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CSIRO Health Sciences and Nutrition, Adelaide, South Australia, Australia, 5000
2To whom correspondence should be addressed. E-mail: peter.clifton{at}csiro.au.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • bone turnover • calcium • dairy • humans • weight loss
Energy restriction and weight loss in overweight and obese adults is associated with increased bone resorption (1,2) and a reduction in bone mineral density (BMD)3 (1,3). This has been attributed in part to reduced dietary calcium intake during energy restriction (4). Indeed, calcium supplementation attenuates these changes in bone metabolism (5,6). This effect may be maximized by providing calcium from dairy sources because these foods are associated with greater intestinal calcium absorption compared with supplemental forms (7).
High-protein diets, which are currently popular among dieters, have been criticized for potentially detrimental effects on bone health. These claims are based on metabolic studies that reported acutely elevated urinary calcium excretion after a large intake of isolated protein (8,9). The acid produced as a consequence of protein metabolism obligates increased urinary calcium losses (10,11).
Increased calcium losses, however, do not appear to adversely affect bone metabolism. The literature reports an overall beneficial relationship between high dietary protein and bone health. Large prospective studies showed a positive correlation between dietary protein and high BMD and/or low fracture rate (12–15), although this is not consistently observed (16). Intervention studies also demonstrated that mixed diets rich in protein do not raise calcium excretion (17) or bone turnover (18–20).
Heaney (21) proposed an explanation for this discrepancy between metabolic and "free living" studies. Increases in calcium excretion may reduce extracellular calcium concentration, which stimulates parathyroid hormone circulation (a hormone that increases intestinal calcium absorption). Because dietary calcium is positively associated with protein intake in self-selected diets (22), greater calcium intake and absorption may match the losses associated with increased protein metabolism. In support of this, the relation previously described in prospective studies was not significant at lower calcium intakes (less than 
500 mg/d) (15,19,23,24).
Two longer-term, controlled intervention studies compared the effect of high-protein and high-carbohydrate diets on bone metabolism during weight loss. A 6-mo study that employed high-protein and high-carbohydrate diets consumed ad libitum reported that the change in bone mineral content was correlated with the change in fat mass, independently of protein intake (3). In an energy-controlled 16-wk weight loss study, increased pyridinoline (Pyr) and deoxypyridinoline (Dpr) (markers of bone resorption) excretions were associated with energy restriction, independently of the protein to carbohydrate ratio (25).
The purpose of this study was to investigate whether a protein-rich diet that is also high in calcium minimizes the effect of energy restriction and weight loss on bone turnover. Additionally we tested the effect of high-protein intake on urinary calcium excretion.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Study design. Sixty subjects matched for BMI, gender, age and menopausal status were randomly assigned to one of two treatment groups, high dairy protein diet (DP) or high mixed protein diet (MP). The study consisted of a 12-wk phase of energy restriction (ER) followed by a 4-wk phase of energy balance (EB). Subjects attended the CSIRO Clinical Research Unit (Adelaide, Australia) every 2 wk for consultation with a qualified dietitian and/or clinical measurements; 24-h urine samples were collected in wk 0, 12, 16. Venous blood samples from subjects who had fasted overnight were collected in wk 0, 12, 16. Assessments made during wk 0 represent baseline data; wk 12 and 16 represent the end of ER and EB phases, respectively.
Dietary intervention.
The DP and MP diets were matched in energy (5.5 MJ/d) and macronutrient composition, i.e., high protein (34% energy, 110g/d), moderate carbohydrate (41% energy) and low fat (24% energy). The two diets differed in the type of protein foods (Table 1) and calcium intake (DP, 2400 mg/d; MP, 500 mg/d). An increase in energy intake (up to 7 MJ/d) was made at baseline for active individuals without changing the macronutrient profile.
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60% of total energy intake for 7 d and was equivalent in macronutrient composition between treatment groups. The energy intake to achieve energy balance during wk 12–16 was calculated on an individual basis, i.e., 2000 kJ/d for each 0.5 kg of weight lost per week averaged over wk 8–12. The increased energy was provided mainly by carbohydrate and foods rich in fat (Tables 1, 2).
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Clinical measurements
Body weight and composition. Subjects were weighed every 14 d (Mettler scales, model AMZ14) in light clothing and without shoes after an overnight fast. Height was measured on a stadiometer (Seca) in wk 0. BMI was calculated by weight (kg)/height (m)2. Dual energy X-ray absorptiometry (DEXA; Norland Medical Systems) was performed to assess BMD at wk 0 and 16 (Royal Adelaide Hospital).
