Minerals, trace elements, Vit. D and bone health

Effect of a dairy- and calcium-rich diet on weight loss and appetite during energy restriction in overweight and obese adults: a randomized trial

Abstract

Background/objectives:

A diet rich in dairy and calcium (Ca) has been variably associated with improvements in body composition and decreased risk of type 2 diabetes. Our objective was to determine if a dietary pattern high in dairy and Ca improves weight loss and subjective appetite to a greater extent than a low dairy/Ca diet during energy restriction in overweight and obese adults with metabolic syndrome.

Subjects/methods:

A total of 49 participants were randomized to one of two treatment groups: Control (low dairy, 700 mg/day Ca, −500 kcal/day) or Dairy/Ca (high dairy, 1400 mg/day Ca, −500 kcal/day) for 12 weeks. Body composition, subjective ratings of appetite, food intake, plasma satiety hormones, glycemic response and inflammatory cytokines were measured.

Results:

Control (−2.2±0.5 kg) and Dairy/Ca (−3.3±0.6 kg) had similar weight loss. Based on self-reported energy intake, the percentage of expected weight loss achieved was higher with Dairy/Ca (82.1±19.4%) than Control (32.2±7.7%; P=0.03). Subjects in the Dairy/Ca group reported feeling more satisfied (P=0.01) and had lower dietary fat intake (P=0.02) over 12 weeks compared with Control. Compared with Control, Dairy/Ca had higher plasma levels of peptide tyrosine tyrosine (PYY, P=0.01) during the meal tolerance test at week 12. Monocyte chemoattractant protein-1 was reduced at 30 min with Dairy/Ca compared with Control (P=0.04).

Conclusions:

In conclusion, a dairy- and Ca-rich diet was not associated with greater weight loss than control. Modest increases in plasma PYY concentrations with increased dairy/Ca intake, however, may contribute to enhanced sensations of satisfaction and reduced dietary fat intake during energy restriction.

Introduction

The consumption of dairy foods and calcium (Ca) has been variably linked to regulation of body weight and risk of type 2 diabetes.1 Part of the variability stems from the examination of low-fat dairy foods and/or Ca intake within two distinct contexts, one of which is energy balance and weight maintenance and the other of which is energy restriction and weight loss.1, 2, 3, 4 Furthermore, discrepancies between studies may be due to variation in the type of dairy foods (yogurt versus milk), in total Ca intake or source of Ca. A threshold of Ca intake of 600–800 mg/day has been proposed for the beneficial effects on weight regulation.1 Moreover, whether elemental Ca supplementation in combination with increased dairy food intake is effective for weight management in humans requires clarification.

The individual dairy proteins (whey and casein) may enhance satiety via increases in circulating appetite-regulating hormones including glucagon-like peptide-1 (GLP-1).5, 6 A recent 6-month study found an attenuation in desire to eat and hunger during weight loss when participants consumed milk,7 although the mechanism remains unclear as there were no changes in ghrelin or leptin. Similarly, a single meal study found no effect of dairy foods on GLP-1, ghrelin, peptide tyrosine tyrosine (PYY), and cholecystokinin.8 Ca may affect energy intake as seen in a 15-week study where Ca plus vitamin D supplementation reduced spontaneous fat intake, although the effect was only seen in a small sub-population with very low-Ca intake.9 In addition to regulating appetite, dairy and/or Ca may influence metabolic health via upregulation of genes associated with metabolic rate;10 enhanced fecal fat excretion;11 and by mediating the inflammatory response.12

As reviewed by Teegarden and Gunther,2 evidence in support of the hypothesis that dairy foods and/or dietary Ca influence appetite control and food intake remains inconclusive. Our primary objective was to determine if a dietary pattern high in dairy and Ca, derived from both dairy foods and a Ca supplement, would improve weight loss and appetite regulation during energy restriction (−500 kcal/day). Specifically, we examined plasma glucose-dependent insulinotropic polypeptide, GLP-1, ghrelin, leptin and PYY concentrations and subjective appetite ratings in overweight and obese adults with metabolic syndrome. Glycemic, insulinemic and inflammatory cytokine responses were also examined.

