点击显示 收起
1 From the Program on Prevention Outcomes and Practices, Stanford Prevention Research Center, Stanford University, Palo Alto, CA
2 Supported by grants from GlaxoSmithKline Consumer Healthcare and Procter & Gamble Pharmaceuticals. 3 Address reprint requests to RS Stafford, Program on Prevention Outcomes and Practices, Stanford Prevention Research Center, Stanford University, 211 Quarry Road N161, Stanford, CA 94305. E-mail: rstafford{at}stanford.edu.
ABSTRACT
Background:Recent research has raised doubts about the efficacy of calcium supplementation in preventing fractures; however, adequate calcium intake remains important.
Objective:Using data from the 1999–2002 National Health and Nutrition Examination Survey, we assessed dietary and supplemental calcium consumption among US men and women according to risk of osteoporosis and stratified by sex, race/ethnicity, and socioeconomic status.
Design:We categorized risk of osteoporosis as high (having an osteoporosis diagnosis or treatment), moderate (aged >50 y), or low (aged 19–50 y). Main study outcomes included milligrams of dietary and supplemental calcium intake, likelihood of meeting national calcium adequate intake (AI) levels, and likelihood of taking supplemental calcium.
Results:Mean (95% CI) total calcium consumption was 944 (846, 1043) mg in the high-risk group, 821 (788, 854) mg in the moderate-risk group, and 846 (812, 871) mg in the low-risk group. Overall, 40% of the sample met the calcium AI amount and 48% reported taking supplemental calcium. After adjustment for daily caloric intake, the greater likelihood of meeting calcium AI levels was associated with [odds ratio (95% CI)] low [versus moderate, 1.5 (1.2, 1.7)] and high [versus moderate, 1.9 (1.3, 2.6)] osteoporosis risk, female sex [1.6 (1.3, 1.8)], non-Hispanic white ethnicity [versus nonwhite, 1.9 (1.7, 2.3)], and education beyond high school [versus less than high school, 1.5 (1.2, 1.9)]. These same factors were also associated with an increased likelihood of taking supplemental calcium, except for a consistent increase with higher osteoporosis risk.
Conclusion:Many Americans—particularly men, ethnic minorities, and the socially disadvantaged—are not meeting the current recommendations for adequate calcium intake through diet alone or with supplements.
Key Words: National Health and Nutrition Examination Survey • osteoporosis risk • dietary calcium consumption • calcium supplementation
INTRODUCTION
Osteoporosis and low bone mass (osteopenia) are major public health threats in the United States that affected almost 44 million adults aged 50 y in 2002 and that are associated with enormous health care spending (1). The deterioration of bone mass significantly increases the risk of osteoporotic fracture, with 40% of white women and 13% of white men aged 50 y expected to experience an osteoporotic fracture in their remaining lifetimes (2). The 2004 Surgeon General's report on bone health and osteoporosis for the first time placed these topics in the center of a nationwide discussion. The report calls for a coordinated national effort toward improving the bone health of all Americans, with men and minority women among the priority subpopulations in addition to the traditionally targeted older white women (3).
Being a fundamental building block of bone, calcium is essential for achieving optimal peak bone mass in the first 2–3 decades of life and for maintaining bone mass later in life (4). Calcium supplementation causes small but significant reductions in bone loss (5, 6); however, its efficacy in terms of fracture prevention remains uncertain. Three recently published, large clinical trials concluded that calcium plus vitamin D supplementation does not protect against fractures in generally healthy, postmenopausal women (6, 7) or in older women with a prior history of low-impact fractures (7, 8). The external validity of all 3 studies has been called into question, however (9, 10). In 2 of those studies, mean daily total calcium intake at baseline was >1000 mg from either diet alone (7) or diet and supplements (6). In the Women's Health Initiative trial, nearly 30% of participants consumed 500 mg supplemental Ca/d at baseline (6). Still, the Women's Health Initiative results showed a significant benefit of calcium and vitamin D supplementation in women with good compliance and in those aged >60 y (6).
Past US national survey studies found that most Americans, including postmenopausal women, consumed significantly lower amounts of dietary calcium than the recommendations and used calcium supplements infrequently (11, 12). Other national data indicated that calcium has increasingly been omitted as a therapy for osteoporosis, particularly since 1994 with rising bisphosphonate use (13). This pattern exists despite participants having been given concomitant calcium and vitamin D supplements in all clinical trials that showed the efficacy of bisphosphonates (14–18).
Using data from the 1999–2002 National Health and Nutrition Examination Survey (NHANES), the present study examined gaps in overall calcium intake and calcium supplement use according to risk of osteoporosis and stratified by sex, race/ethnicity, and socioeconomic status. We hypothesized that meeting age-specific national calcium adequate intake (AI) levels and supplemental calcium use would be least prevalent among those at higher risk of osteoporosis, nonwhites, females, and the socioeconomically disadvantaged, compared with their respective counterparts.
