Am J Clin Nutr 2003;77:257.65. Printed in USA. c 2003 American Society for Clinical Nutrition 257
Milk intake during childhood and adolescence, adult bone density,
and osteoporotic fractures in US women1.3
Heidi J Kalkwarf, Jane C Khoury, and Bruce P Lanphear
Background: Calcium supplements increase bone mass in children,
but the effect does not persist once supplementation is discontinued.
Objective: The objective of this study was to determine whether
milk intake during childhood and adolescence, when controlled
for current calcium intake, is associated with adult bone mass (ie,
bone mineral content), bone mineral density, and the incidence of
Design: We used data from the third National Health and Nutrition
Examination Survey of 3251 non-Hispanic, white women
age . 20 y. Bone density was measured at the hip. History of fracture
of the hip, spine, or forearm was classified as a lifetime fracture
(occurring after age 13 y) or an osteoporotic fracture (occurring
after age 50 y). Subjects reported frequency of milk
consumption during childhood (aged 5.12 y) and during adolescence
(aged 13.17 y). Regression models controlled for weight,
height, age, menopause and use of estrogen, physical activity,
smoking, and current calcium intake.
Results: Among women aged 20.49 y, bone mineral content was
5.6% lower in those who consumed < 1 serving of milk/wk (low
intake) than in those who consumed > 1 serving/d (high intake)
during childhood (P < 0.01). Low milk intake during adolescence
was associated with a 3% reduction in hip bone mineral content
and bone mineral density (P < 0.02). Among women aged . 50 y,
there was a nonlinear association between milk intake during
childhood and adolescence and hip bone mineral content and bone
mineral density (P < 0.04). Low milk intake during childhood was
associated with a 2-fold greater risk of fracture (P < 0.05).
Conclusion: Women with low milk intake during childhood and
adolescence have less bone mass in adulthood and greater risk of
fracture. Am J Clin Nutr 2003;77:257.65.
KEY WORDS Bone density, milk intake during childhood
and adolescence, calcium intake, osteoporosis, peak bone mass,
Recommendations for dietary calcium intake have been
increased for children and adolescents to maximize peak bone
mass and ultimately reduce the risk of osteoporotic fracture (1).
The long-term benefit of increased calcium intake during growth
for reducing disease risk many decades later is uncertain. Calcium
supplementation of children and adolescents increases bone mass
and density (2.9). This benefit, however, appears to be transient,
and bone mass in children supplemented with calcium is similar
1 From the Division of General and Community Pediatrics, Childrenfs Hospital
Medical Center, Cincinnati (HJK and BPL), and the Division of Epidemiology
and Biostatistics, University of Cincinnati (JCK).
2 Supported by the Cincinnati Childrenfs Hospital Research Foundation.
3 Address reprint requests to HJ Kalkwarf, Division of General and Community
Pediatrics, Childrenfs Hospital Medical Center, MLC-7035, 3333 Burnet
Avenue, Cincinnati, OH 45229-3039. E-mail: email@example.com.
Received March 19, 2002.
Accepted for publication July 23, 2002.
to that in children given placebo after supplementation is discontinued
(10.12). Because this effect does not persist, the long-term
benefit of promoting higher calcium intake in children and adolescents,
specifically, is questionable. In contrast, studies supplementing
the diet with milk or milk-derived calcium showed persistent
effects on bone mass 184.108.40.206 y after the supplementation
was discontinued (13, 14).
Although some (15.20), but not all (21.25), epidemiologic
studies have found a relation between lifetime calcium intake and
adult bone mineral density (BMD), few studies have investigated
the independent effects of calcium or milk intake during childhood
and adolescence. Dietary behaviors such as milk and calcium
intakes developed in childhood have been shown to persist
into adulthood (17, 18, 26, 27). Thus, adjustment for current calcium
intake is necessary for the examination of the independent
effects of intake during childhood or adolescence. Results of studies
that examined the effects of milk or calcium intake during
childhood or adolescence and adjusted for current calcium intake
were inconsistent, possibly because of differences in study sample
characteristics. One study found that milk intake in childhood
(. 12 y) was independently related to spine and hip BMD in
women aged 45.49 y (28). Another study found no association
between childhood milk intake and BMD of the total body, hip,
spine, or mid-radius in young women (aged 18.31 y) (27). This
latter study, however, did find that milk intake during adolescence
(13.19 y) was independently associated with total body and radial
shaft BMD but not with spine and hip BMD in young women (27).
In contrast, another study found no significant association between
calcium intake during adolescence and spine, hip, mid-radius, or
distal radius BMD among women aged 30.39 y after adjustment
for current calcium intake (29).
Few studies have examined the relation between childhood diet
and the risk of osteoporotic fracture. Two studies found no association
between milk intake during adolescence and the incidence
of fracture of the forearm and hip in adulthood (30, 31), whereas
See corresponding editorial on page 10.
258 KALKWARF ET AL
one study found that proximal humerus fractures, but not distal
forearm fractures, were more common among elderly women who
had low milk intake during adolescence (32).
Identification of the independent effects of milk and or calcium
intake during specific periods of life is important for efficient targeting
of interventions to maximize their long-term benefit. The
objective of this study was to determine whether milk intakes during
childhood and adolescence are independently associated with
bone mass, bone density, and bone size (area) of the hip during
adulthood after control for current milk and calcium intake in a
nationally representative sample of white women in the United
States. We hypothesized that lower milk intake would be associated
with lower bone mass and density. We also examined the relation
between milk intake during childhood and adolescence and
the risk of lifetime fracture.
