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ORIGINAL RESEARCH COMMUNICATION |
1 From CSIRO Health Sciences and Nutrition, Adelaide, Australia
2 Supported by a Medical Research grant from Meat and Livestock Australia.
3 Address reprint requests to M Noakes, PO Box 10041, Adelaide BC, South Australia, Australia 5000. E-mail: manny.noakes{at}csiro.au.
See corresponding editorial on page 1253.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: The objective was to evaluate the effects of a diet with a high ratio of protein to carbohydrate during weight loss on body composition, cardiovascular disease risk, nutritional status, and markers of bone turnover and renal function in overweight women.
Design: The subjects were randomly assigned to 1 of 2 isocaloric 5600-kJ dietary interventions for 12 wk according to a parallel design: a high-protein (HP) or a high-carbohydrate (HC) diet.
Results: One hundred women with a mean (±SD) body mass index (in kg/m2) of 32 ± 6 and age of 49 ± 9 y completed the study. Weight loss was 7.3 ± 0.3 kg with both diets. Subjects with high serum triacylglycerol (>1.5 mmol/L) lost more fat mass with the HP than with the HC diet (
± SEM: 6.4 ± 0.7 and 3.4 ± 0.7 kg, respectively; P = 0.035) and had a greater decrease in triacylglycerol concentrations with the HP (–0.59 ± 0.19 mmol/L) than with the HC (–0.03 ± 0.04 mmol/L) diet (P = 0.023 for diet x triacylglycerol interaction). Triacylglycerol concentrations decreased more with the HP (0.30 ± 0.10 mmol/L) than with the HC (0.10 ± 0.06 mmol/L) diet (P = 0.007). Fasting LDL-cholesterol, HDL-cholesterol, glucose, insulin, free fatty acid, and C-reactive protein concentrations decreased with weight loss. Serum vitamin B-12 increased 9% with the HP diet and decreased 13% with the HC diet (P < 0.0001 between diets). Folate and vitamin B-6 increased with both diets; homocysteine did not change significantly. Bone turnover markers increased 8–12% and calcium excretion decreased by 0.8 mmol/d (P < 0.01). Creatinine clearance decreased from 82 ± 3.3 to 75 ± 3.0 mL/min (P = 0.002).
Conclusion: An energy-restricted, high-protein, low-fat diet provides nutritional and metabolic benefits that are equal to and sometimes greater than those observed with a high-carbohydrate diet.
Key Words: Weight loss • diet composition • high-protein diet • lipids • dual-energy X-ray absorptiometry • bone turnover • nutritional status
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The purpose of the study was to determine the effect of reduced caloric intake, associated with higher dietary protein from low saturated fat sources compared with a high-carbohydrate diet, on weight loss, body composition, cardiovascular disease risk, nutritional status, and markers of bone turnover in overweight and obese women. We hypothesized as our primary outcome that the high-protein diet would enhance fat loss and minimize lean mass loss compared with the high-carbohydrate diet.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The subjects attended individual consultations with 2 dietitians, alternately every 4 wk, throughout the study for instruction on the dietary requirements and methods of recording food intake and for the assessment of compliance. The subjects were issued with digital kitchen scales to weigh food and were advised to consume 
2 cups of low-carbohydrate vegetables per day; they were advised to not eat potato, sweet potato, and avocado. A range of additional low-energy foods was allowed. Two standard servings of alcohol were permitted per week. Eating at restaurants was limited to once every 2 wk. Every 2 wk, the subjects attended the Clinical Research Unit and were supplied with foods consistent with their allocated diet to encourage compliance. Each allocation provided 
60% of the projected total energy intake for 7 d and was isocaloric for both groups.
