This Article Abstract Full Text (PDF) Submit a related Letter to the Editor Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Copyright Permission Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ho, S. C. Articles by Lam, S. S. H. Search for Related Content PubMed PubMed Citation Articles by Ho, S. C. Articles by Lam, S. S. H.

High Habitual Calcium Intake Attenuates Bone Loss in Early Postmenopausal Chinese Women: An 18-Month Follow-Up Study

Departments of Community and Family Medicine (S.C.H., Y.-M.C., S.S.H.L.) and Medicine and Therapeutics (J.L.F.W.), Chinese University of Hong Kong, Hong Kong SAR, People’s Republic of China; and School of Public Health, Sun Yat-sen University (Y.-M.C.), 510080 Guangzhou, People’s Republic of China

Address all correspondence and requests for reprints to: Dr. Suzanne C. Ho, Department of Community and Family Medicine, Chinese University of Hong Kong, 4th Floor, School of Public Health, Prince of Wales Hospital, Shatin, N.T., Hong Kong SAR, People’s Republic of China. E-mail: suzanneho{at}cuhk.edu.hk.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
This study assessed the association of habitual dietary calcium intake and bone loss in early postmenopausal women. Four hundred fifty-four healthy postmenopausal Chinese women were enrolled for this 18-month cohort study. The subjects were 48–62 yr of age and within 12 yr of natural menopause. Dietary intake was assessed by the food frequency method, and bone mass was measured using dual energy x-ray absorptiometry at baseline and 9 and 18 months. The association between mean habitual dietary intake over the follow-up period and the rate of bone loss was examined. During the 18-month follow-up, the total loss rates of BMD at the whole body, lumber spine, femoral neck, and total hip were 1.28, 0.60, 1.54, and 0.56% (all P < 0.01). Subjects were stratified into four quartiles according to calcium intake during the period of follow-up. Quartiles I–IV had median intakes of 341, 505, 682, and 934 mg Ca/d. Subjects in quartile IV had significantly less BMD loss at the whole body and less BMD/bone mineral content loss at Ward’s triangle, even after adjustments for confounding factors (by analysis of covariance). Multiple linear regression analyses showed significant positive associations between calcium intake and BMD change at the whole body (P = 0.006) and Ward’s triangle (P = 0.021). Calcium intake was significantly associated with bone mineral content change at the trochanter (P = 0.025) and Ward’s triangle (P < 0.001). No significant effect of calcium intake at the spine was found. In conclusion, habitual dietary calcium intake had a beneficial effect on bone loss at the whole body and some regions of the hip. Our findings suggest that an intake exceeding 900 mg calcium/d was helpful in the prevention of cortical bone loss among early postmenopausal Chinese women.

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
ESTROGEN PLAYS A key role in early postmenopausal bone loss. However, the extent of bone loss also depends on environmental factors (1) such as body weight (2) and dietary intakes (3, 4, 5). Meta-analyses have shown that the positive effect of calcium supplementation on bone mineral density (BMD) is usually observed within the first 2 yr, with little further benefit thereafter (6, 7). The positive calcium-associated effect was also more substantial in the first than in the second year of supplementation (6). Bone remodeling is slow process. It requires 6–18 months to reach equilibrium in response to an altered calcium intake. Therefore, it is likely that the benefit of calcium supplementation observed in the first year was the result of an incomplete remodeling transient (8). Longer-term intakes of at least 2 or 3 yr are probably necessary to adequately characterize the response of bone mass to alterations in habitual calcium intake, but few such studies have been conducted (9, 10, 11). Studies of the habitual diet and bone mass could reflect the long-term effect of dietary intake of calcium, but results among early postmenopausal Caucasian women are inconsistent (4, 5, 12, 13, 14, 15, 16). Furthermore, few such data are available in Asian women, among whom life-long calcium intake is lower than in their Caucasian counterparts.

