ArticlePDF Available

Impact of Orange Juice Consumption on Bone Health of the U.S. Population in the National Health and Nutrition Examination Survey 2003–2006

Authors:

Abstract

Orange juice (OJ) fortified with calcium (Ca) and vitamin D has turned OJ into a readily available source of these nutrients for children and adults. However, the impact of OJ consumption on Ca and vitamin D adequacy and bone health has not been documented. The aim of this study was the evaluation of the contribution of 100% OJ consumption to dietary and serum Ca and vitamin D status, and bone health parameters in the U.S. population aged 4 years and older (n = 13,971) using the National Health and Nutrition Examination Survey (NHANES) 2003–2004 and 2005–2006. Food consumption data were coded to produce micronutrient intake values using the USDA Food and Nutrient Database for Dietary Studies 3.0. Serum concentrations of bone-related micronutrients and biomarkers, bone mineral density (BMD), and bone mineral content (BMC) were measured. Analysis of data was conducted using SAS software 9.2 and SUDAAN. OJ consumers showed higher intakes of bone-related micronutrients, compared with nonconsumers (P < .05). In addition, OJ consumers had higher serum Ca levels in adults (P < .01) and had a lower odds ratio for serum 25-hydroxyvitamin D3 < 20 ng/mL in children (P < .05). OJ consumption was positively associated with femur BMD in children (P < .05) and with femur BMC in both children and adults (P < .05). In conclusion, OJ may be recommended as an effective dietary means of improving the status of Ca and vitamin D, acid-base balance, and of promoting bone health in children and adults.
Impact of Orange Juice Consumption on Bone Health of the U.S. Population
in the National Health and Nutrition Examination Survey 2003–2006
Sang Gil Lee,
1
Meng Yang,
2
Ying Wang,
3
Terrence Vance,
1
Beate Lloyd,
4,
*
Sang-Jin Chung,
5
Sung I. Koo,
1
and Ock K. Chun
1
1
Department of Nutritional Sciences, University of Connecticut, Storrs, Connecticut, USA.
2
School of Public Health Cambridge, Harvard University, Cambridge, Massachusetts, USA.
3
American Cancer Society, Inc., Atlanta, Georgia, USA.
4
PepsiCo Nutrition, Global Research & Development, PepsiCo, Valhalla, New York, USA.
5
Department of Foods and Nutrition, Kookmin University, Seoul, Korea.
ABSTRACT Orange juice (OJ) fortified with calcium (Ca) and vitamin D has turned OJ into a readily available source of
these nutrients for children and adults. However, the impact of OJ consumption on Ca and vitamin D adequacy and bone
health has not been documented. The aim of this study was the evaluation of the contribution of 100% OJ consumption to
dietary and serum Ca and vitamin D status, and bone health parameters in the U.S. population aged 4 years and older
(n=13,971) using the National Health and Nutrition Examination Survey (NHANES) 2003–2004 and 2005–2006. Food
consumption data were coded to produce micronutrient intake values using the USDA Food and Nutrient Database for Dietary
Studies 3.0. Serum concentrations of bone-related micronutrients and biomarkers, bone mineral density (BMD), and bone
mineral content (BMC) were measured. Analysis of data was conducted using SAS software 9.2 and SUDAAN. OJ consumers
showed higher intakes of bone-related micronutrients, compared with nonconsumers (P<.05). In addition, OJ consumers had
higher serum Ca levels in adults (P<.01) and had a lower odds ratio for serum 25-hydroxyvitamin D3 <20 ng/mL in children
(P<.05). OJ consumption was positively associated with femur BMD in children (P<.05) and with femur BMC in both
children and adults (P<.05). In conclusion, OJ may be recommended as an effective dietary means of improving the status of
Ca and vitamin D, acid-base balance, and of promoting bone health in children and adults.
KEY WORDS: bone mineral content bone mineral density calcium fortification orange juice vitamin D
INTRODUCTION
Osteoporosis is a major skeletal disease caused by low
bone mineral density (BMD) and microarchitectural
deterioration of bone tissue, resulting in increased bone fra-
gility and vulnerability to fracture.
1
BMD is affected by ge-
netic, endocrine, mechanical, and nutritional factors, with
extensive interactions between these factors.
2–4
Among them,
nutritional factors are considered to be of particular impor-
tance to bone health because they are potentially modifiable.
5
Calcium (Ca) is responsible for structural functions, in-
volving the skeleton and soft tissues, and regulatory functions.
6
Children with long-term Ca insufficiency have submaximal
accumulation of bone mass and density as adults.
7,8
Insufficient
Ca intake is prevalent in the U.S. population.
9–11
Recent Ca
intake levels, reflected in the data from the National Health and
Nutrition Examination Survey (NHANES) 2003–2006 for U.S.
adolescents and adults, were well below the U.S. adequate
intake levels, except for adult men.
11
Low Ca intake has also
been reported among U.S. preschool children living in a low
socioeconomic community.
12
Vitamin D status depends on the
production of vitamin D3 in the skin under the influence of
ultraviolet radiation and vitamin D intake through diet or
supplements. Serum 25-hydroxyvitamin D3 (25-OH-D3)
concentration is the parameter of choice for the assessment of
vitamin D status.
13
Even though vitamin D deficiency is un-
common in the United States, vitamin D insufficiency is
prevalent with serum 25-OH-D3 concentrations between 25
and50nMconsiderednormal.
14,15
Positive associations have been reported between fruit
and vegetable consumption and bone health in older
adults
16,17
and fruit and vegetable intake and bone size in the
girls between 8 and 13 years.
18
Orange juice (OJ) accounts
for almost 50% of worldwide fruit juice consumption and
ranks as the number one contributor to fruit intake in the
American diet.
19
Our recent study on the health impacts of
OJ consumption in the U.S. population has reported that
*Current affiliation: Global Scientific and Regulatory Affairs, The Coca-Cola Company,
Atlanta, Georgia, USA.
Manuscript received 5 March 2013. Revision accepted 27 April 2014.
Address correspondence to: Ock K. Chun, PhD, MPH, Department of Nutritio nal Sci-
ences, University of Connecticut, 3624 Horsebarn Road Extension Unit 4017, Storrs, CT
06269-4017, E-mail: ock.chun@uconn.edu
JOURNAL OF MEDICINAL FOOD
J Med Food 17 (10) 2014, 1142–1150
#Mary Ann Liebert, Inc., and Korean Society of Food Science and Nutrition
DOI: 10.1089/jmf.2013.0072
1142
100% OJ consumption accounts for 22% of total fruit con-
sumption in the American diet.
20,21
OJ contains various
essential nutrients and functional compounds, such as vita-
min C, b-cryptoxanthin, potassium, folate, and flavo-
noids, like hesperidin and naringin, and contributes to the
micronutrient intakes as shown in our previous result.
21,22
Vitamin C is a key micronutrient implicated for bone health,
since vitamin C is essential for the synthesis of collagen that
constitutes most of the organic matrix of bone.
23
In addition,
vitamin C could theoretically protect the connective tissue
of bone from oxidative stress, playing a role as an antioxi-
dant.
24
Potassium has been known to be associated with
BMD and bone mineral content (BMC). Several epidemio-
logic studies showed a positive correlation between potas-
sium intake and BMD and BMC.
25
Bone mineral loss might
be partially attributable to life-long mobilization of skeletal
salts to neutralize endogenous acid generated from acid-
producing foods.
17
A number of population-based studies
published in the last decade have demonstrated a beneficial
effect of fruit, vegetable, and potassium intake on axial and
peripheral bone mass and bone metabolism in men and wo-
men across age ranges.
16–18
Regarding magnesium (Mg), it is
known that Mg deficiency can cause osteoporosis.
26
Various
carotenoids may also be associated with BMD and BMC.
27
Carotenoids, especially b-carotene, b-cryptoxanthin, and ly-
copene, have been reported to improve bone health.
1,28
In addition, fortification with Ca and vitamin D has made
OJ a potentially good source of these nutrients for children
and adults especially those who do not drink milk or have
lactose intolerance. While it is well established that Ca,
vitamin D, and several micronutrients are essential for
bone health, other compounds rich in citrus fruits, such as b-
cryptoxanthin and hesperidin, show potential for bone-pro-
tective effects.
17,28
An animal study demonstrated that orange
consumption can enhance BMD, which may decrease the risk
of osteoporosis.
29
However, information on the contribution
of OJ consumption to human bone health is still limited.
Therefore, this study aimed to investigate the contribution of
OJ consumption to the intakes of Ca, vitamin D, and other
micronutrients, and bone health by utilizing a nationally
representative health and nutrition dataset of the free-living
U.S. population.
