Introduction

One potential intervention to aid weight management is to consume foods that offer a metabolic advantage (1)(2). This may occur if a food is inefficiently absorbed and metabolized or increases sensations of fullness disproportionately to its energy contribution and thereby moderates intake (2). Consequently, the actual impact of energy from the food is less than that predicted based on simple energy calculations. Regular consumption of such foods would be predicted to promote a modest weight loss or accelerate weight loss on an energy-reduced diet. One group of foods that purportedly imparts a metabolic advantage is dairy products.

Epidemiologic data have revealed a small, but statistically significant, inverse relationship between BMI and calcium intake (3) or dairy consumption (4). These observational studies are supported by some intervention studies, where increased dairy consumption resulted in weight loss (5) or augmented weight loss on an energy-restricted diet (6)(7)(8). However, other studies report no effect of increased calcium or dairy consumption on body weight (9)(10)(11). A plausible physiologic basis for the positive observations is provided by cell studies that indicate calcium stimulates lipolysis in the adipocyte and increases fat oxidation (12). It was subsequently noted that, in humans, acute calcium intake is associated with increased fat oxidation over a 24-hour period (13)(14), although other studies have failed to find such an effect (15)(16). In addition, high calcium intake (1800 mg/d) increases excretion of fat through the feces because of the formation of calcium soaps (15).

In addition to these metabolic effects, the consumption of dairy products may increase sensations of fullness and elicit strong dietary compensation (i.e., subsequent energy intake will be reduced by an amount equal to or greater than the amount of energy contained in the dairy food). Dairy products are rich sources of protein, a macronutrient with strong satiety properties (17)(18)(19). Release of the satiety hormone cholecystokinin (20)(21)(22) may be especially strong after ingestion of caseinomacropeptide, a breakdown product of dairy proteins (23). However, other studies reported no effect of caseinomacropeptide on appetite (24).

Data from the aforementioned studies have led to the suggestion that consuming the recommended three portions of dairy each day (milk, yogurt, or cheese) may reduce the incidence of obesity by 85% (25). Because the effect of metabolic advantage on body weight is likely to be limited (2)(26), increased dairy product consumption would need to elicit a substantial compensatory dietary response if energy balance was to be maintained or a negative energy balance induced. To date, there is a paucity of data detailing the effects of increased dairy consumption on appetite and overall energy intake. This study aimed to determine the effect of consuming one or three portions of dairy foods each day on energy intake and appetite. Because of potential sex differences in the sensitivity to cholecystokinin and, subsequently, subjective appetite sensations (22), men and women were analyzed separately. In addition, habitual low or high dairy consumers were recruited to determine whether habitual dairy intake affects the putative satiating properties of dairy product consumption.

Research Methods and Procedures

Potential participants were screened using a questionnaire that collected information regarding demographics, health status, and habitual dairy intake. To be enrolled into the study, participants were required to be of good general health, 18 to 50 years of age, have a BMI between 25 and 32 kg/m², be willing to consume the test foods, not be lactose intolerant, and be a habitual low (<200 mg/d of calcium from dairy products that was deemed equivalent to one or fewer servings) or high (>600 mg/d of calcium from dairy sources that was equivalent to three servings or more servings) dairy user (Table 1). Habitual dairy use was determined using a food frequency questionnaire designed for assessing dairy food intake (10).

Table 1. - Age, body composition, and dietary calcium intake of study participants according to sex and habitual dairy consumption.

Full table

Sixty individuals who met the eligibility criteria were asked to sign an informed consent form before being randomly assigned to a low dairy or high dairy condition. Equal numbers of men and women were purposely recruited. Each condition lasted 7 consecutive days and was separated by a 7-day washout period. Depending on the condition, participants were supplied with one or three portions of dairy products each day, which they were required to eat in their entirety. During the low dairy condition, the participants could choose their dairy product from milk (white or chocolate), yogurt, or hard cheese. During the high dairy condition, participants were required to eat a milk serving, a yogurt serving, and a hard cheese serving each day (Table 2). They were allowed to choose the flavor or type of product to consume. No guidance was provided to the participants on how to incorporate the dairy products into their diet, the only stipulation being a 4-hour interval between eating each serving.

Table 2. - Nutrient composition of the dairy products used in the study and mean standard deviation of selected daily nutrient intakes during each of the study periods.