We report the effect of habitual calcium intake and bone loss in early postmenopausal Chinese women in an 18-month cohort study.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The study population consisted of 454 postmenopausal healthy women, aged 48–62 yr, recruited from community subjects residing in housing estates in Shatin. The stratified cluster sampling method was used to select the housing estates in the Shatin district of Hong Kong. The methods of recruitment included both door to door as well as written invitations placed in mailboxes. Women within the specified age range were screened for eligibility. Respondents who were taking hormonal replacement therapy and those who had malabsorption syndromes, chronic liver kidney diseases, parathyroid and thyroid diseases, gastric operation, or cancer were excluded from the study. Women who had undergone oophorectomy and/or hysterectomy were also excluded because of inability to determine menopausal status. We confined the subjects to women within the first 12 yr of natural menopause, defined as at least 12 months since the last menstrual cycle. After initial screening for eligibility, we invited the eligible women to the Prince of Wales Hospital (a regional teaching hospital) for structured face to face interviews, BMD, and anthropometric measurements. The study received approval from the Chinese University of Hong Kong, Faculty of Medicine, ethics committee. All women signed the written informed consent form before being enrolled in the study.

Four hundred fifty-four subjects completed the baseline assessments. Three hundred sixty-nine subjects attended the first follow-up, and 339 attended the second follow-up study. Three hundred ten subjects completed all three assessments. Three hundred ninety-eight subjects who attended the baseline study and at least one follow-up study were included in the analysis for the cohort study.

Data collection

Data collection was conducted at baseline and at both follow-up studies. Dependent variables included BMD and bone mineral content (BMC) at the whole body, lumbar spine (L1–L4), and left hip. Independent variables included habitual dietary calcium (Ca) over the past year at baseline and the intakes over the follow-up period. Covariables encompassed age; years since menopause (YSM); baseline BMD; body weight; height; percentage change in body weight over the follow-up period; physical activities, including average hours spent in sitting, standing, walking, and performing mild and vigorous physical activities; dietary energy; and total protein and phosphorus intake at baseline and over the follow-up period.

Questionnaire interview.

Information was collected by trained interviewers with face to face interviews based on a structured and previously validated questionnaire on sociodemographic data, YSM, and physical activities. The assessment of dietary intake was based on a quantitative food frequency questionnaire (FFQ) that included 60 food group/items. The FFQ for Ca intake has been validated and previously used in the Chinese population (17). Reproducibility of Ca intake based on the FFQ between the baseline and 9 and 18 month measurements were r = 0.55; P < 0.001 and r = 0.52; P < 0.001, respectively, among the selected subjects.

We asked the participants to report the average intake of food per week or month (depending on the frequency intake) using the previous 12 months before the interview as a reference period. Foods with frequency of intake less than once per month, or 12 times/yr, were ignored. Pictures of food items in the reference portion sizes were provided as visual aids. Dietary Ca and other nutrients were derived from food composition tables (18, 19).

Anthropometric and bone measurements

Height was measured to the nearest 0.5 cm, and weight to the nearest 0.1 kg with subjects in light clothing and without shoes. Body mass index was calculated as weight (kilograms)/height (meters)². The BMC and BMD of the whole body, the lumber spine (L1–L4), as well as the left hip were measured by dual energy x-ray absorptiometry (QDR-4500, Hologic, Waltham, MA). The same staff conducted the scans and analysis for baseline and follow-up measurements. The coefficient of variation for the measurements of the lumbar spine BMD based on the spine phantom was 0.39%. The in vivo reproducibilities of the machine were 1.53, 1.72, 1.15, 4.86, and 1.2% for the spine, femoral neck, trochanter, intertrochanter, and whole body, respectively.

Statistical analysis

BMD/BMC changes over the follow-up period were calculated as the slopes of linear functions of BMD/BMC (dependent variable) and duration (independent variable) between the follow-up and baseline measurements. Mean dietary intakes and physical activities over the observation period were estimated from measurements at baseline and 9- and 18-month follow-ups. If any subject missed one test, the remaining two measurements would be considered for the mean intake. Because some subjects missed one observation in either the first and/or the second follow-up studies, a weight factor (calculated as [number of tests/3 (maximum tests)] x maximum observational time length) was given to each subject in the longitudinal data analysis.

