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Journal of Clinical Endocrinology & Metabolism, doi:10.1210/jc.2004-0924
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The Journal of Clinical Endocrinology & Metabolism Vol. 90, No. 9 5127-5133
Copyright © 2005 by The Endocrine Society

Dietary Calcium Intake Protects Women Consuming Oral Contraceptives from Spine and Hip Bone Loss

Dorothy Teegarden, Pamela Legowski, Carolyn W. Gunther, George P. McCabe, Munro Peacock and Roseann M. Lyle

Interdepartmental Nutrition Program (D.T., P.L., C.W.G.) and Departments of Statistics (G.P.M.) and Health and Kinesiology (R.M.L.), Purdue University, West Lafayette, Indiana 47907; and Department of Medicine, Indiana University (M.P.), Indianapolis, Indiana 46202

Address all correspondence and requests for reprints to: Dr. Dorothy Teegarden, Interdepartmental Nutrition Program, 700 West State Street, Stone Hall-1264, Purdue University, West Lafayette, Indiana 47907. E-mail: dteegard{at}purdue.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: It is estimated that 80% of all women have used oral contraceptives (OCP), but OCP use may prevent attainment of maximal peak bone mass in young women and thus increase the risk of osteoporosis later in life.

Objective: This study examined whether increased calcium intake could reduce the detrimental effects of OCP use on bone mass in young women.

Design: The study design was a 1-yr intervention.

Setting: The study was performed in a general community setting.

Subjects: One hundred fifty-four young (18–30 yr old) healthy women with a dietary calcium intake of less than 800 mg/d began the study, and 135 completed the trial.

Intervention: Subjects were randomly assigned to one of three diet intervention groups: 1) control, continuous established (<800 mg/d) dietary calcium intake; 2) medium dairy, increase calcium intake to approximately 1000–1100 mg/d; and 3) high dairy, increase calcium intake to approximately 1200–1300 mg/d. Randomization was stratified by OCP use.

Main Outcome Measures: The main outcome measures were total body bone mineral density (BMD) and content (BMC); total hip BMD, BMC, and bone area; and spine BMD, BMC, and bone area.

Results: Dairy product intervention positively impacted the percentage change in total hip BMD and BMC. In addition, dairy product intake prevented a negative percentage change in total hip and spine BMD in OCP users.

Conclusion: Dairy product intake, at levels necessary to achieve the recommended intakes of calcium, protected the total hip BMD and spine BMD from loss observed in young healthy women with low calcium intakes who were using OCP.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
OSTEOPOROSIS IS A disease characterized by decreased bone mass and increased risk of bone fractures. In the United States, an estimated 10 million individuals have osteoporosis, and an additional 34 million are estimated to have low bone mass, a prominent risk factor for osteoporosis. Optimizing bone mass in adolescence and young adulthood is believed to prevent low bone density and osteoporosis later in life (1). The age at which peak bone mass is accrued in females is still under debate. Studies indicate that total hip and femoral neck reach their peak between the age of 14 and 18 yr, whereas lumbar spine peak attainment occurs between 14 and 35 yr of age, and total body bone mineral density (BMD) and bone mineral content (BMC) are believed to reach their peak between the age of 18 and 30 yr (2, 3, 4, 5, 6, 7, 8). It is estimated that a 5–10% difference in peak adult bone mass is sufficient to account for an approximately 25–50% difference in hip fracture rate later in life (9). Although genetics play an important role, environmental factors, including, nutrition, hormonal status, and physical activity, also contribute to maximizing bone accrual and reducing the incidence of osteoporosis and bone fractures.

The primary nutritional factor known to affect bone is calcium. A review of 139 reports investigating the role of calcium on bone mass by Heaney (10) clearly demonstrates the positive effects of calcium on bone mass across the life span. These studies included observational studies, dairy product-supplemented randomized controlled trials, and balance studies that examined the effects of dairy products on optimal bone mass in adolescents and young adults. A retrospective study from our laboratory also demonstrated a significant positive relationship between dairy product consumption in adolescence and BMD in young adult women (11). This is important because dairy products are the primary source of dietary calcium in the United States, representing approximately 70% of total calcium intake (12). Thus, increasing the level of calcium consumed in the form of dairy products or supplements contributes to maximizing peak BMD.