MATERIALS AND METHODS
Participants
Individuals aged 4 years and older in NHANES 2003–
2004
30
and 2005–2006
31
with reliable and complete diet
recall (DR) data were included in analyses (n=13,971).
From the records of all respondents with reliable DR data, as
defined by the National Center for Health Statistics (NCHS),
we excluded pregnant or lactating women. Participants were
grouped into two age subgroups (4–18 and 19 +years).
Dietary supplement users were defined as people who have
taken any dietary supplements during the last 30 days. Ex-
ercise levels were expressed as the metabolic equivalent of
task score, which was calculated by combining the intensity
level, mean duration, and frequency of the leisure time ac-
tivities reported. This study was reviewed by the University
of Connecticut Institutional Review Board (IRB) and met
the criteria for an exemption.
Dietary intake data analysis
NHANES 2003–2004
30
and 2005–2006
31
were utilized
for the present study. The NHANES has been conducted by
the NCHS in order to obtain information on the health and
nutritional status of the U.S. population. The NHANES used
a stratified, multistage probability sample design and
weighting methodology that allows for unbiased national
estimates to be produced for the civilian, noninstitutional-
ized U.S. population.
32
The dietary intake data were estimated from nonconsecu-
tive two 24-h DR collected by trained interviewers.
33
USDA
Automated Multiple Pass Method (AMPM) program, a five-
step computerized DR instrument, was used for both dietary
interviews.
34
The purpose of releasing 2-day data was to
permit the estimate of usual dietary intake of the participants,
since repeated measures can reduce measurement error.
Previously, two AMPM DR were validated for total energy
and several energy-adjusted micronutrients, including Ca and
vitamin D intakes.
33
The day-1 recalls were conducted in
person in the NHANES Mobile Examination Center (MEC).
All interviewed people were invited to the MEC, where the
24-h DR and questionnaires on dietary and lifestyle behaviors
were administered. The second recalls were conducted by
telephone interview *3–10 days after the first.
33
Proxy re-
spondents reported for children who were 5 years and
younger and for other persons who cannot self-report; proxy
respondents assisted children 6–11 years. Food consumption
data were coded using the USDA Food and Nutrient Database
for Dietary Studies (FNDDS) 2.0 for NHANES 2003–2004
and 3.0 for NHANES 2005–2006 to produce micronutrient
intake values.
35,36
The values for vitamin D content represent
the sum of both ergocalciferol (vitamin D2) and cholecal-
ciferol (vitamin D3). Since a food composition table for vi-
tamin D was not available in FNDDS 3.0, a special vitamin D
database (an addendum to FNDDS 3.0) developed by the
USDA was utilized for estimating vitamin D intake.
37
To investigate the contribution of OJ to Ca and vitamin D
intakes and their adequacy among the U.S. population, daily
average intakes of Ca and vitamin D, daily intakes of Ca and
vitamin D after excluding OJ from the food list consumed,
and the percentages of participants having Ca and vitamin D
intakes below the estimated average requirement (EAR)
levels were calculated among OJ nonconsumers and tertiles
of OJ consumers. In this study, OJ included nonsweetened
100% OJ and nonsweetened 100% OJ fortified with Ca and
vitamin D. OJ consumers were then defined as the subjects
who reported that they consumed OJ as a beverage at least
once in the nonconsecutive two 24-h DR, while noncon-
sumers were defined as the rest of the participants.
Biochemical analyses
Serum concentrations of total Ca and phosphorus were
measured using ion selective electrode methodology for Ca
ORANGE JUICE CONSUMPTION AND BONE HEALTH 1143
and a timed-rate method for phosphorus with LX 20 system
(Beckman, Urbana, IL, USA). Diasorin 25-OH-D3 assay was
used to measure the serum concentration of 25-OH-D3.
38
Alkaline phosphatase (ALP), bone-specific alkaline phos-
phatase (BSAP), and parathyroid hormone (PTH) concen-
trations were measured using Beckman UniCel DxC800
Synchron, and Beckman Coulter Access Ostase assay, and
Elecsys 1010 analyzer (Roche Diagnostics, Mannheim,
Germany), respectively. The percentage of people with serum
25-OH-D3 <20 ng/mL and PTH >65 pg/mL was calculat-
ed.
39,40
Total femur BMD and BMC data in the NHANES
2005–2006 were used to investigate the effect of OJ con-
sumption on bone mass (n=2111 for 4–18 years, n=3028 for
19 years). The BMC and BMD of total femur bone were
measured by dual-energy X-ray absorptiometry.
41
Statistical analysis
All data analyses were conducted using SAS software,
release 9.2, 2009 (SAS Institute, Inc., Cary, NC, USA) and
the Survey Data Analysis for multistage sample designs
professional software package (SUDAAN), release 10.0.1,
2009 (Research Triangle Institute, Research Triangle Park,
NC, USA). Sample weighting was applied to all analyses.
30,31
Chi-square tests were applied for assessing the distribu-
tions of categorical variables. ANOVA was used to compare
means for interval-scale variables and to test overall dif-
ferences in percentages of OJ consumption by socio-
demographic and lifestyle variables. Arithmetic means of
micronutrient intake of subpopulations grouped by socio-
demographic and lifestyle variables were determined.
Standard error was calculated by the linearization (Taylor
series) variance estimation method for population parame-
ters by SUDAAN. Student’s t-test and ANOVA were used
to compare means for interval-scale variables and to test
overall differences of micronutrient intake, bone-related
markers, and BMD between OJ nonconsumers and tertiles
of OJ consumers. Age, gender, ethnicity, milk consumption,
dietary supplement use, and energy intake were adjusted as
confounding variables. Multivariate linear regression ana-
lyses were performed to determine correlation between OJ
consumption and femoral BMD and BMC with age, gender,
BMI, exercise, and supplement use in the model. All
P-values reported were two-tailed, and statistical signifi-
cance was defined as P<.05.
RESULTS
Twenty-five percent of all participants aged 4 years
consumed OJ on either day with a mean daily intake of 7 fl
oz. In this study population, the consumption of OJ fortified
with Ca and vitamin D was prevalent accounting for 56% of
overall OJ consumption (data not shown). Daily average
intakes of Ca and vitamin D among OJ nonconsumers and
tertiles of OJ consumers were investigated in both age
groups (Tables 1 and 2). Daily Ca and vitamin D intakes of
OJ consumers were higher than those of OJ nonconsumers
and increased by the amount of OJ consumed after adjusting
for age, gender, ethnicity, milk consumption, dietary sup-
plement, and energy intake (P<.05). In the OJ consumers,
however, the linear trends still existed even after excluding
OJ from the food items consumed (P<.001), implying that
Table 1. Nutrient Intakes and Concentrations of Bone Turnover Markers by Orange Juice Consumption
in the U.S. Population Aged 4–18 Years in the NHANES 2003–2006
OJ nonconsumer
(n=4040)
OJ consumer
T1 (n=651)
OJ consumer
T2 (n=559)
OJ consumer
T3 (n=606)
Pfor
trend
OJ consumption range (fl oz/day) 0.0 <4.1 4.1–7.3 >7.3
OJ consumption (mean, oz/day) 0.0 2.8 0.0 5.4 0.0 12.5 0.2
Dietary nutrients
Ca (mg/day) 975.5 15.9 1022.5 31.6 1057.6 26.0 1311.0 45.5 P<.05
Ca after excluding OJ (mg/day) 975.5 15.9 967.6 30.4 975.7 25.5 1098.8 42.8 P<.001
Participants below EAR for Ca (%) 57.7 1.6 47.7 3.3 50.1 3.0 36.2 3.1 P<.05
Vitamin D (IU/day) 222.9 5.7 256.6 12.0 250.3 10.1 316.3 13.9 P<.05
Vitamin D after excluding OJ (IU/day) 222.9 5.7 226.7 11.0 214.7 9.9 241.6 15.0 P<.001
Participants below EAR for vitamin D (%) 87.5 1.0 83.0 2.5 83.4 2.5 71.7 3.1 .16
Serum concentrations
Serum total Ca (mM) 2.44 0.00 2.43 0.01 2.44 0.01 2.45 0.01 .06
Phosphorus (mM) 1.45 0.01 1.48 0.01 1.43 0.02 1.46 0.02 .55
Alkaline phosphatase (U/L) 149.0 3.1 161.2 7.1 145.2 7.6 149.5 7.1 .11
Bone-specific alkaline phosphatase (mg/L) 66.1 3.3 73.5 2.6 66.6 3.3 54.9 3.4 .65
Serum 25-OH-D3 (ng/mL) 25.1 0.5 25.3 0.5 25.8 0.6 24.8 0.8 .50
Odds ratio for serum 25-OH-D3 <20 ng/mL 1.00 (1.00–1.00) 0.98 (0.73–1.32) 0.71 (0.51–0.97) 0.75 (0.58–0.98) P<.05
Serum PTH (pg/mL) 37.6 0.6 36.5 1.0 35.7 1.1 36.9 1.0 .09
Odds ratio for serum PTH 65 pg/mL 1.00 (1.00–1.00) 0.96 (0.68–1.35) 0.58 (0.32–1.05) 0.70 (0.38–1.28) .13
P-values for the difference of means between OJ consumer and nonconsumer groups. Nutrient intakes were adjusted for age, gender, ethnicity, milk consumption,
dietary supplement, and energy intake. Serum variables were adjusted for age, gender, ethnicity, milk consumption, dietary supplement, and energy intake. Bone-
specific alkaline phosphatase data are from NHANES 2003–2004 (n=2090). OJ consumers were divided into tertiles, based on their daily average OJ consumption.