SUBJECTS AND METHODS
We used data from the third National Health and Nutrition
Examination Survey (NHANES III) for this study. NHANES III,
conducted by the National Center for Health Statistics, is a crosssectional
survey of noninstitutionalized persons in the United
States that was conducted between 1988 and 1994 (33). The survey
used a stratified, multistage probability design to select a
nationally representative sample. Children aged 2 mo.5 y, adults
aged > 60 y, and African Americans and Mexican Americans
were oversampled. The survey included a household interview
and a physical examination conducted in a mobile examination
Bone mineral content (BMC), BMD, and bone area of the left
hip were measured by dual-energy X-ray absorptiometry (DXA)
at the MEC. Bone area (cm2) was the projected or two-dimensional
bone area determined from the DXA scan (34). Measurements
were made on the right hip in subjects whose left hip was
previously fractured (1%). DXA scans were acquired with the use
of a densitometer (QDR 1000; Hologic, Waltham, MA) in pencil-
beam mode. Quality-control measures were described elsewhere
(35). Measurements were obtained for the total hip and 4
subregions (ie, femoral neck, trochanter, Wardfs triangle, and
intertrochanter). We restricted our analyses to the total hip because
the hip subregions were highly correlated with the total hip measurements
(r = 0.76.0.98). Bone measurements were obtained on
14 646 persons, or 88% of persons reporting to the MEC who
were . 20 y old and eligible for a BMD measurement. Measurements
were not obtained on persons aged < 20 y, on women who
were pregnant or who may be pregnant, or on persons who had a
history of fractures of both hips. Of the DXA scans performed,
2% were considered unacceptable because of motion artifacts,
incomplete scans, and grossly abnormal scans (35, 36).
Because of the known sex, racial, and ethnic differences in
BMD and risk of osteoporotic fracture (34), we restricted our sample
for these analyses to non-Hispanic, white women.the group
at greatest risk of osteoporosis.with acceptable bone measurements
(n = 3251).
Subjects reported whether they had ever experienced a fracture
of the hip, wrist, or spine and specified their age when the fracture
occurred. We created 2 fracture variables. Lifetime fractures
included fractures that occurred at age 13 y and later. The cutoff
of age 13 y was chosen so that milk-intake information pertained
to the period either before or concurrent with the fracture. Osteoporotic
fractures were those that occurred at age 50 y and later.
This variable was created only for women . 50 y old. Information
on the severity of trauma associated with the fracture was obtained
only for fractures that occurred at age 50 y and later. Of the
women classified with an osteoporotic fracture, only 6% had fractures
due solely to severe trauma. Exclusion of fractures associated
with severe trauma did not affect the results.
Questions regarding milk consumption during specific periods
of life were asked in the household interview. The questionnaire
targeted 5 distinct age periods: childhood (5.12 y), adolescence
(13.17 y), young adulthood (18.35 y), middle adulthood (36.65 y),
and later adulthood (> 65 y). Subjects were asked to recall how
often they consumed any type of milk, including milk added to
cereal but not including small amounts added to coffee or tea, during
each age period. Possible responses included: more than once
a day, once a day, less than once a day but more than once a week,
once a week, less than once a week, never, and donft know. To
facilitate analyses, responses were collapsed into 4 categories: > 1/d,
1/d, 1.6/wk, and < 1/wk. gDonft knowh responses were classified
as missing. Information on current milk intake was derived from
the food-frequency questionnaire (FFQ) that also was administered
as part of the household interview. Information from the FFQ
included the number of servings in the last month of both regular
and chocolate milk. Information on portion size was not collected.
We categorized current milk intake information into the same categories
as the historical milk intake information.
Quantitative information on calcium intake was obtained from
the 24-h recall conducted during the MEC visit. The 24-h recall
was conducted with the use of an automated, interactive dietary
data-collection system that was developed by the University of
Minnesota Nutrition Coordinating Center (33). Food composition
data were based on the US Department of Agriculture data files
specific for that time period. Nutrient intake from the 24-recall
does not include intakes from nutritional supplements and
antacids. Specific questions regarding the use of antacids and vitamins
were asked as part of the household questionnaire. Subjects
reported the brand name of vitamin, mineral, and antacids that they
regularly consumed and the frequency of use in the last month. We
calculated the amount of calcium in the vitamin and mineral supplement
preparations by using data from the NHANES III CD
ROM 11, no. 2A (National Center for Health Statistics, 1998)
and the amount of calcium in the antacids by using information
from the Physiciansf Desk Reference for Nonprescription Drugs
(37) and from product labels. Total calcium intake was calculated
from the sum of the 24-h food recalls plus all the aforementioned
To control for potential confounding and to reduce overall variability
in the data, we evaluated other variables known to affect
BMC or BMD in our analyses. These variables included age,
weight, height, menopausal status, tobacco use, alcohol consumption,
physical activity, and medications used, including estrogen
replacement therapy. Age, weight, and height were directly
available from the household and MEC interviews. Other variables
were constructed by combining information from several sources
as described below.
There was no direct question regarding menopausal status on
the questionnaire. We categorized women as premenopausal or
postmenopausal according to an iterative procedure involving 8
CHILDHOOD MILK INTAKE AND ADULT BONE DENSITY 259
criteria using information on age, occurrence of a menstrual
period or pregnancy in the previous year, hormonal contraceptive
or other estrogen use, and serum follicle-stimulating hormone
concentration. Serum follicle-stimulating hormone was measured
only in women aged 35.60 y (33). The criteria were assessed in
sequential order so that the successive rules were applied only
to those women not already categorized. The decision rules were
as follows: 1) age > 61 y = postmenopausal; 2) bilateral
oophorectomy = postmenopausal; 3) period/pregnancy in the
previous year = premenopausal; 4) follicle-stimulating hormone
> 40 IU/L = postmenopausal; 5) age < 35 y = premenopausal; 6)
birth control pills in the previous year = premenopausal; 7) age > 50 y =
postmenopausal; and 8) age < 50 y = premenopausal. To account
for the fact that some postmenopausal women were taking estrogen,
we further categorized women as estrogen-deficient if they
were postmenopausal and were not taking some form of estrogen.