Subjects and methods

Subjects

Forty-nine men and women (body mass index 27–37 kg/m2), 20 to 60 years with metabolic syndrome were recruited from Calgary, AB, Canada. In all, 23 were randomized to Control and 26 to Dairy/Ca (Supplementary Figure 1). The National Cholesterol Education Program Adult Treatment Panel III guidelines were used to identify metabolic syndrome.13 Exclusion criteria included: type 1 diabetes; type 2 diabetes treated with oral hypoglycemic agents or insulin therapy; hemoglobin A1c >8%; liver or pancreas disease; major gastrointestinal surgeries; pregnancy or lactation; cardiovascular disease; alcohol or drug dependence; milk allergy or lactose intolerance; use of a diet, supplement or exercise regime designed for weight loss; body mass >159 kg; fibrate or statin use; chronic use of laxatives, antacids, Ca, or vitamin D; or high habitual Ca intake. A registered dietitian assessed typical Ca intake using verbal recall. All enrolled participants had self-reported low dairy and Ca (<700 mg/day)7, 9 intake at baseline. All participants provided written informed consent. Ethical approval was provided by the Calgary Conjoint Health Research Ethics Board. This study was registered at ClinicalTrials.gov (NCT00564551). A power calculation with an α of 0.05 and power of 0.80 indicated a minimum of 18 participants per group would be required.

Intervention

Before the start of the intervention, participants attended an orientation in which motivational interviewing was used to encourage adherence.14 Instructions regarding use of a food scale, meal plans and 3-day food records were provided. Participants were randomized (random number generator; stratified according to body mass index and sex) to either Control or Dairy/Ca and provided with an individualized meal plan that prescribed a 500 kcal/day energy deficit. Control meal-plans included one serving of dairy (non-fat or 1% milk or yogurt) with total Ca 700 mg/day. Dairy/Ca meal-plans prescribed 3–4 servings of dairy (non-fat or 1% milk or yogurt) and included a daily 350 mg Ca supplement (Cal-Chews, Jamieson Laboratories Ltd, Windsor, ON, Canada) with total Ca 1400 mg/day.

An initial 3-day food record was completed by participants before the first meal tolerance test (MTT) to gain a baseline estimate of energy requirements.15 This estimate was refined using the Mifflin-St. Jeor equation and an activity factor.16 Individualized diet plans providing a 500 kcal/day energy deficit and based on Canada’s Guidelines for Healthy Eating (30% fat, 20% protein and 50% carbohydrates) were devised. The majority of carbohydrates were whole grains, vegetables and fruit. Dietary intake during the study was measured via 3-day food records at 3, 6, 9 and 12 weeks. Diet Analysis Plus 8.0 software was used for analysis (Thomson Wadsworth, Toronto, ON, Canada).

Physical activity

Participants were instructed not to change their exercise habits during the study. Exercise levels were quantified at baseline and week 12 using Godin’s Leisure Score Index Questionnaire.17

Physical characteristics

At baseline and week 12, body composition was assessed with dual-energy x-ray absorptiometry (DXA) (Hologic QDR 4500, Hologic, Inc., Bedford, MA, USA). Weight was measured using a balance beam scale at baseline, weeks 3, 6, 9 and 12. At baseline and week 12, height, waist circumference and blood pressure were measured.

MTT and blood sampling

At baseline and week 12, a blood sample was collected in the morning after 12 h of fasting. Participants then consumed a standardized meal consisting of 50 g white bread, 50 g rye bread, 30 g cheddar cheese, 10 g butter, 20 g fruit jam and 200 ml unsweetened orange juice (605 kcal; 56% carbohydrate, 11% protein, and 32% fat).18 Postprandial blood samples were collected via antecubital vein cannula at 30, 60, 90, 120 and 240 min following the first bite of the meal according to our previous protocol.19

Plasma analysis

Glucose was determined via Trinder assay (Stanbio Laboratory, Boerne, TX, USA). Ghrelin (active), GLP-1 (active), glucose-dependent insulinotropic polypeptide (total), leptin, insulin and PYY (total) concentrations were quantified using a Human Gut Hormone Milliplex kit (Millipore, St Charles, MO, USA). Concentrations of interleukin 1 beta (IL-1ß), IL-6, monocyte chemoattractant protein-1 (MCP-1), and tumor necrotic factor alpha were quantified using Human Adipokine Milliplex kits (Millipore). Calgary Laboratory Services (Calgary, AB, Canada) measured hemoglobin A1c.

