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Grand Forks Human Nutrition Research Center, Agricultural Research Service, U.S. Department of Agriculture, Grand Forks, ND 58202-9034 and * Physics Department, University of North Dakota, Grand Forks, ND 58202
3To whom correspondence should be addressed. E-mail: froughea{at}gfhnrc.ars.usda.gov.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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600 mg), but either low or high in meat (12 vs. 20% of energy as protein) for 8 wk each, in a randomized crossover design. After 4 wk of equilibration of each diet, calcium retention was measured by extrinsically labeling the 2-d menu with 47Ca, followed by whole body scintillation counting for 28 d. Urinary and blood indicators of bone metabolism were also determined for each diet. Calcium retention was not different during the high and low meat dietary periods (d 28, mean ± pooled SD: 17.1 and 15.6%, ±0.6%, respectively; P = 0.09). An initially higher renal acid excretion in subjects consuming the high meat compared with the low meat diet decreased significantly with time. The diets did not affect urinary calcium loss or indicators of bone metabolism. In conclusion, under controlled conditions, a high meat compared with a low meat diet for 8 wk did not affect calcium retention or biomarkers of bone metabolism in healthy postmenopausal women. Calcium retention is not reduced when subjects consume a high protein diet from common dietary sources such as meat.
KEY WORDS: • calcium • meat protein • postmenopausal • osteoporosis • renal acid
The high protein content of the Western diet is often cited as a risk factor for osteoporosis or bone fractures (1 –7 ). The calciuretic effect of ingesting purified proteins can result in a negative calcium balance (8 –11 ). However, common protein sources such as meat also provide phosphorus, which reduces urinary calcium (12 ,13 ), and adding meat to the diet may have little or no effect on calcium balance (14 –16 ). Although human balance results suggest that dietary phosphorus reduces protein-induced hypercalciuria, Kerstetter and Allen (17 ) in a review of 15 studies conclude that the presence of phosphorus may not fully restore calcium balance and project that a negative calcium balance of only 25–30 mg/d could reduce body calcium (primarily from bone) by 10% per decade (17 ).
Unfortunately, the balance methodology used in such studies (17 ) is insensitive because of the variability associated with fecal collections and the inability to distinguish the endogenously excreted calcium from the unabsorbed fecal calcium. Only four reports have addressed the effect of meat protein on calcium isotope retention, as measured in blood or stools (15 ,18 –20 ). Spencer et al. (15 ,18 ) have concluded that meat protein does not affect calcium retention, although this conclusion is based on studies with few subjects. Breslau et al. (19 ) have reported that animal compared with vegetable protein increases urinary calcium without influencing calcium absorption, but the phosphorus content of the diet was kept constant and the calcium isotope was not administered with the diet. Heaney (20 ) has reported that, although coingested phosphorus counterbalances the calciuretic effect of protein, it increases intestinal calcium excretion; thus, there is no net effect of phosphorus on calcium balance. However, this finding relies on a statistical correction for the variability in phosphorus intake, rather than on a direct control of phosphorus in the diet.
Cross-sectional studies have only contributed to the controversy about dietary protein and bone health. Dietary protein, assessed from self-reported food intakes, has been correlated positively (21 –23 ), negatively (24 ,25 ) or not at all (26 ,27 ) with bone mineral density and/or fracture risks.
To test whether increasing dietary protein from meat adversely affects calcium retention and bone metabolism, healthy postmenopausal women were studied using controlled high and low meat diets for 8 wk each in a randomized crossover design. Radiotracer and whole body scintillation counting methodology enabled sensitive measurement of total calcium retention, a net function of differences in absorption, urinary excretion, intestinal excretion or any other routes of calcium loss.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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-2, as determined by dual-energy X-ray absorptiometry (Hologic QDR 2000, Waltham,MA); they had normal thyroid, liver and kidney functions; they were willing to discontinue any nutritional supplements as soon as their applications were received; they did not regularly use any medications (except for hormone replacement therapy); and had body mass index (BMI) 
32 kg/m2. The study was approved by the University of North Dakota’s Radioactive Drug Research Committee and Institutional Review Board, and by the USDA Radiological Safety Office. The study was explained verbally and in writing by the investigators and written informed consent was given by each woman.