Information on the use of cigarettes, pipe, cigar, chewing
tobacco, snuff, and nicotine gum was obtained in the household
interview. These questions were redefined into current or not current
smoker, ever or never a smoker, and the number of years a
smoker. Most persons (34/44 or 77.3%) who smoked a pipe or
cigar or used chewing tobacco also smoked cigarettes.
Alcohol intake was assessed as part of the FFQ. Subjects
reported the frequency of beer, liquor, and wine consumption in
the previous month. We coded alcohol consumption as the total
number of servings of beer, wine, and hard liquor into categories:
0, < 5, 5.29, and . 30 servings in the previous month.
Information on leisure-time physical activity was obtained from
self-reports. Subjects reported the frequency of participation in
specific activities: walking at least 1 mile, jogging or running,
bicycling, aerobics, dancing, calisthenics, weight lifting, and other
activities. Information coded under gother activitiesh also was
included if the activity fell into the following categories: bicycling,
conditioning, dancing, running, team sports, walking, and
winter activities. The frequency of each event was combined to
create a total activity frequency, which was then categorized for
analysis as 0, 1.8, 9.31, and . 32 episodes/mo.
We examined the reported use of medications known to affect
BMD. Categories of medications that were considered in this
study were anticoagulants and thrombolytics, metabolic drugs and
nutrients, medications that affect calcium metabolism, adrenal
corticosteroids, and thyroid and antithyroid medications (study
drug codes 409, 900, 916, 1032, and 1027). Only thyroid medications
had an incidence high enough (ie, > 5%) for meaningful
inclusion in further analyses.
Multiple regression was used to examine the relations between
milk intake during childhood and adolescence and adult BMC,
BMD, and bone area of the hip. All analyses were conducted with
SUDAAN software (Research Triangle Institute, Research Triangle
Park, NC) to account for the complex sample design and allow
calculation of appropriate variance estimates. The MEC sample
weights were used for statistical analyses. These are the sample
weights recommended for use in analysis of data collected at the
MEC (33). Models were developed separately for BMC, BMD,
and bone area. The sample was divided by age into 2 categories,
20.49 y and . 50 y, because earlier reports of these data showed
that age-related trends in BMC and BMD were not linear. A
greater rate of decline in BMC and BMD was associated with
increasing age after 50 y, which coincides with the average age of
menopause (34). The relation between milk intake during childhood
and adolescence and BMC, BMD, and bone area was first
tested with an overall F test. If the overall test was significant
(P < 0.05), the 3 lowest categories were compared with the highest
category by the use of Dunnettfs test to account for multiple
A two-step modeling strategy was used to adjust for potential
confounding and to improve the precision in estimating the effects
of milk intake on BMC, BMD, and bone area. First, we examined
the bivariate relations between potential covariates and bone
measurements. Potential covariates that were considered included
age, weight, height, menopausal and estrogen status, physical
activity, alcohol consumption, tobacco use, and current milk or
current calcium intake. Age, weight, height, and current calcium
intake were fitted as continuous variables. Menopausal and estrogen
status, physical activity, alcohol consumption, and tobacco
use were fitted as categorical variables. Variables that were associated
with BMC or BMD with P . 0.25 in bivariate analyses were
included in the full model for that bone measure. In addition to
childhood or adolescent milk intake variables, all final models
included variables for age, weight, estrogen deficiency or
menopause, and current calcium intake (either current milk intake
or total mg of calcium) because of their known associations with
BMC and BMD. A backward-elimination approach was used to
exclude other potential covariates (smoking, alcohol intake, medication
use, and physical activity) from the final models. Covariates
were retained in the final model if the P value was . 0.10 or
if exclusion of that variable affected the coefficients for childhood
or adolescent milk intake by > 10%. Height was not included in
the models for bone area to prevent an overcorrection of the potential
mediating effects of linear growth on hip bone area.
Logistic regression was used to assess the relation between
milk intake during childhood and adolescence and fracture occurrence,
lifetime fractures (all women), and osteoporotic fractures
(for women . 50 y old). Models were computed with SUDAAN
software using the MEC sample weights. Potential confounders
considered in the models were age, height, weight, smoking, and
estrogen deficiency. Criteria for inclusion in the logistic regression
models were as described above for the multiple regression.
The proportion of fracture cases that could be attributed to low
milk intake during childhood, also known as the population attributable
risk, was estimated by use of the weighted prevalence estimate
of low milk intake during childhood and the odds ratio from
the logistic regression model.
There were 3251 non-Hispanic, white women . 20 y old with an
acceptable DXA scan of the hip. Of these, 1371 (42.2%) were aged
20.49 y (x . } SD: 35 } 8) and 1880 (57.8%) were aged .50 y (69 } 11;
range: 50.90). Women aged 20.49 y had mean (} SE) weight of
67.6 } 0.6 kg and height of 163.9 } 0.2 cm, and women aged . 50 y
had mean (}SE) weight of 69.9 } 0.5 kg and height of 160.1 } 0.2 cm.