Full table

On each day of the two treatment periods, participants were required to attend the laboratory so their previous day's food intake could be determined using Nutrition Data System multipass software (Version 5.0; University of Minnesota, Minneapolis, MN). Standard operating procedures for the software were followed. While in the laboratory, the participant also completed a number of diversionary tasks, such as the measurement of hand to eye coordination, that were conducted to mask the true purpose of the study.

Further measurements were taken outside of the laboratory. Participants recorded their appetitive sensations on a hand-held computerized system each waking hour of the day (Palm m100; Palm, Inc., Sunnyvale, CA). This system stamped each entry with a time and date so compliance could be monitored. This validated system posed standard appetite questions (27). Questions posed were: 1) How hungry are you right now? 2) How full do you feel right now? 3) How preoccupied with food are you right now? and 4) What is your desire to eat right now? Each visual analogue scale was anchored with "not at all" and "extremely." Analysis of the collected appetite data was limited to the hours between 8:00 AM and 10:00 PM. Analysis was restricted to these hours because at least 75% of the participants responded at each hourly time-point. Moreover, on each day of the treatment periods, the participant attached an accelerometer (RT3 tri-axial research tracker; Stay Healthy, Inc., Monrovia, CA) to their belt to ascertain daily total energy expenditure. To confirm the accelerometer data, participants also completed a daily activity diary. These methods provided a measure of total energy expenditure by estimating the basal metabolic rate of the participant and adding to this the energy cost of the activity. Estimation of basal metabolic rate and energy cost of activity was based on the participant's body weight.

After completion of the first 7-day treatment period, participants underwent a 7-day washout period before starting the alternative treatment. The study was approved by the Purdue University Institutional Review Board.

Statistical analyses were conducted using SPSS v12.0 software (SPSS, Inc., Chicago, IL). All data are reported as means standard deviation. Differences between groups were determined using a mixed-model ANOVA using sex and habitual dairy intake as between-subject factors and dairy condition as a within-subject factor. The criterion for statistical significance was set at p < 0.05 (two-tailed).

Results

Participant Characteristics

Sixty individuals were enrolled into the study. Of these, two individuals failed to complete the protocol. Although attempts were made to determine the reason for attrition, no information was forthcoming.

There were no significant differences among the four groups in terms of age [ F(3,54) = 0.440, p > 0.05] or BMI [ F(3,54) = 2.503, p > 0.05] . The female groups were lighter than their male counterparts [ F(3,54) = 13.843, p < 0.05] ; however, no within-sex differences were detected (Table 1).

Food, Energy, and Macronutrient Intake

Table 2 shows that, overall, participants consumed an additional 209 kcal/d during the high dairy treatment [ F(1,52) = 28.088, p < 0.05] . There was a statistically significant treatment-by-sex interaction [ F(1,52) = 4.100, p < 0.05] in that the high dairy condition elicited a greater increase of energy intake in men than in women. There was no statistically significant interaction between treatment and habitual dairy intake.

Although some energy compensation (reduction of energy intake from other sources) did occur for the additional calories consumed during the high dairy treatment, it was incomplete. Group 1 (male high habitual dairy) reduced their energy intake from other sources by 31% . Group 2 (male low habitual dairy) failed to compensate for the extra energy contained in the additional dairy products. Indeed, their energy intake actually increased by 12% more than would be predicted by inclusion of two additional dairy products in the daily diet. The female groups compensated incompletely as well, but to a greater extent than men (p < 0.05), with Group 3 (female high habitual dairy) reducing energy intake from other sources by 72% and Group 4 (female low habitual dairy) reducing energy intake by 50% of the dairy load.

During the high dairy treatment, mean carbohydrate intake increased from 285 87 to 310 87 grams [ F(1,52) = 14.065, p < 0.05] . A significant treatment-by-habitual dairy intake interaction indicated that this increase in carbohydrate intake was accounted for by increased carbohydrate consumption among the low habitual dairy participants [ F(1,52) = 13.675, p < 0.05] . There was no statistically significant treatment-by-sex interaction.

Protein intake was higher during the high dairy treatment, rising from 79 25 to 95 32 grams [ F(1,52) = 54.711. p < 0.05] . No statistically significant differences were detected between sexes or the low and higher habitual dairy intake groups.