ANOVA for repeated measures was used to compare the mean differences in dietary intakes at baseline and follow-ups. A paired sample t test was used to test the bone changes at follow-up compared with the baseline values. The long-term reproducibility of the FFQ was evaluated by comparing the cross-classification of quartile rankings of energy, protein, and Ca intake at baseline and at the second follow-up using Pearson correlation coefficients of the same nutrients at the three phases. Multiple linear regression analyses were used to examine the association between habitual dietary Ca and the rates of change in BMD and BMC. Comparison of the mean rates of change in BMD and BMC among subjects in the different quartiles of average dietary Ca intake over the follow-up period was also made using one-way ANOVA and analysis of covariance. The following potential confounding factors were included in the multivariate analyses: YSM, age, baseline body weight, percentage change in body weight over the follow-up period, height, baseline BMD/BMC at the relevant sites, mean dietary protein and phosphorus, and physical activities over the follow-up period. SPSS for Windows (releases 10.1 and 11, SPSS, Inc., Chicago, IL) was used for the analysis.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The characteristics of the women included in the analyses were similar to those of the women who were lost to follow-up (Table 1). The study subjects had similar levels of energy intake at the three phases (baseline and first and second follow-ups) of the study. However, the mean intakes of protein, Ca, and phosphorus increased by 7.5, 9.3, and 6.3% at the first follow-up and by 10.8, 25.7, and 12.3% at the second follow-up compared with those at baseline. The mean animal protein intake increased by about 15% over the 18-month follow-up period, whereas that for plant protein was similar. An increase in Ca intake from milk and milk products, vegetables, and soy products over the follow-up period was noted. The proportions of Ca intake from dairy sources were 23.1% at baseline and 24.3% and 28.4% at the first and second follow-ups, respectively, whereas that from vegetable and soy sources remained similar.

The means of the BMD/BMC rates of change among the quartiles were compared (Table 2). Univariate analysis showed that women belonging to the top quartile of Ca intake had lower BMD loss at the whole body compared with women belonging to the bottom quartile (P < 0.01). The test for trend also showed a dose-response association with decreasing bone loss with higher Ca intake quartiles. Similar changes were observed in BMC at the Ward’s region. The beneficial effect of dietary Ca on the other bone sites was not observed. Analyses of covariance taking into account the effects of the potential confounding factors (age, baseline body weight, height, YSM, baseline bone mass at the same bone site, percentage change in body weight, and mean overall intake of dietary protein and phosphorus over the follow-up periods) showed that dietary Ca had a significant effect on BMD at the whole body and Ward’s triangle and on BMC at Ward’s region only. However, no significant benefit was observed at other sites. Confining the analyses to women 3 or more YSM yielded similar results (data not shown).

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

Our cohort study in postmenopausal Chinese women within the first 12 yr of menopause has observed significant associations between Ca intake and BMD changes at the whole body and Ward’s triangle, and BMC changes at the trochanter and Ward’s triangle. Many intervention studies have reported the effect of Ca on retarding bone loss at the sites containing mainly cortical bone, such as distal forearm, proximal femur, and whole body (7, 11, 20, 21, 22, 23, 24). It was also reported that the skeleton as a whole was more sensitive than any other regional site of the body to the increased Ca intake (22, 24). Our findings are generally consistent with previous results in observing a favorable effect of dietary Ca at the sites containing more cortical rather than trabecular bone, with the strongest association observed at the whole body (P = 0.006).

In this study, dietary Ca intake was estimated using the FFQ. The FFQ is believed to obtain a better measure of long-term habitual intake than dietary records or 24-h recalls (25), and its validity has been demonstrated in many previous studies (25, 26, 27, 28). Our findings showed that the FFQ method has a good long-term reproducibility, with over 80% having within 1 U quartile agreement. In this study to improve the adherence of the subjects periodic health talks (although not specifically on dietary Ca) were given. Dietary and health counseling was also provided on request. Possibly due to the effects of education, dietary Ca intake had significantly increased at the follow-ups, with increases in the consumption of vegetables, milk and soy foods, and noticeably the proportion of Ca intake from dairy sources. However, the quartile ranking remained quite consistent and should not have greatly influenced the association of Ca intake and bone loss. We had also used the mean dietary Ca intake over the follow-up period to obtain a better precision of the nutrient estimates. However, as the 18-month observation period is relatively short, the cumulative bone changes are relatively small. The 1–2% precision errors of the dual energy x-ray absorptiometry might also attenuate the association between Ca intake and bone loss.