SUBJECTS AND METHODS
Data source and processing
The NHANES is conducted by the National Center for Health Statistics in the 50 states and the District of Columbia. It provides a representative sample of the US noninstitutionalized, civilian population generated by using a stratified, multistage sampling design. It also includes oversampling of low-income persons, persons aged 60 y, non-Hispanic blacks, and Mexican Americans. We obtained calcium intake data from 1999–2002. Detailed descriptions of the survey design and public-use data files can be found at http://www.cdc.gov/nchs/about/major/nhanes/datalink.htm.
For the purposes of this study, we were interested in elemental calcium consumption from both food and supplements. Milligrams of dietary calcium consumed by an individual during the 24-h, midnight-to-midnight period before the interview was extracted from the total nutrition intakes file. In 1999–2001, dietary intake data were collected with the NHANES computer-assisted dietary interview system. The year 2002 marked the inception of the new NHANES dietary component called "What We Eat in America," which represents the integration of the original NHANES dietary component with the US Department of Agriculture's Continuing Survey of Food Intakes by Individuals. The 2002 dietary data were coded in a fashion similar to the 1999–2001 data. Please refer to the following website for more details regarding dietary data collection procedures: http://www.cdc.gov/nchs/data/nhanes/nhanes_01_02/drxtot_b_doc.pdf.
We used the dietary supplement file to estimate average daily supplemental calcium intake over the past 30 d. This file includes both prescription and nonprescription dietary supplements and calcium-containing antacids. Supplemental calcium data were collected by obtaining supplement containers from the participant when possible; otherwise, participant-reported supplement-identifying information was recorded. For calcium-containing compounds not included on an NHANES-provided list (http://www.cdc.gov/nchs/data/nhanes/frequency/dsqdoc.pdf), we used the Merck Index (http://themerckindex.cambridgesoft.com) and, when necessary, drug product websites to determine the milligrams of elemental calcium in a compound. The daily frequency of consumption or the number of tablets taken at a time was missing for 19% (n = 773) of the participants reporting calcium supplement use. Of the calcium supplement reports with missing data, 56% were missing only the daily frequency, 7% were missing only the number of tablets taken at a time, and 37% were missing both. For both of these variables, >70% of the observations with complete data had a value of 1.0. Thus, when these variables were missing, a value of 1.0 was substituted for the missing value.
Study sample
The 1999–2002 NHANES included 5094 men and 5760 women aged 19 y. After we limited the sample to participants with dietary data determined by NHANES to be "reliable and meeting minimum criteria," 4477 men and 5000 women remained and represented the base sample for our analysis.
We defined high osteoporosis risk as men (n = 69) and women (n = 444) aged 19 y who reported ever receiving an osteoporosis diagnosis or treatment, including those who reported taking an osteoporosis medication (selective estrogen receptor modulators, bisphosphonates, estrogens, or calcitonin) in the past month or who had experienced a low-impact fracture after the age of 50 y. The remaining survey participants were classified by age as being at moderate risk (aged >50 y, n = 3649) and at low risk (aged 19–50 y, n = 5315). This age cutoff corresponds with the current calcium AIs developed by the Institute of Medicine of 1200 mg for those aged >50 y and 1000 mg for adults aged 19–50 y, including pregnant and lactating women (19).
We conformed to the NHANES analytic guidelines for classifying race/ethnicity, income, and education. We classified race/ethnicity into 4 categories: non-Hispanic white (hereafter, white), non-Hispanic black (black), Mexican American, and other. The "other" category includes participants reporting multiple racial/ethnic identities. We categorized participants by annual family income (> or <$20 000) and highest achieved education level [less than high school, high school or GED (general equivalency diploma), or more than high school] as indicators of socioeconomic status.
Statistical analysis
All analyses were performed in SAS-callable SUDAAN (version 9; RTI, Research Triangle Park, NC) and incorporated the NHANES sampling weights and complex survey design measures (http://www.cdc.gov/nchs/data/nhanes/nhanes_general_guidelines_june_04.pdf) to generate national estimates. We used PROC CROSSTAB to determine the frequency and percentage distributions of categorical variables. Factors associated with the likelihood of meeting age-specific calcium AIs and of taking supplemental calcium were examined in 2 separate multiple logistic regression models by using PROC RLOGIST, with adjustment for daily caloric intake. The factors included were osteoporosis risk, sex, race/ethnicity, income, education, survey year (2001–2002 versus 1999–2000), and, for the likelihood of meeting age-specific AIs, calcium supplement use.