There are conflicting data on the effects of oral contraceptive (OCP) use on bone mass. OCP use has been shown to be protective of spine BMD in women between the ages of 20 and 40 yr (13, 14), but no differences were found in total body BMD and BMC or total hip BMD in adolescents using OCP compared with nonusers (15). In contrast, a negative relationship between total hip BMD or spine BMD and OCP use in young, active, healthy women has been reported (16). Previous results from our laboratory indicated a negative impact on spine and hip bone density in OCP users initiating an exercise program, demonstrating that OCP use may have a negative interaction with physical activity (17, 18). Thus, the impact of OCP on bone mass in young women remains controversial. The present study assessed changes in bone during a randomized 12-month intervention of increased dairy products in 18- to 30-yr-old OCP users vs. OCP nonusers.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

Young healthy women (18–30 yr; n = 156) were solicited through flyers, radio announcements, direct mailings, and information booths located outside of residence hall cafeterias. The Purdue University institutional review board approved the study according to the principles outlined in the Declaration of Helsinki, and all participants provided written informed consent. Subjects with calcium intakes less than 800 mg/d, energy intakes less than 2200 kcal/d, who were willing to consume dairy products and would be living in the community for the next year were invited to participate. Potential participants were prescreened via a calcium-screening questionnaire (19), followed by a food frequency questionnaire (20) to confirm calcium and energy intakes before randomization. Exclusion criteria included chronic intake of medications that would alter calcium metabolism; pregnancy or lactation within the previous 6 months; bone, kidney, malabsorptive, or hormonal disorders that might affect calcium metabolism; bone or muscle disorders; more than 20% overweight or 15% underweight according to the Metropolitan Life Insurance Tables (21); self-reported lactose intolerance; eating disorders; and high alcohol consumption (more than two drinks per day). Fifty-seven of the 135 subjects who completed the study reported using OCPs.

Bone density measurements

At baseline and 6 and 12 months, total body, spine (lumbar 2–4), and total hip BMD and BMC were measured with a dual energy x-ray absorptiometer (Lunar Corp, Madison, WI; software version 4.3e). The technician was blinded as to group assignment of subjects. The coefficients of variation for the spine BMD and total hip BMD were 1.45% and 0.35%, respectively. Bone variables are expressed as the percentage change from baseline to 12 months [(12 months – baseline)/baseline].

Assessment of lifestyle factors

Weight, in light clothing, was measured on a calibrated balance scale, and height, without shoes, was measured with a wall-mounted stadiometer. Three-day food records, completed at baseline and 3, 6, 9, and 12 months, were reviewed and analyzed by one trained nutritionist employing the Nutrient Data System (Minneapolis, MN). Three-day physical activity records were collected at the same 3-month intervals to assess energy expenditure (kilocalories per day) (22). Lifestyle questionnaires assessed previous and current medical history and medication use, including OCP use at baseline and 12 months.

OCP use

All women who reported OCP use were consuming them from baseline throughout the period of observation. At baseline, 22% of women reported using OCPs for less than 1 yr, and 78% reported using OCP for 1–5 yr. The average length of OCP use before the study was 1.77 ± 1.8 yr (n = 57), and the number of years by diet intervention and OCP use is shown in Table 1Go. Participants using OCPs consumed both monophasic (39%) and triphasic (57%) pills (see Table 1Go for distribution by diet intervention and OCP use groups). Two percent reported using progesterone.


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  		TABLE 1. Baseline characteristics (mean ± SD) of diet intervention groups (n = 135)

 
Intervention groups

The study design was a randomized, controlled intervention trial of dietary counseling to increase dairy intake, stratified by OCP use. After completion of baseline testing, participants (n = 156) were randomized into one of three groups: control group (maintain current dietary consumption, calcium <800 mg/d from all sources), medium dairy group (1000–1100 mg calcium/d from dairy), and high dairy group (1200–1300 mg/d calcium from dairy). Randomization was stratified by OCP use or nonuse.