Most women reported consuming . 1 glasses of milk/d during
childhood (84.2%) and adolescence (70.4%) (Table 1). Reported
current milk intake was lower: only 41.8% of women aged 20.49 y
and 52.2% of women aged . 50 y reported drinking . 1 glasses of
milk/d. Overall, the degree of concordance between milk intake
during childhood and adolescence and current milk intake was
low. For women aged 20.49 y, the kappa statistics for the comparison
of current milk intake with childhood and adolescence
260 KALKWARF ET AL
Distribution of milk and calcium intake among non-Hispanic, white
20.49 y .50 y
Childhood milk intake (servings)
<1/wk 5.6 9.8
1.6 wk 8.8 7.8
1/d 27.2 26.5
>1/d 58.4 55.8
Adolescent milk intake (servings)
<1/wk 13.2 16.0
1.6 wk 17.1 12.4
1/d 29.8 29.5
>1/d 39.8 42.1
Current milk intake (servings)
<1/wk 27.2 25.1
1.6 wk 31.0 22.7
1/d 19.8 32.1
>1/d 22.0 20.1
Current calcium intake (mg/d)2
Dietary intake3 630 (617, 658) 565 (544, 587)
Mineral supplements and antacids4 143 (124, 166) 223 (195, 257)
Total calcium intake 699 (669, 730) 672 (644, 701)
1 The unweighted sample size for women aged 20.49 y was n = 1371
and that for women aged .50 y was n = 1880. The results presented reflect
the weighted sample.
2 Geometric mean (95% CI).
3 According to the 24-h recall.
4 Among those who reported consumption of supplemental calcium in the
previous month (31% of women aged 20.49 y and 38% of women aged .50 y).
Distribution of covariates among study subjects1
20.49 y .50 y
Postmenopausal (%)2 7.0 90.1
Estrogen deficient (%)3 3.3 73.8
Ever a smoker (%) 51.8 45.0
Number of years a smoker (%)4 12 (1.36) 25 (1.71)
Current smoker (%) 33.5 15.8
Leisure-time physical activity, episodes/mo (%)
0 19.9 36.7
1.8 28.6 19.3
9.31 32.3 30.6
. 32 19.2 13.4
Alcohol, servings in the previous mo (%)
0 39.0 63.9
<5 25.3 15.5
5.29 30.4 12.1
. 30 5.2 8.5
1 The unweighted sample size for women aged 20.49 y was n = 1371
and that for women aged .50 y was n = 1880. The results presented reflect
the weighted sample.
2 Percentage of total group.
3 Postmenopausal and not using some form of estrogen.
4 Median (range) among those who ever were smokers.
milk intakes were 0.14 and 0.25, respectively. For women
aged . 50 y, the kappa statistics were 0.13 and 0.22, respectively.
The geometric mean dietary calcium intakes determined from the
24-h recall were 630 mg/d (95% CI: 617, 658 mg/d) and 565 mg/d
(95% CI: 544, 587 mg/d) for women aged 20.49 and . 50 y,
respectively. Calcium from mineral supplements and antacids
increased the mean calcium intake by 11% for women aged 20.49 y
and by 19% for women aged . 50 y.
The numbers of women successively categorized as postmenopausal
by each criterion are shown in Table 2. Descriptive
information on menopausal and estrogen status and the other potential
covariates by age group is given in Table 3. Estrogen usage was
reported by 16.3% of postmenopausal women . 50 y old.
Milk intake and bone density among women aged 20.49 y
Among women aged 20.49 y, final regression models predicting
total hip BMC and BMD included current calcium intake,
age, weight, height (BMC model only), estrogen deficiency, and
physical activity. Models for bone area included weight, age,
menopausal status, and current dietary calcium intake. Current
dietary calcium intake was positively associated with BMC,
BMD, and bone area in all models (P values, 0.007.0.12). Total
calcium intake (dietary calcium + supplements) was less consistently
associated with bone measures; therefore, dietary calcium
intake was used for all analyses. Results for current milk intake
determined from the FFQ were similar to those for current dietary
Milk intake during childhood, adjusted for confounders, was
associated (P = 0.003) with total hip BMC. Hip BMC was 5.6%
lower among women who consumed < 1 serving of milk/wk than
among women who consumed > 1 serving of milk/d during childhood
(P < 0.01). In contrast, the BMC of women who consumed
intermediate frequencies of milk was not lower than that of
women with the highest consumption frequency (Figure 1). There
was no association between childhood milk intake and hip BMD
(overall P = 0.31). Childhood milk intake was associated with
bone area (P = 0.003). Bone area was 4.6% less among women
with the lowest milk intake than among women with the highest
intake (P < 0.01) during childhood. Milk intake during adolescence
was associated (P . 0.02) with hip BMC and BMD, and the
greater values were associated with greater milk intake. The mean
BMC and BMD of women who consumed < 1 serving of milk/wk
was 3% lower than those of women who consumed > 1 serving
of milk/d during adolescence (P < 0.02). Milk intake during adolescence
was not associated with bone area (P = 0.13).
Categorization of menopause1
Criteria Postmenopausal No. of subjects
Age > 61 y Yes 1385 (42.6%)
Bilateral oophorectomy Yes 147 (4.5%)
Period or pregnancy in previous year No 1275 (39.2%)
Follicle-stimulating hormone > 40 IU/L Yes 274 (8.4%)
for women aged 35.60 y
Age < 35 y No 18 (0.5%)
Use of birth control pills in previous year No 101 (3.1%)
Age . 50 y Yes 30 (0.9%)
Age 20.49 y No 21 (0.6%)
1Women (total n = 3251) were categorized as premenopausal or postmenopausal
according to 8 criteria, in sequential order as listed above, so that
the successive rules were applied only to those women not already categorized.
CHILDHOOD MILK INTAKE AND ADULT BONE DENSITY 261
FIGURE 1. Mean total hip bone mineral content (BMC), bone mineral density (BMD), and bone area according to milk intake during childhood and
adolescence among non-Hispanic, white women who participated in the third National Health and Nutrition Examination Survey. For women aged 20.49
y (n = 1371), BMC and BMD means were adjusted for current calcium intake, age, weight, height (BMC only), estrogen deficiency, and physical activity.
