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Greater Fruit Intake was Associated With Better Bone Mineral Status Among Chinese Elderly Men and Women: Results of Hong Kong Mr. Os and Ms. Os Studies

  • Zhao-min Liu
    Correspondence
    Address correspondence to Zhao-min Liu, PhD, Division of Family Medicine and Primary Care, Jockey Club School of Public Health and Primary Care, The Chinese University of Hong Kong, Hong Kong SAR or Jean Woo, MD, Division of Geriatrics, Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong SAR.
    Affiliations
    Division of Family Medicine and Primary Care, Jockey Club School of Public Health and Primary Care, The Chinese University of Hong Kong, Hong Kong SAR
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  • Jason Leung
    Affiliations
    Jockey Club Centre for Osteoporosis Care and Control, The Chinese University of Hong Kong, Shatin, Hong Kong SAR
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  • Samuel Yeung-shan Wong
    Affiliations
    Division of Family Medicine and Primary Care, Jockey Club School of Public Health and Primary Care, The Chinese University of Hong Kong, Hong Kong SAR
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  • Carmen Ka Man Wong
    Affiliations
    Division of Family Medicine and Primary Care, Jockey Club School of Public Health and Primary Care, The Chinese University of Hong Kong, Hong Kong SAR
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  • Ruth Chan
    Affiliations
    Department of Medicine and Therapeutics, and the Centre for Nutritional Studies, The Chinese University of Hong Kong, Shatin, Hong Kong SAR
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  • Jean Woo
    Correspondence
    Address correspondence to Zhao-min Liu, PhD, Division of Family Medicine and Primary Care, Jockey Club School of Public Health and Primary Care, The Chinese University of Hong Kong, Hong Kong SAR or Jean Woo, MD, Division of Geriatrics, Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong SAR.
    Affiliations
    Department of Medicine and Therapeutics, and the Centre for Nutritional Studies, The Chinese University of Hong Kong, Shatin, Hong Kong SAR
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Published:December 15, 2014DOI:https://doi.org/10.1016/j.jamda.2014.11.001

      Abstract

      Objectives

      Although studies in white populations have reported the beneficial effects of intakes of fruit and vegetables (F&V) on bone mass, limited data are available in Asians, especially among the elderly population. We examined the association of F&V intakes and bone mineral status in Chinese elderly adults and explored the potential mechanisms.

      Design, setting, and participants

      The study was a population-based cross-sectional study among 4000 Hong Kong Chinese men and women aged 65 years and older.

      Measurements

      Habitual F&V intakes were ascertained from a validated food frequency questionnaire. Bone mineral measurements of the whole body, hip, lumber spine, and femoral neck were made by dual-energy X-ray absorptiometry. Information on demographic, health, and lifestyles factors was obtained by standardized questionnaire. Relations between F&V intakes and bone mass at various sites were assessed by regression models.

      Results

      Whole-body and femoral neck bone mineral density and content were significantly and positively associated with fruit intake in both men and women, even when adjustment for a range of potential confounders was made. A daily increase of 100 g/kcal total fruit intake was associated with 4.5% and 6.4% increase of BMD at whole body, and 3.9% and 4.8% increase at the femoral neck in men and women, respectively. No significant association was found between vegetable intake and bone mass. The adjustment for vitamin C intake, but not dietary acid load, attenuated the association between fruit intake and bone mass.

      Conclusions

      Greater fruit intake was independently associated with better bone mineral status among Chinese elderly men and women. The association is probably modified by dietary vitamin C.

      Keywords

      Osteoporosis is a chronic and often asymptomatic disease that is estimated to affect more than 200 million people worldwide.
      • Reginster J.Y.
      • Burlet N.
      Osteoporosis: A still increasing prevalence.
      The prevalence of osteoporosis is escalating with the increasingly elderly population. Nearly 75% of hip, spine, and distal forearm fractures occur among patients older than 65. Half of the hip fractures worldwide are projected to occur in Asia by 2050,
      • Cooper C.
      • Campion G.
      • Melton 3rd, L.J.
      Hip fractures in the elderly: A world-wide projection.
      with Hong Kong expected to be one of the leading regions in terms of hip fracture incidence.
      • Lau E.M.
      • Lee J.K.
      • Suriwongpaisal P.
      • et al.
      The incidence of hip fracture in four Asian countries: The Asian Osteoporosis Study (AOS).
      Pharmacological agents on osteoporosis are often limited by the potential side effects and the restricted applicability.
      • Recker R.R.
      Clinical review 41: Current therapy for osteoporosis.
      Nutritional factors are therefore of particular importance to bone health because they are potentially modifiable.
      • Cashman K.D.
      Diet, nutrition, and bone health.
      Studies have shown some nutrients (eg, vitamins C and K) and phytochemicals (eg, polyphenols, isoflavones, and lignans) found abundantly in fruits and vegetables (F&V) were associated with increased bone mass or reduced urinary calcium excretion.
      • Tucker K.L.
      • Hannan M.T.
      • Chen H.
      • et al.
      Potassium, magnesium, and fruit and vegetable intakes are associated with greater bone mineral density in elderly men and women.
      • Trzeciakiewicz A.
      • Habauzit V.
      • Horcajada M.N.
      When nutrition interacts with osteoblast function: Molecular mechanisms of polyphenols.
      • Tucker K.L.
      Osteoporosis prevention and nutrition.
      In addition, high dietary acid load is known to inhibit osteoblast function and increase osteoclast activity.
      • Brandao-Burch A.
      • Utting J.C.
      • Orriss I.R.
      • Arnett T.R.
      Acidosis inhibits bone formation by osteoblasts in vitro by preventing mineralization.
      Due to the high potassium and magnesium content, diets high in F&V have a lower acid load and may promote a positive calcium balance.
      • New S.A.
      Intake of fruit and vegetables: Implications for bone health.
      These findings have led researchers to explore the potential link between F&V consumption and bone health.
      F&V are essential components of a healthy diet. The protective effects against osteoporosis among children and adults have been suggested in several observational studies,
      • Xie H.L.
      • Wu B.H.
      • Xue W.Q.
      • et al.
      Greater intake of fruit and vegetables is associated with a lower risk of osteoporotic hip fractures in elderly Chinese: A 1:1 matched case-control study.
      • New S.A.
      • Robins S.P.
      • Campbell M.K.
      • et al.
      Dietary influences on bone mass and bone metabolism: Further evidence of a positive link between fruit and vegetable consumption and bone health?.
      • Macdonald H.M.
      • New S.A.
      • Golden M.H.
      • et al.
      Nutritional associations with bone loss during the menopausal transition: Evidence of a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients and of a detrimental effect of fatty acids.
      • Prynne C.J.
      • Mishra G.D.
      • O'Connell M.A.
      • et al.
      Fruit and vegetable intakes and bone mineral status: A cross sectional study in 5 age and sex cohorts.
      but not all.
      • Monma Y.
      • Niu K.
      • Iwasaki K.
      • et al.
      Dietary patterns associated with fall-related fracture in elderly Japanese: A population based prospective study.
      • Kaptoge S.
      • Welch A.
      • McTaggart A.
      • et al.
      Effects of dietary nutrients and food groups on bone loss from the proximal femur in men and women in the 7th and 8th decades of age.
      • Benetou V.
      • Orfanos P.
      • Zylis D.
      • et al.
      Diet and hip fractures among elderly Europeans in the EPIC cohort.
      A 1-month DASH trial
      • Lin P.H.
      • Ginty F.
      • Appel L.J.
      • et al.
      The DASH diet and sodium reduction improve markers of bone turnover and calcium metabolism in adults.
      showed that a diet high in F&V significantly reduced bone turnover markers in adults, but a 2-year supplementation of 300 g/d F&V did not significantly and persistently reduce bone turnover or prevent bone mineral density (BMD) loss in healthy postmenopausal women.
      • Macdonald H.M.
      • Black A.J.
      • Aucott L.
      • et al.
      Effect of potassium citrate supplementation or increased fruit and vegetable intake on bone metabolism in healthy postmenopausal women: A randomized controlled trial.
      Thus, the effects of F&V on bone health remain inconclusive. Most of the current evidence is derived from white populations, and there are limited studies among Asians.
      • Hamidi M.
      • Boucher B.A.
      • Cheung A.M.
      • et al.
      Fruit and vegetable intake and bone health in women aged 45 years and over: A systematic review.
      Most of the previous studies were among women and few were among men.
      • Hamidi M.
      • Boucher B.A.
      • Cheung A.M.
      • et al.
      Fruit and vegetable intake and bone health in women aged 45 years and over: A systematic review.
      Little is known of these associations among the Chinese elderly population, who generally have dietary patterns and cooking practices different from those of whites.
      • Hamidi M.
      • Boucher B.A.
      • Cheung A.M.
      • et al.
      Fruit and vegetable intake and bone health in women aged 45 years and over: A systematic review.
      The aim of this study was to investigate the associations between bone mineral status and reported F&V intakes in a large, representative sample of apparently healthy Hong Kong Chinese elderly men and women, and explore the potential mechanisms related to dietary acid load, vitamin C, and isoflavones.