Medium dairy and high dairy intervention group participants received dietary counseling by trained nutritionists and were instructed to increase daily calcium intakes by substituting dairy products rich in calcium, with an emphasis on non- and low-fat milk. To maintain isocaloric intakes, participants were instructed to remove other dietary components from their diets that were approximately equal to the added dairy intake calories. The counseling that was provided for the medium and high dairy intake groups differed by one serving of dairy per day. A daily record of dairy intake and foods removed from the diet was returned monthly and used to assess compliance. The logs were checked for accuracy by a nutritionist, and if errors were found, the participant was contacted and retrained to the dietary protocol.

Laboratory methods

Blood samples were collected at baseline and 12 months during d 3–11 of the menstrual cycle (follicular phase), between 0700 and 1100 h after a 12-h fast. After collection, blood samples were immediately centrifuged, and serum was stored at –80 C. Serum PTH was measured by a two-site immunoradiometric assay, which assessed the biologically intact 84-amino acid chain of PTH using the Allegro Intact PTH Immunoassay (Nichols Institute, San Juan Capistrano, CA). Serum 25-hydroxyvitamin D (25OHD) was determined by ELISA (DiaSorin, Stillwater, MN). Serum 1,25-dihyroxyvitamin D [1,25(OH)2D] was extracted with acetonitrile and partially purified with a C18 silica cartridge. Serum 1,25(OH)2D was assessed using a competitive protein-binding assay based on calf thymus receptor (Incstar, Inc., Stillwater, MN).

Statistical analyses

The subjects in this study were classified by OCP use or nonuse and randomized to three diet intervention groups resulting in a two by three ANOVA design. The outcome variables were total body BMD and BMC, spine BMD and BMC, spine bone area, and total hip BMD, BMC, and bone area. Covariates included baseline weight, age, physical activity (energy expenditure per kilogram), and height as well as mean level of physical activity during the study, because these variables are related to the outcome variables (5). The dairy intervention groups were collapsed for some analyses, and contrasts were used to examine the effects of placebo vs. the mean of the two dairy diet intervention groups (23). Using the smallest group size (control diet group, OCP users, n = 18) of the completers and employing an SD of 0.6, there was 80% power to detect a change of 0.51 in the spine BMD and 90% power to detect a change of 0.60 at P = 0.05. An intention to treat analysis, using the last observation carried forward procedure (either baseline or 6 months, as available), was also performed. SAS statistical software (SAS Institute, Cary, NJ) was used for all computations, and 0.05 was used as the threshold for declaring statistical significance.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Data for 135 subjects were analyzed; 21 subjects did not complete the trial after baseline testing. One participant died due to unrelated causes. Reasons for withdrawal (n = 20; 13%) included loss of interest or time constraints (n = 14; 9%), leaving the area (n = 4; 3%), and pregnancy (n = 2; 1%). No significant differences (age, weight, calcium intake, energy intake, OCP use, total body BMD and BMC, hip and spine area, BMD, and BMC) at baseline were found between those who discontinued the study protocol and those who remained in the intervention. The number of dropouts across the groups were as follows: control group, n = 9; medium dairy, n = 8; and high dairy, n = 3.

A summary of the diet intervention and OCP use group baseline characteristics of those who completed the trial is shown in Table 1Go. Baseline differences observed between OCP nonusers and users are shown in Table 1Go. The OCP users were older, their PTH levels were lower, and both their 25OHD and 1,25(OH)2D levels were higher than in OCP nonusers. There were no significant differences in physical activity between OCP groups or diet intervention groups. Dietary intakes of calcium in the dairy intervention groups increased and were not different between OCP use groups (Table 2Go). Energy intake did not differ by diet intervention group or by time period (mean ± SD for all groups combined, 1693 ± 470, 1599 ± 446, and 1604 ± 461 kcal/d for baseline, 6 month, and 12 month, respectively). Other dietary factors, including phosphorous and protein intakes, were not different by intervention group assignment or OCP use group.