Urinalysis. Collection of total 24-h urine output commenced at 0700 h, (not including first morning void) on the day before attending the research clinic and was completed at 0700 h on the day of clinic attendance (including first morning void) in wk 0, 12, and 16. Samples were refrigerated during the collection process; 24-h samples were weighed and aliquots stored at -20°C. Urine samples were measured at the Institute of Medical and Veterinary Science (Adelaide) for creatinine (Cr), urea, calcium, phosphate, and sodium using proprietary techniques on the Olympus AU5400 chemistry analyzer (Japan). Dpr and Pyr were measured using HPLC (27) and expressed per mmol Cr.
Biochemistry. Blood was collected in sodium fluoride/EDTA (1 g/L) tubes for plasma osteocalcin determination and stored on ice until processed. The plasma was isolated by centrifugation for 10 min at 2000 x g (5°C) (Beckman GS-6R Centrifuge CA) and stored at -80°C. Biochemical analyses were performed after study completion and all samples for each individual were measured in one assay. Plasma osteocalcin was measured by an immunometric assay (catalog number LKOC1) on an Immulite Analyzer.
Statistics. All subjects who completed the study were included in the data analysis, independent of reported dietary compliance, indicated by food record, body weight, and urinary urea excretion relative to Cr. Results are presented for 50 subjects, except DEXA (n = 49 subjects) and urinary analysis (n = 47 subjects) due to incomplete data.
Statistical analysis was performed using SPSS11.0 for WINDOWS. Data were assessed for normal distribution. An independent t test was used to assess differences between treatment groups at baseline. Diet data were analyzed using an unpaired t test. ANOVA with repeated measures was used to determine the effects of time (factor), diet (i.e., DP or MP), and gender (between-subject factors). Data were reanalyzed with baseline BMI as a covariate. BMD data were analyzed for interactions with diet, gender, menopausal status, and weight loss. Differences were considered significant if P < 0.05. All data are presented as means ± SEM.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1.2 g protein/kg body weight. Of total protein, 62% was from dairy sources in the DP diet compared with 5% in the MP diet (P < 0.01). Calcium intake was 3.7-fold greater in the DP group than in the MP group, 2371 ± 45 and 509 ± 24 mg/d during ER (P < 0.001) (Table 2). Total energy and the percentage of energy from protein, fat, and carbohydrate during ER and the increase in total energy, carbohydrate, protein, and fat from ER to EB was similar for both diet groups (Table 2). Dietary cholesterol intake was 28% lower in the DP group compared with the MP group during ER and 36% lower during EB. The two diets differed in the percentage of fat from monounsaturated (MUFA), PUFA, and SFA (Table 2). Reported dietary compliance was high. Baseline urinary urea:Cr excretion was not significantly different between treatments or gender (34.3 ± 1.0). Excretion was 18% above baseline during ER (42.0 ± 1.3, P < 0.02) and remained elevated during EB (42.0 ± 1.8, P < 0.02) independent of treatment, indicating similar protein intakes and good dietary compliance. Reported energy intake was consistent with weight loss during ER and weight stability during EB. Two subjects from the DP group had no change in weight or urea:Cr throughout the study.
Weight loss. Overall, body weight decreased by 10% during ER independently of diet and gender (DP; -9.0 ± 0.6 kg, MP; -9.3 ± 0.7 kg). There was no further weight loss during EB (DP; -9.4 ± 0.7 kg, MP; -9.5 ± 0.8 kg).
Bone. There was no change in total BMD from baseline to EB, nor were there any interactions with diet, gender, menopausal status, or weight loss (data not shown).
Urinary markers. Changes in urinary calcium, phosphate, and sodium were independent of diet and gender. There was a trend for decreased urinary calcium excretion from baseline to the end of ER, which was significant at the end of the EB phase, with 33% lower urinary calcium excretion compared with baseline (-1.13 ± 0.3 mmol/d, P = 0.004) (Fig. 1). ER (29.9 ± 1.5 mmol/d) was associated with an 18% reduction (-6.4 ± 2.7 mmol/d, P = 0.012) in urinary phosphate compared with baseline (36.4 ± 2.7 mmol/d) and returned to baseline level by EB (32.8 ± 1.9 mmol/d). Urinary sodium excretion did not change throughout the study (173 ± 14, 160 ± 12, 184 ± 12 mmol/d for baseline, ER, and EB, respectively).
