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Interdepartmental Nutrition Program, Purdue University, West Lafayette, IN 47907
2To whom correspondence should be addressed. E-mail: dteegard{at}purdue.edu.
ABSTRACT
Recent epidemiologic research suggests that dairy product intake or its components (calcium, vitamin D, and amount or source of protein) are associated with lower body weight or body fat. Clinical intervention trials designed to test this association during weight loss are promising, but still controversial. Few data are available on the effect of calcium or dairy products on prevention of weight gain in long-term trials. The mechanisms proposed to mediate the putative effect of dietary calcium are primarily the formation of fecal fatty acid complexes to reduce fat absorption and the regulation of energy metabolism, including lipolysis from adipocytes and fatty acid oxidation, through the calciotropic hormones, parathyroid hormone, and 1,25-dihydroxyvitamin D. Increased energy expenditure, increased satiety, or a shift from fat to lean mass must accompany these changes in lipid metabolism to achieve changes in fat mass; however, measurable changes in these other parameters either have not been tested or have not been noted uniformly. If dairy products or their components have an effect on altering fat mass, it is likely to be a small change that may have a substantial effect on the incidence of obesity over time.
KEY WORDS: • calcium • dairy • body fat • body composition • weight
The incidence of obesity in the United States is reaching epidemic proportions. Despite efforts to reduce the prevalence of obesity, 30% of adults 
20 y old are estimated to be obese (1). In 2003 it was estimated that >25% of the adult population in 4 states was obese (1). Further, 16% of the children and adolescents in the United States were overweight, and this percentage has tripled since 1980 (1). The recent rapid rise demonstrates that environmental factors play a substantial role, and thus it is not surprising that bioactive components of foods, such as the dairy product components calcium, protein, or vitamin D, may play a role in the regulation of energy balance.
An association between higher calcium intakes and lower body weight was noted in a few publications in the late 1980s (2,3). McCarron et al. (2) reported an inverse association between calcium intake (of which dairy products are the predominant dietary source) and body weight based on data from the first National Health and Nutritional Examination Survey. In 1988 Metz et al. (3) demonstrated a reduction in body fat mass in 2 strains of hypertensive rats with higher calcium. Little was published on the topic until 2000, when 3 publications were released that supported a relation in epidemiologic studies (4), an animal model (4), as well as prospective (5–7) and human intervention (7) trials.
Subsequent to these publications, numerous investigators began exploring the topic, initially by employing existing data from clinical observational trials (8,9). Many, but not all of these studies supported an association between higher calcium or dairy product intake and reduced fat mass. However, a number of issues must be considered when reviewing this literature. In epidemiologic studies, dairy product intake is often used as a surrogate measure for calcium intake because dairy products comprise the primary source of dietary calcium in the U.S. diet. There is evidence that other components of dairy products may have a synergistic effect with calcium, or an independent effect that may be obscured in many of the studies to date. Second, low dietary calcium intake is associated with a less healthy lifestyle or diet (10), and a cause and effect relation cannot be established in epidemiologic investigations. Third, it is unlikely that an effect of dietary calcium on body composition is independent of energy intake (5). Many of the human trials to date were not designed to study the effect of calcium on body composition or weight, but are secondary analyses. Higher energy intakes are likely to obscure any effects of dietary calcium on body composition. In many of the studies, a measurement of energy intake is not available or results were not controlled for individual energy intakes. Fourth, dietary calcium intake may have an effect only under certain circumstances, such as weight loss, in obese individuals, in individuals who are vitamin D sufficient or during periods of low physical activity. Finally, like any nutrient, there may be a threshold effect such that a sufficient intake is necessary for change to be evident, and at the current low calcium intakes in the United States, these intakes may not be achieved; thus, an effect is not noted in epidemiologic studies. The results of epidemiologic studies are promising, therefore, but intervention studies are warranted to fully understand the relation between dairy product intake and body composition.
Of the 17 calcium supplementation intervention studies reviewed by Barr (11), only one showed greater weight loss in the calcium-supplemented group than in the controls (7,12). When authors reported energy intakes, they were not different between groups, but the published study of Davies et al. corrected for individual energy intakes, using protein intakes (7). In addition, the time frame of these studies may limit the ability to detect differences in weight or fat mass loss. It should be noted that the difference between the placebo control and the calcium-supplemented groups in the study of Davies et al. (7) was 0.346 kg/y. This demonstrates a small but significant effect; the length of this trial (
4 y) may have enhanced the ability to measure these small changes. Trials of shorter duration, those with small numbers, or those in which individual energy intake is not taken into account may not have sufficient power to detect the small changes in body fat that dietary calcium may elicit.