Of 18 women enrolled, one was dismissed for illness, and two were excluded for noncompliance. The remaining 15 (14 white, one Asian; 6 using hormone replacement therapy) were age 60.5 ± 7.8 y (mean ± SD), with BMI of 26.5 ± 4.0 kg/m2 and femoral bone mineral density of 0.707 ± 0.121 g/cm2. As estimated from 3-d food records, their calcium and protein intakes before the study were 774 ± 279 mg/d and 71 ± 14 g/d, respectively.
Diets.
Weighed high and low meat diets using ordinary foods in a 2-d menu cycle (Table 1
) provided similar amounts of calcium (600 mg/d) and energy (9.6 ± 0.9 MJ, or 2286 ± 222 kcal), with 20 and 12% of energy as protein (1.62 ± 0.15 and 0.94 ± 0.09 g/kg body weight), and 297 and 45 g/d of meat (10.5 and 1.6 oz/d), respectively (Table 1)
. The amount of calcium in the diet was chosen to mimic typical intakes by postmenopausal women in the United States (599 ± 16 mg/d) (28
). Furthermore, the effects of dietary protein on calcium retention were expected to be more pronounced when calcium intake was inadequate. To keep the diets isoenergetic without substantially increasing the phytate content, added vegetable fat and low fiber complex carbohydrates were used as substitutes for meat. To maintain body weights, energy intakes were adjusted by proportionally changing the amounts of all foods. Coffee, tea and artificially sweetened, noncola carbonated beverages (containing citric acid rather than phosphoric acid) were individualized, limited to two total servings daily and kept constant. Similarly, salt consumption was individualized and kept constant during the two dietary periods; mean sodium intake was 3759 and 3782 mg during the low and high meat dietary periods, respectively. City water and chewing gum were consumed as desired, after analyses indicating minimal mineral content. The participants were given a list of approved over-the-counter medications, toothpaste and dental adhesives that contained minimal amounts of calcium or other minerals. All diet ingredients except water were weighed to 1% accuracy, prepared and provided to the participants. The participants consumed the food quantitatively, with the aid of spatulas and rinse bottles, consuming one meal at the research center on weekdays, and the remaining foods elsewhere. Because the study was scheduled during the winter months in North Dakota (latitude 47.5° N), all participants received a daily multivitamin supplement that included 20 µg of cholecalciferol (see footnote Table 1
).
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Dietary calcium retention was measured with a 47Ca radiotracer and whole body scintillation counting (29 ), with adjustments to disregard 47Sc activity. The 47Ca isotope was obtained by neutron activation (University of Missouri, Columbia, MO) of stable 46Ca (as calcium carbonate, 30.89% enriched; Oak Ridge National Research Laboratory, TN). The custom-made scintillation counter (30 ) detects gamma emissions with 32 crystal NaI(T1) detectors (10 x 10 x 41 cm each), arranged in two planes above and below a bed.
After 4 wk of dietary equilibration, the 2-d menu was labeled with 148 kBq (4 µCi) 47Ca (<4 µg elemental calcium). Because of the concern that ingested calcium from some dietary sources may not form a common absorptive pool (31 ), both diets were designed with milk as the primary source of calcium. For each meal, the tracer was mixed with milk and allowed to equilibrate overnight. The specific activity (ratio of 47Ca to elemental calcium) was constant for all meals for each individual. The energy provided by the radiolabeled meals was constant between the two diets for each participant. All labeled meals were consumed at the research center.
The initial total body activity was determined from the whole body count 1–3 h after the first labeled meal (before any isotope was excreted), divided by the fraction of the total activity in the first meal. Whole body calcium retention was monitored for 28 d. Activity was corrected to the midpoint of the 2nd d of labeled meals and adjusted for background and minor fluctuations in the measurement of a 47Ca standard distributed in water (32 ). The precision of the whole body counting measurements was 1.4%.