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  		TABLE 2. Intervention calcium intake and physical activity level and 1-yr change in physical activity and weight in diet intervention groups by OCP use (3–12 month mean ± SD)

 
The baseline 25OHD levels were positively correlated to baseline 1,25(OH)2D (r = 0.36; P = 0.0005) and negatively correlated to baseline PTH levels (r = –0.36; P = 0.0004). However, baseline PTH did not correlate to 1,25(OH)2D levels (r = –0.07; P = 0.50). Results did not differ when age and OCP use were controlled in the model.

Diet intervention group results

The ANOVA results, using age, weight, and height at baseline as covariates, indicated no statistically significant main effects of diet intervention group assignment on any bone site (listed in Table 1Go), except for total hip BMD (P = 0.006) and total hip BMC (P = 0.02). Because results were essentially the same for the model run without the covariates, total hip BMD results were also analyzed using contrasts based on the unadjusted means. This analysis showed that the diet intervention group main effect for total hip BMD was primarily due to the 0.45% loss in the control diet group vs. the gain of 0.43% in the dairy intervention groups combined (P = 0.008).

Effects of diet and OCP use

Addition of OCP use to the model yielded a significant interaction with diet intervention group for spine BMD (P = 0.03). Diet intervention group did not significantly predict the percentage change in spine BMD in OCP nonusers (model P = 0.14; Fig. 1AGo), but did predict the percentage change in spine BMD, but not spine BMC or area, in the OCP users (model P = 0.02; Fig. 1BGo). Results were similar when energy expenditure (kilocalories per kilogram) was included in the model. As described above, because results were similar for the model run without the covariates, these effects were also analyzed for spine BMD using contrasts based on the unadjusted means. This analysis indicated that the diet intervention group by OCP use interaction for spine BMD was primarily due to the difference between a loss of 1.33% in the control diet group OCP users vs. the 0.67% gain in the combined dairy intervention groups OCP users (P = 0.002). Although the interaction between diet group and OCP use was not statistically significant for the percentage change in total hip BMD and BMC, the effect of the intervention at this site was similar to that described above for spine BMD, with a loss of 1.05% in the control diet group OCP users vs. a composite gain of 0.35% in the dairy intervention groups. Means for percentage change in hip BMD for the OCP nonusers and users by diet intervention group are shown in Fig. 2Go, A and B, respectively. There was a trend toward a difference from baseline in hip BMD (Fig. 2AGo). See Table 3Go for percentage changes in bone by diet and OCP groups.



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  		FIG. 1. Medium and high dairy intervention group assignment protected spine BMD in OCP users (B), but not in OCP nonusers (A). The results of subjects completing the trial are expressed as the mean ± SE. For spine BMD, the significance of diet intervention by OCP use interaction was P = 0.03. *, Difference (P < 0.05) from zero (by paired t test); **, a trend (0.1 > P > 0.05). Bars with different letters are significantly different (by independent t test; P < 0.05).

 


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  		FIG. 2. Medium and high dairy intervention group assignment protected total hip BMD in OCP users (B), but not in OCP nonusers (A). The diet intervention by OCP use interaction was P = 0.36. The results of subjects completing the trial are expressed as the mean ± SE. *, Difference (P < 0.05) from zero (by paired t test); **, a trend (0.1 > P > 0.05). Bars with different letters are significantly different (by independent t test; P < 0.05).

 

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  		TABLE 3. Percentage change in bone sites from baseline to 1 yr in diet intervention groups by OCP use controlled for baseline age, weight, and height

 
In a general linear model, there was a significant interaction between OCP groups and physical activity for the percentage change in spine area (P = 0.02) and spine BMC (P = 0.01), but not for other bone sites. Physical activity did not correlate with percentage change in spine area (r = –0.23; P = 0.18) or spine BMC (r = –11; P = 0.51) in OCP users; however, physical activity positively correlated with spine area (r = 0.39; P = 0.02) and spine BMC (r = 0.36; P = 0.01) in OCP nonusers.