Ca, calcium; 25-OH-D3, 25-hydroxyvitamin D3; EAR, estimated average requirement; OJ, orange juice; NHANES, National Health and Nutrition Examination
Survey; PTH, parathyroid hormone.
1144 LEE ET AL.
OJ consumers overall had Ca- and vitamin D-rich diets. The
percentage of participants below the EAR for Ca was lower
for OJ consumers than OJ nonconsumers in both age groups.
The adequacy of Ca intake was increased by the amount of
OJ consumed (P<.05). However, there was no significant
difference in the percentage of participants below the EAR
for vitamin D between the OJ consumers and nonconsumers.
These results were consistent, when the age groups were
subdivided into 4–8, 9–13, 13–19, 19–30, 31–50, and >51
years (Supplementary Tables S1–S6; Supplementary Data
are available online at www.liebertpub.com/jmf ).
Intakes of other nutrients related to bone remodeling were
compared between OJ consumers and the OJ nonconsumers
(Tables 3 and 4). Daily intakes of micronutrients, including
Table 2. Nutrient Intakes and Concentrations of Bone Turnover Markers by Orange Juice Consumption
in the U.S. Population Aged 19 Years in the NHANES 2003–2006
OJ nonconsumer
(n=5921)
OJ consumer
T1 (n=754)
OJ consumer
T2 (n=709)
OJ consumer
T3 (n=731)
Pfor
trend
OJ consumption range (fl oz/day) 0 <4.1 4.1–7.5 >7.5
OJ consumption (mean, oz/day) 0 3.0 0.0 5.7 0.0 12.3 0.2
Dietary nutrients
Ca (mg/day) 873.8 12.2 859.4 21.8 959.7 21.6 1196 28.0 P<.001
Ca after excluding OJ (mg/day) 873.8 12.2 805.3 21.4 861.3 22.6 991.0 25.5 P<.01
Participants below EAR for Ca (%) 57.1 1.1 58.2 2.4 49.1 1.8 30.6 1.5 P<.001
Vitamin D (IU/day) 176.0 3.9 184.0 7.9 200.6 6.8 263.0 9.1 P<.01
Vitamin D after excluding OJ (IU/day) 176.0 3.9 156.5 7.7 160.8 6.4 190.3 8.6 P<.01
Participants below EAR for vitamin D (%) 91.5 0.5 92.3 1.2 92.3 1.3 81.2 1.4 .07
Serum concentrations
Serum total Ca (mM) 2.38 0.00 2.38 0.00 2.39 0.00 2.4 0.00 P<.01
Phosphorus (mM) 1.23 0.00 1.23 0.01 1.22 0.01 1.24 0.01 .41
Alkaline phosphatase (U/L) 68.5 0.6 68.3 1.3 68.2 1.5 67.8 0.9 .74
Bone-specific alkaline phosphatase (mg/L) 14.1 0.3 13.2 0.7 14.2 0.3 14.3 0.5 .67
Serum 25-OH-D3 (ng/mL) 23.6 0.4 23.1 0.5 24.1 0.6 23.8 0.6 .35
Odds ratio for serum 25-OH-D3 <20 ng/mL 1.00 (1.00–1.00) 0.90 (0.72–1.12) 0.81 (0.61–1.07) 1.04 (0.79–1.36) .97
Serum PTH (pg/mL) 43.7 0.5 47.7 1.3 45.8 0.9 42.6 0.9 .72
Odds ratio for serum PTH 65 pg/mL 1.00 (1.00–1.00) 1.28 (0.89–1.85) 1.11 (0.83–1.49) 1.29 (0.97–1.72) .21
P-values for the difference of means between OJ consumer and nonconsumer groups. Nutrient intakes were adjusted for age, gender, ethnicity, milk consumption,
dietary supplement, and energy intake. Serum variables were adjusted for age, gender, ethnicity, milk consumption, dietary supplement, and energy intake. Bone-
specific alkaline phosphatase data are from NHANES 2003–2004 (n=1978). OJ consumers were divided into tertiles, based on their daily average OJ consumption.
Table 3. Micronutrient Intakes by Orange Juice Consumption in U.S. Population Aged 4–18 Years in the NHANES 2003–2006
OJ consumer
Nutrient Unit OJ nonconsumer (n=4040) T1 (n=651) T2 (n=559) T3 (n=606) Pfor trend
OJ consumption (range) fl oz/day 0 <4.1 4.1–7.3 >7.3
OJ consumption (mean) oz/day 0 2.8 0.0 5.4 0.0 12.5 0.2
Magnesium mg/day 225 2.1 228 4.5 250 5.3 299 9.0 P<.01
Excluding OJ mg/day 225 2.1 219 4.4 233 5.3 259 8.6 .53
Potassium mg/day 2160 25.7 2300 48.8 2500 48.6 3180 82.0 P<.001
Excluding OJ mg/day 2160 25.7 2150 48.6 2210 49.3 2530 75.3 .79
Carotenoids mg/day 7580 223 7540 360 8790 486 10,600 660 P<.05
Excluding OJ mg/day 7580 223 7300 359 8320 485 9510 650 .54
a-Carotene mg/day 230 14.6 270 28.3 240 24.4 313.1 34.0 .25
b-Carotene mg/day 1107 46.5 1170 76.8 1210 89.0 1400 100 .27
b-Cryptoxanthin mg/day 50.0 3.2 179 6.3 279 6.2 581 18.4 P<.001
Lycopene mg/day 5470 199 5100 310 6019 485 7130 605 .51
Lutein +zeaxanthin mg/day 727 28.8 815 41.0 1034 72.1 1160 50.0 P<.001
Vitamin C mg/day 62.6 1.6 92.0 2.6 124 3.2 200 5.5 P<.001
Excluding OJ mg/day 62.6 1.6 62.7 2.7 67.5 3.2 70.8 3.5 .81
Micronutrient intakes were estimated based on the 2-day 24-h DR in NHANES 2003–2006. OJ included nonsweetened 100% OJ and nonsweetened 100% OJ
fortified with Ca and vitamin D. Values were mean SE. ‘‘OJ consumers’’ were defined as the subjects who reported that they consumed OJ as a beverage at least
once in the nonconsecutive two 24-h DR, while nonconsumers were defined as the rest of the participants. OJ consumers were divided into tertiles, based on their
daily average OJ consumption. Ptrend values were adjusted for age, gender, ethnicity, and energy intake; P-value for energy intake was adjusted for age, gender, and
ethnicity. ‘‘Excluding OJ’’ refers to estimating the micronutrient intakes after excluding OJ from the food list consumed.
DR, diet recall; SE, standard error.
ORANGE JUICE CONSUMPTION AND BONE HEALTH 1145
Mg, potassium, and vitamin C, were higher in OJ consumers
than OJ nonconsumers. The increases were associated with
the amount of OJ consumed in both age groups after ad-
justing for age, gender, ethnicity, and energy intake
(P<.05). The linear trends were no longer significant once
OJ was removed from the food items consumed, suggesting
that OJ was a major contributor to the intakes of these nu-
trients. Also, in both age groups, intakes of carotenoids, such
as b-carotene (only for adults), b-cryptoxanthin, and
lutein +zeaxanthin, were higher in OJ consumers than in OJ
nonconsumers (P<.05). After adjusting for age, gender,
ethnicity, milk consumption, dietary supplement, and en-
ergy intake, the serum concentration of total Ca was higher
in adults consuming OJ (P<.01), but not in children (Tables
1 and 2). The percentages of participants having serum 25-
OH-D3 <20 ng/mL were significantly lowered among OJ
consumers in children (P<.05), but not in adults.