      Methods

      Subject Recruitment

      Mr Os and Ms Os (Hong Kong) are the largest cohort studies on osteoporosis in Asian men and women to date. The methodology of this project has been reported elsewhere.
      • Chan R.
      • Leung J.
      • Woo J.
      No association between dietary vitamin K intake and fracture risk in Chinese community-dwelling older men and women: A prospective study.
      In brief, we recruited 2000 men and 2000 women aged 65 years and older living in the community between 2001 and 2003. Participants were volunteers and were able to walk or take public transport to the study sites. They were recruited via notices and talks in community centers and housing estates by using a stratified sampling method to ensure that approximately one-third of the participants fell into each of the following age strata: 65 to 69, 70 to 74, and 75 and older. The study was approved by the Clinical Research Ethics Committee of The Chinese University of Hong Kong. Written informed consent was obtained from all participants.

      Dietary Assessment

      Dietary intake was assessed using a validated semiquantitative food frequency questionnaire (FFQ).
      • Woo J.
      • Leung S.S.F.
      • Ho S.C.
      • et al.
      A food frequency questionnaire for use in the Chinese population in Hong Kong: Description and examination of validity.
      Each participant was asked by a trained interviewer to report the frequency and the usual amount of consumption of each food item over the past year. Portion size was explained to participants using a catalog of pictures of individual food portions. The FFQ consisted of 7 categories: bread/pasta/rice; vegetables/fruits; meat/fish/eggs; beverages; dim sum/snacks; soups; and oil/salt/sauces. Dietary nutrient intakes, such as dietary energy, protein, fat, calcium, and vitamin C, were calculated using food tables derived from McCance and Widdowson
      • Paul A.A.
      • Soughgate D.A.T.
      McCance & Widdowson’s: The composition of Foods.
      and the Chinese Food Composition Table.
      • Yang Y.
      • Wang G.
      • Pan X.
      China Food Composition 2002.
      Fruit intake was assessed by the inclusion of fresh fruit, cooked or canned fruit, dried fruit, and fruit juices based on 28 fruit items, such as apple, apricot, banana, cherry, grape, raisins, lemon, lychee, logan, mango, melon, papaya, pear, plum, peach, pineapple, prunes, orange, persimmon, watermelon, kiwi, pomelo, strawberry, and carambola. Total vegetable intakes included intake of green vegetables, root vegetables, pulses, salad vegetables, and mixed-vegetable dishes based on 64 vegetable items, such as green leafy vegetables, corn, onion, cucumber, pepper, asparagus, eggplant, bamboo shoot, Chinese radish and chives, Chinese water chestnut, lotus root, celery, leeks, peppers, lily, pumpkin, taro, tomatoes, and legumes. Only F&V specifically reported were assessed.
      Frassetto's method
      • Yang Y.
      • Wang G.
      • Pan X.
      China Food Composition 2002.
      • Frassetto L.A.
      • Todd K.M.
      • Morris Jr., R.C.
      • Sebastian A.
      Estimation of net endogenous noncarbonic acid production in humans from diet potassium and protein contents.
      was used to calculate the estimated net endogenous acid production (NEAP) based on the dietary protein-to-potassium ratio, expressed as grams per milliequivalent. The rationale and algorithm of this method have been described previously and the estimated NEAP could account for approximately 70% of the variation in renal net acid excretion.
      • Frassetto L.A.
      • Todd K.M.
      • Morris Jr., R.C.
      • Sebastian A.
      Estimation of net endogenous noncarbonic acid production in humans from diet potassium and protein contents.

      Bone Mineral Assessment

      BMD, bone mineral content (BMC), and bone area (BA) at whole-body, the total hip, lumbar spine (L1–L4), and femoral neck were measured by dual-energy X-ray absorptiometry (DXA) in a Hologic QDR-4500 W densitometer (Hologic, Waltham, MA). The coefficient of variation in our laboratory was 0.7%, 0.9%, and 1.3% at the total hip, the lumbar spine (L1–L4), and the femoral neck, respectively.
      • Lau E.M.
      • Leung P.C.
      • Kwok T.
      • et al.
      The determinants of bone mineral density in Chinese men—results from Mr. Os (Hong Kong), the first cohort study on osteoporosis in Asian men.
      DXA software (version 5.61; Hologic) was used for whole-body measurements (enhanced analysis), and the performance mode (version 4.47P) was used for spine and hip measurements. Quality assurance was performed daily, and long-term instrument stability was assessed 2 to 3 times per week.

      Covariates Measurements

      A standardized, structured questionnaire was administered by face-to-face interview to obtain demographic information, smoking habit, alcohol intake, physical activity, medical history, and use of calcium supplements. Physical activity was measured by a validated Physical Activity Scale for the Elderly Questionnaire.
      • Washburn R.A.
      • Smith K.W.
      • Jette A.M.
      • Janney C.A.
      The Physical Activity Scale for the Elderly (PASE): Development and evaluation.
      This is a 12-item scale measuring the average number of hours per day spent in leisure, household, and occupational physical activities over the previous 7-day period. A summary score of all the items reflects the daily physical activity level.
      Tobacco and alcohol consumptions were estimated by self-report using validated methods.
      • Lau E.M.
      • Chan H.H.
      • Woo J.
      • et al.
      Normal ranges for vertebral height ratios and prevalence of vertebral fracture in Hong Kong Chinese: A comparison with American Caucasians.
      Information on the duration and level of past and current use of cigarettes, cigars, and pipes was obtained. Smoking habit was classified in terms of former, current, or never smoking. Participants were asked to report their daily frequency of intake of alcohol and other beverages in portion sizes specified on the semiquantitative FFQ. Drinking status was defined as never, former, or current drinker.
      Body weight was measured to the nearest 0.1 kg with participants wearing a light gown, using the Physician Balance Beam Scale (Healthometer, Alsip, IL). Height was measured to the nearest 0.1 cm using the Holtain Harpenden standiometer (Holtain, Crosswell, UK). Body mass index (BMI) was calculated as body weight (kg)/height (m2). Parameters of body composition including body fat%, lean muscle mass, and fat mass were assessed by DXA.

