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American Journal of Clinical Nutrition, Vol. 87, No. 3, 771-777, March 2008
© 2008 American Society for Nutrition

ORIGINAL RESEARCH COMMUNICATION

The skeletal benefits of calcium- and vitamin D3–fortified milk are sustained in older men after withdrawal of supplementation: an 18-mo follow-up study1,2,3

Robin M Daly, Nicole Petrass, Shona Bass and Caryl A Nowson

1 From the Centre for Physical Activity and Nutrition Research, School of Exercise and Nutrition Sciences, Deakin University, Melbourne, Australia

2 Supported by grants from the Geoffrey Gardiner Dairy Foundation and the Helen M Schutt Trust and by a National Health and Medical Research Council Career Development Award (to RMD and SB).

3 Reprints not available. Address correspondence to RM Daly, Centre for Physical Activity and Nutrition Research, School of Exercise and Nutrition Sciences, Deakin University, 221 Burwood Highway, Burwood, Melbourne, Australia 3125. E-mail: robin.daly{at}deakin.edu.au.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: In a previous 2-y randomized controlled trial, we showed that calcium- and vitamin D3–fortified milk stopped or slowed bone loss at several clinically relevant skeletal sites in older men.

Objective: The present study aimed to determine whether the skeletal benefits of the fortified milk were sustained after withdrawal of the supplementation.

Design: One hundred nine men >50 y old who had completed a 2-y fortified milk trial were followed for an additional 18 mo, during which no fortified milk was provided. Bone mineral density (BMD) of the total hip, femoral neck, lumbar spine, and forearm was measured by using dual-energy X-ray absorptiometry.

Results: Comparison of the mean changes from baseline between the groups (adjusted for baseline age, BMD, total calcium intake, and change in weight) showed that the net beneficial effects of fortified milk on femoral neck and ultradistal radius BMD at the end of the intervention (1.8% and 1.5%, respectively; P < 0.01 for both) were sustained at 18-mo follow-up (P < 0.05 for both). The nonsignificant between-group differences at the total hip (0.8%; P = 0.17) also persisted at follow-up (0.7%; P = 0.10), but there were no lasting benefits at the lumbar spine. The average total dietary calcium intake in the milk supplementation group at follow-up approximated recommended amounts for Australian men >50 y old (1000 mg/d) but did not differ significantly from that in the control subjects (1021 versus 890 mg/d).

Conclusion: Supplementation with calcium- and vitamin D3–fortified milk for 2 y may provide some sustained benefits for BMD in older men after withdrawal of supplementation.

Key Words: Milk supplementation • fortified milk • supplement withdrawal • men • bone mineral density • osteoporosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Increasing or maintaining adequate intakes of dietary calcium and vitamin D is recognized as an important strategy for the prevention and management of osteoporosis. In both elderly men and women, numerous randomized controlled trials (RCTs) have shown that the combined use of calcium and vitamin D supplements can reduce secondary hyperparathyroidism, slow the rate of bone turnover, and attenuate or even prevent age-related bone loss (1-3). The greatest benefits of supplementation are generally observed in persons who adhere to the supplementation regimen (4) or who have low dietary calcium intakes, low circulating concentrations of serum 25-hydroxyvitamin D [25(OH)D], or both (5-7). In a recent 2-y RCT in men >50 y old, we found that daily supplementation with 400 mL low-fat, calcium- and vitamin D3–enriched milk containing 1000 mg Ca and 800 IU vitamin D3 was effective for increasing serum 25(OH)D, reducing parathyroid hormone (PTH) concentrations, and stopping or slowing the rate of bone loss at the femoral neck, total hip, and ultradistal radius (8). Whereas these findings support the use of a food-based approach to increase dietary calcium and vitamin D intakes to help maintain bone status or prevent age-related bone loss in older men, an important clinical question that remains to be answered is whether there are any residual skeletal benefits after withdrawal of supplementation. Numerous follow-up studies have investigated the residual effects of supplementation with calcium, vitamin D, or both or of milk supplementation on BMD in older adults, but the findings have been inconsistent and predominantly limited to older women (9-11). Therefore, the aim of the present study was to determine whether the skeletal benefits obtained after supplementation with calcium- and vitamin D3–fortified milk were sustained 18 mo after withdrawal of the supplementation in ambulatory community-dwelling men >50 y old. We hypothesized that the rates of change in BMD would not differ significantly between the milk supplementation and control groups during the follow-up period.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study design and subjects
This study was an 18-mo follow-up to a 2-y RCT designed to assess the effects of calcium- and vitamin D3–fortified milk on BMD in middle-aged and older men. In the initial 2-y intervention (8), 167 men aged >50 y (x ± SD age: 61.9 ± 7.7 y) were randomly allocated to either a calcium- and vitamin D3–fortified milk group (milk supplementation group; n = 85) or a usual-care control group (n = 83). Men assigned to the fortified milk group were asked to consume daily 400 mL reduced-fat ({approx}1% fat) ultra-high-temperature (UHT) milk that contained {approx}1000 mg Ca and 800 IU vitamin D3. All participants enrolled in this study were healthy, ambulatory, community-dwelling white men who had a total hip, femoral neck, or lumbar spine BMD z score within ±2 SDs. Participants were initially excluded if they had taken supplements of calcium (>200 mg/d), vitamin D (>200 IU/d), or both in the preceding 12 mo; had participated in regular high-intensity resistance training in the previous 6 mo or participated in >150 min/wk of moderate- to high-impact weight-bearing exercise in the previous 6 mo; had a BMI > 35; were lactose intolerant; consumed >4 alcoholic beverages/d; or had a history of osteoporotic fracture or medical disease or of the use of any medication known to affect bone metabolism.