The foods prescribed to obtain the planned dietary intakes in both diet groups are outlined in Table 2. The total energy content of each diet was initially 5600 kJ, but was adjusted upward for very active subjects so that weight loss would be 1 kg/wk for the first 2–3 wk. The fiber content and fatty acid profile were planned to be the same between diets. Key foods were supplied to the subjects, and the energy content of the foods provided was the same for both diet groups. Specifically, lean red meat was provided in 200-g portion packs and lunch meat, chicken, or fish in 100-g portion packs for 6 meals/wk for the HP group; 80-g packs of chicken and pork plus pasta, rice, biscuits, and whole-meal bread were provided to the HC group. To simulate a quasi ad libitum approach, we advised the HP group that it was compulsory to eat 200 g red meat plus 100 g lunch meat, chicken, or fish daily; the other food items could be consumed according to appetite but not to exceed the amounts specified. Similarly for the HC group, we advised that 80 g chicken or pork plus the bread needed to be consumed daily, and this was isocaloric with the meat component in the HP diet. Checklists of all foods consumed were completed daily, and 3-d weighed food records were analyzed in each 2-wk period. The subjects were interviewed by a dietitian individually every 4 wk. Two qualified dietitians provided the dietary counseling and conducted the nutrient analyses. Both dietitians were trained to provide consistent information to the subjects and on the methods for analysis. Advice on physical activity was also consistent with a recommendation to increase physical activity to 30 min 3 times/wk and to document these occasions in their daily checklist.
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Body weight and composition
Subjects were weighed every 14 d (model AMZ14; Mercury Digital Scales, Japan) while wearing light clothing and no shoes and after fasting overnight. Height was measured with a stadiometer (Seca, Hamburg, Germany) at week 0. BMI was calculated as weight (kg)/height squared (m). Dual-energy X-ray absorptiometry (Norland Medical Systems Inc, Fort Atkinson, WI) was performed at weeks 0 and 12 (Royal Adelaide Hospital, Adelaide, Australia).
Urinalysis
Collection of total 24-h urine output commenced at 0700 (not including the first morning void) on the day before the subjects attended the research clinic and was completed at 0700 on the day of clinic attendance (including the first morning void) at weeks 0 and 12. Urine samples were measured at the Institute of Medical and Veterinary Science (Adelaide, South Australia) for creatinine, urea, calcium phosphate, and sodium by using proprietary techniques with the Olympus AU5400 chemistry analyzer (Tokyo, Japan). Deoxypyridinoline and pyridinoline were measured by using HPLC (13) and expressed per mmol creatinine.
Biochemistry
Fasting blood samples were collected at weeks 0, 4, 8, and 12 in tubes containing either no additives [for the measurement of lipids, insulin, and C-reactive protein (CRP)] or sodium fluoride EDTA for the measurement of glucose. Plasma or serum was isolated by centrifugation at 2000 x g for 10 min at 5 °C (model GS-6R centrifuge; Beckman, Fullerton, CA) and frozen at –20 °C. Biochemical assays were performed in a single assay at the completion of the study. Plasma glucose and serum total cholesterol and triacylglycerol concentrations were measured with a Cobas-Bio centrifugal analyzer (Roche Diagnostica, Basel, Switzerland) with the use of enzymatic kits (Hoffmann-La Roche Diagnostica, Basel, Switzerland) and control sera. Serum HDL-cholesterol concentrations were measured with a Cobas-Bio analyzer after precipitation of LDL and VLDL cholesterol with polyethylene glycol 6000 solution. A modified Friedewald equation was used to calculate LDL cholesterol (14). Insulin was measured in duplicate with a radioimmunoassay kit (Pharmacia & Upjohn Diagnostics AB, Uppsala, Sweden). CRP was measured with an enzymatic kit (Roche, Indianapolis, IN) on a Hitachi auto analyzer (Roche). Osteocalcin was measured with an immunometric assay (catalogue no. LKOC1) on an Immulite Analyzer (Diagnostics Products Corp, Los Angeles, CA).
Homocysteine, iron, ferritin, folate, vitamin B-6, and vitamin B-12 were measured at weeks 0 and 12 in a certified commercial laboratory (Institute of Medical and Veterinary Science, Adelaide, South Australia).