Analyses.
The subjects provided total 48-h urine collections during wk 3, 5 and 8 of each dietary period. Blood samples were drawn at wk 4 and 8 of each dietary period. Calcium in the urine and acid-digested diet aliquots (33 ) was determined by inductively coupled argon plasma emission spectrophotometry. Mean (±SD) measurements were 98 ± 4% of certified values for calcium in a standard reference material (Typical Diet, 1548b, U.S. National Institute of Standards and Technology).
Urinary ammonium was determined colorimetrically (34
) (Raichem; Hemagen Diagnostics, San Diego, CA). Titratable acidity was determined in undiluted urine by titrating to pH 7.40 with 0.1 mol/L NaOH. Free organic acids were measured by the method of Van Slyke and Palmer (35
) as modified by Lemann et al. (36
). Urinary sulfates were determined turbidometrically (37
). Enzyme-linked immunoassays were used to determine serum bone-specific alkaline phosphatase (Metra Biosystems, Mountain View, CA), estradiol (Abbott Laboratories, Abbott Park, IL) and urinary cyclic adenosine monophosphate (cAMP; Biomedical Technology, Shoughton, MA). Serum tartrate-resistant acid phosphatase activity was determined using 
-naphthylphosphate and diazotized-2-amino-5-chlorotoluene as substrates (38
). Creatinine clearance was calculated from serum and urinary creatinine, which were measured using alkaline picric acid (39
). Serum parathyroid hormone (PTH), calcitonin, osteocalcin (Diasorin, Stillwater, MN) and 25-hydroxy vitamin D (INSTAR, Stillwater, MN) were determined by radioimmunoassay. Serum insulin-like growth factor 1 (IGF-1; Diagnostic Systems Laboratory, Webster, TX) and urinary N-telopeptides (Ostex, Seattle, WA) were determined by enzyme-linked immunosorbant assays. Plasma-ionized calcium was measured with an electrode (Nova 8+ Electrolyte Analyzer, Waltham, MA) (40
).
Statistics.
Individual 47Ca retention data were modeled with a two-component exponential equation:
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where y represents 47Ca retention as a percentage of the administered dose, t represents the time (in h) and coefficients ß1 and ß2 represent the turnover of the radiotracer (%) at rates k1 and k2, respectively. Because of the early delay in isotope elimination related to the gastrointestinal transit of unabsorbed isotope, calcium retention data for d 2–5 were not included in the model. The percentage of 47Ca absorbed was separately estimated from the y-intercept of the linear portion (d 9–28) of a semilogarithmic retention plot [ln (% 47Ca retained) vs. time].
Diet and sequence effects were evaluated using repeated-measures ANOVA followed by Tukey’s contrasts (41
). Variances in the data were expressed as pooled SD from the ANOVA. When data were not normally distributed, they were logarithmically transformed and both transformed and geometric means are reported. Using two-tailed probabilities, P 0.05 was considered significant. The diet sequence did not significantly affect any of the reported variables.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Calcium retention was not adversely affected by the high meat diet; rather, calcium retention was similar, if not slightly improved, compared with that of the low meat diet (Fig. 1 , Table 2 ). As indicated by the two-component exponential model, about 74% of the calcium tracer was cleared rapidly from the body. This represented early elimination of the unabsorbed isotope as well as short-term endogenous urinary and fecal excretion, with biological half-lives of 1.7 and 1.5 d, associated with the high and low meat diets, respectively (Table 2) . The remaining calcium tracer was eliminated less rapidly with biological half-lives of 56 and 40 d in subjects consuming the high compared with the low meat diets, respectively (P = 0.04; Table 2 ). Thus, loss of calcium tracer from the body was slightly but significantly greater in subjects consuming the low meat compared with the high meat diet. Other measures from the exponential model of calcium retention were not affected by diet (Table 2) .