Regression models for women aged . 50 y (n = 1880) also included alcohol intake and any history as a smoker. Regression models for bone area
included age, weight, current calcium intake, and menopause. P values in the graph are for the overall F test comparing groups. Follow-up analyses comparing
the 3 lowest milk-intake categories with the highest milk-intake category were performed with the use of Dunnettfs test to account for multiple
comparisons (38) and a two-sided test of significance. *P . 0.05, +P . 0.10.
262 KALKWARF ET AL
Milk intake during childhood and adolescence and fracture occurrence in
women aged .50 y
Odds ratio (95% CI)
Child milk intake P = 0.0083 P = 0.04
<1 serving/wk 2.02 (1.13, 3.59) 2.25 (1.26, 4.00)
1.6 servings/wk 1.72 (0.84, 3.54) 1.39 (0.67, 2.89)
1 serving/d 1.39 (0.97, 1.99) 1.00 (0.67, 1.49)
>1 serving/d 1.00 1.00
Adolescent milk intake P = 0.02 P = 0.29
<1 serving/wk 1.49 (0.90, 2.46) 1.29 (0.75, 2.19)
1.6 servings/wk 2.07 (1.27, 3.37) 1.59 (0.84, 3.04)
1 serving/d 1.13 (0.78, 1.64) 0.87 (0.57, 1.29)
>1 serving/d 1.00 1.00
Childhood and adolescent milk P = 0.008 P = 0.36
Childhood and adolescence .1/wk 1.60 (1.17, 2.18) 1.19 (0.83, 1.70)
Childhood > 1/wk and 0.96 (0.58, 1.57) 0.85 (0.49, 1.48)
Childhood and adolescence >1/wk 1.00 1.00
1 Fractures that occurred at .13 y of age. Odds ratios are adjusted for
age and weight.
2 Fractures that occurred at .50 y of age. Odds ratios are adjusted for
age and estrogen deficiency.
3P values are for the overall F test comparing groups.
To investigate the association between different patterns of milk
intake during childhood and adolescence and adult BMD, we categorized
women according to whether they had consistently low
(. 1 serving/d) or high (> 1 serving/d) milk intake during both
childhood and adolescence or whether their milk intakes during
the 2 periods of growth differed. Women were categorized into 3
groups: 1) low milk intake during both childhood and adolescence
(42.0% of sample); 2) high milk intake during childhood but low
intake during adolescence (18.9%); and 3) high milk intake during
both childhood and adolescence (38.4%). The proportion of
women with low intake during childhood and high intake during
adolescence (0.7%) was too small to permit meaningful analysis
of this group. Hip BMD, adjusted for potential confounders, was
1.7% lower among women in group 1 (low intake in childhood
and adolescence) and 2.1% lower among women in group 2 (high
intake in childhood, low intake in adolescence) than among
women in group 3 (high intake in childhood and adolescence)
(P . 0.05). There was no association between milk-intake group
and hip BMC (P = 0.41) or bone area (P = 0.11).
Milk intake and bone density among women aged . 50 y
Among women aged . 50 y, final regression models predicting
total hip BMC and BMD included current calcium intake, age,
weight, height (BMC model only), estrogen deficiency, physical
activity, ever a smoker, and alcohol intake. Models for bone area
included age, weight, menopause, and dietary calcium intake. Current
dietary calcium intake was positively associated with BMC,
BMD, and bone area in all models (P values, 0.004.0.11).
Total hip BMC and BMD differed significantly (P < 0.02)
according to milk intake during childhood and adolescence, but
the relations were not linear (Figure 1). BMC was 2.0% lower and
BMD was 2.1% lower (P = 0.10) among women with the lowest
frequency of milk intake (< 1 serving/wk) than among those with
the highest frequency of milk intake (> 1 serving/d) during childhood.
This same pattern of association was apparent for milk
intake during adolescence: women reporting the lowest intakes
had hip BMC that was 2.4% lower (P < 0.10) and BMD that was
2.2% lower than those measures in women reporting the highest
frequency of milk intake. Milk intake during childhood (P = 0.44)
and adolescence (P = 0.21) was not associated with total hip bone
area in women . 50 y old.
There was no significant association between the combined classification
of high or low milk intake during both childhood and adolescence
(the 3 groups outlined above) and hip BMC (P = 0.58),
BMD (P = 0.98), or bone area (P = 0.09) among women aged . 50 y.
Milk intake and fracture
Among women aged 20.49 y, 4.7% reported a fracture of the
hip, spine, or forearm at age 13 or later (lifetime fracture). Among
women aged . 50 y, 12.9% reported a fracture at age 13 or later,
and 8.4% reported a fracture after age 50 (gosteoporotich fracture).
There was no association between milk intake in childhood and
adolescence and the incidence of lifetime fracture among women
aged 20.49 y (P . 0.39). Among women aged . 50 y, milk intake
during childhood and adolescence was associated with a significantly
greater incidence of lifetime fracture (P < 0.05), but only
low childhood milk intake was significantly (P = 0.04) associated
with an increased risk of osteoporotic fractures. Odds ratios,
adjusted for age, weight, and estrogen deficiency (osteoporotic
fractures only), are presented in Table 4. Among women aged .50 y,
low milk intake during childhood was associated with 11% of
Current dietary recommendations for calcium intake are
designed to maximize bone mass accretion during growth and
peak bone mass to reduce risk of osteoporotic fracture many
decades later. There is, however, growing evidence that some of
the benefit of increased calcium intake is transient and that the
gain in BMD is lost once supplemental calcium intake is discontinued
(10.12). This calls into question the long-term benefit of
promoting higher calcium intake during childhood to reduce
osteoporosis many decades later. In a nationally representative
sample of women, we found that low milk intake during childhood
and adolescence was associated with low BMC or BMD of
the hip in adulthood. Hip BMD was 2.3% lower in women who
reported consuming < 1 serving of milk/wk than in women who
consumed > 1 serving/d during childhood and adolescence. This
presumably represents a persistent negative effect of low milk
intake during growth on bone mass and density of the hip that is
not completely ameliorated by current calcium or milk intake.