Statistical analysis
All subjects who completed the study were included in the data analysis, independent of reported dietary compliance, as indicated by food records, weight loss, and urinary urea excretion relative to creatinine. The statistical analysis was performed with the use of SPSS 11.0 for WINDOWS (SPSS Inc, Chicago, IL). A univariate analysis of variance was used to assess differences between treatment and triacylglycerol status at baseline and to assess changes in weight and body-composition variables. Dietary data were analyzed by using an unpaired t test. Univariate analysis using the study endpoints, with baseline variable as a covariate, was used to assess the effects of diet (ie, HP or HC). Analysis of variance with repeated measures was also used to determine the effects of time, diet (within-subject factors), and triacylglycerol status (between-subject factors) and interaction effects. Data were reanalyzed with baseline BMI as a covariate. If an interaction was noted, a post hoc subgroup analysis on the differences was performed by using Tukey's test. Differences were considered significant if P < 0.05. All data except baseline characteristics are presented as means ± SEMs.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. There were no significant differences in total energy, alcohol, and dietary fiber intakes between the diet groups. Total, saturated, and monounsaturated fat intakes were significantly lower in the HC group, as was the dietary cholesterol intake. Intakes of the micronutrients thiamine, riboflavin, niacin equivalents, calcium, and iron were significantly higher in the HP group.
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Weight loss was 25% greater with the HP diet in subjects with a triacylglycerol concentration >1.5 mmol/L (P = 0.005), whereas there was no differential effect of diet in women with a low triacylglycerol concentration (Table 4).
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), but a significant interaction was observed with diet and triacylglycerol status on total (P = 0.019) and midriff (P = 0.03) fat. In women with high triacylglycerol concentrations, the total fat loss was 6.4 ± 0.7 kg in the HP group and 3.4 ± 0.7 kg in the HC group (P = 0.035 for diet difference; Figure 2). The amount of weight lost specifically from the midriff area in the HP group was twice that in the HC group, but the difference was not statistically significant by post hoc analysis across the 4 groups (1.0 ± 0.2 kg compared with 0.5 ± 0.1 kg; P = 0.12).
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). Creatinine clearance decreased with weight loss, from 82 ± 3.3 75 ± 3.0 mL/min (8%; P = 0.002), with no significant difference between the diets (P = 0.346). There was no significant change in serum creatinine (74.0 ± 0.9 µmol/L at baseline compared with 75.4 ± 0.8 µmol/L at week 12); therefore, the difference was due to the amount of creatinine excreted in the urine—from 8.9 ± 0.32 to 8.1 ± 0.21 mmol/d. There was no correlation between weight loss and change in creatinine clearance or creatinine excretion. However, adjustment for the change in weight rendered the change in clearance insignificant (P = 0.621), ie, the change in calculated creatinine clearance was due to the weight change and not to a change in renal function.
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). LDL cholesterol decreased overall by 6%, HDL cholesterol decreased by 7%, and glucose concentrations decreased by 4% with both diets. Diet composition affected the decrease in triacylglycerols, which decreased by 8% with the HC diet and by 22% with the HP diet (P = 0.007). Because subjects with high triacylglycerol concentrations may be more responsive to factors that alter triacylglycerols, we reanalyzed the data according to triacylglycerols status (above or below the median of 1.5 mmol/L). There was a diet x triacylglycerol status interaction for triacylglycerol (P = 0.023). In the women with a high triacylglycerol concentration, the HP diet lowered triacylglycerols significantly, by 28% compared with only 10% with the HC diet. In the low- triacylglycerol group, there was no significant effect of diet composition on triacylglycerol (Figure 3). Fasting glucose, insulin, and free fatty acid concentrations all decreased significantly with weight loss, with no differential effect of diet composition (Table 7). CRP decreased significantly overall, by 19% (P < 0.001), with no significant effect of diet (P = 0.447). The change in CRP in the low- triacylglycerol group was 0.74 ± 0.27 mg/L, and the change in the high- triacylglycerol group was 1.90 ± 0.41 mg/L (P = 0.03 for the difference). This difference was enhanced (P = 0.018) after adjustment for weight loss.