      Statistical Analysis

      Data analysis was performed by using IBM SPSS Statistics, version 19.0 (IBM SPSS Statistics, IBM Corporation, Chicago, IL) software. To correct for skewed distributions and to examine proportional associations, all bone data and the dietary intakes of F&V were converted to natural logarithms. Independent sample t-test was used to examine the differences in general characteristics between men and women and χ2 tests were used for categorical variables. Univariate regression models were first carried out to assess the association between F&V consumption and bone mineral data (BMD, BMC, and BA) at the various bone sites. Multiple stepwise regression analyses were further constructed to examine whether the associations were independent after adjustment for potential confounders, including age, education, BMI, dietary total energy, smoking, alcohol and coffee drinking, scores of physical activities, calcium intake, years since menopause (women only), and ever estrogen or hormone usage (women only).
      Studies
      • Cole T.J.
      Sympercents: Symmetric percentage differences on the 100 log(e) scale simplify the presentation of log transformed data.
      have shown when regression analyses are carried out with the use of natural log-transformed data and when the independent variable is continuous, the regression coefficient multiplied by 100 will correspond closely to the percentage of change in the dependent variable associated with each 100% change in the independent variable, as defined by (difference/mean) × 100. Therefore, the results of the regression analyses in our study were presented as percentage coefficients.
      Because BMD may not be adequately corrected for bone and body size, models also were constructed in which BMC was adjusted for BA, height, weight, and the confounders listed previously (SA-BMC model
      • Prentice A.
      • Parsons T.J.
      • Cole T.J.
      Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants.
      ). Model variables were chosen based on their known or potential confounding effects on the relationship between F&V and bone, the review of literature, and results of univariate analyses. Results from the regression models are presented as mean (±SE) percentage coefficients. To avoid collinearity, fruits, vegetables, or their total intakes were separately forced into regression models. Significance level for entry and removal from the model were 0.05 and 0.10. To explore the potential mechanisms of F&V intakes on bone mass, univariate models were carried out to examine the association of bone mass parameters with dietary levels of acid load, vitamin C, and isoflavones.