Furthermore, neither baseline 25OHD nor PTH levels correlated with percentage change in any bone measure even when controlled for OCP use, age, baseline weight, and height. However, the change in PTH (Table 4Go) correlated with the percentage change in total hip area (r = –0.22; P = 0.05) and total body BMD (r = –0.27; P = 0.01). Results were similar when controlled for OCP use, age, baseline weight and height, baseline 25OHD, or change in 25OHD.


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  		TABLE 4. Change in hormones, 25OHD, physical activity, and weight from baseline to 1 yr in diet intervention groups by OCP use controlled for baseline age, weight, and height

 
An intention to treat analysis was also conducted. Of the 21 subjects who did not complete the protocol, 11 had baseline measurements, and 10 had both baseline and 6 month measurements. These analyses demonstrated consistency in the strength and direction of the results compared with the treated analysis.


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
The results of this study demonstrate that increased dairy intake improved total hip BMD and BMC as well as protected OCP users from both total hip and spine BMD loss. There was an approximately 1.6% difference between OCP users and OCP nonusers with low calcium intakes in percentage change in both spine and total hip BMD during this 1-yr intervention. The OCP users lost bone density, whereas the OCP nonusers maintained bone density at both sites. The loss of spine and total hip BMD poses a significant health threat; it is estimated that eight of 10 of women in the United States use OCP at some time during the years in which peak bone mass is developing, and many will use OCP for several years. It is estimated that small changes in bone mass can reduce the risk of fractures substantially (9). Thus, a 1%/yr loss is significant and may be more significant with additional years of continued OCP use.

Although the BMD and BMC of some bone sites, particularly the spine, are changing during this age frame, the changes are small compared with those during adolescence. Thus, a limitation of the study is that it may not be of sufficient length or sufficient power to see small changes mediated by increased dairy intake in the OCP nonusers.

The results of this study demonstrate the importance of calcium intake on total hip BMD and spine BMD of OCP users, but unfortunately, most young women are not consuming adequate amounts of calcium daily. The National Health and Nutrition Survey reported that young women between the ages of 20–29 yr consumed approximately 75% of the recommended calcium amount of 1000 mg/d (24). In the United States, the largest and most frequently consumed calcium sources are milk and dairy products (12). These results indicate that increased dairy product intake can enhance peak bone mass in 18- to 30-yr-old women and, in particular, protect young women who choose to use OCP from bone loss.

In the current study, the significantly lower level of serum PTH in the OCP users compared with nonusers suggests a reduced bone turnover, consistent with previous studies supporting the idea that OCP use suppresses turnover (25). It is also consistent with the higher level of 25OHD in the OCP users, because 25OHD levels are negatively correlated with PTH (26). In contrast, OCP users had an elevated level of serum 1,25(OH)2D. The lower level of PTH concurrent with a higher level of 1,25(OH)2D seems contradictory, because it is well established that PTH up-regulates renal 1{alpha}-hydroxylase to produce 1,25(OH)2D. However, several recent studies suggest that 1,25(OH)2D levels may be regulated by other elements in addition to PTH. First, recent studies demonstrate the presence of extrarenal 1{alpha}-hydroxylases, which may not be regulated by PTH in the same manner as the renal form (27). In addition, 1,25(OH)2D levels are mobilized in PTH knockout mice (28), suggesting an alternative or redundant system to PTH regulation. It is intriguing to speculate that an increase in calcium absorption mediated by an increase in 1,25(OH)2D levels may explain the positive response in bone accrual noted in OCP users after dairy product intervention compared with non-OCP users.

The result of the current study, showing that 25OHD levels are higher in OCP users, is consistent with previous reports (29, 30). 25OHD levels were higher in estrogen users compared with nonusers across a wide age range of 20–80 yr (29). Sowers et al. (30) demonstrated a 41% higher level of 25OHD in estrogen users compared with nonusers, similar to the 31% higher level in the current study. This may not mean a difference in vitamin D status, because other reports suggest that the level of serum vitamin D-binding protein is increased after estrogen treatment in pubertal girls (31). Thus, the higher level of binding protein may lead to a higher level of bound serum 25OHD.