Of the 149 men who completed the original 2-y intervention, 109 (73%) completed the 18-mo follow-up evaluation: 55 (72%) from the milk supplementation group and 54 (74%) from the control group. The reasons for not attending the follow-up visit in the milk supplementation group were that the subject was not interested (n = 12), had been diagnosed with cancer (n = 2), could not be contacted (n = 4), had moved away (n = 2), or had died (n = 1). For the control group, the main reasons were that the subject was not interested (n = 13), had been diagnosed with cancer (n = 2), could not be contacted (n = 2), or had moved away (n = 2). During the follow-up period, participants were not provided with the fortified milk, and they were not asked to avoid taking supplements that might have an affect on bone metabolism. At the completion of the 2-y intervention, all participants were informed of the results of the study and provided with a booklet outlining their individual results, including their changes in BMD. At baseline and at 24 mo, there were no significant differences in the subject characteristics (ie, age, anthropometry, diet, physical activity, or baseline BMD) between the men who did (n = 109) and did not (n = 58) attend the final follow-up visit.

Written informed consent was obtained from all participants. The study was approved by the Deakin University Human Research Ethics Committee.

Measurements
To minimize the potential effects of seasonal variations on the key outcome measures, all testing for each data collection for both groups was completed within a 3-mo period, starting between April and June (which, in Australia, is from autumn to winter). Femoral neck, total hip, lumbar spine (L2–L4), ultradistal radius, and 33% radius BMD measurements were assessed by using dual-energy X-ray absorptiometry (DPX-L; Lunar Corp, Madison, WI) with DPX-L analysis software (version 4.7e; Lunar Corp). Patients were positioned for each scan according to standard procedures, and all follow-up scans were analyzed by using the manufacturer's scan-comparison mode. The short-term CV for repeated measurement in our laboratory ranged from 0.9% to 1.9% for the BMD measures. Quality control over the 42-mo study period was monitored by using the manufacturer's external spine phantom (CV: 0.65%).

As described previously (8), height (in cm) was measured by using a stadiometer (Holtain Ltd, Crosswell, United Kingdom). Body weight (in kg) was assessed by using electronic scales that were correct to the nearest 0.1 kg (Seca GmbH, Hamburg, Germany). Body mass index (BMI; in kg/m2) was calculated. At each visit, nutrient intakes were estimated from 3-d (2 weekdays and 1 weekend day) measured food diaries, with the option of weighing items, and intakes were analyzed by using FOODWORKS nutrient analysis software (version 4.0; Xyris Software, Brisbane, Australia). The Community Health Activities Model Program for Seniors physical activity survey (developed by the Institute for Health & Aging, University of California, San Francisco, and the Stanford Center for Research in Disease Prevention, Stanford University) was used to assess participation in recreational and organized physical activity (h weight-bearing exercise/wk) throughout the study (12). Information on the use of medication and supplements—including calcium, vitamin D, and multivitamin supplementation—and on alcohol consumption was obtained with the use of questionnaires and was confirmed by interview at each visit. The amount of milk consumed (glasses/d) was also determined from an interview-administered dairy-based food-frequency questionnaire at each time-point. At month 24, participants were asked not to include the calcium- and vitamin D–fortified milk in their responses to this questionnaire.