      Results

      Table 1 shows the general characteristics of men and women and the summary statistics for BMC, BA, and BMD at various sites of both sexes. The mean age of the participants was 72.5 ± 5.2 years. Men were more likely to be smokers; drank more alcohol and coffee; had higher dietary nutrient or food intake; were more physically active; and had higher BMD, BMC, and BA at various sites than women.
      Table 1General Characteristics and Bone Mineral Status in Men and Women
      Men, n = 2000Women, n = 2000P Value
      Age, y72.4 ± 5.072.6 ± 5.4.254
      Education, university or above (%)271 (13.6)119 (6.0).000
      Smoking (%)
       No724 (36.2)1810 (90.5).000
       Past1038 (51.9)153 (7.7)
       Current238 (11.9)37 (1.9)
      Alcohol drinking (%)471 (23.6)51 (2.6).000
      Coffee drinking (%)563 (28.2)299 (15.0).000
      Chinese tea drinking (%)1696 (84.9)1502 (75.2).000
      Calcium supplements (%)193 (9.7)361 (18.1).000
      Age of first pregnancy, y24.5 ± 4.5NA
      Age of menopause, y48.9 ± 5.0NA
      Ever contraceptive use (%)388 (19.4)NA
      Ever estrogen use (%)64 (3.2)NA
      Current estrogen use (%)11 (5.5)NA
      Body weight, kg62.4 ± 9.454.5 ± 8.5.001
      Height, cm163.1 ± 5.7150.9 ± 5.3.001
      BMI, kg/m223.4 ± 3.123.9 ± 3.4.001
      Body fat percentage, %24.4 ± 4.934.6 ± 5.3.035
      Body lean muscle mass, kg44.2 ± 5.533.8 ± 4.1.000
      Body fat mass, kg15.3 ± 4.719.1 ± 5.2.000
      Dietary intakes
       Energy, kcal/d2099.5 ± 586.51583.1 ± 461.6.000
       Protein, g/d87.7 ± 35.365.3 ± 27.4.000
       Fat, g/d67.7 ± 24.548.6 ± 19.2.000
       Calcium, mg/d628.3 ± 297.6569.8 ± 267.1.000
       Vitamin C, mg/d160.0 ± 112.9154.1 ± 86.6.000
       Isoflavones, mg/d15.6 ± 23.112.6 ± 15.3.000
       Fruits, g/d274.8 ± 207.8247.0 ± 185.9.000
       Fruits ≥200 g/d (%)
      Reference intakes of fruits and vegetables were based on Chinese Dietary Guideline 2007 with 300∼500 g/d for vegetables and 200∼400 g/d for fruits.
      1209 (60.5)1099 (55.0).000
       Fruits ≥400 g/d (%)
      Reference intakes of fruits and vegetables were based on Chinese Dietary Guideline 2007 with 300∼500 g/d for vegetables and 200∼400 g/d for fruits.
      332 (16.6)231 (11.6).000
       Vegetables, g/d245.6 ± 167.1238.1 ± 153.4.001
       Vegetables ≥300 g/d (%)
      Reference intakes of fruits and vegetables were based on Chinese Dietary Guideline 2007 with 300∼500 g/d for vegetables and 200∼400 g/d for fruits.
      747 (37.4)646 (32.3).000
       Vegetables ≥500 g/d (%)
      Reference intakes of fruits and vegetables were based on Chinese Dietary Guideline 2007 with 300∼500 g/d for vegetables and 200∼400 g/d for fruits.
      199 (10.0)163 (8.2).000
       Fish, g/d92.8 ± 83.475.6 ± 74.6.000
       Legumes, seeds, and nuts, g/d46.6 ± 78.537.8 ± 39.4.000
       Soy foods, g/d53.9 ± 83.844.9 ± 52.6.000
       Milk and milk products, g/d39.4 ± 83.226.6 ± 58.9.000
      Physical activity, PASE
       Total score97.3 ± 50.385.4 ± 33.2.000
       Works48.0 ± 38.945.5 ± 23.2.000
       Sports10.4 ± 12.710.5 ± 10.6.000
       Leisure, walking34.2 ± 21.627.3 ± 17.8.000
      Bone mineral status
       Whole body
      BMD, g/cm21.064 ± 0.1010.906 ± 0.094.000
      BMC, g2060.5 ± 331.61446.3 ± 263.7.000
      BA, cm21927.9 ± 167.71587.1 ± 165.4.000
       Spine
      BMD, g/cm20.951 ± 0.1800.753 ± 0.148.000
      BMC, g54.8 ± 16.535.6 ± 11.3.000
      BA, cm251.2 ± 7.641.7 ± 7.4.000
       Femoral neck
      BMD, g/cm20.688 ± 0.1110.584 ± 0.100.000
      BMC, g3.7 ± 0.62.8 ± 0.5.000
      BA, cm25.3 ± 0.34.7 ± 0.3.000
       Hip
      BMD, g/cm20.864 ± 0.1280.709 ± 0.117.000
      BMC, g33.6 ± 6.022.6 ± 4.4.000
      BA, cm238.9 ± 3.531.8 ± 2.8.000
      Data are presented as mean ± SD or n (%). Independent t-test for continuous variables and χ2 test for categorical variables. Physical activity was measured by a validated Physical Activity Scale for the Elderly Questionnaire (PASE). Dietary fruit and vegetable intakes were assessed from a validated food frequency questionnaire. Bone mineral parameters at various sites were measured by DXA in a Hologic QDR-4500 W densitometer.
      NA, not applicable.
      Reference intakes of fruits and vegetables were based on Chinese Dietary Guideline 2007 with 300∼500 g/d for vegetables and 200∼400 g/d for fruits.
      The arithmetic mean, median, and interquartile range for intakes of fruits, vegetables, and total F&V by men and women are shown in Table 2. The mean intakes of F&V were 132.5 and 140.5 g/1000 kcal/d for men and 155.9 and 175.0 g/1000 kcal/d for women, respectively.
      Table 2Daily Intakes of Fruits and Vegetables in Men and Women
      Fruits, g/1000 kcalVegetables, g/1000 kcalTotal Fruits and Vegetables, g/1000 kcal
      MeanMedianIQRMeanMedianIQRMeanMedianIQR
      Men, n = 1998132.5 ± 88.5116.688.5140.5 ± 86.7124.285.7273.0 ± 132.4251.5142.7
      Women, n = 1997155.9 ± 95.2142.3100.1175.0 ± 93.4157.292.8331.0 ± 143.0310.3156.6
      Total144.2 ± 92.6128.597.6157.8 ± 91.7141.392.3302.0 ± 140.8281.6155.3
      IQR, interquartile range.
      Dietary fruit and vegetable intakes were assessed from a validated food frequency questionnaire.
      The univariate associations between bone mass and intakes of fruit, vegetables, and total F&V in men and women are shown in Table 3. Significant and positive associations were observed with fruits and total F&V intake at nearly all skeletal sites in both sexes, but not with vegetable intake. In the multivariate regression models (Table 4), whole-body and femoral neck BMD and BMC were positively associated with fruit intake in both men and women after controlling for potential covariates. In women, whole-body SA-BMC, spine BMD, and BMC were also significantly and positively associated with fruit intake. A daily increase of 100 g/kcal fruit intake was associated with 4.5% and 6.4% increase in BMD at whole body, 3.9% and 4.8% increase in femoral neck in men and women, respectively. No significant association was observed between vegetable intake and bone parameters in various sites in both sexes.
      Table 3Results of Univariate Analysis Between Bone Mineral Status at Various Sites and Dietary Fruit, Vegetable, and Total Fruit and Vegetable Intakes in Men and Women
      FruitsVegetablesTotal Fruits and Vegetables
      MenWomenMenWomenMenWomen
      n199219641996197219961972
      Whole body
       BMD, g/cm26.7 ± 0.38.0 ± 0.31.3 ± 0.40.8 ± 0.56.1 ± 0.46.3 ± 0.5
       BMC, g8.0 ± 0.57.4 ± 0.62.5 ± 0.72.7 ± 0.97.7 ± 0.86.9 ± 1.0
       BA, cm27.6 ± 0.35.3 ± 0.43.2 ± 0.43.9 ± 0.57.7 ± 0.46.1 ± 0.6
      Spine
       BMD, g/cm27.7 ± 0.67.3 ± 0.71.4 ± 0.81.3 ± 0.96.9 ± 0.95.6 ± 1.1
       BMC, g7.6 ± 0.97.0 ± 0.10.7 ± 1.2−0.6 ± 1.56.2 ± 1.44.3 ± 1.7
       BA, cm24.6 ± 0.55.4 ± 0.61.7 ± 0.6−1.2 ± 0.95.0 ± 0.73.1 ± 1.0
      Total hip
       BMD, g/cm28.3 ± 0.55.7 ± 0.63.3 ± 0.63.4 ± 0.88.3 ± 0.75.4 ± 0.9
       BMC, g7.1 ± 0.64.1 ± 0.72.2 ± 0.82.2 ± 0.97.5 ± 0.93.7 ± 1.1
       BA, cm20.3 ± 0.3−1.6 ± 0.3−1.3 ± 0.4−1.7 ± 0.40.9 ± 0.4−2.1 ± 0.5
      Femoral neck
       BMD, g/cm27.6 ± 0.56.0 ± 0.62.5 ± 0.72.9 ± 0.87.3 ± 0.85.2 ± 0.9
       BMC, g7.8 ± 0.55.8 ± 0.62.8 ± 0.72.9 ± 0.87.7 ± 0.85.5 ± 0.9
       BA, cm21 ± 0.20.4 ± 0.20.1 ± 0.30.5 ± 0.31.8 ± 0.31.4 ± 0.3
      All values are x¯ ± SE (% standardized coefficients B and SE). Intakes were assessed from food frequency questionnaire. The % coefficient is the percentage of change in the dependent variable associated with each 100% change in the independent variable. Analysis was by univariate linear regression. Bone mineral and area measurements in elderly men and women were made by using Hologic QDR 1000 W BXA. Bone parameters and fruit and vegetable intakes were natural log transformed. Significance for univariate associations: *P ≤ .01, P ≤ .05.
      Table 4Results of Multivariate Analyses on Associations of Bone Mineral Status at Various Sites and Fruits, Vegetables, and Combined Fruit and Vegetable Intakes in Men and Women
      FruitsVegetablesTotal Fruits and Vegetables
      MenWomenMenWomenMenWomen
      n199219641996197219961972
      Whole body
       BMD, g/cm24.5 ± 0.36.4 ± 0.3−1.5 ± 0.4−1.2 ± 0.52.5 ± 0.43.8 ± 0.5
       BMC, g4.0 ± 0.55.5 ± 0.5−1.9 ± 0.60.1 ± 0.82.0 ± 0.73.9 ± 0.9
       SA-BMC, g1.0 ± 0.22.1 ± 0.2−0.5 ± 0.3−1.1 ± 0.40.5 ± 0.31.2 ± 0.4
      Spine
       BMD, g/cm23.4 ± 0.55.2 ± 0.6−1.5 ± 0.4−0.1 ± 0.81.8 ± 0.83.3 ± 1.0
       BMC, g3.9 ± 0.95.1 ± 1.0−1.9 ± 0.6−2.1 ± 1.41.5 ± 1.32.1 ± 1.6
       SA-BMC, g1.6 ± 0.72.4 ± 0.8−2.2 ± 0.70.1 ± 0.70.3 ± 0.81.1 ± 0.8
      Total hip
       BMD, g/cm23.5 ± 0.43.2 ± 0.5−0.2 ± 0.50.4 ± 0.72.8 ± 0.72.1 ± 0.8
       BMC, g2.3 ± 0.51.8 ± 0.6−1.8 ± 0.70.3 ± 0.82.5 ± 0.72.9 ± 0.8
       SA-BMC, g0 ± 0.3−0.9 ± 0.4−0.6 ± 0.5−0.7 ± 0.72.1 ± 0.60.8 ± 0.9
      Femoral neck
       BMD, g/cm23.9 ± 0.54.8 ± 0.5−0.6 ± 0.60.1 ± 0.73.1 ± 0.62.0 ± 0.8
       BMC, g3.9 ± 0.53.9 ± 0.5−1.4 ± 0.60.6 ± 0.72.0 ± 0.70.7 ± 0.9
       SA-BMC, g1.3 ± 0.31.6 ± 0.4−1.1 ± 0.60.4 ± 0.72.4 ± 0.62.9 ± 0.8
      All values are x¯ ± SE (% standardized coefficients B and SE). Intakes were assessed from food frequency questionnaires. The % coefficient is the percentage of change in the dependent variable associated with each 100% change in the independent variable. Analysis was by stepwise multivariate linear regression. Bone mineral and area measurements in elderly men and women were made by using Hologic QDR 1000 W DXA. Bone parameters and fruit and vegetable intakes were natural log transformed. Significance for multivariate associations: P ≤ .01, P ≤ .05.
      Adjusted variables for elderly men included age, education level, BMI, body fat%, current use of provera, calcium intake, smoking, alcohol use, energy intake, coffee intake, PASE total scores, and calcium supplement use. For elderly women, further adjustment was made for age at menopause, ever use of contraceptive drugs, current use of estrogen or provera. For the multivariate analysis models of SA-BMC, further adjustment was made for height, weight, and BA.
      The univariate associations between dietary acid load, vitamin C, and isoflavone intake with bone mineral parameters are shown in Table 5. Significant and positive associations were found between dietary vitamin C intake and bone mineral status at whole body, total hip, and femoral neck in both sexes. In men, but not women, isoflavone intake was positively associated with BMC in total hip and BA at whole body and spine. There were no significant associations between dietary acid-base and bone mineral parameters. The adjustment for vitamin C intake attenuated the association between fruits and BMD in multivariate regression models; however, little change was observed with adjustment for dietary acid load and isoflavones (data not shown).
      Table 5Results of Univariate Analysis Between Bone Mineral Status at Various Sites and Dietary Acid Load, Vitamin C, and Isoflavone Intake in Elderly Men and Women
      Dietary Acid LoadVitamin CIsoflavones
      MenWomenMenWomenMenWomen
      n199219641992196419921964
      Whole body
       BMD, g/cm20.7 ± 0.50.3 ± 0.55.3 ± 0.46.2 ± 0.4−1.3 ± 0.23.5 ± 0.2
       BMC, g2.6 ± 0.8−1.7 ± 0.98.2 ± 0.67.9 ± 0.81.9 ± 0.43.5 ± 0.4
       Area, cm24 ± 0.5−2.6 ± 0.59.5 ± 0.37.7 ± 0.54.9 ± 0.22.7 ± 0.2
      Spine
       BMD, g/cm22.9 ± 1.0−1.9 ± 0.93.3 ± 0.73.2 ± 0.82.2 ± 0.43.8 ± 0.4
       BMC, g2.9 ± 1.5−2.6 ± 1.54.5 ± 1.13.1 ± 1.43.4 ± 0.63.0 ± 0.7
       Area, cm22.4 ± 0.80 ± 0.95.5 ± 0.62.9 ± 0.84.6 ± 0.33.7 ± 0.4
      Total hip
       BMD, g/cm20.9 ± 0.80.6 ± 0.88.0 ± 0.66.1 ± 0.73.4 ± 0.34.1 ± 0.4
       BMC, g2.4 ± 0.91.3 ± 0.98.1 ± 0.75.1 ± 0.84.5 ± 0.44.1 ± 0.4
       Area, cm23.3 ± 0.51.7 ± 0.42.6 ± 0.30.2 ± 0.43.2 ± 0.21.6 ± 0.2
      Femoral neck
       BMD, g/cm2−0.3 ± 0.8−1.0 ± 0.86.8 ± 0.66.2 ± 0.72.1 ± 0.43.1 ± 0.4
       BMC, g0.5 ± 0.9−1.7 ± 0.87.2 ± 0.76.5 ± 0.83.2 ± 0.42.9 ± 0.4
       Area, cm21.8 ± 0.3−1.1 ± 0.31.9 ± 0.22.6 ± 0.32.8 ± 0.10.6 ± 0.1
      All values are expressed as x ± SE (% coefficient). The percentage coefficient is the percentage of change in the dependent variable associated with each 100% change in the independent variable. Acid base, vitamin C, and isoflavone intakes were assessed from food frequency questionnaires. Significant for univariate association (linear regression): P ≤ .01, P ≤ .05.