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). Transferrin decreased by 9–12% with both diets. There were no significant changes in iron status. Ferritin concentrations were outside the normal range of 150 µg/L in 17 subjects, which suggested that iron stores were likely to be replete and nonresponsive to dietary changes. When these subjects were excluded from the analysis, there was a significant 41% increase in serum ferritin in the HP group but no change in this marker of iron stores in the HC group (P = 0.004 for diet effect; Figure 4). It is interesting to note that ferritin, which has been argued to be an additional marker for metabolic syndrome, was positively correlated with serum homocysteine concentrations at baseline (r = 0.209, P = 0.037).
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). The difference between diets was significant (P < 0.0001). Vitamin B-6 increased with both diets, with no significant difference between them, whereas homocysteine did not change significantly over the intervention. Serum folate increased marginally with time (P = 0.045), with no effect of diet composition (P = 0.234 for diet).
Markers of bone turnover
Osteocalcin increased by 23%, with no significant difference between dietary interventions (Table 8). There was no correlation between the amount of weight lost and changes in urinary crosslinks or the calcium-creatinine ratio. The urinary crosslinks and the calcium-creatinine ratio, however, were inversely related (r = 0.36 for pyridinoline and r = 0.28 for deoxypyridinoline), ie, the greater the decrease in calcium excretion, the smaller the increase in crosslink excretion. Changes in crosslinks or osteocalcin were unrelated to menopausal or triacylglycerol status.
Osteocalcin at week 12 was correlated with the urinary crosslinks at week 12 (P < 0.01) after the adjustment for baseline osteocalcin, but was not related to weight changes (P = 0.723). However, the urinary crosslinks at week 12 were both correlated with the change in weight (P < 0.01) and in osteocalcin (P < 0.05) after the adjustment for baseline values. This suggests that weight loss drives increased bone loss and there is partial compensation with increased bone formation.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Concerns that diets high in meat protein may have deleterious effects on renal function and bone turnover were not substantiated by this study, which showed similar reductions in creatinine clearance with both dietary patterns as a consequence of body mass change. Skov et al (21) assessed changes in renal function by measuring the glomerular filtration rate during high-protein and high-carbohydrate diets over a 6-mo period and also concluded that the HP diet had no adverse effects on kidney function. Johnston et al (15) observed that creatinine clearance was not altered by dietary protein in the context of weight loss, and nitrogen balance was more positive in subjects who consumed the HP diet than in those who consumed the HC diet. Whether this is also true in subjects with compromised kidney function has not been studied, although we have shown an improvement in microalbuminuria in subjects with type 2 diabetes after weight loss with either a high-protein or a high-carbohydrate diet, which suggests that weight loss and consequent blood pressure reduction may be more important in ameliorating renal function than is dietary protein. Last, although the amount of dietary protein was proportionally high, it was not high in absolute terms. The HP diet provided 104 g and the HC diet provided 58 g protein, which is within the range of protein intakes in the Australian population (22). In fact, these intakes represent the 95th percentile and the 20th percentile of protein intakes for women of this age group in Australia.
The effect of this level of protein on markers of bone turnover was similarly not deleterious. Although weight loss appears to enhance both bone breakdown and, secondarily, bone formation, these variables were not significantly different between the 2 diet groups. Other studies have shown that diet-induced weight loss in postmenopausal women is associated with general bone loss, probably because of reduced mechanical strain on the skeleton (23), but that premenopausal women do not lose bone even if they have a low calcium intake during weight loss (24). Evidence also indicates that higher protein intakes, particularly higher animal protein intakes, are associated with decreased bone loss in older persons (25). The reduction in urinary calcium in this study was also unusual because dietary protein metabolism is associated with increased urinary calcium (26). The high vegetable consumption with both dietary patterns may have prevented this because high vegetable intakes have been shown to decrease urinary calcium (27). An increase in calcium excretion was observed with the consumption of a high-protein diet in the study by Johnston et al (15), who state that this was due to the high calcium content of the high-protein diet in this study. However, we did not observe this in other studies of high-protein patterns in which dietary calcium was very high, ie, 2400 mg/d (28).