Statistical analysis
Statistical analysis was conducted by using STATA statistical software (version 8.0; Stata Corp, College Station, TX). Baseline characteristics between the groups were compared by using independent t tests for continuous variables and chi-square tests for categorical variables. Pooled time series regression analysis for longitudinal data with random-effects models was used to analyze time, group, and interaction effects for all continuous variables (ie, anthropometry, physical activity, diet, and BMD) in the 109 men who completed the study. To compare the changes in BMD between the groups, results were analyzed after adjustment for baseline age, BMD, total calcium intake (or total calcium intake at month 42), and change in weight. The changes in BMD were expressed as the absolute and percentage changes from baseline or from the end of the 24-mo intervention. Between-group differences were calculated by subtracting the within-group changes from baseline (or the follow-up) in the milk supplementation group from those in the control group. Generalized estimating equations (GEE modeling) with the logit link function (calcium and vitamin D supplementation use) and longitudinal ordinal regression (frequency of milk consumption) were used to test within-group changes and between-group differences in the change in each of these measures. All data are presented as means ± SDs or 95% CI unless stated otherwise.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The characteristics of the 109 men at baseline, at the end of the 2-y intervention (beginning of follow-up), and at the 18-mo follow-up are shown in Table 1Go. There were no differences in anthropometric measures, physical activity levels, or dietary habits between the 2 groups at baseline or at the end of the intervention (month 24) except that dietary calcium intakes were greater in the milk supplementation group than in the control group at both of these time-points; vitamin D and phosphorus intakes were also greater in the milk supplementation group than in the control group at month 24. This difference was due to the inclusion of the calcium- and vitamin D3–fortified milk in the 24-mo dietary analysis. During the follow-up period, total energy, protein (in g), dietary and total calcium, and vitamin D and phosphorus intakes decreased significantly from the month 24 values in the milk supplementation group (Table 1Go). The mean reduction in dietary calcium and vitamin D was 801 mg/d and 17.6 µg/d, respectively. There were no changes in any of the dietary variables in the control group from month 24 to month 42. Similarly, at the end of the follow-up period, there were no significant differences between the milk supplementation and control groups with respect to any of the dietary variables. Physical activity levels remained unchanged in both groups throughout the study. Body weight decreased in the milk supplementation group during the follow-up (mean change: –1.2 kg; 95% CI, 0.07, 2.4 kg), but this change did not differ significantly from that in control subjects (mean change: –0.6 kg; 95% CI, –0.4, 1.5 kg).


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  		TABLE 1. Age, anthropometric, physical activity, and dietary characteristics of the study participants at baseline and at the end of the intervention (month 24) and follow-up (month 42) for the milk supplementation and control groups1

 
There were no group x time interactions for calcium or vitamin D supplement use or the frequency of milk consumption after 24 or 42 mo (Table 2Go). However, the number of men who reported using calcium and vitamin D supplements increased significantly from baseline to month 42 in both the milk supplementation and control groups (P < 0.05 for both). However, at follow-up (month 42), there were no differences between the 2 groups in total calcium and vitamin D supplementation use (18.2% and 16.7%, respectively). Although dietary calcium decreased significantly (P < 0.001) in the milk supplementation group from month 24 to month 42, there was a trend for total calcium intake (dietary plus supplemental) to be greater in the milk than in the control group at follow-up (P = 0.10). Similarly, there was a greater trend for the men in the milk supplementation group than in the control group (69% and 51%, respectively; P = 0.09) to have a total calcium intake at follow-up (month 42) greater than the current Australian estimated average requirement (EAR) of 840 mg/d for men 51–70 y old (13). The EAR represents the daily calcium intake estimated to meet the requirements of 50% of Australian men in that age range. However, milk drinking habits did not differ significantly between the groups in the present study at any time during the intervention (Table 2Go). At the end of the intervention (month 24), however, the proportion of men in the milk supplementation group who reported regularly consuming milk tended to decrease (P = 0.051), which is likely to be due to the exclusion during follow-up of the fortified milk used throughout the intervention; the men were asked during the interviewer-administered FFQ not to include the fortified milk as part of their postintervention daily milk consumption. At follow-up (month 42), 41% of all men reported that they consumed <1 glass of milk/d, whereas 45% reported consuming 1–2 or >2 glasses/d.


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  		TABLE 2. Proportion of men by treatment group who used a calcium or vitamin D supplement (or both), total calcium and vitamin D intake (supplements plus diet), and the frequency of milk consumption at baseline and at the end of the intervention and follow-up periods

 
Consistent with our previous report (8), there were no differences in baseline BMD at any skeletal site between the milk supplementation and control groups (Table 3Go). The mean adjusted between-group differences in the changes from baseline to the end of the intervention (month 24) and through follow-up (42 mo), and also in the duration of the follow-up (month 24 –month 42), by treatment group for the 109 men who completed the study are reported in Table 4Go. The mean unadjusted within-group changes are shown in Figure 1Go. Consistent with our previous report that included the full data set (n = 149) (8), there was a significant between-group difference in the change in BMD relative to baseline after the 24-mo intervention in favor of the milk supplementation group at both the femoral neck (1.8%) and ultradistal radius (1.5%). In contrast, the between-group difference at the total hip and the trend toward a difference at the lumbar spine in favor of the milk supplementation group in our previous study did not persist in this cohort [net adjusted percentage difference: total hip, 0.8% (P = 0.17); lumbar spine, 0.9% (P = 0.15)].