      Discussion

      The results of this study showed that greater fruit intake was independently associated with increased bone mineral status in Chinese elderly men and women. We found that a daily increase of 100 g/1000 kcal fruit intake was associated with a 4.5% and 6.4% BMD increase in whole body, and 3.9% and 4.8% in femoral neck in men and women, respectively. Greater fruit intake may be a low-cost but beneficial way to prevent bone loss in the elderly Chinese population.
      It was estimated that a 1% improvement in femoral neck BMD was associated with a 3% decrease in vertebral fracture.
      • Cummings S.R.
      • Karpf D.B.
      • Harris F.
      • et al.
      Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs.
      The observed change at femoral neck (3.9% and 4.8% for men and women) with increase of 100 g/1000 kcal fruit intake in the present study could translate to 11.7% and 14.4% reduction in fractures in men and women. This magnitude may thus be of substantial clinical and public health importance. Our results also showed that although beneficial effects with fruit intake were present in both sexes, women had a relatively greater increase of bone mass than men. This is an important finding considering the overall higher age-adjusted risk of osteoporosis in women, implying a larger potential of bone health improvement in women than in men.

      The F&V Intake Among Hong Kong Chinese Elderly Men and Women

      In general, a typical Chinese diet comprises higher components of vegetables and fruits, and lower intake of animal foods than a Western diet.
      • Li Y.
      • Li D.
      • Ma C.Y.
      • et al.
      Consumption of, and factors influencing consumption of, fruit and vegetables among elderly Chinese people.
      The Chinese Dietary Guideline 2007
      • Chinese Nutrition Society
      Chinese Dietary Guideline 2007.
      recommended daily consumption of approximately 300 to 500 g vegetables and 200 to 400 g/d of fruits. Our findings in Chinese elderly indicated that quite a portion of men and women (39.5% and 45.0%) had fruit intake lower than 200 g/d, and approximately two-thirds (62.6% and 67.7%) had vegetable intake less than 300 g/d. F&V are important components of a healthy diet. Our data suggested room for improvement of F&V consumption in Chinese elderly. However, in comparison with 2009 China Health and Nutrition Surveys,
      • Li Y.
      • Li D.
      • Ma C.Y.
      • et al.
      Consumption of, and factors influencing consumption of, fruit and vegetables among elderly Chinese people.
      our elderly participants had remarkably higher fruit intake (260.9 vs 50.6 g/d
      • Li Y.
      • Li D.
      • Ma C.Y.
      • et al.
      Consumption of, and factors influencing consumption of, fruit and vegetables among elderly Chinese people.
      ) but slightly lower vegetable intake (284 vs 328 g/d
      • Li Y.
      • Li D.
      • Ma C.Y.
      • et al.
      Consumption of, and factors influencing consumption of, fruit and vegetables among elderly Chinese people.
      ) than those of nationally representative samples of similar age. The relatively high fruit intake and wide interquartile range might be one of the reasons of a significant association of fruits intake and bone mass in our study.