The concentration of serum PTH and odds ratio for se-
rum PTH 65 pg/mL did not show significant differences
by OJ consumption in both age groups (Tables 1 and 2).
Multivariate linear regression analyses showed that OJ
consumption, as well as age, gender, BMI, exercise, and
dietary supplement usage (only for femur BMD for chil-
dren), was a strong predictor of femoral BMD and BMC in
both age groups (P<.05) except for femur BMD in adults
(Tables 5 and 6).
DISCUSSION
OJ ranks number one in 100% fruit juice consumed by
Americans
19
and more than half of the OJ products con-
sumed are fortified with Ca and vitamin D. Thus, OJ forti-
fied with Ca and vitamin D has become a readily available
source of these nutrients for children and adults. To our
Table 4. Micronutrient Intakes by Orange Juice Consumption in U.S. Population Aged 19 Years in the NHANES 2003–2006
OJ consumer
Nutrient Unit OJ nonconsumer (n=5921) T1 (n=754) T2 (n=709) T3 (n=731) Pfor trend
OJ consumption (range) fl oz/day 0.0 <4.2 4.2–7.5 >7.5
OJ consumption (mean) oz/day 0.0 3.0 0.0 5.7 0.0 12.3 0.2
Magnesium mg/day 281 3.3 274 5.5 299 5.3 356 7.2 P<.001
Excluding OJ mg/day 281 3.3 264 5.6 281 5.3 316 7.0 .50
Potassium mg/day 2620 28.0 2640 41.7 2910 44.6 3520 53.2 P<.001
Excluding OJ mg/day 2620 28.0 2480 42.1 2600 44.2 2860 51.5 P<.01
Carotenoids mg/day 9760 250 10,490 492 10,750 636 12,350 553 P<.05
Excluding OJ mg/day 9760 250 10,230 493 10,260 637 11,310 553 .64
a-Carotene mg/day 374 13.3 425 31.2 507 52.8 432 36.8 .14
b-Carotene mg/day 1980 52.9 2370 123 2520 145.5 2320 130 P<.05
b-Cryptoxanthin mg/day 64.2 3.2 189 4.8 309 5.7 577 12.2 P<.001
Lycopene mg/day 5970 201 5880 450 5630 500 7060 465 .79
Lutein +zeaxanthin mg/day 1360 37.8 1620 103 1780 110 1950 134 P<.001
Vitamin C mg/day 68.7 1.3 96.8 2.5 135 3.5 207 4.5 P<.001
Excluding OJ mg/day 68.7 1.3 64.4 2.6 74.3 3.5 76.0 3.0 .56
Micronutrient intakes were estimated based on the 2-day 24-h DR in NHANES 2003–2006. OJ included nonsweetened 100% OJ and nonsweetened 100% OJ
fortified with Ca and vitamin D. Values were mean SE. ‘‘OJ consumers’’ were defined as the subjects who reported that they consumed OJ as a beverage at least
once in the nonconsecutive two 24-h DR, while nonconsumers were defined as the rest of the participants. OJ consumers were divided into tertiles, based on their
daily average OJ consumption. Ptrend values were adjusted for age, gender, ethnicity, and energy intake; Pvalue for energy intake was adjusted for age, gender, and
ethnicity. ‘‘Excluding OJ’’ refers to estimating the micronutrient intakes after excluding OJ from the food list consumed.
Table 5. Multivariate Linear Regression Analysis
for Bone Mineral Density and Bone Mineral Content
of U.S. Population Aged 4–18 Years (n=2111)
in the NHANES 2005–2006
Femur BMD (g/cm
2
)
Variables Slope (bcoeff.) Pvalue
(A) BMD
OJ consumption (g/day) 0.000095 P<.05
Age (years) 0.033 P<.001
Gender (men =1, women =2) 0.062 P<.001
BMI (kg/m
2
) 0.011 P<.001
Exercise (MET) 0.000046 P<.01
Dietary supplement usage
(nonuse =2, use =1)
-0.014 .03
Femur BMC (g)
Variables Slope (bcoeff.) Pvalue
(B) BMC
OJ consumption (g/day) 0.0043 P<.05
Age (years) 2.00 P<.001
Gender (men =1, women =2) 8.06 P<.001
BMI (kg/m
2
) 0.50 P<.001
Exercise (MET) 0.0026 P<.05
Dietary supplement usage
(nonuse =2, use =1)
-0.54 .34
Bone mineral density is from total femur BMD in the NHANES 2005–2006.
Slope refers to regression coefficient. P-value from t-test for regression
coefficient (bcoeff.) is zero. Exercise levels, expressed on the MET score,
were calculated by combining the intensity level of the leisure time activities
reported, mean duration, and frequency.
BMC, bone mineral content; BMD, bone mineral density; MET, metabolic
equivalent of task.
1146 LEE ET AL.
knowledge, this is the first study to document the contri-
bution of OJ to the intake and adequacy of Ca and vitamin D
in association with bone health in the U.S. population.
Bone remodeling is controlled by two subprocesses,
which are known as bone formation and bone resorption.
42
Since Ca and vitamin D are essential nutrients for bone
remodeling, it can be assumed that fortified Ca and vitamin
D in OJ may impact bone remodeling and bone health.
43
In
the present study, in both age groups, Ca and vitamin D
intakes were significantly higher in OJ consumers than OJ
nonconsumers. In addition, the percentage of participants,
whose Ca intake was below the EAR, was significantly
lower in OJ consumers and the adequacy of Ca was im-
proved by the increase in OJ consumption. Interestingly, Ca
and vitamin D intakes after excluding OJ from the food list
consumed were also significantly higher among OJ con-
sumers than OJ nonconsumers. The possible explanation of
these results might be due to other major dietary sources of
Ca and vitamin D in their diets.
44,45
Major sources of dietary
Ca are dairy products and dark leafy vegetables. Even
though our data were adjusted for milk consumption, they
were not adjusted for other dairy products, such as yogurt or
cheese. It is possible that higher OJ consumers might eat
more of these dairy foods high in Ca that are considered as
healthy diet.
46
The major sources of vitamin D are fatty fish
species, whole eggs, beef liver, fish oil, and milk and for-
tified dairy products. Thus, these dietary sources might af-
fect vitamin D intake. However, since intake of vitamin D
from these major natural sources is still insufficient to
reach the adequate intake level, it is apparent that vitamin
D-fortified OJ consumption considerably contributes to the
adequacy of vitamin D intake.
47
Therefore, these results
support the assertion that OJ consumers can have a healthier
dietary pattern and OJ consumption is an important source
of Ca and vitamin D.
48
Serum concentrations of various bone-related markers
were measured to examine the relationship between OJ
consumption and bone health. The serum concentrations of
phosphorus, ALP, BSAP, 25-OH-D3, and PTH were not
significantly different between OJ consumers and noncon-
sumers. OJ consumption was not associated with the serum
concentration of Ca in children. However, serum Ca was
positively associated with OJ consumption in adults. As the
serum Ca concentration is tightly regulated with the normal
total Ca range of 2.2–2.6 mM,
40
serum Ca does not seem to
reflect true Ca intake status.
44,49
Nevertheless, this study
shows that OJ consumption is positively associated with the
nutritional adequacy of Ca intake. 25-OH-D3, which is a
main vitamin D metabolite circulating in blood, is an im-
portant indicator of Ca absorption and PTH regulation,
an essential hormone for bone resorption by osteoclast
activity.
50
Deficiency of serum vitamin D causes an increase
in PTH secretion that increases bone resorption resulting in
transient hypercalcemia.
50,51
In both age groups, there were
no significant differences in serum 25-OH-D3 between OJ
consumers and OJ nonconsumers. However, in children, the
odds ratio for serum 25-OH-D3 <20 ng/mL was signifi-
cantly decreased by OJ consumption. This finding implies
that fortified OJ consumption could contribute to vitamin D
intake as well as improving serum vitamin D status.
47
ALP
is an important enzyme for bone turn-over and it promotes
bone mineralization and Ca uptake. There are various iso-
forms of ALP present in several organs and tissues, in-
cluding bone, liver, kidney, and pancreas.
52
Among them,
BSAP accounts for 12.5–85%. Therefore, BSAP may serve
as a stronger marker of bone turn-over relative to total
ALP.