During the high dairy condition, fat intake increased from 74 25 to 79 32 grams [ F(1,52) = 4.030, p < 0.05] . A significant treatment-by-sex interaction was evident [ F(1,52) = 4.655, p < 0.05] , with the male groups accounting for the increased fat intake.

Appetite Ratings

There were no significant differences in ratings of mean hunger, fullness, desire to eat, or preoccupation with foods in any group.

Energy Expenditure

Energy expenditure did not differ statistically in either of the conditions regardless of the method of measurement used (Table 3). Daily total energy expenditure was significantly higher than total energy intake, which suggests under-reporting of food intake. However, there are significant limitations associated with these measures of energy expenditure, and the accuracy of the results is uncertain. However, these data indicate that energy expenditure was consistent across the treatment periods.

Table 3. - Energy expenditure of the groups as determined by activity log and accelerometer.

Full table

Discussion

Increasing dairy consumption purportedly provides an aid to weight maintenance or accelerates weight loss. Indeed, it has been suggested that increasing intake of dairy foods to the recommended level of three to four servings each day would reduce the incidence of obesity by 25% over a 5-year period and result in a savings of $37.5 billion in health care expenditures (28). However, the results from this short-term study cast doubt on a role for increased dairy product consumption in weight management. Consuming three portions of dairy products each day resulted in significantly increased energy intake compared with consuming a single dairy product each day. The increase in energy intake was greater in men than in women. Moreover, the increased dairy product intake did not elicit any changes in hunger or fullness sensations that would suggest a compensatory appetitive response for the additional calories.

Dairy and Body Weight

The role of calcium or dairy products in weight management remains controversial. A critical review of the epidemiologic literature indicates that, whereas some studies suggest an inverse association between calcium intake and adiposity, the evidence is not compelling. For instance, an early study that described a moderate inverse relationship between calcium intake and BMI also reported a similar inverse relationship between BMI and energy intake (29). Because increased BMI is primarily a result of excess energy intake, such results cast doubt on the validity of the dietary records. A subsequent epidemiologic study reported a statistically significant correlation coefficient of - 0.21 between calcium intake and BMI in middle-aged women (30). Indeed, the modest nature of the association between calcium intake and body weight was shown by a retrospective analysis of a number of studies that concluded that calcium intake explained 3% of the variability in body weight (3).

Moreover, other observational studies suggested the relationship between calcium and body weight is not robust, and an association is only reported for segments of the population (4)(31)(32). Studies targeting populations such as adolescent girls (33) and Pima Indians (34) revealed no significant association between calcium intake and body weight.

Data from intervention studies are also inconclusive. Findings include increased dairy consumption results in unchanged body weight (10)(35)(36), increased body weight (37)(38), or accelerated weight loss when incorporated in an energy-restricted diet (6). These equivocal results may be the result of several factors. First, a number of these studies were not designed with body weight as an outcome measure and may be underpowered or inadequately designed to detect changes in body weight. Second, the discrepant outcomes may be caused by different characteristics of the study groups. The two studies indicating weight gain tested postmenopausal or elderly participants. Data indicate that, with advancing age, the ability to modify food intake to maintain body weight is reduced (39), and the increased body weight may be caused by a reduced ability to compensate for the additional energy intake caused by increasing dairy product consumption. Third, dairy products may have more of an effect when body weight is changing, such as when following an energy-restricted diet. This effect was shown in a study by Zemel et al. (6).

Dairy and Metabolic Advantage

Recent data have raised the possibility that the consumption of a high dairy diet offers a significant metabolic advantage that may negate an increased energy intake. Harvey-Berino et al. (9) and Gunther et al. (10) noted that weight loss was not significantly different between control and dairy groups despite reported intakes that were 150 or 75 kcal/d higher in the supplemented groups. Although these results were not statistically significant, it should be considered that interindividual variation in energy intake and the errors associated with diet diaries would make differences of this magnitude difficult to detect. Thus, there is a risk for a type II error. However, these differences in energy intake, if real, are clinically significant and suggest the possibility of a metabolic advantage from consuming calcium or dairy products.

Dairy or calcium consumption could elicit a metabolic advantage through increased thermogenesis and fecal fat excretion. However, the increase in thermogenesis needed for a metabolic advantage to occur has only been observed by one study (40), and this was only apparent in the high calcium intervention group after a low calcium meal challenge. Other studies report no effect (15)(16)(40). Increased fat excretion through the formation of calcium–fatty acid soaps could also contribute to an explanation for the lack of effect of positive energy balance associated with dairy consumption on body weight (15).