      Compared With Other Studies

      The positive association between fruits and bone mass observed in our study is in agreement with previous observational studies in early pubertal children and adolescents,
      • Macdonald H.M.
      • New S.A.
      • Golden M.H.
      • et al.
      Nutritional associations with bone loss during the menopausal transition: Evidence of a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients and of a detrimental effect of fatty acids.
      • Vatanparast H.
      • Baxter-Jones A.
      • Faulkner R.A.
      • et al.
      Positive effects of vegetable and fruit consumption and calcium intake on bone mineral accrual in boys during growth from childhood to adolescence: The University of Saskatchewan Pediatric Bone Mineral Accrual Study.
      peri- and postmenopausal women,
      • New S.A.
      • Robins S.P.
      • Campbell M.K.
      • et al.
      Dietary influences on bone mass and bone metabolism: Further evidence of a positive link between fruit and vegetable consumption and bone health?.
      • Macdonald H.M.
      • New S.A.
      • Reid D.M.
      Longitudinal changes in dietary intake in Scottish women around the menopause: Changes in dietary pattern result in minor changes in nutrient intake.
      and elderly white adults,
      • Tucker K.L.
      • Hannan M.T.
      • Chen H.
      • et al.
      Potassium, magnesium, and fruit and vegetable intakes are associated with greater bone mineral density in elderly men and women.
      but not all.
      • Monma Y.
      • Niu K.
      • Iwasaki K.
      • et al.
      Dietary patterns associated with fall-related fracture in elderly Japanese: A population based prospective study.
      • Kaptoge S.
      • Welch A.
      • McTaggart A.
      • et al.
      Effects of dietary nutrients and food groups on bone loss from the proximal femur in men and women in the 7th and 8th decades of age.
      • Benetou V.
      • Orfanos P.
      • Zylis D.
      • et al.
      Diet and hip fractures among elderly Europeans in the EPIC cohort.
      The null association could be due to the relatively weak effect of F&Vs, limited study size, large random error in the assessment of long-term intake of F&V, potential regression dilution bias in cohort studies, or other environmental and genetic heterogeneity in populations.
      In this study, we were unable to show a significant relation between vegetable intake and bone mass. The lack of association may be due to the relatively small quantities and limited consumption variability of vegetables in the present study. Vegetable intake is possibly underestimated, because vegetables included in some composite dishes may not be adequately accounted for. In addition, it is well established that sodium intake accelerates calcium excretion.
      • Woo J.
      • Kwok T.
      • Leung J.
      • Tang N.
      Dietary intake, blood pressure and osteoporosis.
      Vegetables are often consumed in cooked form with salt being added in Chinese cuisine. Thus, the intake of sodium with vegetables might offset the benefit of vegetables
      • Anderson C.A.
      • Appel L.J.
      • Okuda N.
      • et al.
      Dietary sources of sodium in China, Japan, the United Kingdom, and the United States, women and men aged 40 to 59 years: The INTERMAP study.
      as compared with fruits, which mainly are consumed fresh. Furthermore, the typical cooking practices for vegetables in Chinese elderly were stir-frying, boiling, or steaming, which may lead to the substantial loss of water-soluble, heat-sensitive, and oxygen-labile nutrients
      • Rickman J.C.
      • Barrett D.M.
      • Bruhn C.M.
      Nutritional comparison of fresh, frozen and canned fruits and vegetables. Part 1. Vitamins C and B and phenolic compounds.
      (vitamins C, K and so forth) and further attenuate the association of dietary vegetables and bone health.

      Dietary Acid Load and BMD

      Previous studies have proposed several mechanisms by which F&V improve bone health.
      • Lampe J.W.
      Health effects of vegetables and fruit: Assessing mechanisms of action in human experimental studies.
      The most important theory might be the acid-based hypothesis in which an acidic environment leads to progressive bone loss.
      • Brandao-Burch A.
      • Utting J.C.
      • Orriss I.R.
      • Arnett T.R.
      Acidosis inhibits bone formation by osteoblasts in vitro by preventing mineralization.
      • Macdonald H.M.
      • New S.A.
      • Fraser W.D.
      • et al.
      Low dietary potassium intakes and high dietary estimates of net endogenous acid production are associated with low bone mineral density in premenopausal women and increased markers of bone resorption in postmenopausal women.
      Our separate analysis did not find a significant relation between dietary acid load and bone mineral parameters in men and women, and adjustment of acid load level had little alteration in the associations of F&V intakes and bone. Thus, the positive association between fruit intake and bone in our participants might not be related to a more alkaline environment from fruit consumption.
      The extent to which the dietary net acid load contributes to bone mass is still unknown and findings are inconsistent. Our findings were consistent with several observational studies that null associations were observed between diet net acid load and bone measurement.
      • Ginty F.P.C.
      • Muniz-Terrera G.
      • Mishra G.D.
      • et al.
      No evidence for a negative association between bone mineral status and indirect estimates of renal net acid excretion in adolescents.
      • Wynn E.
      • Lanham-New S.A.
      • Krieg M.A.
      • et al.
      Low estimates of dietary acid load are positively associated with bone ultrasound in women older than 75 years of age with a lifetime fracture.
      Although NEAP was significantly and negatively associated with fruit intakes (r = −0.211, P < .001) in our study, other nutrients or food components, such as animal protein, cereals, and calcium, also may affect acid balance.
      • Gannon R.H.
      • Millward D.J.
      • Brown J.E.
      • et al.
      Estimates of daily net endogenous acid production in the elderly UK population: Analysis of the National Diet and Nutrition Survey (NDNS) of British adults aged 65 years and over.
      The negative association between dietary acid load with bone also might be explained in part by decreased excretion of metabolic acids due to the normal decline in renal function with aging.
      • Bushinsky D.A.
      Acid-base imbalance and the skeleton.
      In addition, the lack of association might reflect the measurement error in dietary potassium or protein intake, inherent in assessing diet acid load by FFQ.
      • Smith-Warner S.A.
      • Elmer P.J.
      • Fosdick L.
      • et al.
      Reliability and comparability of three dietary assessment methods for estimating fruit and vegetable intakes.