Because of insufficient scientific evidence to provide a Recommended Daily Allowance (RDA), the Institute of Medicine has issued an AI for calcium, which is generally an overestimation of the average person's needs. We therefore performed a sensitivity analysis to examine the association between the selected factors and the likelihood of meeting age-specific calcium AIs minus 500 mg. The results were not reported because they were largely consistent with those for meeting the AI. We included interaction terms in the initial modeling between race/ethnicity (condensed as white versus non-white) and sex and between income and education, respectively. None of these interaction terms was statistically significant; thus, they were omitted from the final models.
To examine mean differences in total calcium consumption among subpopulations of selected demographic characteristics (ie, sex, race/ethnicity, income, and education), we performed analysis of covariance on the natural logs of calcium intake quantities by using PROC REGRESS with daily caloric intake as a covariate. Log transformation was used to correct for the skewness of the calcium intake data. We reported the inverse natural logs of mean calcium intakes and 95% CIs derived by using PROC DESCRIPT. Statistical significance was set at two-tailed P < 0.05.
RESULTS
About 5% of the sample was at high osteoporosis risk, 30% was at moderate risk, and the remaining 65% was at low risk (Table 1). Overall, 40% of the sample met daily calcium AI levels. Meeting the AI target was significantly less likely among those at moderate osteoporosis risk [odds ratio (OR): 0.68; 95% CI: 0.58, 0.81] than among those at high (OR: 1.26; 95% CI: 0.89, 1.79) or low (reference) risk (Table 2). Women were 1.56 (95% CI: 1.34, 1.82) times as likely as men to meet the AI target after control for total calories. Compared with whites, the likelihood of meeting the AI target was significantly lower for blacks (OR: 0.38; 95% CI: 0.32, 0.45) and for those of other race (OR: 0.49; 95% CI: 0.39, 0.62), but was not significantly different for Mexican Americans (OR: 0.90; 95% CI: 0.77, 1.06). Greater odds of meeting the calcium AI levels were also associated with having a greater than high school education (versus less than high school education, OR: 1.51; 95% CI: 1.22, 1.86) and taking calcium supplements (OR: 4.07; 95% CI: 3.52, 4.71). Neither total nor supplemental calcium intake changed significantly from 1999–2000 to 2001–2002.
View this table:
TABLE 1. Demographics of the population by osteoporosis risk level, 1999–2002 National Health and Nutrition Examination Survey
View this table:
TABLE 2. Factors associated with meeting calcium recommendations and taking calcium-containing supplements, 1999–2002 National Health and Nutrition Examination Survey1
Forty-eight percent of the entire sample reported taking calcium supplements. Persons at both high (OR: 3.04; 95% CI: 2.22, 4.11) and moderate (OR: 1.61; 95% CI: 1.42, 1.83) osteoporosis risk were more likely to use calcium supplements than were those at low risk. More women (54%) than men (41%) reported taking calcium supplements (OR: 1.75; 95% CI: 1.56, 1.96). Mexican Americans and persons of nonwhite race were 39–53% as likely to be consuming supplemental calcium as were non-Hispanic whites. Higher income (OR: 1.55; 95% CI: 1.36, 1.76) and education [high school, OR: 1.29 (95% CI: 1.08, 1.55); greater than high school, OR: 1.89 (95% CI: 1.54, 2.31)] were associated with a greater likelihood of taking calcium supplements.
The aforementioned patterns of calcium intake and calcium supplementation are further supported by the quantitative data shown in Table 3. Mean total calcium consumption was 944 (95% CI: 846, 1043) mg in the high-risk group, 821 (95% CI: 788, 854) mg in the moderate-risk group, and 846 (95% CI: 812, 871) mg in the low-risk group. Mean total calcium intake was lower than the recommended AIs across all osteoporosis risk groups and major demographic characteristics (all P values < 0.01). Supplements were a main source of calcium for those at high risk of osteoporosis. However, supplemental calcium was inadequate to overcome the deficits between dietary intake and the recommended AIs.
View this table:
TABLE 3. Daily calcium intake by osteoporosis risk and demographic characteristics, 1999–2002 National Health and Nutrition Examination Survey1
DISCUSSION
Given that AI levels are generally overestimates of an average person's needs, we can be fairly confident that populations in whom a large percentage meets these levels have a low prevalence of insufficient calcium intake. By default, a greater potential for concern exists for those populations who do not meet these levels even though the current knowledge precludes a definitive conclusion regarding the extent of the insufficiency.