53
However, in this study, the BSAP data were avail-
able only in NHANES 2003–2004 and the number of sub-
jects included in this analysis was limited to half of the total
participants, weakening the statistical power. This might be
a possible explanation for the lack of association between
serum ALP and OJ consumption. Serum PTH is highly as-
sociated with serum Ca level. The secretion of PTH is
regulated by serum Ca and vitamin D status.
54
In the present
study, there was no significant difference in PTH levels
between OJ nonconsumers and OJ consumers. This might be
explained by the normal serum Ca and vitamin D levels of
participants.
The results from multivariate linear regression analysis
show that OJ consumption is an independent predictor for
femur BMD and BMC in both age groups except for femur
BMD in adults. There might be several possible reasons for
the association of OJ consumption with BMD and BMC.
17
Ca intake from OJ consumption might be one of main
Table 6. Multivariate Linear Regression Analysis
for Bone Mineral Density and Bone Mineral Content
of U.S. Population Aged 19 Years (n=3028)
in the NHANES 2005–2006
Femur BMD (g/cm
2
)
Variables Slope (bcoeff.) P-value
(A) BMD
OJ consumption (g/day) 0.000030 .07
Age (years) -0.0033 P<.001
Gender (men =1, women =2) 0.11 P<.001
BMI (kg/m
2
) 0.011 P<.001
Exercise (MET) 0.000045 P<.01
Dietary supplement usage
(nonuse =2, use =1)
0.0048 .43
Femur BMC (g)
Variables Slope (bcoeff.) P-value
(B) BMC
OJ consumption (g/day) 0.0026 P<.05
Age (years) -0.048 P<.001
Gender (men =1, women =2) 13.88 P<.001
BMI (kg/m
2
) 0.45 P<.001
Exercise (MET) 0.0020 P<.01
Dietary supplement usage
(nonuse =2, use =1)
0.39 .26
Bone mineral content is from total femur BMC in the NHANES 2005–2006.
Slope refers to regression coefficient. P-value from t-test for regression
coefficient (bcoeff.) is zero. Exercise levels, expressed on the MET score,
were calculated by combining the intensity level of the leisure time activities
reported, mean duration, and frequency.
ORANGE JUICE CONSUMPTION AND BONE HEALTH 1147
reasons for the increases in BMD and BMC. Therefore, the
higher intake of Ca along with increased vitamin D intake
from OJ consumption might positively influence BMD and
BMC by enhancing Ca absorption and bone formation. In
the present study, there were significant differences in the
intakes of micronutrients related to bone health, such as Mg,
potassium, carotenoids, and vitamin C, between OJ con-
sumers and nonconsumers. This result showed a good
agreement with a previous study by O’Neil et al. that indi-
cates that OJ consumption seemed to help to reach the ad-
equate intake level of micronutrients related to improvement
of bone health.
55
Other variables, including age, gender,
BMI, and exercise, showed significant correlations with
femoral BMD and BMC. Among the variables, age is posi-
tively correlated with BMD and BMC in children, but neg-
atively correlated in adults. These age-dependent associations
might be attributable partly to endocrine changes including
sex steroids related to the stages of development and growth
and aging.
56,57
In terms of the positive correlations between
BMI and BMD, our result agrees with other studies.
58,59
Even
though the precise mechanism is not clear, the adipokines for
metabolic regulation, including leptin and adiponectin, from
adipose tissue could be involved in bone regulation.
59
The
gender difference regarding BMD and BMC could be par-
tially explained by difference of bone size.
60
OJ consumption was positively associated with increased
Ca and vitamin D intake and higher femoral BMD and BMC in
the U.S. population. These results imply that OJ consumption
could be positively associated with improved bone health. OJ
is a significant contributing factor to the nutritional status of Ca
and vitamin D and provides readily available sources of vari-
ous nutrients that may promote bone health in the U.S. pop-
ulation. The findings from this study may help nutrition
educators or investigators address benefits of OJ fortified with
Ca and vitamin D on bone health, especially in individuals at
high risk of bone loss. However, the present study had several
limitations. First, this study used 100% OJ but not Ca- and
vitamin D-fortified OJ as a dependent factor, although 100%
OJ showed significant difference between entire OJ consumers
and nonconsumers. Second, since this study is a cross-sectional
study, the results of this study cannot illustrate causality be-
tween OJ consumption and improvement of bone health.
Third, dietary intake data were based on two nonconsecutive
24-h DR, which might be a limitation of this study since there
is no scientific agreement on the minimum period of dietary
data collection needed to obtain an approximation of usual
intake. However, the 24-h DR can produce adequate estimates
of mean intake of a group that can be useful for contrasting the
dietary status of the group with different levels of risk factors
for certain diseases.
61
In addition, this study could not adjust
for all confounding factors, although many confounders have
been adjusted. Further studies are needed to evaluate causality
and examine how OJ and its bioactive components influence
bone metabolism and health.
ACKNOWLEDGMENT
This study was supported by PepsiCo., Inc.
AUTHOR DISCLOSURE STATEMENT
At the time of the study, Dr. Beate Lloyd was an em-
ployee of PepsiCo, Inc. No competing financial interests
exist for any of the authors.
REFERENCES
1. Yamaguchi M: Beta-cryptoxanthin and bone metabolism: the
preventive role in osteoporosis. J Health Sci 2008;54:356–369.
2. Foldes J, Tarjan G, Szathmari M, Varga F, Krasznai I, Horvath
C: Bone mineral density in patients with endogenous subclinical
hyperthyroidism: is this thyroid status a risk factor for osteopo-
rosis? Clin Endocrinol (Oxf ) 1993;39:521–527.
3. Tuppurainen M, Honkanen R, Kroger H, Saarikoski S, Alhava E:
Osteoporosis risk factors, gynaecological history and fractures in
perimenopausal women—the results of the baseline postal en-
quiry of the Kuopio Osteoporosis Risk Factor and Prevention
Study. Maturitas 1993;17:89–100.
4. McGuigan F, Murray L, Gallagher A, et al.: Genetic and envi-
ronmental determinants of peak bone mass in young men and
women. J Bone Miner Res 2002;17:1273–1279.
5. McGartland C, Robson P, Murray L, et al.: Fruit and vegetable
consumption and bone mineral density: the Northern Ireland
Young Hearts Project. Am J Clin Nutr 2004;80:1019–1023.
6. Arnaud CD, Sanchez SD: Calcium and phosphorus. In: Present
Knowledge of Nutrition (Ziegler EE, Filer LJ, eds.) International
Life Sciences Institute, Washington, DC, 1996, pp. 245–255.
7. Kalkwarf HJ, Khoury JC, Lanphear BP: Milk intake during
childhood and adolescence, adult bone density, and osteoporotic
fractures in US women. Am J Clin Nutr 2003;77:257–265.
8. Matkovic V, Jelic T, Wardlaw GM, et al.: Timing of peak bone
mass in Caucasian females and its implication for the prevention
of osteoporosis. Inference from a cross-sectional model. J Clin
Invest 1994;93:799–808.
9. Miller GD, Jarvis JK, McBean LD: The importance of meeting
calcium needs with foods. J Am Coll Nutr 2001;20(2 Suppl):
168S–185S.
10. Popkin BM, Zizza C, Siega-Riz AM: Who is leading the change?.
U.S. dietary quality comparison between 1965 and 1996. Am J
Prev Med 2003;25:1–8.
11. Bailey RL, Dodd KW, Goldman JA, et al.: Estimation of total
usual calcium and vitamin D intakes in the United States. J Nutr
2010;140:817–822.
12. Nitzan Kaluski D, Basch CE, Zybert P, Deckelbaum RJ, Shea S:
Calcium intake in preschool children—a study of dietary patterns
in a low socioeconomic community. Public Health Rev 2001;29:
71–83.
13. Lips P: Worldwide status of vitamin D nutrition. J Steroid Bio-
chem Mol Biol 2010;121:297–300.
14. Looker AC, Pfeiffer CM, Lacher DA, Schleicher RL, Picciano
MF, Yetley EA: Serum 25-hydroxyvitamin D status of the US
population: 1988–1994 compared with 2000–2004. Am J Clin
Nutr 2008;88:1519–1527.
15. Thomas MK, Lloyd-Jones DM, Thadhani RI, et al.: Hypovi-
taminosis D in medical patients. N Engl J Med 1998;338:777–783.
16. Tucker K, Hannan M, Kiel D: The acid-base hypothesis: diet and
bone in the Framingham Osteoporosis Study. Eur J Nutr 2001;
40:231–237.
17. New S, Robins S, Campbell M, et al.: Dietary influences on bone
mass and bone metabolism: further evidence of a positive link
1148 LEE ET AL.
between fruit and vegetable consumption and bone health? Am J
Clin Nutr 2000;71:142–151.