      Mechanisms of Fruit Intake on Bone Health

      The mechanism whereby fruit may affect bone is not clear. F&V are rich sources of antioxidant vitamins, such as vitamins C and K and β-carotene, which are involved in the synthesis of bone matrix.
      • Tucker K.L.
      Osteoporosis prevention and nutrition.
      These could act by combating oxidative stress, which has been shown to be negatively associated with BMD in adults.
      • Basu S.
      • Michaelsson K.
      • Olofsson H.
      • et al.
      Association between oxidative stress and bone mineral density.
      Vitamin C also has an essential regulatory role in osteoblast differentiation and collagen formation and therefore may positively influence bone health.
      • Franceschi R.T.
      • Iyer B.S.
      • Cui Y.
      Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3–E1 cells.
      Additionally, phytochemicals, including phytoestrogens present in fruits could protect bone by quenching oxidative stress
      • Tucker K.L.
      Osteoporosis prevention and nutrition.
      • Hunter D.C.
      • Skinner M.A.
      • Lister C.E.
      Impact of phytochemicals on maintaining bone and joint health.
      or imitating the estrogen effects via estrogen receptors.
      • Arjmandi B.H.
      • Smith B.J.
      Soy isoflavones' osteoprotective role in postmenopausal women: Mechanism of action.
      Additionally, high F&V intake may be a surrogate measure of multiple healthy lifestyle characteristics that are beneficial for bones. However, the results remained similar even when adjustment for possible confounding variables in our analyses was made, suggesting an independent effect of fruits on bone.

      Strengths

      The present study has several strengths, including the relatively large sample size and the comprehensive measurement of bone mineral parameters at various sites and extensive collection of potential confounders. Dietary intake was assessed using a validated FFQ with good validity and reliability in the assessment of habitual intake of F&Vs in this population. The study also determined the dietary acid load, and vitamin C and isoflavone levels for exploring the potential mechanisms. In addition, the analyses treating F&V intake as a continuous variable tended to have more power than categorical analyses.

      Limitations

      Our study has some limitations. First, the study was cross-sectional in design, thus causal relationship may not be addressed. However, adults generally maintain relatively stable dietary habits over a long period.
      • Macdonald H.M.
      • New S.A.
      • Reid D.M.
      Longitudinal changes in dietary intake in Scottish women around the menopause: Changes in dietary pattern result in minor changes in nutrient intake.
      In addition, the general population is not expected to have sophisticated awareness of the potential influence of F&V on bone health, and bone mineral measures were not extensively examined among Chinese elderly. Thus, the reversal relationship between F&V and bone seems unlikely. In addition, the exclusion of those with medication for treatment of osteoporosis (n = 5 and 36 for men and women) did not alter the results, suggesting the validity of the relationship between F&V consumption and bone mass.
      Second, as in most nutritional epidemiological studies, the misclassification of dietary intake may have occurred because of inaccurate self-reporting. However, this would bias the results only toward the null. Third, although we adjusted for a number of confounders, we may not fully rule out residual confounding by unmeasured or unadjusted factors. Further investigations based on a randomized controlled trial would be necessary to confirm the beneficial effects of fruits on bone health. Finally, our participants had a higher education level (12%–18% vs 3%–9%
      Department of Census and Statistics
      Hong Kong 2006 Population Bycensus Thematic Report: Older Persons.
      with tertiary education), the results thus may not be entirely generalizable to other populations. Nevertheless, to our knowledge, this is the largest report on the associations of F&V intake with bone health among elderly Chinese adults with a population-based design.

      Conclusions

      Our findings in Chinese elderly men and women showed that greater fruit intakes were associated with better bone mineral status. The specific mechanism remains to be determined, but vitamin C may play a role. Intervention studies are necessary to clarify the effect of F&V intake on bone health.

      Acknowledgments

      We are grateful to all of our participants.