Our findings support previous observations of Americans having dietary calcium intakes below AI levels and uncommon calcium supplement use. Using 1999–2000 NHANES data, Ervin et al (11) found median daily calcium intake from food sources for adults aged 60 y to be 716 mg for men and 563 mg for women compared with the national AI of 1200 mg. Using the same data, Radimer et al (12) found that 29% of non-Hispanic white, 9% of non-Hispanic black, and 14% of Mexican American adults reported calcium supplement or calcium-containing antacid use in the past month. Unlike our calcium supplement definition,Radimer et al did not include calcium-containing multivitamins/multiminerals. We found that neither overall calcium consumption nor calcium supplement use increased between 1999–2000 and 2001–2002. Previous research also supports our findings that those with greater dietary calcium intake are more likely to take supplemental calcium, but many supplemental calcium users still do not achieve total calcium AI levels (20–23).
Consuming sufficient amounts of calcium is an important component for preventing osteoporosis and low bone mass, both of which are major public health threats. Recent clinical trial results galvanize the debate regarding calcium with vitamin D supplementation for the protection of fracture (6–8). Those results, however, must not be mistakenly interpreted as being sufficient to alter currently recommended calcium AI levels. We should not ignore the possible benefits of calcium with vitamin D supplementation for reducing the risk of fracture in selected subpopulations, such as women over the age of 60 y, persons unable to obtain adequate intake through diet alone, and those at high risk of fracture (6, 10).
Until more is known, achieving adequate calcium—primarily from the diet—should remain an important health promotion recommendation for all Americans. Those with low dietary calcium intake should be targeted, particularly because we found this group also to be consuming less supplemental calcium than did those with higher dietary calcium intakes. Among individuals at various risk levels for osteoporosis, those over the age of 50 y who did not have a clinical diagnosis of osteoporosis were the least likely to meet AI levels. Osteoporosis and osteopenia are historically underdiagnosed and undertreated conditions, even among those already experiencing a fracture (24–29). Therefore, just because a person does not have a diagnosis of osteoporosis or osteopenia does not mean that the person is not at risk. It behooves physicians to perform a thorough evaluation of individual absolute risk of fracture by using published risk estimation algorithms (30) beyond a dichotomous determination of presence versus absence of osteoporosis or osteopenia.
Partly because of the commonly held misconception that osteoporosis is a disease of older white women, men and ethnic minorities have traditionally been underrepresented in osteoporosis-related clinical research and intervention activities. Whereas the prevalence of low bone mass and osteoporosis is admittedly lower in men than in women and in blacks than in whites (31–35), underappreciation of the importance of osteoporosis prevention in men and ethnic minorities would be a public policy error. We found from our analyses that unlike women, men's calcium intake does not increase with osteoporosis risk group and that men are almost half as likely to take supplemental calcium as are women. Men also consume a less calcium-rich diet than do women. We also found that ethnic minorities are less likely to meet calcium AI levels and to take calcium supplements than are whites. Targeting men and ethnic minorities of moderate and high osteoporosis risk to increase their calcium consumption through diet, or through diet and supplements when necessary, is an important consideration.
Although the 1999–2002 NHANES data represent the latest, most comprehensive data source for examining calcium intake at the national level, the reported data should be interpreted in light of their potential limitations. Among the most outstanding limitations are, first, that calcium intake from food sources is determined through a "multiple pass" 24-h dietary recall, which, despite being a well-used method for collecting dietary information, is nonetheless subject to reporting and recall biases. Second, information collected for prescription medications and dietary supplements may not be accurate or complete despite the fact that, when possible, participants showed their medication and supplement containers to the NHANES interviewers. Finally, because of insufficient scientific evidence, the Institute of Medicine has not issued an Estimated Average Requirement (EAR) for calcium. Use and interpretation of AI levels, which are generally an overestimation of the average person's needs, should be done with caution. Although we can be fairly confident that groups meeting AI levels have a low prevalence of insufficient calcium intake, we cannot determine the prevalence of insufficient intake among those not meeting those levels.
In conclusion, our results show that, overall, most US adults do not meet daily calcium AI levels through diet alone, and that, among those taking supplements, supplemental calcium is often inadequate to overcome the deficits between dietary intake and the recommendations. Our finding of lower calcium consumption among men, ethnic minorities, and the socioeconomically disadvantaged than in their respective counterparts supports the Surgeon General's call for including these subpopulations, along with the traditionally targeted older white women, among the priority populations in bone health improvement interventions (3). Furthermore, older men and women who do not have a clinical diagnosis of osteoporosis are another group of individuals for whom attention is warranted in future interventions because they are least likely to be compliant with the calcium recommendations.
ACKNOWLEDGMENTS
The contributions of the authors were as follows—JM: designed the study and analysis plan, RAJ: managed the data and conducted the analyses, RSS: provided expert advice and guidance. All 3 authors contributed to data interpretation and writing. The funding sources had no influence on the study's design or interpretation of results.
REFERENCES