18. Tylavsky A, Holliday K, Danish R, Womack C, Norwood J,
Carbone L: Fruit and vegetable intakes are an independent pre-
dictor of bone size in early pubertal children. Am J Clin Nutr
2004;79:311–317.
19. Pollack SL, Lin B-H, Allshouse J: Characteristics of U.S. Orange
Consumption: Economic Research Service, USDA, 2003.
20. Kimmons J, Gillespie C, Seymour J, Serdula M, Blanck HM:
Fruit and vegetable intake among adolescents and adults in the
United States: percentage meeting individualized recommenda-
tions. Medscape J Med 2009;11:26.
21. Yang M, Lee SG, Wang Y, et al.: Orange juice, a marker of diet
quality, contributes to essential micronutrient and antioxidant
intakes in the U.S. population. J Nutr Educ Behav 2013;45:340.
22. Arabi A, Nabulsi M, Maalouf J, et al.: Bone mineral density by
age, gender, pubertal stages, and socioeconomic status in healthy
Lebanese children and adolescents. Bone 2004;35:1169–1179.
23. Hara K, Akiyama Y: Collagen-related abnormalities, reduction in
bone quality, and effects of menatetrenone in rats with a con-
genital ascorbic acid deficiency. J Bone Miner Metab 2009;27:
324–332.
24. Miller NJ, Rice-Evans CA: The relative contributions of ascorbic
acid and phenolic antioxidants to the total antioxidant activity of
orange and apple fruit juices and blackcurrant drink. Food Chem
1997;60:331–337.
25. Tucker KL, Hannan MT, Chen H, Cupples LA, Wilson PW, Kiel
DP: Potassium, magnesium, and fruit and vegetable intakes are
associated with greater bone mineral density in elderly men and
women. Am J Clin Nutr 1999;69:727–736.
26. Yamamoto S, Uenishi K: Nutrition and bone health. Magnesium-
rich foods and bone health. Clin Calcium 2010;20:768–774.
27. Sahni S, Hannan MT, Blumberg J, Cupples LA, Kiel DP,
Tucker KL: Inverse association of carotenoid intakes with 4-y
change in bone mineral density in elderly men and women:
the Framingham Osteoporosis Study. Am J Clin Nutr 2009;89:
416–424.
28. Sugiura M, Nakamura M, Ogawa K, et al.: Dietary patterns of
antioxidant vitamin and carotenoid intake associated with bone
mineral density: findings from post-menopausal Japanese female
subjects. Osteoporos Int 2011;22:143–152.
29. Morrow R, Deyhim F, Patil BS, Stoecker BJ: Feeding orange
pulp improved bone quality in a rat model of male osteoporosis.
J Med Food 2009;12:298–303.
30. National Center for Health Statistics: National Health and Nu-
trition Examination Survey, 2003–2004 Data Files. www.cdc
.gov/nchs/nhanes/nhanes2003-2004/nhanes03_04.htm (accessed
November 2005).
31. National Center for Health Statistics: National Health and Nu-
trition Examination Survey, 2005–2006 Data Files. www.cdc
.gov/nchs/nhanes/nhanes2005-2006/nhanes05_06.htm (accessed
November 2007).
32. Analytical and Reporting Guidelines: The National Health and
Nutrition Examination Survey (NHANES): Centers for Disease
Control and Prevention, 2005. http://www.cdc.gov/nchs/data/nhanes/
nhanes_03_04/nhanes_analytic_guidelines_dec_2005.pdf (accessed
February 2013).
33. Blanton CA, Moshfegh AJ, Baer DJ, Kretsch MJ: The USDA
automated multiple-pass method accurately estimates group total
energy and nutrient intake. Nutr Epidemiol 2006;136:2594–2599
34. MEC In-Person Dietary Intervewers Procedures Manual 2002.
http://www.cdc.gov/nchs/data/nhanes/nhanes_03_04/DIETARY_
MEC.pdf (accessed February 2013).
35. USDA Food and Nutrient Database for Dietary Studies, 2.0.
Agricultural Research Service, Food Surveys Research Group,
Beltsville, MD, 2006.
36. USDA Food and Nutrient Database for Dietary Studies 3.0.
Agricultural Research Service, Food Surveys Research Group,
Beltsville, MD, 2008.
37. Vitamin D Addendum to USDA Food and Nutrient Database for
Dietary Studies 3.0. Agricultural Research Service, Food Surveys
Research Group, Beltsville, MD, 2009.
38. National Health and Nutrition Examination Survey 2003–2004
Data Documentation, Codebook, and Frequencies. www.cdc.gov/
nchs/nhanes/nhanes2003-2004/L06VID_C.htm (accessed January
2013).
39. Melamed ML, Michos ED, Post W, Astor B: 25-hydroxyvitamin
D levels and the risk of mortality in the general population. Arch
Intern Med 2008;168:1629–1637.
40. Nussbaum SR, Zahradnik RJ, Lavigne JR, et al.: Highly sensitive
two-site immunoradiometric assay of parathyrin, and its clinical
utility in evaluating patients with hypercalcemia. Clin Chem
1987;33:1364–1367.
41. Baeksgaard L, Andersen KP, Hyldstrup L: Calcium and vitamin
D supplementation increases spinal BMD in healthy, postmeno-
pausal women. Osteoporos Int 1998;8:255–260.
42. Fazzalari NL: Bone remodeling: a review of the bone microen-
vironment perspective for fragility fracture (osteoporosis) of the
hip. Semin Cell Dev Biol 2008;19:467–472.
43. Andon MB, Peacock M, Kanerva RL, De Castro JA: Calcium
absorption from apple and orange juice fortified with calcium
citrate malate (CCM). J Am Coll Nutr 1996;15:313–316.
44. Skibniewska KA, Zakrzewski J, Siemianowska E, Polak-Juszc-
zak L, Aljewicz M: Calcium availability from yogurt by itself or
yogurt-cereal-containing products. J Toxicol Environ Health A
2010;73:1150–1154.
45. Nikooyeh B, Neyestani TR, Farvid M, et al.: Daily consumption
of vitamin D -or vitamin D +calcium-fortified yogurt drink
improved glycemic control in patients with type 2 diabetes: a
randomized clinical trial. Am J Clin Nutr 2011;93:764–771.
46. Nicklas TA, Baranowski T, Baranowski JC, Cullen K, Ritten-
berry L, Olvera N: Family and child-care provider influences on
preschool children’s fruit, juice, and vegetable consumption.
Nutr Rev 2001;59:224–235.
47. Biancuzzo RM, Young A, Bibuld D, et al.: Fortification of or-
ange juice with vitamin D(2) or vitamin D(3) is as effective as an
oral supplement in maintaining vitamin D status in adults. Am J
Clin Nutr 2010;91:1621–1626.
48. Pak CY, Stewart A, Haynes SD: Effect of added citrate or malate
on calcium absorption from calcium-fortified orange juice. JAm
Coll Nutr 1994;13:575–577.
49. Houillier P, Nicolet-BarousseL, Maruani G, Paillard M: What keeps
serum calcium levels stable? Joint Bone Spine 2003;70:407–413.
50. Feldman D: Vitamin D, parathyroid hormone, and calcium: a
complex regulatory network. Am J Med 1999;107:637–639.
51. Arnaud C, Glorieux F, Scriver CR: Serum parathyroid hormone
levels in acquired vitamin D deficiency of infancy. Pediatrics
1972;49:837–840.
52. Morote J, Trilla E, Esquena S, et al.: Analysis of bone alkaline
phosphatase as a marker for the diagnosis of osteoporosis in
ORANGE JUICE CONSUMPTION AND BONE HEALTH 1149
men under androgen ablation. Int J Biol Markers 2003;18:
290–294.
53. Nawawi HM, Yazid TN, Ismail NM, Mohamad AR, Nirwana SI,
Khalid BA: Serum bone specific alkaline phosphatase and uri-
nary deoxypyridinoline in postmenopausal osteoporosis. Malays
J Pathol 2001;23:79–88.
54. Fu L, Tang T, Miao Y, Hao Y, Dai K: Effect of 1,25-dihydroxy
vitamin D3 on fracture healing and bone remodeling in ovari-
ectomized rat femora. Bone 2009;44:893–898.
55. O’Neil CE, Nicklas TA, Rampersaud GC, Fulgoni VL, 3rd: One
hundred percent orange juice consumption is associated with better
diet quality, improved nutrient adequacy, and no increased risk for
overweight/obesity in children. Nutr Res 2011;31:673–682.