Subjective appetite scores

Subjective sensations of appetite were determined with 100 mm visual analog scales (VAS).20 Weekly VAS were distributed at baseline for completion by the participants each week at home. Participants were asked to complete VAS following a meal, at the same time on the same day each week. In addition, each subject was asked to complete VAS throughout the MTT. Questions took the form of ‘How full do you feel?’ or ‘How much do you think you can eat?’ and were anchored by ‘not at all full’ or ‘nothing at all’ and ‘totally full’ or ‘a lot’.

Statistical analysis

Data is presented as mean±s.e. and only includes those who completed the trial. Physiological measures, food record and VAS data were analyzed via two-factor repeated-measures analysis of variance with Bonferroni adjustment (time (week 0 and week 12) and diet (Control or Dairy/Ca)). Change from baseline was determined by subtracting initial value from final value and analyzed by analysis of variance. Hormone and glucose concentrations during the MTT were analyzed via two-factor repeated-measures analysis of variance with a Bonferroni adjustment (time (0–240 min) and diet) as variables or two-factor analysis with week (0, 3, 6, 9, 12 weeks) and diet). Data were analyzed with SPSS v. 17.0 software (SPSS Inc, Chicago, IL, USA).

Results

Baseline characteristics

Forty-nine individuals were enrolled with 38 participants completing the study (Table 1). Reasons for dropping out included pregnancy (n=1), change in employment (n=2), illness (n=2) or personal (n=6). There were no differences in the baseline characteristics between groups (all: P>0.05) except for bone mineral density (P=0.04; Table 1). Physical activity did not change during the study (P>0.05).

Table 1 Clinical and biochemical characteristics of participants at baseline and after 12 weeks of dietary treatment in the control or dairy/Ca groupsa

Body composition

Weight loss was −2.2±0.5 kg and −3.3±0.6 kg (P=0.16) in the Control and Dairy/Ca groups, respectively (Table 1). The change in lean body mass (LBM), from week 0 to week 12, was significantly different between groups (P=0.03) with a slightly greater decrease in Dairy/Ca versus Control (Table 1). Bone mineral content was significantly higher in Dairy/Ca compared with Control at week 12 and the change in bone mineral content showed a decrease in Control (−2.8±9.6 g) and increase (32.2±12.9 g) in Dairy/Ca (P=0.04; Table 1).

Satiety and hunger hormones

The change in PYY total area under the curve (tAUC) from baseline to week 12 was significantly greater for Dairy/Ca compared with Control (P=0.01; Figure 1a). During the MTT, the change from baseline to week 12 was significantly greater for Dairy/Ca versus Control at 0 min (P=0.04), 30 min (P=0.01) and at 240 min (P=0.01; Figure 1b). PYY, GLP-1, glucose-dependent insulinotropic polypeptide and ghrelin curves are shown in Supplementary Figure 2. At the end of the study, the change between baseline and week 12 GLP-1 concentrations at 240 min was significantly greater with Dairy/Ca (P=0.02; Supplementary Figure 2B). There were no differences in leptin (Supplementary Figures 3A and D), although there was a positive correlation between body fat and fasting leptin (r=0.70, P<0.01) and leptin total area under the curve (r=0.68, P<0.01).

Figure 1
figure1

Delta total area under the curve (a) and change from baseline values for plasma PYY (b) during a 4-h MTT in participants consuming control or dairy/Ca at week 0 and week 12. Values are means±s.e., n=18 (control) and n=20 (dairy/Ca). Control, □Dairy/Ca. *Different from control at indicated time point, P<0.05.

Subjective appetite scores

Dairy/Ca reported feeling ‘more satisfied’ in the weekly assessment of subjective appetite sensations (P=0.01; Figure 2a). There was a significant interaction between time and diet (P=0.03) for the question ‘how comfortable do you feel?’ wherein Control felt less comfortable from baseline (63±7 mm) to week 12 (45±6 mm) and Dairy/Ca felt more comfortable at week 12 (59±4 mm) compared with week 0 (50±5 mm). At week 0 and week 12, participants also completed VAS during the MTT (Supplementary Figure 4), wherein there was a significant effect of time for ratings related to hunger, satisfaction, fullness, prospective consumption, and desire to eat something sweet, salty or meat and fish (P<0.05). There were no diet differences at week 12, although there was a trend (P=0.1) for greater fullness in Dairy/Ca versus Control when ratings were normalized for fasting scores.