Results from the current study are consistent with those of our previous study, which showed that OCP users who initiated an exercise protocol lost spine BMC and BMD in the first 6 months and returned to baseline by 1 yr (17, 18). The OCP users in the exercise intervention group remained at the baseline level, whereas the other groups gained spine BMC and BMD during the 2-yr intervention. In our previous study, sedentary women, aged 18–30 yr, were recruited into a randomized 2-yr exercise intervention trial. The mean calcium intake was approximately 900 mg/d. In the current study, exercise was not a component of the intervention; however, the women were more physically fit than the subjects in the previous trial (17) (mean ± SD, 39.8 ± 3.6 vs. 28.2 ± 5 ml/kg·min estimated maximal oxygen consumption, respectively). Thus, in these active young women, OCP use was detrimental to bone mass in the absence of adequate calcium intake. In addition, the results of the current study, demonstrating that physical activity was positively correlated with percentage change in spine area and BMC in OCP nonusers, but not OCP users, are consistent with those of our previous study (17, 18). Current public health recommendations to increase physical activity levels (32), in the absence of adequate calcium intake, may contribute to reduced peak bone mass in OCP users and lead to a subsequent increased incidence of osteoporosis among women overall as they reach midlife.

It is difficult to understand the mechanism by which OCP use leads to bone loss in young healthy women. However, if physical activity plays a role, as suggested by our previous trial, a physiological model may be proposed. Exercise stimulates bone remodeling by increasing bone resorbing influences (such as PTH) and bone formation influences (such as estrogen and progesterone). OCP users have reduced estrogen and progesterone levels (33). If during exercise there is an increase in hormones that promote bone resorption, but estrogen and progesterone (stimulators of bone formation) levels are suppressed, the overall balance of bone remodeling may shift toward resorption, leading to a loss of bone density.

The results of this study suggest that achieving the recommended level of 1000 mg/d calcium may prevent bone loss from occurring in OCP users. In our previous study (17), OCP users consuming more than 1200 mg/d calcium had increases in percentage spine BMC compared with OCP users consuming less than 1200 mg/d calcium 6 months after being randomized into an exercise intervention. Specker et al. (34) reviewed exercise interventions in a meta-analysis and demonstrated that adequate calcium intake (~1000–1200 mg/d) is essential to exercise-induced increases in bone mass in young adults. Taking the above into account, the current 1000 mg/d recommended calcium intake for this age group appears to be sufficient to prevent bone loss in OCP users and aid in maximizing peak total hip BMD in young women. Although there may be additional protective benefits in BMD from greater increases in calcium intake, this was not noted in the current study.

The results of the current study have important implications for the U.S. female population, because they suggest that many women who are in their peak bone development years may be increasing their risk for osteoporosis later in life because of OCP use combined with lower than recommended calcium intake. It is estimated that up to 80% of young women consume OCPs, and few young women achieve the recommended intakes of calcium. It is a critical national issue to prevent the risk of osteoporosis in these women. The extent of the differences in bone mass noted in this study (1–2%) suggest that with the calcium intakes recommended by the National Academy of Sciences (1000 mg/d), women using OCP could reduce their risk of osteoporosis by approximately 3–10% over 1 yr, because a 5–10% increase is estimated to reduce the risk of fracture by 25–50% (9). Thus, physicians and public health professionals need to encourage young women, particularly those using OCPs, to consume recommended levels of calcium (1000 mg/d) in their diets to prevent compromising bone mass.


   Footnotes
 
This work was supported by Dairy Management, Inc.

First Published Online July 5, 2005

Abbreviations: BMC, Bone mineral content; BMD, bone mineral density; OCP, oral contraceptive; 1,25(OH)2D, 1,25-dihyroxyvitamin D; 25OHD, 25-hydroxyvitamin D.

Received May 14, 2004.

Accepted June 21, 2005.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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