also be observed in a
Japanese population (6), as reported by Hu et al for Chinese pop-
ulations (5). We also investigated the relation of urinary calcium
with urinary sulfate.
SUBJECTS AND METHODS
Subjects
Selection of the subjects for the survey was described in detail
in a previous publication (6). Briefly, 1011 men and women
between the ages of 20 and 79 y with good general health and
normal ambulation were recruited in Nagano Prefecture, which
is located in the central part of the main island of Japan. Dietary
patterns and other lifestyle elements of the residents in this area
were fairly homogeneous and typically Japanese. The health sta-
1
From the Department of Home Economics, Tokyo Kasei Gakuin Univer-
sity, and the Physical Fitness Institute, Meiji Life Foundation of Health and
Welfare, Tokyo.
2
Supported by a grant from the Ministry of Health and Welfare of Japan,
Tokyo.
3
Address reprint requests to R Itoh, the Department of Home Economics,
Tokyo Kasei Gakuin University, 2600 Aiharamachi, Machida-city, Tokyo
194–02. E-mail: ysuyama@tky0.attnet.or.jp.
Received April 1, 1997.
Accepted for publication August 25, 1997.
 ITOH ET AL
tus of the subjects was assessed by their medical history and
results of blood counts and laboratory tests. Subjects were
excluded if they showed evidence of impaired renal function,
used medications known to affect electrolyte metabolism, had
any problem with the urine collection, or had inadequate dietary
records. The number of subjects selected for the final multivari-
ate regression of analyses was 755 (349 men and 406 women).
Informed consent was obtained from each participant. The
study protocol was approved by the Council of Health Statistics
of the Nagano Prefectural Government.
Collection of urine and dietary data
Methods for collection of urine and dietary data were
described in detail in a previous publication (6). Briefly, subjects
were asked to collect all urine excreted after the first quantity
voided in the morning until and including the first morning urine
voided the next day. Urine samples were assessed for complete-
ness by self-reported information and the creatinine index
method (7).
Dietary intakes on the day of urine collection were assessed with
dietary records by essentially the same method as described by
Garry et al (8). All food records were coded by food item and
amount and analyzed for nutrient composition with a computerized
nutrient database compiled from a food-composition table (9).
Determination of urinary constituents
Urinary sulfate was determined by turbidimetry with barium
chloride in agarose solution (10). Urinary urea was determined
by a urease-glutamate dehydrogenase method (11). The other
urinary constituents were determined as described in our previ-
ous publication (6).
Statistics
The data were analyzed by techniques included in the SPSS-
X statistical software package (12). Because of the previously
described changes with age in the excretion profiles of urinary
calcium observed in this population (6), the subjects of both
sexes were divided into two groups for statistical purposes: those
aged 20–49 y and those aged 50–79 y.
Two-way analysis of variance (ANOVA) was used to deter-
mine the effect of age, sex, and their interactions on anthropo-