In conclusion, habitual dietary Ca intake had a significant positive association with bone changes at the whole body and some regions of the hip. Our findings suggested that Ca intakes, at least of the top intake quartile (>900 mg Ca/d), would be helpful in the prevention of bone loss at sites containing mostly cortical bone among early postmenopausal Chinese women.

	Footnotes

 
This work was supported by the Health Services Research Fund of Hong Kong.

Abbreviations: BMC, Bone mineral content; BMD, bone mineral density; Ca, calcium; FFQ, food frequency questionnaire; YSM, years since menopause.

Received August 1, 2003.

Accepted February 18, 2004.

	References

Top Abstract Introduction Subjects and Methods Results Discussion References

 

1. Kelly PJ, Eisman JA, Sambrook PN 1990 Interaction of genetic and environmental influences on peak bone density. Osteop Int 1:56–60[CrossRef][Medline]
2. Holbrook TL, Barrett-Connor E 1993 The association of lifetime weight and weight control patterns with bone mineral density in an adult community. Bone Miner 20:141–149[Medline]
3. Aloia JF, Vaswani AN, Yeh JK, Ross P, Ellis K, Cohn SH 1983 Determinants of bone mass in postmenopausal women. Arch Intern Med 143:1700–1704[Abstract/Free Full Text]
4. Dawson-Hughes B, Jacques P, Shipp C 1987 Dietary calcium intake and bone loss from the spine in healthy postmenopausal women. Am J Clin Nutr 46:685–687[Abstract/Free Full Text]
5. Stepan JJ 2000 Prediction of bone loss in postmenopausal women. Osteop Int 11(Suppl 6):S45–S54
6. Mackerras D, Lumley T 1997 First- and second-year effects in trials of calcium supplementation on the loss of bone density in postmenopausal women. Bone 21:527–533[Medline]
7. Shea B, Wells G, Cranney A, Zytaruk N, Robinson V, Griffith L, Ortiz Z, Peterson J, Adachi J, Tugwell P, Guyatt G 2002 Meta-analyses of therapies for postmenopausal osteoporosis. VII. Meta-analysis of calcium supplementation for the prevention of postmenopausal osteoporosis. Endocr Rev 23:552–559[Free Full Text]
8. Frost HM 1973 Remodeling as a determinant of envelope physiology. In: Frost HM, ed. Bone remodeling and its relationship to metabolic bone disease. Orthopedic lectures. Springfield: Charles C Thomas; vol 3:28–53
9. Kanis JA 1984 Treatment of osteoporotic fracture. Lancet 1:27–33[CrossRef][Medline]
10. Reid IR, Ames RW, Evans MC, Gamble GD, Sharpe SJ 1995 Long-term effects of calcium supplementation on bone loss and fractures in postmenopausal women: a randomized controlled trial. Am J Med 98:331–335[CrossRef][Medline]
11. Riggs BL, O’Fallon WM, Muhs J, O’Connor MK, Kumar R, Melton III LJ 1998 Long-term effects of calcium supplementation on serum parathyroid hormone level, bone turnover, and bone loss in elderly women. J Bone Miner Res 13:168–174[CrossRef][Medline]
12. Devine A, Criddle RA, Dick IM, Kerr DA, Prince RL 1995 A longitudinal study of the effect of sodium and calcium intakes on regional bone density in postmenopausal women. Am J Clin Nutr 62:740–745[Abstract/Free Full Text]
13. van Beresteijn EC, ’t Hof MA, Schaafsma G, de Waard H, Duursma SA 1990 Habitual dietary calcium intake and cortical bone loss in perimenopausal women: a longitudinal study. Calcif Tissue Int 47:338–344[Medline]
14. van Beresteijn EC, van’t Hof MA, de Waard H, Raymakers JA, Duursma SA 1990 Relation of axial bone mass to habitual calcium intake and to cortical bone loss in healthy early postmenopausal women. Bone 11:7–13[Medline]
15. Stevenson JC, Whitehead MI, Padwick M, Endacott JA, Sutton C, Banks LM, Freemantle C, Spinks TJ, Hesp R 1988 Dietary intake of calcium and postmenopausal bone loss. Br Med J 297:15–17