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Percentage calcium absorption was not different in subjects consuming the high compared with low meat diets (29.9 vs. 28.4%, Table 2 ), with about 178 and 175 mg calcium absorbed daily, respectively. Calcium retention also was not different in the two diets in women using hormone replacement therapy (n = 6). Although the mean calcium retention in subjects consuming the two diets tended to be slightly lower in these women, compared with the women not using hormone replacement (n = 9), this difference was not significant (d 28: 14.4 and 18.0%, ±2.0, respectively; P = 0.08). At least 12 subjects per group would have been needed (with 90% power) to detect a 5 percentage point difference in calcium retention between the hormone replacement therapy users and nonusers.
Biomarkers of bone metabolism.
Diet did not affect biomarkers of bone formation (serum bone-specific alkaline phosphatase, osteocalcin and IGF-1) or of bone resorption (serum tartrate-resistant acid phosphatase, urinary N-telopeptides) (Tables 3 and 4 ). Several other indices of bone and mineral metabolism, such as intact PTH (and urinary cAMP, an indicator of PTH secretion), estradiol, 25-hydroxy-vitamin D and plasma ionized calcium, were also unaffected (Tables 3 and 4) . Although urinary hydroxyproline concentration was greater when subjects consumed a high meat diet than when they consumed a low meat diet (P < 0.001), this was likely attributable to the greater dietary collagen content (39 ), rather than to bone resorption (Table 4) .
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Urinary acidity adapted with time in subjects consuming the two diets. Although the urinary pH was lower after 3 wk when women consumed the high compared with the low meat diet (5.68 and 6.02), this difference decreased with time, from 0.34 to 0.02 and 0.03 pH units at 3, 5 and 8 wk, respectively (P < 0.05; Table 4 ). Similarly, a greater urinary titratable acidity when women consumed the high compared with the low meat diet was moderated by time with differences of 15.6, 11.1 and 4.9 mEq/d, at 3, 5 and 8 wk (P < 0.05; Table 4 ), respectively. This continually diminishing difference suggests that further adaptation may have occurred beyond 8 wk. Urinary free organic acid excretion, representing compounds such as citric, lactic and acetic acids, was marginally, but not significantly, higher (P = 0.07) when women consumed the high meat diet (Table 4) , and this difference was also smallest at 8 wk.
As expected, the higher exogenous substrates provided by the high compared with the low meat diet (Table 1) significantly increased urinary ammonium, sulfate, creatinine and phosphorus at all time points (Table 4) . The high compared with the low meat diet increased creatinine clearance (1.38 and 1.21 mL/s, respectively, P < 0.05; Table 4 ), without affecting blood creatinine concentrations (80 ± 9 µmol/L). This likely reflected a difference in the substrate load, rather than in the glomerular filtration rate (GFR) of these healthy women (see Discussion).
Despite differences in urinary acidity and excreta, urinary calcium loss between 3 and 8 wk was unaffected by diet. Urinary calcium was 2.45 and 2.38 ± 0.88 mmol/d in subjects consuming the high and low meat diets, respectively, without detectable change over time (Table 4) .
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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= 0.05, two-tailed test). Data from 14 subjects did not show the hypothesized difference. The calciuretic effect of dietary protein has been partially attributed to an increased GFR (17 ,42 ). Increased protein intake from isolated protein sources has been repeatedly reported to increase GFR (10 ,11 ,13 ,42 ,43 ) by 10–20%, as measured by creatinine clearance, a magnitude similar to the present results with meat as the protein source (Table 4) . However, creatinine clearance is not a direct measure of GFR, given that small quantities of creatinine are reabsorbed or secreted in the renal tubules, and because a stable intake and endogenous production of creatinine is assumed (39 ). The latter assumption cannot be applied in the present study because meat was an exogenous source of creatinine. The assumption also may not be applicable with an increased intake of isolated proteins, which may increase endogenous creatinine production (44 ,45 ). Unfortunately, previous studies of increased GFR with increased intake of isolated proteins (10 ,11 ,13 ,42 ,43 ) did not report total creatinine excretion. In the present study, the apparent greater creatinine clearance associated with the high meat diet was proportional to a comparable increase in urinary creatinine excretion, without affecting urinary calcium (Table 4) .