metric measures, dietary intakes, and urinary excretion of cal-
cium, urea, sulfate, and sodium.
A stepwise regression analysis was used to examine the con-
tribution of urinary urea excretion or sulfate excretion as a pre-
TABLE 1
Two-way ANOVA of anthropometric characteristics of the subjects by age and sex1
20–49 y
Men
(n = 163)
Age (y) 37.0 ± 7.7
Weight (kg)2 66.4 ± 9.4
Height (cm)3 169 ± 6
BMI (kg/m2)4 23.2 ± 2.9
1 –
x ± SD.
2
Significant effect of age (P < 0.001), sex (P < 0.001), and an interaction of sex and age (P < 0.001).
3
Significant effect of age (P < 0.001) and sex (P < 0.001).
4
Significant effect of sex (P = 0.045) and an interaction of sex and age (P < 0.001).
439
dictor of calcium excretion. For the analyses of the relation
between calcium excretion and urea excretion, daily urinary cal-
cium excretion was used as a dependent variable, and sex, age,
body weight, daily urea excretion, daily sodium excretion, and
daily calcium intake were used as independent variables. For the
analyses of the relation between calcium excretion and sulfate
excretion, daily sulfate excretion was used instead of daily urea
excretion as an independent variable. Urea excretion and sulfate
excretion were not included in the same model because of their
high degree of colinearity. Sex was coded as a dummy variable:
1 = males and 2 = females. P < 0.05 was used as the level of sig-
nificance for all tests.
RESULTS
Anthropometric measures and dietary intakes
The means and SDs of age and anthropometric measures for
each sex and age group are shown in Table 1. In Table 2, mean
± SD daily dietary intakes of energy, protein, calcium, and
sodium for each sex and age group are shown. The mean total
protein intake of the subjects was 20–30% higher than the rec-
ommended dietary allowances (RDAs) for Japanese (13) of cor-
responding age groups (70 g/d for males aged 20–79 y and 60
g/d for females aged 20–79 y). Mean energy intakes were simi-
lar to the RDA for corresponding sex and age groups (10 400 and
9100 kJ for men aged 20–79 y and 50–79 y, respectively, and
8300 and 7400 kJ for women aged 20–49 and 50–79 y, respec-
tively). Mean calcium intakes were also similar to the RDA for
Japanese men and women aged ≥ 20 y (15 mmol/d). In this pop-
ulation <53% of total protein intake was of animal origin
whereas <47% of the plant protein intake was from cereals. The
results of the two-way ANOVA for the effect of age, sex, and
their interactions on these variables are also shown in both
Tables 1 and 2.
Urinary calcium, urea, sulfate, and sodium excretion
Mean (± SD) daily urinary excretions of calcium, urea, sul-
fate, and sodium in each sex and age group are given in Table 3.
Mean (± SD) urinary calcium-creatinine, urea-creatinine, sul-
fate-creatinine, and sodium-creatinine ratios in each sex and age
group are shown in Table 4. The results of the two-way ANOVAs
for the effect of age, sex, and their interactions on the excretion
of these urinary constituents are also shown in both Tables 3 and
4.
Age group
50–79 y
Women Men Women
(n = 216) (n = 227) (n = 231)
37.1 ± 7.5 62.8 ± 7.8 62.4 ± 7.1
53.3 ± 7.4 58.7 ± 8.1 51.1 ± 7.5
157 ± 6 161 ± 6 149 ± 6
21.8 ± 2.8 22.6 ± 2.7 23.1 ± 3.0
440 PROTEIN AND URINARY CALCIUM IN JAPAN