56. Iida H, Fukuda S: Age-related changes in bone mineral density,
cross-sectional area and strength at different skeletal sites in male
rats. J Vet Med Sci 2002;64:29–34.
57. Khosla S, III LJM, Atkinson EJ, O’Fallon WM: Relationship
of serum sex steroid levels to longitudinal changes in bone
density in young versus elderly men. Endocr Soc 2001;86:3555–
3561.
58. Fawzy T, Muttappallymyalil J, Sreedharan J, et al.: Association
between body mass index and bone mineral density in patients
referred for dual-energy X-ray absorptiometry scan in Ajman,
UAE. J Osteoporos 2011;876309.
59. Morin S, Leslie WD: High bone mineral density is associated
with high body mass index. Osteoporos Int 2009;20:1267–
1271.
60. Henry YM, Eastell R: Ethnic and gender differences in bone
mineral density and bone turnover in young adults: effect of bone
size. Osteoporos Int 2000;11:512–517.
61. Willett WC. Nutritional Epidemiology. 2nd ed. Oxford Uni-
versity Publishers, New York, NY, 1998.
1150 LEE ET AL.
... To illustrate, scientific studies have shown that citrus fruits improve human diets by supplying essential nutrients, including Vitamin C, flavonoids, phenolic compounds, carotenoids, folic acid, pectin, potassium, and dietary fiber [1,[4][5][6][7]. Consumption of these fruits also positively affects important biomarkers and contributes to a fit physical condition, such as measured in cholesterol parameters [8,9], bone health [10], intestinal microbiota [11], antioxidant status [12] and anthropometrics [13,14]. Furthermore, citrus fruits are beneficial in preventing illnesses, such as cancer [15][16][17], dementia [18], diabetes [19,20], metabolic syndrome [21], and cardiovascular, kidney and dental diseases [17,22,23]. ...
... Consistent with Gao and colleagues [26] who stressed the potential to develop market strategies for citrus fruits based on demographics, future studies should probably focus on consumption patterns of children and the elderly. These categories of individuals have been shown to receive particular benefits from consuming citrus fruits [4,10,18,38]. The current study also provided information to market practitioners about Italian consumers' preferences for citrus fruits, thus contributing to the ...
Article
Full-text available
While the medical community supports the growth of citrus consumption as part of a healthy diet, there is limited knowledge about consumer preferences for these fruits. The current study analyzed the purchasing patterns and drivers of fresh citrus fruits from a convenience sample of 346 Italian food shoppers. Results revealed that clementines were the citrus fruit purchased most, followed by oranges and tangerines. Sweetness and smell were important product attributes for respondents. Different drivers affect the purchasing frequencies of various citrus fruits. Taste motivation, with a specific preference for acidity, impacts orange purchasing. Similarly, clementines are purchased primarily for taste motivation, however, the core sensory attribute for respondents in this case was sweetness. Meanwhile, for tangerines, the taste motivation is less important than the energy motivation, and the size together with the color are the core purchasing drivers. These outcomes provide food scientists, agronomists and market practitioners with new insights into Italian consumers’ preferences for citrus fruits, thus contributing to a potential expansion of this market.
... A key determinant of skeletal growth is nutrition (47,48) , of which Ca and vitamin D play significant roles (49) . OJ consumption is positively associated with serum concentrations and intakes of Ca and vitamin D, as well as femoral bone mineral density and content (50) , highlighting the importance of bone-related micronutrient intake as an integral component of skeletal growth. Fang et al. previously linked Ca intake to height velocity in male adolescents (51) , and others (52,53) have identified that deficiencies in micronutrients such as vitamins A and D, P, ...
Article
Objective: Evaluate associations between orange juice (OJ) consumption and anthropometric parameters. Design: Prospective cohort study assessing the association between OJ intake and changes in BMI and height-for-age Z-score (HAZ) using mixed linear regression. Setting: 2004-2008, USA. Participants: Children from the Growing Up Today Study II (n 7301), aged 9-16 years at enrollment. Results: OJ consumption was positively associated with 2-year change in HAZ in girls (mean (se)): 0·03 (0·01) for non-consumers, 0·03 (0·02) for 1-3 glasses/month, 0·06 (0·01) for 1-6 glasses/week and 0·09 (0·02) for ≥1 glass/d after full adjustment (Ptrend = 0·02). However, OJ consumption was not associated with 2-year change in BMI percentile (kg/m2, mean (se)): -0·44 (0·36) for non-consumers, 0·20 (0·41) for 1-3 glasses/month, -0·04 (0·34) for 1-6 glasses/week and -0·77 (0·62) for ≥1 glass/d in girls, Ptrend = 0·81; -0·94 (0·53) for non-consumers, -1·68 (0·52) for 1-3 glasses/month, -0·81 (0·38) for 1-6 glasses per week and -1·12 (0·61) for ≥1 glass/d in boys, Ptrend = 0·49. Conclusion: OJ consumption was favourably associated with height growth but unrelated to excess weight gain. OJ may be a useful alternative to whole fruit in the event that whole fruit intake is insufficient.
... Low dose PPA had convincing effects on promoting osteoblastogenesis and gene expression, suggesting differentiation of mesenchymal stem cells toward tissue specific lineages, for example to either osteoblasts or adipocytes, is sensitive to environmental conditions. We suspect very little changes of bone metrics, or plasticity or local acid-base balance (30,31) by PPA may alter stem cell differentiation program. ...
Article
Full-text available
Phenolic acids (PAs) are metabolites derived from polyphenolic compounds found in fruits and vegetables resulting from the actions of gut bacteria. Previously, we reported that the levels of seven individual PAs were found to be at least 10 times higher in the serum of rats fed a blueberry (BB)‐containing diet compared to those fed a control diet. We have characterized the effects of one such BB‐associated serum PA, 3‐(3‐hydroxyphenyl)‐propionic acid (PPA), on senescence signaling and promotion of mesenchymal stem cell differentiation toward osteoblasts, while suppressing adipogenesis in the stem cells. To better understand the mechanistic actions of PPA on bone formation in vivo, we administered four doses of PPA (0.1, 0.5, 1 and 5 mg/kg/d; daily i.p.) to one‐month‐old female C57BL6/J mice for 30 days. We did not observe significant effects of PPA on cortical bone, however, there were significantly higher bone volume and trabecular thickness, increased osteoblastic cell number but decreased osteoclastic cell number in PPA‐treated groups compared to controls. These morphological and cellular outcomes of bone were reflected in changes of bone formation markers in serum and bone marrow plasma. PPA treatment reduced senescence signaling as evaluated by senescence‐associated β‐galactosidase activity, PPARγ, p53 and p21 expression in bone. In conclusion, PPA is capable of altering the mesenchymal stem cell differentiation program and bone cell senescence. This raises the possibility that BB‐rich diets promote bone growth through increasing systemic PAs, a question that merits additional investigation. This article is protected by copyright. All rights reserved.
... Some studies have reported the chemopreventive properties of orange juice associated with its effect on metabolic enzymes and its anti-inflammatory, cytoprotective/apoptotic, hormonal, cell signaling-modulating, antioxidant, and antigenotoxic effects (Franke et al. 2013). Also, orange juice provides several kinds of minerals and vitamins necessary to healthy state (Lee et al. 2014). ...
Article
Full-text available
Recent reports have shown that commercial orange juice is rich in biogenic amines. Consumption of foods containing large amounts of biogenic amines increase hypertensive crisis and high levels of histamine and tyramine, which have been implicated as causative agents in a number of food poisoning episodes. In addition, accumulation of tryptamine in plasma may be associated with mood disorders. The aim of this study was to determine whether chronic administration of orange juice extract and tryptamine affects the behavior and c-fos expression in the rat. For this purpose, Wistar male rats were injected with saline solution, tryptamine or orange juice extract. Sucrose preference test and elevated plus maze were evaluated to determine hedonic and anxiety behavior, respectively. Rats treated with orange juice extract showed increased anxiety behavior and sucrose consumption, similar to those treated with tryptamine. In addition, dorsal raphe nucleus, accumbens nucleus, and hippocampus showed an increase of c-fos positive cells in rats treated with orange juice extract. In conclusion, the chronic and lengthy consumption of orange juice or their derivatives in the diet could be a factor responsible to induce mood disorders and may promote excess caloric consumption.