Figure 2
figure2

Weekly subjective rating of satisfaction (a) and regression analysis (b) showing the relationship between delta energy intake from week 0 to week 12 (kcal) and Ca (mg) intake. In (a), values are means±s.e., n=18 (control) and n=20 (dairy/Ca). Control, □Dairy/Ca. *Different from control at indicated time point, P<0.05. In (b), the regression is represented by R=0.40, r2=0.16, df=28, P=0.027.

Food intake and ‘feed efficiency’

Energy intake

Total energy intake was significantly higher at baseline compared with weeks 3, 6, 9 and 12 (P<0.05; Table 2) but did not differ between groups. As expected, there was a reduction in daily energy intake throughout the study in both groups (Table 2; P<0.01). There was an effect of week (P<0.01) and diet (P<0.03) on fat intake. Both groups reduced their fat intake during the study, however, Dairy/Ca consumed less energy as fat compared with Control (P=0.02). Expressed as a function of body weight, Dairy/Ca consumed less fat (0.58±0.04 g/kg) versus Control (0.78±0.07 g/kg; P=0.015). Using the self-reported reduction in energy intake, we calculated the percent expected weight loss achieved by subjects (observed weight loss/expected weight loss × 100). Dairy/Ca achieved a greater percentage of expected weight loss (82.1±19.4%) compared with Control (32.2±7.7%; P=0.03). The correlation between percent expected weight loss achieved and delta energy intake approached significance (r=0.351; P=0.086). Feed efficiency, classically measured as weight gain per unit energy consumed in animal studies,21 was similarly calculated in this study to capture weight loss per unit restricted energy intake. There was no significant difference (P=0.35) between Control (0.053±0.012 g weight loss/kcal restricted) and Dairy/Ca (0.100±0.038 g weight loss/kcal restricted).

Table 2 Daily dietary intake of participants at baseline and during the 12 weeks of dietary treatment in the Control or Dairy/Ca groupsa

Ca and vitamin D intake

Daily Ca intake during the study was significantly higher in Dairy/Ca versus Control (Table 2; P<0.001). Baseline dairy intake was similar between groups but as expected higher in Dairy/Ca versus Control during the study. Vitamin D intake at baseline and during the study was significantly higher in Dairy/Ca (P<0.05; Table 2). The relationship between delta energy intake from baseline to week 12 (kcal) and Ca (mg) intake was significant (R=0.40, r2 =0.16, df=28, P=0.027; Figure 2b). The r2 value implies that 16.3% of variation in total energy intake can be explained by Ca intake. There was no significant relationship between anthropometric measures (LBM or fat mass) and Ca intake (P>0.05).

Glucose homeostasis and inflammation

The change in glucose total area under the curve from week 0 to week 12 was −111±48.4 mmol/l 240/min in Dairy/Ca and −23.3±71.7 mmol/l 240/min in Control, which did not differ (P>0.05). No differences in fasting or total area under the curve were detected for insulin (Supplementary Figures 3C and F).

Fasting IL6, tumor necrotic factor alpha, MCP-1 and IL1ß remained constant over the 12 weeks (Supplementary Table 1). There was a significant reduction (P=0.04) in baseline adjusted MCP-1 concentration at 30 min for Dairy/Ca (−18.7±7.5 pg/ml) versus Control (4.6±7.5 pg/ml).

Discussion

Across a range of human and rodent studies there have been inconsistent results regarding the role of dairy and/or Ca in regulating body weight, appetite and glucose homeostasis.1 Our findings demonstrate that in the context of energy restriction, a dietary pattern rich in dairy foods and Ca results in modest increases in plasma PYY concentrations, enhanced subjective ratings of feeling satisfied and reduced dietary fat intake, but does not accelerate weight loss compared with a low dairy/Ca diet.