TABLE 2
Two-way ANOVA of daily dietary intakes of energy and selected nutrients by age and sex1
Age group
20–49 y 50–79 y
Men Women Men Women
(n = 145) (n = 201) (n = 203) (n = 205)
Energy intake (kJ/d)2 9870 ± 2067 7573 ± 1477 9397 ± 2330 7282 ± 1540
Total protein intake (g/d)3 89 ± 28 72 ± 24 88 ± 32 74 ± 27
Animal protein intake (g/d)3 48 ± 23 38 ± 19 46 ± 27 38 ± 21
Plant protein intake (g/d)3 41 ± 13 34 ± 12 42 ± 12 36 ± 11
Cereal protein intake (g/d)3 22 ± 8 15 ± 6 21 ± 8 15 ± 5
Calcium intake (mmol/d) 14.7 ± 6.9 14.7 ± 7.1 15.8 ± 8.1 15.0 ± 8.3
Sodium intake (mmol/d)3 246 ± 91 210 ± 77 247 ± 103 228 ± 93
1 –
x ± SD.
2
Significant effect of age (P = 0.012) and sex (P < 0.001).
3
Significant effect of sex (P < 0.001).

Univariate analyses of correlations between urinary

calcium, urea sulfate, and sodium excretion
As shown in Table 5, we observed significant positive correla-
tions between urinary calcium and urea excretion, calcium and sul-
fate excretion, calcium and sodium excretion, and sulfate and urea
excretion for each sex and age group, except for that between cal-
cium excretion and sulfate excretion in men aged 20–49 y.
As shown in Table 6, we observed significant positive corre-
lations between calcium-creatinine and urea-creatinine ratios,
calcium-creatinine and sulfate-creatinine ratios, calcium-creati-
nine and sodium-creatinine ratios, and sulfate-creatinine and
urea-creatinine ratios for each sex and age group, except for that
between calcium-creatinine and sulfate-creatinine ratios in men
aged 20–49 y.
Univariate analyses on correlations between urinary vari-
ables and dietary intakes
As shown in Table 7, simple correlation coefficients between
both total protein intake and urea excretion and sodium intake
and its excretion were significantly positive for each sex and age
group. The association between calcium intake and its excretion
was significantly positive in each sex and age group, except in
men aged 20–49 y.
Urinary calcium was associated significantly and positively
with both total protein intake and with animal protein intake in
each sex and age group. The association of calcium with plant
protein intake was significant only in women aged 50–79 y. In
each sex and age group, no significantly positive correlation of
calcium excretion with cereal protein intake was observed.
Urinary sulfate was associated significantly and positively
with intakes of both total protein and animal protein in each sex
and age group. The association of sulfate excretion with plant
protein intake was positively significant in each sex and age
group, except in men aged 20–49 y. In each sex and age group,
no significantly positive correlation of sulfate excretion with
cereal protein intake was observed.
Multiple regression analyses of daily urinary calcium
excretion
Multiple regression models for calcium excretion with urea
excretion as a predictor are given in Table 8. In the 20–49-y olds,
sex, age, daily sodium excretion, and daily urea excretion corre-
lated significantly with daily calcium excretion and accounted
for <18% of the variability in calcium excretion. It was esti-
mated that the increase in calcium excretion was <0.5 mmol for
a 100-mmol increase in urinary urea excretion in this age group.
In the 50–79-y olds, both daily sodium excretion and daily urea
excretion correlated significantly with daily calcium excretion
and accounted for <26% of the variability in calcium excretion.
It was estimated that the increase in calcium excretion was <0.9

TABLE 3
Two-way ANOVA of daily urinary excretion of calcium, urea, sulfate, and sodium by age and sex1
Age group
20–49 y 50–79 y
Men Women Men Women
(n = 163) (n = 216) (n = 227) (n = 231)
Calcium (mmol/d)2 4.8 ± 2.2 3.8 ± 1.8 4.4 ± 2.2 3.8 ± 1.7
Urea (mmol/d)3 362 ± 94 301 ± 80 322 ± 99 260 ± 72
Sulfate (mmol/d)4 30.4 ± 12.4 25.5 ± 10.9 27.3 ± 15.3 22.8 ± 10.8
Sodium (mmol/d)5 203 ± 73 182 ± 64 194 ± 77 168 ± 58
1 –
x ± SD.
2
Significant effect of sex (P < 0.001).
3
Significant effect of age (P < 0.001) and sex (P < 0.001).
4
Significant effect of age (P = 0.001) and sex (P < 0.001).
5
Significant effect of age (P = 0.002) and sex (P < 0.001).
 ITOH ET AL 441

TABLE 4
Two-way ANOVA of urinary ratios of calcium, urea, sulfate, and sodium to creatinine by age and sex1
Age group
20–49 y 50–79 y
Men Women Men Women
Molar ratios (n = 163) (n = 216) (n = 227) (n = 231)
Calcium:creatinine2 0.35 ± 0.16 0.43 ± 0.21 0.43 ± 0.19 0.58 ± 0.24
Urea:creatinine3 26.4 ± 5.6 33.4 ± 7.5 30.8 ± 7.2 38.7 ± 8.0
Sulfate:creatinine3 2.2 ± 0.9 2.8 ± 1.2 2.6 ± 1.4 3.4 ± 1.4
Sodium:creatinine3 14.9 ± 5.1 20.4 ± 6.8 19.2 ± 7.1 25.8 ± 8.7
1 –
x ± SD.
2
Significant effect of age (P < 0.001), sex (P < 0.001), and an interaction of sex and age (P = 0.04).
3
Significant effect of age (P < 0.001) and sex (P < 0.001).