Furthermore, among women . 50 y of age, those with low milk
intake during childhood had a 2-fold greater risk of fracture than
did women with high milk intake during childhood, and this
greater risk could account for 11% of osteoporotic fractures in
this population. It is important that these relations were found in
a sample of non-Hispanic, white women.the subset of the population
with the greatest risk of osteoporotic fracture. These findings
provide support for the potential benefit of nutritional interventions
during childhood and adolescence to reduce the risk of
osteoporosis in later years.
Although several studies have examined the relation between
childhood milk intake and adult bone mass or fracture risk, few
CHILDHOOD MILK INTAKE AND ADULT BONE DENSITY 263
have accounted for current dietary calcium or milk intake. Dietary
intake of calcium and dairy products shows a moderate degree of
tracking from childhood to adulthood (26, 39), so that the assessment
of the independent effects of childhood and adolescence
intake necessitates control for current dietary intake. New et al
(28) found that childhood milk intake was positively related to
spine and hip BMD in 1230 women (aged 45.49 y) after control
for current intake. Nieves et al (29) found that calcium intake during
adolescence was associated with hip BMD but not with spine,
mid-radius, or distal radius BMD among 139 young women after
adjustment for current calcium intake. Teegarden (1999) found
that milk intake during adolescence, but not during childhood, was
independently associated with BMC and BMD of the total body
and radial shaft but not with those of the spine and hip in 224
young women after control for current calcium intake (27). Our
findings extend prior observations in that we found an association
between low milk intake during both childhood and adolescence
and the hip BMD or BMC or both in a large representative sample
of women. Furthermore, we found that low milk intake during
childhood was associated with an increased incidence of selfreported
fractures among women aged . 50 y.
Bone mass and density in adulthood are the net result of factors
that affect both bone mineralization and bone size. Sufficient
calcium intake during growth is essential to support rapid mineralization
of the skeleton. Peak bone mineral accretion, which
occurs during puberty, averages 322 g/y in girls (40). This is
approximately twice the bone mineral accretion rate in the years
before puberty (41). Although positive effects of calcium or milk
supplementation on bone mass and density have been found in
prepubertal (3, 6, 7) and pubertal (4, 5, 9) children and adolescents,
there has been controversy as to whether interventions during
childhood or adolescence are more efficacious. Lloyd et al
(42) found that calcium supplementation was most beneficial in
adolescents in a more advanced Tanner stage. In contrast, Johnson
et al (2) found that supplementation was beneficial for prepubertal
children but not for pubertal children. Our results provide
evidence of beneficial effects on adult BMD of milk intake during
both periods of growth.
Milk provides a variety of nutrients (eg, protein, phosphorous,
vitamin D, zinc, and magnesium) in addition to calcium that may
have positive effects on bone growth and mineralization. In a randomized
milk-supplementation trial, girls consuming additional
milk had higher serum insulin-like growth factor I concentrations,
which may have affected bone growth (4). Bonjour et al (3) found
that children who received a milk-derived calcium supplement
containing phosphorous had larger bone area and greater vertebral
height as well as greater BMC than were seen in children who did
not receive the supplement, which implies that the supplement
affected bone growth (3). It is important that this effect on bone
area and BMC was still apparent 3.5 y after supplementation was
stopped (14). A review of calcium-supplementation trials in children
found that positive effects of calcium supplementation on
BMD were usually a result of increased BMC, not increased bone
area (43), although increases in bone area with nonmilk calcium
supplementation have been reported (42). We found an association
between bone area and milk intake during childhood, but not
during adolescence, among women aged < 50 y. This likely
reflects that fact that relatively more growth occurs during childhood
than during adolescence in girls.
Although women with the lowest level of milk intake had the
lowest BMC and BMD, a dose-response relation for adolescent
milk intake was apparent only in women aged < 50 y. The reason
for our not finding a dose-response relation in older women is not
clear. One possibility is the greater degree of error in reporting
childhood and adolescent milk intake among older women that
results from the longer recall interval (44).
Despite the large and representative sample of subjects who
participated in this study, the conclusions of this study are limited
by potential error in the measurement of historical milk
intake. Milk intake during childhood and adolescence was ascertained
by recall, and other calcium sources were not measured. In
general, past diet is recalled moderately well to poorly (39, 44,
45), but the intake of milk has been found to be recalled better
than that of most foods because of its high frequency and stability
in the diet (39, 44). The actual milk intake during childhood
and adolescence may be different from the recalled intake, but
recalled milk intake may be suitable for ranking persons in this
study.Welton et al (45) found that the relative ranking of subjects
according to recalled milk intake was moderate; there was exact
quartile agreement of 36% to 51% of subjects between the milk
intake reported for age 13 and recalled 16 y later. Dwyer et al (39)
found a correlation of 0.25 between the intake of dairy foods
reported for ages 5.7 y and recalled at age 50. Random error in
recalled milk intake will lead to an underestimation of the true
magnitude of the relation between milk intake and bone density.
Women were aware of their fracture history (but not BMD) at the
time of reporting prior and current dietary intake, which could
lead to a differential recall bias.