Cardiovascular disease markers improved with weight loss with both diets; triacylglycerol concentrations decreased more with the HP diet in women with elevated triacylglycerol concentrations. This finding reflects a lower carbohydrate load with the HP diet, which results in reduced VLDL TG production (29). CRP, which is known to decrease with weight loss (30), was not influenced by dietary composition, although there was a suggestion that the HP diet lowered CRP more effectively in women with higher triacylglycerol concentrations. This observation warrants further investigation.
Dietary patterns intended for weight loss, which sustain or improve nutritional status, are important for optimum health. The HC diet pattern was designed to provide a contrasting intake of protein and, as such, did not fully meet the recommended dietary allowance (RDA) for some nutrients, notably calcium and iron. In contrast, nutrient intakes with the HP diet were adequate or exceeded the RDA, which reflected the higher proportion of nutrient-dense protein foods from dairy foods and lean meat in the diet. Hemoglobin concentrations were maintained with both diets. This is in contrast with the findings of Kretsch et al (31), who fed dieting obese women dietary iron at twice the US RDA—half of which was from food and half of which was from an oral supplement—yet found a significant reduction in hemoglobin concentrations. This group also found that hemoglobin and transferrin saturation were both positively correlated with mean performance on a measure of sustained attention. The stability of iron status in the HC group was surprising given both the quantitatively lower iron intake and the theoretically lower bioavailability of iron with this diet, but the higher fruit and vegetable intake may have contributed to optimizing iron absorption.
Pyridoxal phosphate activation, a marker of vitamin B-6 status, decreased with weight loss with both diets, which indicated improved vitamin B-6 status. Vitamin B-6 functions as a cofactor in enzymes involved in transamination reactions required for the synthesis and catabolism of the amino acids as well as in glycogenolysis as a cofactor for glycogen phosphorylase. Vitamin B-6 is found in a wide variety of foods, including beans, meat, poultry, fish, and some fruit and vegetables. Improved vitamin B-6 status is likely to be a function of the improved nutrient density of both dietary patterns compared with baseline eating patterns.
The greatest difference in nutrient status was observed with serum vitamin B-12, which increased by 9% with the HP diet but decreased by 13% with the HC diet. This finding reflected the difference in animal protein sources between the 2 dietary patterns. Ames (32) postulated that micronutrient deficiencies are a major cause of DNA damage by the same mechanism as radiation and many chemicals. Intervention studies in humans have shown that DNA damage is minimized when, among other micronutrients such as folate, serum concentration of vitamin B-12 are >300 pmol/L, which is precisely the concentration achieved with the HP diet in this study without supplementation.
In conclusion, both the HP and HC, which were intended for weight loss, resulted in significant improvements in markers of cardiovascular disease risk, although the HP diet resulted in a greater reduction in triacylglycerol concentrations and improvements in hemoglobin and vitamin B-12 status. An energy-restricted diet high in protein from lean red meat and low-fat dairy products seems to provide a weight loss advantage in subjects with elevated triacylglycerol concentrations—a marker of the metabolic syndrome. This finding requires confirmation in future studies in hypertriglyceridemic women. There was no evidence of adverse effects on bone or renal metabolism with either diet over the 12-wk study period.
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ACKNOWLEDGMENTS |
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MN and PMC designed the study, performed the statistical analysis, and wrote the manuscript. PRF and JBK contributed both to the interpretation of the dietary data and to the preparation of the manuscript and were involved in the dietetic counseling and data analysis. None of the authors had a conflict of interest.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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