mmol for a 100-mmol increase in urinary urea excretion in this
age group.
Results of multiple regression analysis with daily calcium
excretion as a dependent variable and sulfate excretion as a pre-
dictor are shown in Table 9. In the 20–49-y olds, no significant
association of calcium excretion with sulfate excretion was
observed. In the 50–79-y olds, daily calcium intake, daily
sodium excretion, and daily sulfate excretion correlated signifi-
cantly with daily calcium excretion and accounted for <20% of
the variability in calcium excretion. It was estimated that the
increase in calcium excretion was <0.2 mmol for a 10-mmol
increase in urinary sulfate excretion.
DISCUSSION
As reported previously (6), calcium excretion in the subjects of
the present study correlated positively with protein intake esti-
mated from dietary records by using a food-composition table.
First, we tried to confirm the previous results using urinary urea
excretion data because of many sources of error inherent in the
methods used in the study for estimating daily dietary intake.
In this population, the average of the estimated protein intake
of the subjects was well above the RDA for Japanese (13), and
their average energy intake was similar to that. It is reasonable to
hypothesize that, on average, nitrogen balance of this apparently
healthy population was in equilibrium and their urea excretion
reflected their actual protein intake.
The results of the univariate analyses revealed that urinary
calcium excretion correlated positively with urinary urea excre-
tion, and simple correlation coefficients between calcium excre-
tion and urea excretion were higher than those between calcium
excretion and estimated protein intake in each sex and age group
(Tables 5–7). The results of multiple regression analyses showed
that urea excretion, which possibly reflected the actual protein
intake, was associated with calcium excretion independently of
the confounding factors included in the model: sex, body weight,
sodium excretion, and calcium intake.
The significant positive correlation between calcium excretion
and urea excretion implies that, in this free-living population resid-
ing in a restricted area where dietary patterns and lifestyles are
fairly homogeneous, increases in habitual protein intake from self-
selected diets enhance urinary excretion of calcium. From the mul-
tiple regression equations obtained, it was estimated that an
increase in urinary calcium excretion was 1–2 mg with a 1-g
increase in protein catabolized to energy, assuming that protein
contains 16% of nitrogen on average, and 75% of nitrogen ingested
as protein is excreted as urinary urea nitrogen (14).
Sodium intake has long been known to be an important pre-
dictor of calcium excretion (15). Dietary sodium intakes esti-
mated from dietary records (Table 2) are, however, unreliable
because of the variability in sodium content from one prepara-
tion to another of the same food and because of the difficulty in
assessing discretionary salt use (16). Therefore, daily urinary
sodium excretion was used as a more accurate and definitive
measure of actual sodium intake in this multiple regression
model (Table 3). Sodium excretion was shown to be associated
with calcium excretion independently of the other factors
included in the model. From the multiple regression equations
obtained, it was estimated that urinary calcium excretion
increased 0.5–1 mg with a 100-mg increase in sodium intake,
assuming that average urinary excretion was 86% of sodium
from food (17).
Phosphorus intake has also been recognized as another con-
founding factor affecting urinary calcium excretion. Phosphorus

TABLE 5
Simple correlation coefficients between daily urinary excretion of calcium, urea, sulfate, and sodium
Age group
20–49 y 50–79 y
Men Women Men Women
Daily excretion (n = 163) (n = 216) (n = 227) (n = 231)
Calcium and urea 0.2271 0.3011 0.4511 0.5311
Calcium and sulfate 0.092 0.1841 0.2701 0.3061
Calcium and sodium 0.2831 0.2031 0.3441 0.4301
Sulfate and urea 0.5921 0.5211 0.5121 0.5551
1
P < 0.01.
442 PROTEIN AND URINARY CALCIUM IN JAPAN

TABLE 6
Simple correlation coefficients between the urinary ratio of calcium, urea, sulfate, and sodium to creatinine
Age group
20–49 y 50–79 y
Men Women Men Women
(n = 163) (n = 216) (n = 227) (n = 231)
Calcium:creatinine, 0.1921 0.3182 0.2572 0.4052
urea:creatinine
Calcium:creatinine, 0.097 0.1902 0.1521 0.1451
sulfate:creatinine
Calcium:creatinine, 0.3092 0.2232 0.2612 0.3332
sodium:creatinine
Urea:creatinine, 0.5522 0.4312 0.4112 0.3782
sulfate:creatinine
1
P < 0.05.
2
P < 0.01.