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  		TABLE 3. Baseline bone mineral density in the fortified milk and control groups1

 

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  		TABLE 4. Net adjusted mean absolute and percentage differences (and 95% CIs) in the change in bone mineral density (BMD) from baseline between the milk supplementation and control groups after the intervention and follow-up periods1

 

Figure 1
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  		FIGURE 1.. Mean (±SE) unadjusted percentage changes from baseline in femoral neck (A), total hip (B), lumbar spine (C), and ultradistal radius (D) bone mineral density (BMD) in 109 men who were randomly assigned to the calcium- and vitamin D3–fortified milk (•) or control ({circ}) group and then followed up after 18 mo with no supplementation. *Significant between-group difference from baseline (group x time interaction) after adjustment for baseline age, BMD, total calcium intake (or total calcium intake at follow-up), and change in weight (P < 0.05).

 
During the follow-up period (month 24–month 42), there was a small, nonsignificant decrease in BMD in both groups at the total hip and femoral neck, but there were no significant between-group differences in the changes in BMD at any skeletal site. Analysis of the mean changes from baseline between the groups showed that the net benefits of the fortified milk on femoral neck and ultradistal radius BMD after the intervention were sustained at the 18-mo follow-up. Similar results were also observed at the total hip, but the between-group difference remained nonsignificant at follow-up (net adjusted percentage difference, 0.7%; P = 0.10). At the lumbar spine, the nonsignificant (0.9%) beneficial effect of the fortified milk on BMD was lost at follow-up (–0.1%). There were no between-group differences in the change in BMD at the 33% radius at any time. These results remained unchanged after the inclusion of total calcium intake at follow-up (month 42) as a covariate. Furthermore, there was no significant effect of supplementation use on the changes in BMD at any skeletal site during the follow-up period in either group.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this study of ambulatory community-dwelling older men who had previously participated in a 2-y RCT of calcium- and vitamin D3–fortified milk, we found that the 1.8% and 1.5% net beneficial effects of the fortified milk on BMD at the clinically important femoral neck and ultradistal radius were sustained 18 mo after the end of the intervention. The 0.8% nonsignificant between-group differences at the total hip in favor of the milk supplementation group after the intervention also persisted at follow-up (0.7%), but there were no remaining supplement-related benefits at the lumbar spine. It is likely that the residual skeletal benefits of the fortified milk in the men in this study were due to the maintenance of habitual calcium intakes at or above the current EAR (and recommended dietary intakes) for Australian men 51–70 y old.

Consistent with the findings from the present study, a recent follow-up study to a 2-y milk supplementation trial in postmenopausal Chinese women showed that the significant net beneficial effects of milk on lumbar spine and femoral neck BMD (1.2% and 1.7%, respectively) were maintained after a 21-mo follow-up (mean between-group difference: 1.3% and 1.9%, respectively) (10). In that study, the residual effects of the milk supplementation on BMD were attributed, at least partly, to the maintenance of a higher dietary calcium (and protein intake) in the milk supplementation group during the follow-up period. The mean total calcium intake of the women previously assigned to the milk supplementation group was 273 mg/d greater than that of the controls (768 and 495 mg/d, respectively). In contrast to these findings, in the only previous calcium and vitamin D supplementation follow-up study to have included older men (it also included older women), Dawson-Hughes et al (9) reported that the supplement-related benefits to lumbar spine and femoral neck BMD were lost 2 y after the supplementation ended in the older men and women (aged ≥ 68 y), although there were some residual benefits to total-body BMD in the men. Dietary calcium intakes in the men in that study during the follow-up were {approx}800 mg/d, which was considerably below the US National Academy of Sciences recommendation for dietary calcium of 1200 mg/d, and thus may have been inadequate to prevent bone loss. Contrary to these findings, the mean total calcium intake in the milk supplementation group at the end of the follow-up period in the present study was 1021 mg/d. Although this intake did not differ significantly from baseline values or from values in the control group at follow-up, which averaged 890 mg/d, it was greater than the current Australian EAR of 840 mg/d for men 51–70 y old (13). Therefore, it would appear that maintaining a habitual calcium intake that exceeds the EAR for older men may be sufficient to prevent bone loss after withdrawal of supplementation. It is also possible that the provision of calcium in food products may result in a more sustained effect on BMD than do supplements. Partially supporting this possibility, the findings from a study in older women showed that those who obtain calcium primarily from the diet or from both diet and supplements had greater BMD than did those who obtain calcium primarily from supplements (14).