Fracture ascertainment was by self-reporting of fractures of the
wrist, spine, and hip, which may be subject to error. Spine fractures
may be underestimated, because many go undiagnosed. Hip
fracture is associated with increased risk of mortality and institutionalization,
and thus hip fractures may be underrepresented in
these data. Nevitt et al (46) found that elderly women tended to
overreport wrist and hip fractures by 8% to 11%, and that overreporting
was greater among women who believed they had osteoporosis
and who had lower education.
Because of the observational nature of this study, we statistically
adjusted for many factors known to be associated with bone
density to prevent possible confounding of our results. It is possible
that there were other factors that may have affected bone density
that we were not able to account for, such as occupationrelated
physical activity. In addition, information on current
calcium intake was limited to that from a single 24-h recall, which
imperfectly characterizes a personfs long-term usual intake. The
fact that similar results were obtained when milk-intake frequency
from the semiquantitative FFQ was used in the analyses provides
some assurance that we adequately adjusted for the effects of current
More than half of subjects reported milk intakes during childhood
and adolescence of > 1 serving/d.the highest category
included in the survey. Truncation of potential responses limited
our ability to investigate the relation between hip BMD and milk
intake > 1 serving/d. Current recommendations are for an intake of
2.3 servings of dairy products daily (US Department of Agriculture
food guide pyramid) or the consumption of 800.1300 mg of
calcium/d, depending on the age group (1).
In summary, we found that milk intake in childhood and adolescence
is associated with increased bone mass and density in
adulthood, and this effect is independent of current milk or calcium
intake. These findings support efforts to promote a diet containing
one or more servings of milk/d for girls during childhood
264 KALKWARF ET AL
and adolescence to increase bone mass and density in adulthood
and reduce the risk of osteoporotic fracture. Whether increased
calcium intake from other food sources also provides this benefit
is not known.
HJK was responsible for conception and design of the study, data interpretation,
and manuscript preparation. JK was responsible for data analysis and
interpretation and assisted in conception of the study and manuscript preparation.
BL assisted in the conception and design of the study, data interpretation,
and manuscript preparation. All of the authors are employed by the sponsor of
this research, the Cincinnati Childrenfs Hospital Research Foundation.
1. Standing Committee on the Scientific Evaluation of Dietary Reference
Intakes. Dietary reference intakes for calcium, phosphorus, magnesium,
vitamin D, and fluoride. Washington, DC: National Academy
2. Johnston CC Jr, Miller JZ, Slemenda CW, et al. Calcium supplementation
and increases in bone mineral density in children. N Engl J
3. Bonjour JP, Carrie AL, Ferrari S, et al. Calcium-enriched foods and
bone mass growth in prepubertal girls: a randomized, double-blind,
placebo-controlled trial. J Clin Invest 1997;99:1287.94.
4. Cadogan J, Eastell R, Jones N, Barker ME. Milk intake and bone mineral
acquisition in adolescent girls: randomised, controlled intervention
trial. BMJ 1997;315:1255.60.
5. Chan GM, Hoffman K, McMurry M. Effects of dairy products on bone
and body composition in pubertal girls. J Pediatr 1995;126:551.6.
6. Dibba B, Prentice A, Ceesay M, Stirling DM, Cole TJ, Poskitt EM.
Effect of calcium supplementation on bone mineral accretion in Gambian
children accustomed to a low-calcium diet. Am J Clin Nutr 2000;
7. Lee WTK, Leung SSF,Wang S-H, et al. Double-blind, controlled calcium
supplementation and bone mineral accretion in children accustomed
to a low-calcium diet. Am J Clin Nutr 1994;60:744.50.
8. Lloyd T, Andon MB, Rollings N, et al. Calcium supplementation and
bone mineral density in adolescent girls. JAMA 1993;270:841.4.
9. Nowson CA, Green RM, Hopper JL, et al. A co-twin study of the
effect of calcium supplementation on bone density during adolescence.
Osteoporos Int 1997;7:219.25.
10. Lee WT, Leung SS, Leung DM, et al. Bone mineral acquisition in low
calcium intake children following the withdrawal of calcium supplement.
Acta Paediatr 1997;86:570.6.
11. Lee WTK, Leung SSF, Leung DMY, Cheng JCY. A follow-up study
on the effects of calcium-supplement withdrawal and puberty on bone
acquisition of children. Am J Clin Nutr 1996;64:71.7.
12. Slemenda CW, Peacock M, Hui S, Zhou L, Johnston CC. Reduced
rates of skeletal remodeling are associated with increased bone mineral
density during the development of peak skeletal mass. J Bone
Miner Res 1997;12:676.82.
13. Barker M, Lambert H, Cadogan J, Jones N,Wallace F, Eastell R. Milk
supplementation and bone growth in adolescent girls: is the effect
ephemeral? Bone 1998;23:S606 (abstr).
14. Bonjour JP, Chevalley T, Ammann P, Slosman D, Rozzoli R. Gain in
bone mineral mass in prepubertal girls 3.5 years after discontinuation
of calcium supplementation: a follow-up study. Lancet 2001;358:
15. Halioua L, Anderson JJB. Lifetime calcium intake and physical activity
habits: independent and combined effects on the radial bone of
healthy premenopausal Caucasian women. Am J Clin Nutr 1989;49:
16. Murphy S, Khaw KT, May H, Compston JE. Milk consumption and
bone mineral density in middle aged and elderly women. BMJ 1994;
17. Sandler RB, Slemenda CW, LaPorte RE, et al. Postmenopausal bone
density and milk consumption in childhood and adolescence. Am J
Clin Nutr 1985;42:270.4.