is well known to decrease urinary calcium excretion, which
increases the calcium content of the digestive secretion, and
hence, increases endogenous calcium losses through the gut (18).
Protein is typically ingested as meat, cereals, beans, or dairy
products, all of which contain other nutrients, most notably phos-
phorus. Actually, in the present study, phorphorus intake corre-
lated positively with both protein intake (r = 0.889, P < 0.0001)
and urea excretion (r = 0.433, P < 0.0001). Because of these high
degrees of collinearity with protein intake, phosphorus intake was
not included in this regression model. The effect of protein intake
on calcium excretion observed in the present study appeared to be
the net effect of both protein and phosphorus.
Second, we examined whether the calciuric effect of protein
depends on the protein source. Animal protein intake signifi-
cantly and positively correlated with calcium excretion in each
sex and age group, whereas plant protein intake correlated with
calcium excretion significantly only in women aged 50–79 y, and
the significance of the association was lower than that with ani-
mal protein intake (Table 7). Our findings suggest that the con-
tribution of animal protein intake to the calciuric effect is larger
than that of plant protein. These findings are similar to those of
the epidemiologic study by Hu et al (5) of culturally heteroge-
neous populations living in five different areas in China where
the average protein intake ranged from 49 to 75 g/d, showing that
urinary excretion of calcium correlated positively with animal
protein intake but correlated negatively with plant protein intake.
We examined the correlation between urinary calcium and uri-
nary sulfate on the basis of the following three previously
reported observations: 1) the increase in urinary acid excretion is
accompanied by a loss of urinary calcium (19); 2) protein, espe-
cially that from animal sources, is an important source of
endogenously produced acid (20); and 3) as an index of the
endogenously produced acid, sulfate anions derived from sulfur-
containing amino acids are quantitatively important (21). Fur-
ther, in an experiment on human subjects, a high degree of cor-
relation was observed between an increase in urinary calcium
and an increase in sulfate excretion, which accompanied
increased protein intakes (22).
Univariate analyses of the data obtained in the present study
revealed significant positive correlations of urinary sulfate
excretion with both dietary protein intake and urinary urea
excretion, suggesting that, in this population, the main source of

TABLE 7
Simple correlation coefficients between daily urinary excretions and daily dietary intakes
Age group
20–49 y 50–79 y
Men Women Men Women
Excretion, intake (n = 145) (n = 201) (n = 203) (n = 205)
Urea, total protein 0.1751 0.3052 0.5542 0.3942
Sodium, sodium 0.3262 0.3272 0.3212 0.2422
Calcium, calcium -0.085 0.2672 0.1591 0.3022
Calcium, total protein 0.1691 0.1902 0.1661 0.2612
Calcium, animal protein 0.1661 0.2092 0.2212 0.2532
Calcium, plant protein 0.066 0.056 0.096 0.1471
Calcium, cereal protein 0.086 -0.1571 0.138 0.065
Sulfate, total protein 0.2061 0.2312 0.3152 0.2512
Sulfate, animal protein 0.2011 0.1821 0.2712 0.2332
Sulfate, plant protein 0.083 0.1841 0.2502 0.1611
Sulfate, cereal protein 0.022 0.000 0.092 0.018
1
P < 0.05.
2
P < 0.01.
 ITOH ET AL 443

TABLE 8 protein intake with radial bone mineral content and bone density.
Results of multiple regression analysis with daily calcium excretion as a They reported that the correlation remained significant even after
dependent variable and urea excretion as a predictor1 calcium intake, physical activity, and lean body mass were
P adjusted for.
2 Although further information is needed concerning bone min-
Subjects aged 20–49 y (n = 334)
Calcium (mmol/d) = 20.73 3 sex (M = 1, F = 2) < 0.001
eral content and dietary protein intake, it is probable that excess
+0.035 3 age (y) < 0.01 protein intake, especially that of protein rich in sulfur-containing
+0.0039 3 sodium excretion (mmol/d) < 0.05 amino acids, increases the requirements of calcium, at least in
+0.0047 3 urea excretion (mmol/d) < 0.001 the elderly.
+1.75 < 0.05
Subjects aged 50–79 y (n = 421)3 We thank the members of the team for the health and nutrition examina-
Calcium (mmol/d) = 0.0059 3 sodium excretion (mmol/d) < 0.001 tion survey conducted by the Public Health Department, Nagano Prefectural
+0.0085 3 urea excretion (mmol/d) < 0.001 Government, for helping with this study. We are also grateful to Atsuko Naka-
+0.64 < 0.05 mura for useful suggestions on the methods of sulfate determination.
1
Regression of urea excretion was controlled for sex, age, body weight,
sodium excretion, and calcium intake.
2 2
R = 0.180, P <0.001.
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