16. Riggs BL, Wahner HW, Melton III LJ, Richelson LS, Judd HL, O’Fallon WM 1987 Dietary calcium intake and rates of bone loss in women. J Clin Invest 80:979–982
17. Ho SC, Leung PC, Swaminathan R, Chan C, Chan SS, Fan YK, Lindsay R 1994 Determinants of bone mass in Chinese women aged 21–40 years. II. Pattern of dietary calcium intake and association with bone mineral density. Osteoporos Int 4:167–175[CrossRef][Medline]
18. U.S. Department of Health, Education and Welfare, Food, Agriculture Organization of the United Nations 1972 Food composition table for use in East Asia. U.S. Government Printing Office: Washington DC
19. Wang GY 1991 Food composition tables (in Chinese). Beijing: People’s Medical Publishing House
20. Recker RR, Hinders S, Davies KM, Heaney RP, Stegman MR, Lappe JM, Kimmel DB 1996 Correcting calcium nutritional deficiency prevents spine fractures in elderly women. J Bone Miner Res 11:1961–1966[Medline]
21. Dawson-Hughes B 1991 Calcium supplementation and bone loss: a review of controlled clinical trials. Am J Clin Nutr 54:274S–280S
22. Dawson-Hughes B, Harris SS, Krall EA, Dallal GE 1997 Effect of calcium and vitamin D supplementation on bone density in men and women 65 years of age or older. N Engl J Med 337:670–676[Abstract/Free Full Text]
23. Prince RL, Smith M, Dick IM, Price RI, Webb PG, Henderson NK, Harris MM 1991 Prevention of postmenopausal osteoporosis. A comparative study of exercise, calcium supplementation, and hormone-replacement therapy. N Engl J Med 325:1189–1195[Abstract]
24. Reid IR, Ames RW, Evans MC, Gamble GD, Sharpe SJ 1993 Effect of calcium supplementation on bone loss in postmenopausal women. N Engl J Med 328:460–464[Abstract/Free Full Text]
25. Black AE, Welch AA, Bingham SA 2000 Validation of dietary intakes measured by diet history against 24 h urinary nitrogen excretion and energy expenditure measured by the doubly-labelled water method in middle-aged women. Br J Nutr 83:341–354[Medline]
26. Feskanich D, Rimm EB, Giovannucci EL, Colditz GA, Stampfer MJ, Litin LB, Willett WC 1993 Reproducibility and validity of food intake measurements from a semiquantitative food frequency questionnaire. J Am Diet Assoc 93:790–796[CrossRef][Medline]
27. Hu FB, Rimm E, Smith-Warner SA, Feskanich D, Stampfer MJ, Ascherio A, Sampson L, Willett WC 1999 Reproducibility and validity of dietary patterns assessed with a food frequency questionnaire. Am J Clin Nutr 69:243–249[Abstract/Free Full Text]
28. Tomeo CA, Rich-Edwards JW, Michels KB, Berkey CS, Hunter DJ, Frazier AL, Willett WC, Buka SL 1999 Reproducibility and validity of maternal recall of pregnancy-related events. Epidemiology 10:774–777[CrossRef][Medline]

This article has been cited by other articles:

				M. D. Walker, R. Novotny, J. P. Bilezikian, and C. M. Weaver Race and Diet Interactions in the Acquisition, Maintenance, and Loss of Bone J. Nutr., June 1, 2008; 138(6): 1256S - 1260S. [Abstract] [Full Text] [PDF]

				J. W Nieves Osteoporosis: the role of micronutrients Am. J. Clinical Nutrition, May 1, 2005; 81(5): 1232S - 1239S. [Abstract] [Full Text] [PDF]

				S. C. Ho, Y.-m. Chen, and J. L. F. Woo Educational Level and Osteoporosis Risk in Postmenopausal Chinese Women Am. J. Epidemiol., April 1, 2005; 161(7): 680 - 690. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Submit a related Letter to the Editor Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Copyright Permission Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ho, S. C. Articles by Lam, S. S. H. Search for Related Content PubMed PubMed Citation Articles by Ho, S. C. Articles by Lam, S. S. H.