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Urinary calcium excretion.
Increasing protein intake can increase intestinal calcium absorption and therefore urinary excretion (28). As such, a greater calcium excretion was anticipated in DP subjects, yet both treatments were associated with a 33% decrease.
Metabolism of dietary protein (particularly fish, meat, and cheese) is associated with acid generation, which can reduce blood pH (29) and cause obligatory calcium losses (21). Metabolism of noncheese dairy foods, fruit, and vegetables produces alkali, which can partially ameliorate the effect of acid (29). This was demonstrated in a large study (n = 350) in which increasing fruit and vegetable intake from 3.6 servings/d to 9.5 servings/d (serving size not defined by the author), without changing the amount of dietary protein, decreased urinary calcium by two thirds (30). Indeed, in the context of mixed diets, increasing dietary protein did not affect urinary calcium excretion in elderly men [0.6–2.0 g protein/(kg · d)] (31) or postmenopausal women (12–20% of total energy from protein) (18). It is possible that the overall acid load of both diets in our study was low and may partially explain the reduction in urinary calcium excretion.
Lower calcium intake compared with baseline might account for the reduction in the MP group but does not explain the reduction in the DP group, whose calcium intake was 300% greater compared with baseline.
Finally, the reduction in urinary calcium excretion may reflect the effect of a concomitant increase in dietary phosphorus derived from animal proteins. Phosphorus can increase calcium reabsorption in the distal nephron and therefore counter the calciuric effect of reduced blood pH (7).
Bone turnover.
The increase in urinary excretion of both bone resorption markers by wk 16 in both diet groups is likely to be a result primarily of weight loss (1,2). The increases in Dpr:Cr and Pyr:Cr in this study (+46 and +44%) are similar in magnitude to previous findings in obese women (10% weight loss over 6 mo, 500 mg Ca/d), +53 and + 36%, respectively (2).
The significantly larger increase in Dpr:Cr in MP subjects is likely to reflect an additive effect on bone resorption of moderately reduced calcium intake (compared with baseline). A 25-wk weight loss study (n = 31) of overweight postmenopausal women (-10% ± 5.3% body weight) reported that the placebo-treated subjects had significantly greater Dpr and Pyr excretions (37 and 54% respectively) than the calcium-supplemented (1000 mg/d) subjects (P < 0.05) (5). Further, the literature suggests that Dpr is a more specific marker of bone collagen breakdown with lower variability; Pyr is also derived from tendon (32,33). Indeed, Shapses et al. (34) observed a significant increase only in Dpr excretion in premenopausal women during 6 mo of weight loss.
The elevated bone resorption in the MP group was accompanied by increased plasma osteocalcin. This supports previous findings in which osteocalcin excretion increased 18% in a placebo group and was unchanged in the calcium-supplemented group (5). This overall increase in bone turnover in the present study may be unfavorable for maintaining bone mass.
We did not observe any changes in BMD measured by DEXA due to the relatively short duration of this study. In a study by Ricci et al. (5), there was a trend for the low-calcium, placebo-treated group to have greater BMD loss after weight loss (P = 0.08) compared with the calcium-supplemented group, which is consistent with a similar study (6).
The population in this study was not homogenous due to the inclusion of men and pre- and postmenopausal women. However, gender and menopausal status were controlled at baseline and remained evenly distributed after withdrawals. Despite this variability, differences in bone metabolism were observed and were consistent with similar studies that included only pre- or postmenopausal women (2,5,6,35).
In conclusion, we showed that weight loss achieved by high-protein diets is associated with increased urinary excretion of bone resorption markers. This was moderately higher in MP subjects; however, it was also accompanied by an increase in markers of bone formation in this group. Additionally, increased bone turnover occurred despite a reduction in urinary calcium excretion. The reduction in calcium excretion was independent of diet and may reflect the mixed nature of the foods in the prescribed diet. Long-term studies are warranted to investigate the effect of high-protein intakes and rate of bone turnover on bone mineral density.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: BMD, bone mineral density; Cr, creatinine; CSIRO, Commonwealth Scientific and Industrial Research Organization; DEXA, dual energy X-ray absorptiometry; DP, dairy protein; Dpr, deoxypyridinoline; EB, energy balance; ER, energy restriction; MP, mixed protein; MUFA, monounsaturated fatty acids; Pyr, pyridinoline.
Manuscript received 15 October 2003. Initial review completed 3 November 2003. Revision accepted 26 November 2003.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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