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

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.

Introduction

Osteoporosis is a major skeletal disease caused by low bone mineral density (BMD) and microarchitectural deterioration of bone tissue, resulting in increased bone fragility and vulnerability to fracture.¹ BMD is affected by genetic, endocrine, mechanical, and nutritional factors, with extensive interactions between these factors.^2
–4 Among them, nutritional factors are considered to be of particular importance to bone health because they are potentially modifiable.⁵

Calcium (Ca) is responsible for structural functions, involving 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 uncommon in the United States, vitamin D insufficiency is prevalent with serum 25-OH-D3 concentrations between 25 and 50 nM considered normal.^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 100% OJ consumption accounts for 22% of total fruit consumption in the American diet.^20,21 OJ contains various essential nutrients and functional compounds, such as vitamin C, β-cryptoxanthin, potassium, folate, and flavonoids, 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 antioxidant.²⁴ Potassium has been known to be associated with BMD and bone mineral content (BMC). Several epidemiologic studies showed a positive correlation between potassium 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 women 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 β-carotene, β-cryptoxanthin, and lycopene, 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 β-cryptoxanthin and hesperidin, show potential for bone-protective 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 2003–2004³⁰ and 2005–2006³¹ 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. Exercise 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 activities 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 2003–2004³⁰ and 2005–2006³¹ 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, noninstitutionalized U.S. population.³²

The dietary intake data were estimated from nonconsecutive 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 respondents 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 cholecalciferol (vitamin D3). Since a food composition table for vitamin 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 nonconsumers 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 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 phosphatase (BSAP), and parathyroid hormone (PTH) concentrations 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 calculated.^39,40 Total femur BMD and BMC data in the NHANES 2005–2006 were used to investigate the effect of OJ consumption 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 distributions of categorical variables. ANOVA was used to compare means for interval-scale variables and to test overall differences in percentages of OJ consumption by sociodemographic and lifestyle variables. Arithmetic means of micronutrient intake of subpopulations grouped by sociodemographic and lifestyle variables were determined. Standard error was calculated by the linearization (Taylor series) variance estimation method for population parameters 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 analyses 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 significance 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 supplement, 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 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).

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)	P for trend
OJ consumption range (fl oz/day)	0.0	<4.1	4.1–7.3	>7.3
OJ consumption (mean, fl 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 (μg/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.

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)	P for trend
OJ consumption range (fl oz/day)	0	<4.1	4.1–7.5	>7.5
OJ consumption (mean, fl 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 (μg/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.

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 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 adjusting 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 nutrients. Also, in both age groups, intakes of carotenoids, such as β-carotene (only for adults), β-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 energy 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.

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)	P for trend
OJ consumption (range)	fl oz/day	0	<4.1	4.1–7.3	>7.3
OJ consumption (mean)	fl 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	μg/day	7580±223	7540±360	8790±486	10,600±660	P<.05
Excluding OJ	μg/day	7580±223	7300±359	8320±485	9510±650	.54
α-Carotene	μg/day	230±14.6	270±28.3	240±24.4	313.1±34.0	.25
β-Carotene	μg/day	1107±46.5	1170±76.8	1210±89.0	1400±100	.27
β-Cryptoxanthin	μg/day	50.0±3.2	179±6.3	279±6.2	581±18.4	P<.001
Lycopene	μg/day	5470±199	5100±310	6019±485	7130±605	.51
Lutein+zeaxanthin	μg/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. P trend 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.

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)	P for trend
OJ consumption (range)	fl oz/day	0.0	<4.2	4.2–7.5	>7.5
OJ consumption (mean)	fl 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	μg/day	9760±250	10,490±492	10,750±636	12,350±553	P<.05
Excluding OJ	μg/day	9760±250	10,230±493	10,260±637	11,310±553	.64
α-Carotene	μg/day	374±13.3	425±31.2	507±52.8	432±36.8	.14
β-Carotene	μg/day	1980±52.9	2370±123	2520±145.5	2320±130	P<.05
β-Cryptoxanthin	μg/day	64.2±3.2	189±4.8	309±5.7	577±12.2	P<.001
Lycopene	μg/day	5970±201	5880±450	5630±500	7060±465	.79
Lutein+zeaxanthin	μg/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. P trend 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.

The concentration of serum PTH and odds ratio for serum 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 children), 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).

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/cm²)
Variables	Slope (β coeff.)	P value
(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/m²)	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 (β coeff.)	P value
(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/m²)	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 (β coeff.) 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.

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/cm²)
Variables	Slope (β coeff.)	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/m²)	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 (β coeff.)	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/m²)	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 (β coeff.) 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.

Discussion

OJ ranks number one in 100% fruit juice consumed by Americans¹⁹ and more than half of the OJ products consumed are fortified with Ca and vitamin D. Thus, OJ fortified with Ca and vitamin D has become a readily available source of these nutrients for children and adults. To our knowledge, this is the first study to document the contribution 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 improved 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 consumers 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 fortified dairy products. Thus, these dietary sources might affect 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 nonconsumers. 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 important 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 significantly 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 isoforms of ALP present in several organs and tissues, including 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 available only in NHANES 2003–2004 and the number of subjects 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 associated 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 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 consumers and nonconsumers. This result showed a good agreement with a previous study by O'Neil et al. that indicates that OJ consumption seemed to help to reach the adequate 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 positively correlated with BMD and BMC in children, but negatively 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 partially 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 various nutrients that may promote bone health in the U.S. population. 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 between 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.

Footnotes

Acknowledgment

This study was supported by PepsiCo., Inc.

Author Disclosure Statement

At the time of the study, Dr. Beate Lloyd was an employee of PepsiCo, Inc. No competing financial interests exist for any of the authors.

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

Abstract

Introduction

Materials and Methods

Participants

Dietary intake data analysis

Biochemical analyses

Statistical analysis

Results

Discussion

Footnotes

Acknowledgment

Author Disclosure Statement

References

Supplementary Material