18. Soroko S, Holbrook TL, Edelstein S, Barrett-Connor E. Lifetime milk
consumption and bone mineral density in older women. Am J Public
19. Stracke H, Renner E, Knie G, Leidig G, Minne H, Federlin K. Osteoporosis
and bone metabolic parameters in dependence upon calcium
intake through milk and milk products. Eur J Clin Nutr 1993;47:
20. Tylavsky FA, Anderson JJB, Talmage RV, Taft TN. Are calcium
intakes and physical acitivity patterns during adolescence related to
radial bone mass of white college-age females. Osteoporos Int 1992;
21. Bauer DC, Browner WS, Cauley JA, et al. Factors associated with
appendicular bone mass in older women. The Study of Osteoporotic
Fractures Research Group. Ann Intern Med 1993;118:657.65.
22. Davis JW, Novotny R, Ross PD, Wasnich RD. Anthropometric,
lifestyle and menstrual factors influencing size-adjusted bone mineral
content in a multiethnic population of premenopausal women. J
23. Fehily AM, Coles RJ, Evans WD, Elwood PC. Factors affecting bone
density in young adults. Am J Clin Nutr 1992;56:579.86.
24. McCulloch RG, Bailey DA, Houston CS, Dodd BL. Effects of physical
activity, dietary calcium intake and selected lifestyle factors on
bone density in young women. Can Med Assoc J 1990;142:221.7.
25. Lloyd T, Chinchilli VM, Johnson-Rollings N, Kieselhorst K, Eggli DF,
Marcus R. Adult female hip bone density reflects teenage sportsexercise
patterns but not teenage calcium intake. Pediatrics 2000;
26. Welten DC, Kemper HC, Post GB, Van Staveren WA, Twisk JW. Longitudinal
development and tracking of calcium and dairy intake from
teenager to adult. Eur J Clin Nutr 1997;51:612.8.
27. Teegarden D, Lyle RM, Proulx WR, Johnston CC, Weaver CM. Previous
milk consumption is associated with greater bone density in
young women. Am J Clin Nutr 1999;69:1014.7.
28. New SA, Bolton-Smith C, Grubb DA, Reid DM. Nutritional influences
on bone mineral density: a cross-sectional study in premenopausal
women. Am J Clin Nutr 1997;65:1831.9.
29. Nieves JW, Golden AL, Siris E, Kelsey JL, Lindsay R. Teenage and
current calcium intake are related to bone mineral density of the hip
and forearm in women aged 30.39 years. Am J Epidemiol 1995;141:
30. Feskanich D, Willett WC, Stampfer MJ, Colditz GA. Milk, dietary
calcium, and bone fractures in women: a 12-year prospective study.
Am J Public Health 1997;87:992.7.
31. Nieves JW, Grisso JA, Kelsey JL. A case-control study of hip fracture:
evaluation of selected dietary variables and teenage physical
activity. Osteoporos Int 1992;2:122.7.
32. Kelsey JL, Browner WS, Seeley DG, Nevitt MC, Cummings SR. Risk
factors for fractures of the distal forearm and proximal humerus. Am
J Epidemiol 1992;135:477.89.
33. NCHS. Plan and operation of the Third National Health and Nutrition
Examination Survey, 1988.94. Hyattsville, MD: National Center
for Health Statistics, 1994.
34. Looker AC,Wahner HW, Dunn WL, et al. Proximal femur bone mineral
levels of US adults. Osteoporos Int 1995;5:389.409.
35. Wahner HW, Looker A, Dunn WL,Walters LC, Hauser MF, Novak C.
Quality control of bone densitometry in a national health survey
(NHANES III) using three mobile examination centers. J Bone Miner
36. Looker AC,Wahner HW, Dunn WL, et al. Updated data on proximal
femur bone mineral levels of US adults. Osteoporos Int 1998;8:
37. Arky R. Physiciansf desk reference for nonprescription drugs. Montvale,
NJ: Medical Economics, 1994.
CHILDHOOD MILK INTAKE AND ADULT BONE DENSITY 265
38. Winer BJ. Statistical principles in experimental design. New York:
39. Dwyer JT, Gardner J, Halvorsen K, Krall EA, Cohen A, Valadian I.
Memory of food intake in the distant past. Am J Epidemiol 1989;130:
40. Bailey DB, Martin AD, McKay HM, Whiting S, Mirwald R. Calcium
accretion in girls and boys during puberty: a longitudinal analysis. J
Bone Miner Res 2000;15:2245.50.
41. Martin AD, Bailey DA, McKay HA, Whiting S. Bone mineral and
calcium accretion during puberty. Am J Clin Nutr 1997;66:611.5.
42. Lloyd T, Martel JK, Rollings N, et al. The effect of calcium supplementation
and Tanner stage on bone density, content and area in
teenage women. Osteoporos Int 1996;6:276.83.
43. Specker B,Wosje K. A critical appraisal of the evidence relating calcium
and dairy intake to bone health early in life. In: Burckhardt P,
Dawson-Hughes B, Heaney RP, eds. Nutritional aspects of osteoporosis.
San Diego: Academic Press, 2001:107.23.
44. Friedenreich CM, Slimani N, Riboli E. Measurement of past diet:
review of previous and proposed methods. Epidemiol Rev 1992;14:
45. Welten DC, Kemper HC, Post GB, Van Staveren WA. Relative validity
of 16-year recall of calcium intake by a dairy questionnaire in
young Dutch adults. J Nutr 1996;126:2843.50.
46. Nevitt MC, Cummings SR, Browner WS, et al. The accuracy of selfreport
of fractures in elderly women: evidence from a prospective
study. Am J Epidemiol 1992;135:490.9.
- Casos clínicos