There is some evidence to suggest that participation in nutrition-based interventions, BMD screening, an educational program designed to optimize bone health, or all 3 may lead to long-term behavioral changes with regard to increasing dietary intakes of calcium, vitamin D, or both (10, 15-18). In the present study, however, we found that dietary calcium intakes; the use of supplements with calcium, vitamin D, or both; and daily milk consumption did not differ significantly between the 2 groups 18 mo after the intervention. Although there was a trend for total calcium intake (combined diet and supplement use) to be greater in the milk supplementation group than in the control group at follow-up, dietary calcium intakes did not change significantly in the milk supplementation group from baseline to follow-up. Thus, it would appear that participation in a long-term food-based intervention trial does not significantly influence the dietary behaviors of older men with respect to the intake of dietary calcium. Partially supporting these findings, the results from a 2-y follow-up study to a calcium tablet or milk powder supplementation trial showed that older women were more likely to continue voluntarily taking a tablet than to use a skim-milk powder supplement to maintain calcium intakes (19).

Several factors may explain the lack of a significant difference in total or dietary calcium intakes between the groups at follow-up. First, all of the men in the present study were informed of the study findings, and they received their individual BMD results after the completion of the 2-y intervention. A similar approach was adopted by Dawson-Hughes et al (9), who also reported that both the mean dietary calcium intakes and the use of calcium or vitamin D supplements were no greater in the treatment group than in the control group 2 y after calcium or vitamin D supplementation. Second, it is possible that the measures we used to monitor daily intakes of calcium and milk (3-d food diaries and FFQ) were not sensitive enough to detect any significant between-group differences that may have existed at follow-up. Third, dietary data were collected only at the end of the follow-up period, which may not provide an accurate estimate of the dietary habits of the men throughout the 18-mo follow-up period.

Whereas the strength of this study lies in its long-term follow-up, there were 2 main limitations. First, only 73% of the men who completed the 2-y intervention returned for follow-up testing. However, the characteristics of these men were no different from those of the larger cohort of 149 men who completed the intervention, and the study remained adequately powered to detect significant between-group differences in the change in BMD. For the 2-y intervention, the observed power to detect a significant net beneficial effect of 1.8% and 1.5% at the femoral neck and ultradistal radius, respectively, in favor of the milk supplementation group in this cohort of 109 men was 95% and 82%, respectively. At the end of the follow-up period (month 42), we had 91% and 71% power for the observed 1.4% and 1.1% net differences at these 2 sites. Second, we have no information on the possible mechanism(s) that could explain the sustained effects on BMD in the milk supplementation group. Continued suppression of PTH could reduce the rate of bone loss, and that change could have been achieved by maintenance of a calcium intake equivalent to current recommended intakes in this group, but we did not measure PTH at follow-up. It has also been proposed that the additional protein associated with increased milk consumption may result in an increase in circulating concentrations of insulin-like growth factor-1 (20), an important growth factor known to stimulate bone formation, which may also enhance periosteal apposition. However, it is unlikely that this would explain the sustained benefits for BMD in the milk supplementation group, because we have previously reported no effect of the fortified milk on the quantitative computed tomography–derived total bone cross-sectional area at the midfemur (21).

In conclusion, the results from this study indicate that calcium- and vitamin D3–fortified milk may provide a sustained benefit for BMD in older men, which may help to prevent the development of osteoporosis later in life. Although the underlying mechanism contributing to these long-term beneficial skeletal effects remains to be determined, it is likely to be related to the maintenance of habitual calcium intakes above the current Australian recommended requirements for middle-aged and older men, which may assist in slowing bone loss. However, further long-term follow-up studies are needed to determine whether there is a threshold intake for dietary calcium or vitamin D—or both—above or below which any supplement-related skeletal gains may be maintained.


   ACKNOWLEDGMENTS
 
The authors' responsibilities were as follows—RMD (principal investigator), SB, and CAN: study concept and design; RD and NP: acquisition of data; RD and CAN: analysis and interpretation of the data; RD: drafting of the manuscript; and CAN, SB, and NP: critical revision of the manuscript. None of the authors had a personal or financial conflict of interest.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication July 3, 2007. Accepted for publication September 28, 2007.





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