Article
Childhood obesity is a national epidemic, and many efforts have been made to understand its risk factors. The purpose of this review was to provide an updated account of the observational studies evaluating the relationship between 100% fruit juice intake and obesity in children and adolescents, and to highlight the major risk factors that may impact this relationship. PubMed and Scopus were searched for terms related to fruit juice and childhood obesity, and studies assessing 100% fruit juice intake in participants ≤ 19 years old, with obesity-related outcomes (BMI or adiposity), and published before March 9, 2021 were included. There were 17 prospective cohort and 14 cross-sectional studies included in the analysis. Overall, the evidence does not support a relationship between 100% fruit juice intake and measures of obesity in most children. There is some evidence to suggest a minor positive association in some overweight or very young children, but due to fundamental differences and limitations in methodology, further investigation is required. Significant gaps in literature on this topic exist particularly in regards to randomized clinical trials in children, and in studies in racially diverse populations.
Article
Organic anion transporting polypeptides (OATPs) are a group of membrane transport proteins that facilitate the influx of endogenous and exogenous substances across biological membranes. OATPs are found in enterocytes and hepatocytes and in brain, kidney, and other tissues. In enterocytes, OATPs facilitate the gastrointestinal absorption of certain orally administered drugs. Fruit juices such as grapefruit juice, orange juice, and apple juice contain substances that are OATP inhibitors. These fruit juices diminish the gastrointestinal absorption of certain antiallergen, antibiotic, antihypertensive, and β-blocker drugs. While there is no evidence, so far, that OATP inhibition affects the absorption of psychotropic medications, there is no room for complacency because the field is still nascent and because the necessary studies have not been conducted. Patients should therefore err on the side of caution, taking their medications at least 4 hours distant from fruit juice intake. Doing so is especially desirable with grapefruit juice, orange juice, and apple juice; with commercial fruit juices in which OATP-inhibiting substances are likely to be present in higher concentrations; with calcium-fortified fruit juices; and with medications such as atenolol and fexofenadine, the absorption of which is substantially diminished by concurrent fruit juice intake. © Copyright 2014 Physicians Postgraduate Press, Inc.
Article
Full-text available
Background There continues to be considerable debate about the role of acid vs. basic components of the diet on the long-term status of bone mineral density. Aim In a set of two analyses, we examined the effect of components in the diet thought to have basic effects (magnesium, potassium, fruit, vegetables) and acid effects (protein) on bone mineral density in an elderly cohort. Methods Bone mineral density of participants in the Framingham Osteoporosis Study was measured at three hip sites and one forearm site at two points in time, four years apart. At the time of baseline measurement, participants ranged in age from 69–97 years. Dietary intake was assessed at baseline by food frequency questionnaire. Results As hypothesized, magnesium, potassium, fruit and vegetable intakes were significantly associated with bone mineral density at baseline and among men, with lower bone loss over four years. In contrast to the hypothesis, higher rather than lower protein intakes were associated with lower bone loss. Conclusion Together these results support the role of base forming foods and nutrients in bone maintenance. The role of protein appears to be complex and is probably dependent on the presence of other nutrients available in a mixed diet. A balanced diet with ample fruit and vegetables and adequate protein appears to be important to bone mineral density.
Article
The later stages of the vitamin D deficiency syndrome during infancy are associated with impaired renal tubular reabsorption of amino acids, phosphate, and other metabolites. Secondary hyperparathyroidism has been implicated as the cause of the renal abnormality. Serum immunoreactive parathyroid hormone levels are elevated in infants with vitamin D deficiency (60 to 238 µl Eq/ml; normal < 40 µl q/ml). The highest levels were found in the more advanced stages of vitamin D deficiency.
Article
The objective of this study was to evaluate the usefulness of serum determination of bone alkaline phosphatase (BAP) in the diagnosis of osteoporosis in men with prostate cancer under androgen ablation. Serum levels of BAP and bone mineral density (BMD) were assessed in 110 patients with non-metastatic, treated prostate cancer. Fifty-eight patients were under androgen deprivation during a period between two and 96 months and 52 had been submitted only to radical prostatectomy. Mean serum BAP was 11.8 ng/mL in patients with normal BMD, 16.7 ng/mL in patients with osteopenia (p. 0.058), and 19.3 ng/mL in patients with osteoporosis (p=0.044). The correlation between serum BAP and BMD was significant (p. 0.006) but with an index of only 0.26. Receiver operating characteristic analysis for the diagnosis of osteoporosis showed an area under the curve of 0.608. None of the cutoff points that provided specificities of 75%, 90% and 95% gave significant distributions. The positive and negative predictive values as well as the odds ratios were not of any clinical usefulness. We conclude that serum BAP should not be considered a good marker for the diagnosis of osteoporosis in men with prostate cancer. Therefore, BAP serum determination cannot replace bone densitometry as a diagnostic tool.
Article
Bone loss with aging induces osteoporosis. The most dramatic expression of the disease is represented by fractures of the proximal femur. Pharmacologic and nutritional factors may play a role in the prevention of bone loss with aging. beta-Cryptoxanthin, a kind of carotenoid, is abundant in Satsuma mandarin orange (Citrus unshiu MARC.). Amoung various carotenoids including beta-cryptoxanthin, lutein, lycopene, beta-carotene, astaxanthin, and rutin, beta-cryptoxanthin has been found to have a unique anabolic effect on bone calcification in vitro. Hesperidin, which is contained in Satsuma mandarin orange, did not have an anabolic effect on bone calcification in vitro. beta-Cryptoxanthin has stimulatory effects on osteoblastic bone formation and inhibitory effects on osteoclastic bone resorption in vitro, thereby increasing bone mass. beta-Cryptoxanthin has an effect on the gene expression of various proteins which are related to osteoblastic bone formation and mineralization in vitro. beta-Cryptoxanthin has inhibitory effects on enzyme activity which is related to osteoclastic bone resororption, and the carotenoid induces apoptosis of mature osteoclastic cells in vitro. Oral administration of beta-cryptoxanthin has been shown to have the anabolic effects on bone components in young and aged rats, and the administration has the preventive effects on bone loss in streptozotocin-diabetic rats and ovariectomized rats in vivo. Moreover, the intake of, beta-cryptoxanthin-reinforced juice for longer periods has been shown to have both stimulatory effects on bone formation and inhibitory effects on bone resorption in healthy human or postmenopausal women in evaluating with serum biochemical markers of bone metabolism in vivo. Thus the intake of dietary beta-cryptoxanthin may have a preventive effect on osteoporosis due to stimulating bone formation and due to inhibiting bone resorption. Moreover, epidemiological studies suggest the potential role of beta-cryptoxanthin as a sustainable nutritional approach to improving bone health of human subjects. beta-Cryptoxanthin is an important food factor in maintaining bone healthy and in preventing osteoporosis.
Article
Background Many studies have examined rapidly changing trends in U.S. dietary intake, but not as they correspond to other health inequalities among black and white Americans. The purpose of this study was to explore 30-year trends in diet quality and to examine whether income or education is the key socioeconomic factor linked with these shifts.
Book
This book is intended to increase understanding of the complex relationships between diet and the major diseases of western civilization, such as cancer and atherosclerosis. The book starts with an overview of research strategies in nutritional epidemiology-a relatively new discipline which combines the knowledge compiled by nutritionists during this century with the methodology developed by epidemiologists to study the determinants of disease with multiple etiologies and long latent periods. A major part of the book is devoted to methods of dietary assessment using data on food intake, biochemical indicators of diet, and measures of body size and composition. The reproducibility and validity of each approach and the implications of measurement error are considered in detail. The analysis, presentation, and interpretation of data from epidemiologic studies of diet and disease are discussed. Particular attention is paid to the important influence of total energy intake on findings in such studies. As examples of methodologic issues in nutritional epidemiology, three substantive topics are examined in depth: the relations of diet and coronary heart disease, fat intake and breast cancer, and Vitamin A and lung cancer.
Article
Objective: To evaluate the impact of 100% orange juice (OJ) on the healthy diet and micronutrient intakes of the United States population. Methods: Cross-sectional study of 13,971 people in the United States aged ≥ 4 years using 2 24-hour diet recalls from the National Health and Nutrition Examination Survey, 2003-2006. Results: Consumption of OJ was higher among 4- to 8-year-old children, older adults (> 50 y old), non-Hispanic blacks, those with lower body mass index, those of lower income level, nonsmokers, dietary supplement users, and those participating in regular exercise (P < .05). Consumption of OJ was positively associated with the percentage of participants meeting MyPyramid recommendations for fruit consumption. Increased OJ consumption was correlated with increased daily intakes of certain micronutrients and antioxidants (P < .05). Percentages of participants with intakes below Estimated Average Requirements for these micronutrients decreased with increased OJ consumption (P < .001). Conclusions and implications: The implicated nutritional and potential health benefits of OJ warrant further investigation in clinical research studies.