      References

        • Reginster J.Y.
        • Burlet N.
        Osteoporosis: A still increasing prevalence.
        Bone. 2006; 38: S4-S9
        • Cooper C.
        • Campion G.
        • Melton 3rd, L.J.
        Hip fractures in the elderly: A world-wide projection.
        Osteoporos Int. 1992; 2: 285-289
        • Lau E.M.
        • Lee J.K.
        • Suriwongpaisal P.
        • et al.
        The incidence of hip fracture in four Asian countries: The Asian Osteoporosis Study (AOS).
        Osteoporos Int. 2001; 12: 239-243
        • Recker R.R.
        Clinical review 41: Current therapy for osteoporosis.
        J Clin Endocrinol Metab. 1993; 76: 14-16
        • Cashman K.D.
        Diet, nutrition, and bone health.
        J Nutr. 2007; 137: 2507S-2512S
        • Tucker K.L.
        • Hannan M.T.
        • Chen H.
        • et al.
        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
        • Trzeciakiewicz A.
        • Habauzit V.
        • Horcajada M.N.
        When nutrition interacts with osteoblast function: Molecular mechanisms of polyphenols.
        Nutr Res Rev. 2009; 22: 68-81
        • Tucker K.L.
        Osteoporosis prevention and nutrition.
        Curr Osteoporos Rep. 2009; 7: 111-117
        • Brandao-Burch A.
        • Utting J.C.
        • Orriss I.R.
        • Arnett T.R.
        Acidosis inhibits bone formation by osteoblasts in vitro by preventing mineralization.
        Calcif Tissue Int. 2005; 77: 167-174
        • New S.A.
        Intake of fruit and vegetables: Implications for bone health.
        Proc Nutr Soc. 2003; 62: 889-899
        • Xie H.L.
        • Wu B.H.
        • Xue W.Q.
        • et al.
        Greater intake of fruit and vegetables is associated with a lower risk of osteoporotic hip fractures in elderly Chinese: A 1:1 matched case-control study.
        Osteoporos Int. 2013; 24: 2827-2836
        • New S.A.
        • Robins S.P.
        • Campbell M.K.
        • et al.
        Dietary influences on bone mass and bone metabolism: Further evidence of a positive link between fruit and vegetable consumption and bone health?.
        Am J Clin Nutr. 2000; 71: 142-151
        • Macdonald H.M.
        • New S.A.
        • Golden M.H.
        • et al.
        Nutritional associations with bone loss during the menopausal transition: Evidence of a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients and of a detrimental effect of fatty acids.
        Am J Clin Nutr. 2004; 79: 155-165
        • Prynne C.J.
        • Mishra G.D.
        • O'Connell M.A.
        • et al.
        Fruit and vegetable intakes and bone mineral status: A cross sectional study in 5 age and sex cohorts.
        Am J Clin Nutr. 2006; 83: 1420-1428
        • Monma Y.
        • Niu K.
        • Iwasaki K.
        • et al.
        Dietary patterns associated with fall-related fracture in elderly Japanese: A population based prospective study.
        BMC Geriatr. 2010; 10: 31
        • Kaptoge S.
        • Welch A.
        • McTaggart A.
        • et al.
        Effects of dietary nutrients and food groups on bone loss from the proximal femur in men and women in the 7th and 8th decades of age.
        Osteoporos Int. 2003; 14: 418-428
        • Benetou V.
        • Orfanos P.
        • Zylis D.
        • et al.
        Diet and hip fractures among elderly Europeans in the EPIC cohort.
        Eur J Clin Nutr. 2011; 65: 132-139
        • Lin P.H.
        • Ginty F.
        • Appel L.J.
        • et al.
        The DASH diet and sodium reduction improve markers of bone turnover and calcium metabolism in adults.
        J Nutr. 2003; 133: 3130-3136
        • Macdonald H.M.
        • Black A.J.
        • Aucott L.
        • et al.
        Effect of potassium citrate supplementation or increased fruit and vegetable intake on bone metabolism in healthy postmenopausal women: A randomized controlled trial.
        Am J Clin Nutr. 2008; 88: 465-474
        • Hamidi M.
        • Boucher B.A.
        • Cheung A.M.
        • et al.
        Fruit and vegetable intake and bone health in women aged 45 years and over: A systematic review.
        Osteoporos Int. 2011; 22: 1681-1693
        • Chan R.
        • Leung J.
        • Woo J.
        No association between dietary vitamin K intake and fracture risk in Chinese community-dwelling older men and women: A prospective study.
        Calcif Tissue Int. 2012; 90: 396-403
        • Woo J.
        • Leung S.S.F.
        • Ho S.C.
        • et al.
        A food frequency questionnaire for use in the Chinese population in Hong Kong: Description and examination of validity.
        Nutr Res. 1997; 17: 1633-1641
        • Paul A.A.
        • Soughgate D.A.T.
        McCance & Widdowson’s: The composition of Foods.
        HMSO, London1978
        • Yang Y.
        • Wang G.
        • Pan X.
        China Food Composition 2002.
        University Medical, Peking2002
        • Frassetto L.A.
        • Todd K.M.
        • Morris Jr., R.C.
        • Sebastian A.
        Estimation of net endogenous noncarbonic acid production in humans from diet potassium and protein contents.
        Am J Clin Nutr. 1998; 68: 576-583
        • Lau E.M.
        • Leung P.C.
        • Kwok T.
        • et al.
        The determinants of bone mineral density in Chinese men—results from Mr. Os (Hong Kong), the first cohort study on osteoporosis in Asian men.
        Osteoporos Int. 2006; 17: 297-303
        • Washburn R.A.
        • Smith K.W.
        • Jette A.M.
        • Janney C.A.
        The Physical Activity Scale for the Elderly (PASE): Development and evaluation.
        J Clin Epidemiol. 1993; 46: 153-162
        • Lau E.M.
        • Chan H.H.
        • Woo J.
        • et al.
        Normal ranges for vertebral height ratios and prevalence of vertebral fracture in Hong Kong Chinese: A comparison with American Caucasians.
        J Bone Miner Res. 1996; 11: 1364-1368
        • Cole T.J.
        Sympercents: Symmetric percentage differences on the 100 log(e) scale simplify the presentation of log transformed data.
        Stat Med. 2000; 19: 3109-3125
        • Prentice A.
        • Parsons T.J.
        • Cole T.J.
        Uncritical use of bone mineral density in absorptiometry may lead to size-related artifacts in the identification of bone mineral determinants.
        Am J Clin Nutr. 1994; 60: 837-842
        • Cummings S.R.
        • Karpf D.B.
        • Harris F.
        • et al.
        Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs.
        Am J Med. 2002; 112: 281-289
        • Li Y.
        • Li D.
        • Ma C.Y.
        • et al.
        Consumption of, and factors influencing consumption of, fruit and vegetables among elderly Chinese people.
        Nutrition. 2012; 28: 504-508
        • Chinese Nutrition Society
        Chinese Dietary Guideline 2007.
        Chinese Ministry of Health, Bejing China2007
        • Vatanparast H.
        • Baxter-Jones A.
        • Faulkner R.A.
        • et al.
        Positive effects of vegetable and fruit consumption and calcium intake on bone mineral accrual in boys during growth from childhood to adolescence: The University of Saskatchewan Pediatric Bone Mineral Accrual Study.
        Am J Clin Nutr. 2005; 82: 700-706
        • Macdonald H.M.
        • New S.A.
        • Reid D.M.
        Longitudinal changes in dietary intake in Scottish women around the menopause: Changes in dietary pattern result in minor changes in nutrient intake.
        Public Health Nutr. 2005; 8: 409-416
        • Woo J.
        • Kwok T.
        • Leung J.
        • Tang N.
        Dietary intake, blood pressure and osteoporosis.
        J Hum Hypertens. 2009; 23: 451-455
        • Anderson C.A.
        • Appel L.J.
        • Okuda N.
        • et al.
        Dietary sources of sodium in China, Japan, the United Kingdom, and the United States, women and men aged 40 to 59 years: The INTERMAP study.
        J Am Diet Assoc. 2010; 110: 736-745
        • Rickman J.C.
        • Barrett D.M.
        • Bruhn C.M.
        Nutritional comparison of fresh, frozen and canned fruits and vegetables. Part 1. Vitamins C and B and phenolic compounds.
        J Sci Food Agric. 2007; 87: 930-944
        • Lampe J.W.
        Health effects of vegetables and fruit: Assessing mechanisms of action in human experimental studies.
        Am J Clin Nutr. 1999; 70: 475S-490S
        • Macdonald H.M.
        • New S.A.
        • Fraser W.D.
        • et al.
        Low dietary potassium intakes and high dietary estimates of net endogenous acid production are associated with low bone mineral density in premenopausal women and increased markers of bone resorption in postmenopausal women.
        Am J Clin Nutr. 2005; 81: 923-933
        • Ginty F.P.C.
        • Muniz-Terrera G.
        • Mishra G.D.
        • et al.
        No evidence for a negative association between bone mineral status and indirect estimates of renal net acid excretion in adolescents.
        Proc Nutr Soc. 2005; 64: 80A
        • Wynn E.
        • Lanham-New S.A.
        • Krieg M.A.
        • et al.
        Low estimates of dietary acid load are positively associated with bone ultrasound in women older than 75 years of age with a lifetime fracture.
        J Nutr. 2008; 138: 1349-1354
        • Gannon R.H.
        • Millward D.J.
        • Brown J.E.
        • et al.
        Estimates of daily net endogenous acid production in the elderly UK population: Analysis of the National Diet and Nutrition Survey (NDNS) of British adults aged 65 years and over.
        Br J Nutr. 2008; 100: 615-623
        • Bushinsky D.A.
        Acid-base imbalance and the skeleton.
        Eur J Nutr. 2001; 40: 238-244
        • Smith-Warner S.A.
        • Elmer P.J.
        • Fosdick L.
        • et al.
        Reliability and comparability of three dietary assessment methods for estimating fruit and vegetable intakes.
        Epidemiology. 1997; 8: 196-201
        • Basu S.
        • Michaelsson K.
        • Olofsson H.
        • et al.
        Association between oxidative stress and bone mineral density.
        Biochem Biophys Res Commun. 2001; 288: 275-279
        • Franceschi R.T.
        • Iyer B.S.
        • Cui Y.
        Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3–E1 cells.
        J Bone Miner Res. 1994; 9: 843-854
        • Hunter D.C.
        • Skinner M.A.
        • Lister C.E.
        Impact of phytochemicals on maintaining bone and joint health.
        Nutrition. 2008; 24: 390-392
        • Arjmandi B.H.
        • Smith B.J.
        Soy isoflavones' osteoprotective role in postmenopausal women: Mechanism of action.
        J Nutr Biochem. 2002; 13: 130-137
        • Department of Census and Statistics
        Hong Kong 2006 Population Bycensus Thematic Report: Older Persons.
        2006 (Available at:) (Accessed December 9, 2014)