A further putative beneficial effect of increased dairy or calcium intake is increased fat oxidation (13)(14)(40), although this has not been shown by all studies (15)(16). A calcium-related increase in fat oxidation has been promoted as the mechanism that explains the increased reduction of body fat mass reported by some studies. However, the relationship between dairy or calcium intake and fat oxidation is not predictable. One study found a modest correlation between acute calcium intake but no relationship with habitual calcium intake and fat oxidation (13). A second study reported that, whereas a high dairy intervention caused increased fat oxidation after a high calcium liquid meal (40), fat oxidation was even greater when a low calcium liquid meal was consumed. Another study reported that fat oxidation increased by 30 g/d after a high dairy meal (14). This effect was only noted when the participants' diet was significantly energy deficient (- 600 kcal/d). Moreover, increased fat oxidation seemed confined to the periods when the participants were exercising, and the relevance to those who diet without exercise is unclear. In addition to the increased oxidation of fat, there was a reduced, although statistically non-significant, oxidation of carbohydrate and protein and no overall increase in energy expenditure. Because increased fat oxidation would be predicted to inhibit oxidation of glucose, such an occurrence is to be expected (41). Further research is needed to elucidate the metabolic fates of glucose, fat, and protein after a high dairy or calcium meal and the potential effects on energy balance.

Moreover, the weight lost during dairy or calcium intervention trials is no greater than would be predicted from the energy deficit incurred by the study protocol. During the study by Zemel et al. (6), participants consuming the energy-restricted (- 500 kcal/d) high dairy diet lost 11.07 kg over a 24-week period. This amount is no more than would be expected to occur because of a 500 kcal/d energy deficit. Although the high dairy and high calcium groups lost more weight than the low calcium/dairy group, the reasons behind these cannot be ascertained without knowing how compliant each of the groups were to the energy-restricted diet.

Dairy and Appetite

In addition to the metabolic effects, constituents of dairy products have the potential to increase sensations of satiety and moderate food intake. Dairy products are a good source of protein, which is regarded as the most satiating of the macronutrients (18)(42)(43). However, studies showing a satiating effect of protein have generally used preloads of 50 to 70 grams of protein. In this study, the protein content of the dairy portions ranged from 2.3 to 14.3 grams of protein, and daily protein intake only increased by 16 grams during the high dairy condition. It is possible that a threshold of protein intake is needed before an appetitive effect is elicited. If true, this threshold apparently was not reached during this study.

Previous data have suggested that habitual intake of a highly satiating diet may lead to habituation with a consequent reduction in its effectiveness (44). If dairy products are satiating, it may be that this effect would be lost with habitual intake. To test this, only habitual low or high dairy consumers were recruited for this study. No effects of habitual dairy intake on food intake or appetitive ratings were detected during either treatment arm.

This study indicated sex differences in response to increased dairy consumption. Women compensated to a greater degree for the additional energy than men. Interestingly, this contrasts with previous studies indicating that men may benefit more from increasing calcium or dairy consumption. An epidemiologic study reported a significant relationship between calcium intake and body weight in men but not women (31). Moreover, intervention studies have reported that increased calcium intake results in weight loss in men (5) but not women (11). More research is needed to confirm a potential sex effect.

Although this study reported higher energy intake after increased dairy consumption, the results must be placed in context. The short-term (7-day) nature of this study may not have provided enough time for a compensatory responses to manifest. Leptin is released in proportion to body fat stores and moderates sensitivity to peripheral satiety hormones (45)(46). It may be that greater effects will be apparent with hypocaloric diets that independently promote weight loss. Indeed, one study suggested the strongest effects of dairy products on body weight occur under such conditions (6).

In conclusion, increasing dairy consumption from one to three portions each day led to increased energy intake. These data raise questions regarding the satiating efficiency of dairy products and likelihood they will elicit precise dietary compensation. Whether increased energy intake from dairy is offset by metabolic changes induced by components in these products needs further study because recommendations to increase dairy consumption to promote bone health may pose a challenge for energy balance.

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Acknowledgments

This study was funded by Diary Management, Inc.