Participants consuming dairy/Ca had weight loss that was similar in magnitude to control. This is consistent with findings from Van Loan et al.22 showing no difference in body weight or fat loss between low dairy or high dairy energy-restricted diets. Similarly, a recent meta-analysis showed no differences in body weight changes between dairy intervention and control groups.3 With subgroup analysis, however, dairy was shown to reduce body weight (−0.79 kg) in studies imposing energy restriction.3 This is similar to the meta-analysis of Abargouei et al.4 that found no overall difference for the effect of dairy on body weight but did find a significant reduction in body weight and fat mass within the energy-restricted subgroup. Although weight loss did not differ in our study, the modest indications of improved appetite regulation with dairy may be clinically relevant. In the context of weight management for consumers, foods that oppose the physiological consequences of energy restriction and the feelings of deprivation that accompany restriction are meaningful targets.23

In contrast to the decrease observed in Control, Dairy/Ca resulted in a modest increase in PYY concentration during energy restriction. Attenuated PYY concentrations and blunted meal responses have been reported in obesity;24 whereas administration of 100–200 μg/kg systemic PYY3-36 reduced motivation to seek high-fat food in a rodent relapse model.25 Furthermore, although PYY levels increase following Roux-en-Y gastric bypass surgery,26 weight loss induced by energy-restricted low-fat or low-carbohydrate diets has been shown to reduce serum PYY levels.27 Although weight loss did not differ in this study, it is possible that the modest increase in PYY levels and spontaneous reduction in dietary fat intake seen with Dairy/Ca could help prevent relapse to a maladaptive high-fat diet.25

Analysis by linear regression suggests that Ca intake (reflecting both dairy and Ca supplement) was related to the change in energy intake over the 12 weeks. In contrast, there was no correlation between Ca intake and body mass index or body weight. This relationship suggests that participants who consumed more Ca also consumed more energy, but did not gain weight relative to the increased energy. This finding is consistent with Barr et al.,28 who found that in free-living elderly, those who drank three cups of milk per day did not gain the amount of weight predicted based on additional energy intake. We probed this phenomenon further by calculating the percentage of expected weight loss achieved by our subjects. We acknowledge the limitations that self-reported reductions in energy intake introduce to our calculation but the percentage of expected weight loss achieved by Dairy/Ca was 2.5 times that of the Control (82.1 versus 32.2%). We also calculated a modified version of feed efficiency. Although numerically double, we did not see a significant difference between Dairy/Ca (0.100±0.038 g weight loss/kcal restricted) and Control (0.053±0.012 g weight loss/kcal restricted). Calculating feed efficiency in the traditional sense, Thomas et al.21 did show significantly lower feed efficiency (mg weight gain/kJ consumed) in diet-induced obese mice fed non-fat dry milk (2.3±0.1) compared with control (3.5±0.1) and high-Ca alone (3.8±0.1). The explanation for the altered ‘efficiency’ of dairy/Ca-rich diets may include increased fecal fat excretion,29 increased fat oxidation,30 blunted parathyroid hormone release,31 suppression of circulating calcitriol32 or potentially increased PYY concentrations.

In ob/ob mice, Pittner et al.33 demonstrated that a 4-week pharmacologic infusion of PYY reduced weight gain without a concomitant decrease in total energy intake. Similarly in humans, subcutaneous injections of PYY3-36 result in a lipolytic effect.34 It is important, however, to identify whether physiological concentrations of PYY influence energy homeostasis. To this end, it was shown that peak PYY concentrations after a meal were negatively associated with 24-h respiratory quotient and fasting PYY negatively correlated with resting metabolic rate.35 Although it was impossible to establish causation in this study, the findings do suggest a potential for increased fat oxidation with higher endogenous PYY levels.35 In mice treated with subcutaneous infusion of 1 mg/kg PYY3-36, it was similarly shown that respiratory quotient was decreased during the dark cycle, although the effect was transient.