The calciuretic effect of protein has also been related to an increase in renal acid load, which in this study adapted over time. The potential renal acid load when women consumed the high meat diet was estimated to be about twice that when women consumed the low meat diet (60 vs. 30 mEq/d) using the method of Remer and Manz (46 ), which assumes constant absorption of dietary minerals and electrolytes (without allowing for adaptation over time). The higher dietary acid load during the high meat dietary period was reflected in the higher initial renal acid excretion; however, this difference abated between 3 and 8 wk (Table 4) . Furthermore, despite this early difference in urinary acid excretion and the continuing greater excretion of sulfate and ammonium, urinary calcium excretion was not different at any time point tested. Similarly, in previous studies, although addition of meat to the diet has been associated with hypercalciuria in studies of 3 (47 ) or 15 d (48 ), Spencer and co-workers (15 ) have reported adaptation that almost completely reversed an initial hypercalciuria in a single subject studied for 72 d. Urinary calcium excretion by postmenopausal women, measured during the last 18 d of 7-wk controlled diets (in a crossover design), does not differ between high and low meat diet periods (14 ). The present results concurred with these latter studies (14 ,15 ) and suggest that if early hypercalciuria occurred in response to the high meat diet, it was reversed by adaptation within 3 wk, despite a more gradual adaptation in acid excretion (Table 4) . In contrast to meat protein, with increased intakes of isolated protein sources for 75 (42 ) or 95 d (10 ), no adaptation in renal acid excretion or hypercalciuria was observed. This difference in adaptation may reflect differences in the protein source.
This study’s results were consistent with previous observations that coingested phosphorus offsets the hypercalciuric effect of protein, possibly through a PTH-mediated mechanism (49 ), and that net calcium balance is not reduced (14 –16 ,18 ,50 ). Our calcium retention results were in contrast to the observation, using less controlled protein intakes with subsequent statistical correction of dietary variables, that phosphorus in meat increases endogenous fecal calcium loss (20 ,51 ). The 8 wk of controlled diets in the current study allowed evaluation of calcium retention as a function of both absorption and excretion, after allowing 4 wk for dietary adaptation, and with a constant intake of other factors that may affect calcium retention, such as sodium and caffeine (28 ). In this study, the higher urinary excretion of sodium and potassium (Table 4) suggests that cations other than calcium may be involved in the renal handling of the extra acid ash produced by a high meat diet.
The conclusion that a high meat diet did not adversely affect the net calcium retention is further supported in this study by the absence of changes in clinical indicators of bone formation and resorption and by several cross-sectional studies that indicated a positive association between dietary protein intake and bone health (21 ,23 ,52 –56 ). This is in contrast to short-term (4 d) observations of increased bone resorption, as indicated by hypercalciuria and increased urinary telopeptide, in women who consumed a high protein diet (57 ) or when meat protein was compared to other protein sources (58 ). The present results emphasize the need to allow time for adaptation when investigating changes in protein intake.
In summary, using controlled diets and whole body counting tracer methodology with supportive clinical chemistry, this study indicates that adding meat to the diet does not adversely affect calcium retention and bone metabolism in postmenopausal women. These findings are in contrast to the long-standing belief that a high meat intake negatively affects the body’s calcium status and thus bone health.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products that may also be suitable. The U.S. Department of Agriculture, Agricultural Research Service, Northern Plains Area, is an equal opportunity/affirmative action employer and all agency services are available without discrimination.
4 Abbreviations used: BMI, body mass index; cAMP, cyclic adenosine monophosphate; GFR, glomerular filtration rate; IGF-1, insulin-like growth factor 1; PTH, parathyroid hormone.
Manuscript received 18 October 2002. Initial review completed 7 November 2002. Revision accepted 21 November 2002.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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