When appetite was assessed subjectively, ratings over the 12-week intervention were improved with Dairy/Ca. Specifically, as determined via weekly VAS, Dairy/Ca reported feeling more satisfied. Recently, Gilbert et al.7 showed that a milk supplement was associated with a smaller increase in desire to eat and hunger during weight loss. A Ca-specific effect on appetite appears less robust given that only in a small subset of subjects (n=7 out of 63) with very low baseline Ca intake demonstrated a spontaneous decreased in fat intake with a Ca and vitamin D supplement.9

Our results for LBM and inflammatory markers are in contrast with some but not all studies. With regards to LBM, several studies show protective effects with a high dairy diet,36, 37 while others have shown no difference.22 The high proportion of branched chain amino acids in dairy proteins, particularly leucine, has been suggested to have a role in regulating muscle protein synthesis38 and help reduce LBM loss during energy restriction. Although no benefits for LBM retention were observed in our study, the increase in bone mineral content in the Dairy/Ca group is worth noting when contrasted against the slight decrease seen in Control. Weight loss induced via energy restriction is a risk factor for rapid bone loss.39

With regards to inflammation, previous work in cells, rodents and humans by Zemel et al.40, 41 shows a decrease in inflammatory cytokines with increased dairy. Specifically, reductions in tumor necrotic factor alpha, IL6 and MCP-1 were seen in participants with metabolic syndrome that consumed a high versus low dairy diet.40 We did not observe any change in IL6, tumor necrotic factor alpha or IL1ß levels and MCP-1 was only reduced in Dairy/Ca at 30 min during the final MTT. The difference in findings may relate to the composition of the control diet in the two studies (Stancliffe et al.40 control diet included prepackaged processed foods, some of which contained trans fatty acids) or the presence of significant weight loss. For example, in mice fed control, high Ca or high nonfat dry milk, diet-associated differences in most inflammatory marker mRNA levels disappeared when body weight was included as a covariate.21 The notion that reduced body weight drives the anti-inflammatory effects of dairy/Ca is interesting in light of a study by Van Loan et al.,22 which similar to us did not find a difference in body weight and no difference in circulating cytokines.

Our study adds to others designed to examine a high versus low dairy/Ca dietary pattern in free-living adults. We recognize that dietary Ca is not the same as dairy foods, and we tested a ‘portfolio-style’ diet similar in principle to that devised by Jenkins et al. for cardiovascular health.42 We combined two bioactive food components aimed at maximizing efficacy and to address suggestions that at a population level, elemental Ca, either as a supplement or fortified foods may be needed to reach target Ca intake levels.43, 44 Our study is limited in that we did not measure energy expenditure and fecal fat loss, both of which would provide valuable information given the discrepancy we saw between energy intake and estimated weight loss.

In conclusion, a dietary pattern rich in dairy foods and Ca did not influence weight loss during a 12-week energy-restricted period. However, Dairy/Ca resulted in a modest increase in circulating PYY in response to a standardized meal and was associated with reduced dietary fat intake and enhanced feelings of satisfaction. Given the demonstration that energy-restricted diets can reduce PYY levels,27 the ability of Dairy/Ca to prevent this decline and result in a modest increase in PYY levels may be important for appetite regulation during weight loss. Although the ability of Dairy/Ca to augment weight loss during energy restriction is not substantiated by this study, the higher percentage of expected weight loss achieved is intriguing and warrants further investigation into the effect of dairy/Ca on energetics.

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Acknowledgements

We thank the participants for their role in this study and MC Hallam, DT Reid and J Tunnicliffe for assistance on test days. Special thanks to the dietitians at the Diabetes, Hypertension and Cholesterol Center for help with recruitment. This project has been funded in part by research grants from the Canadian Foundation for Dietetic Research and Canadian Institutes of Health Research (MOP 86460). KWJ was supported by an Obesity Training Grant from the University of Calgary. LKE was supported by NSERC and Canadian Diabetes Association graduate scholarships.

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Correspondence to R A Reimer.

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Competing interests

RAR previously held research funding from the Dairy Farmers of Canada for work distinct from this study. The remaining authors declare no conflict of interest.

Additional information

Contributors: RAR, ALE and PKDB designed research; KWJ and JAP conducted research; RAR and LKE analyzed data and wrote the paper; RAR had primary responsibility for final content. All authors read and approved the final manuscript.

Supplementary Information accompanies this paper on European Journal of Clinical Nutrition website

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Jones, K., Eller, L., Parnell, J. et al. Effect of a dairy- and calcium-rich diet on weight loss and appetite during energy restriction in overweight and obese adults: a randomized trial. Eur J Clin Nutr 67, 371–376 (2013). https://doi.org/10.1038/ejcn.2013.52

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Keywords

  • calcium
  • dairy
  • peptide YY
  • clinical trial
  • satiety

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