Recently, several calcium and/or dairy product intake intervention studies were completed that were designed to address specifically the effect on body composition, both for the prevention of weight gain or for enhancing weight loss. To test whether dairy products prevent weight gain, a 1-y dairy product intervention trial in normal weight young women was completed. There was no effect of higher dairy product intakes, which led to dietary calcium levels > 1000 mg/d, on change in weight or fat mass. However, unlike the results of Lin et al. (5) in a similar cohort, in which low calcium intakes predicted a weight gain, the control (low dairy product intake) participants did not gain weight in this recent trial. Further, the participants in this trial were younger, more fit, and weighed less, suggesting that dairy products will not contribute to significant losses in weight in young healthy, active, normal-weight young women during weight maintenance.
To date, 4 randomized intervention trials also were published that tested the effect of the inclusion of dairy products in weight loss trials with controversial results. In a 16-wk randomized, controlled, weight loss study, participants (BMI > 27 kg/m2) who consumed an isoenergetic milk-only diet lost significantly more weight (9.4 kg) than those consuming the conventional diet (1.7 kg) (13). In a 12-wk study of 34 obese adults consuming a reduced-energy diet, those consuming a dairy-rich diet (3 servings of yogurt/d) lost 22% more weight and 66% more body fat than those consuming the low-dairy diet (14). In this study, the higher dairy intake group lost 81% more fat from the trunk compared with the low calcium intake group (14). The inclusion of calcium and dairy products was tested in another 24-wk 2092-kJ deficit diet trial in obese participants (n = 32) (14). Participants were randomly assigned to 1 of 3 groups: 1) low-calcium placebo (400–500 mg/d, 2) calcium supplemented (1200–1300 mg total), or 3) dairy products included in diet (1200–1300 mg calcium). Participants in the calcium-supplemented and dairy product intake groups lost more body weight (26 and 70%, respectively) and body fat (38 and 64%, respectively) than the low calcium intake controls. This study was followed by a multisite trial with a similar study design of a 2092-kJ deficit diet (15); however, the study duration was 12 wk compared with the previous trial of 24 wk (16). In this shorter trial (n = 68), the dairy intake group achieved significantly greater decreases in fat loss, trunk fat loss, and waist circumference, compared with the low calcium or supplemental calcium groups. A similar 6-mo weight loss trial was completed by Shapses et al. (17) of pre- and postmenopausal obese women (n = 100) randomly assigned to either a low-calcium placebo or calcium supplementation (1000 mg/d) group. This study did not include a high dairy product intake arm. Like the multisite trial (15), the low-calcium and calcium-supplemented groups did not differ in weight loss, but this was contradictory to the trial of Zemel et al. (16). Given these contradictory results, another as yet unidentified factor that is either dietary (such as in dairy) or environmental, may play a role in the putative effect of dietary calcium on the regulation of fat mass. In summary, further trials are warranted to clarify the effects of calcium and dairy product intake incorporated into weight loss diets on fat mass; however, the results of the recent trials, particularly with dairy products, are promising.
Mechanisms of Body Weight Regulation. To decrease body weight, there must be a shift in the balance between available energy and energy utilization, leading to a net energy deficit. Dairy products and dietary calcium intake were proposed to affect both components (Fig. 1). On one side of the energy equation, the mechanisms proposed for reducing energy availability include decreasing the absorption of fatty acids through the formation of calcium/fatty acid "soaps" in the intestine or increasing satiety. Few data are currently available to support the idea that dairy products increase satiety (8). However, several studies demonstrated that higher calcium intakes lead to greater fecal fat loss in rats (18) and in humans (n = 10) in a 1-wk crossover study (19). These studies demonstrated that dietary calcium leads to fecal fat losses, but the contribution of this factor to overall energy balance is not clear.
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In humans, higher intakes of dietary calcium or dairy products are associated with increased fat oxidation (20–22). The results of Melanson et al. (20) showed that higher self-selected calcium intakes were associated with higher rates of fat oxidation in 35 nonobese subjects over 24 h. In addition, fat oxidation was increased during a 12-wk 2092-kJ deficit diet in overweight and obese women (n = 24) after a low-calcium meal challenge (21). Similarly, in a 1-y randomized intervention trial in nonobese young women (n = 19), increased dairy product intakes (1057 ± 362 mg calcium intake/d) compared with low dairy product and calcium intake controls (673 ± 213 mg/d) led to increased fat oxidation after both a low- (100 mg) and high-calcium (500 mg) meal challenge (22). In addition, the intervention group increased the thermic effect of a meal after a low-calcium meal challenge. It is intriguing that although there was an increase in fat oxidation after 1 y of increased dairy product consumption, there was no measurable difference in weight change between dietary intervention groups in these normal-weight young women. Thus, the effect of dietary calcium to increase fat oxidation may not translate into changes in weight without another dietary or environmental factor. Further, the effect on weight may be small, particularly during weight maintenance; it may be measurable only when energy balance is shifting, such as during weight gain or weight loss, or in studies of longer duration.
Mechanisms by which dietary calcium may regulate energy metabolism have not been clearly determined, although the mechanism most often cited to explain a specific effect of dietary calcium on energy utilization is through the ability of calcium to regulate, at least acutely, levels of the hormones, parathyroid hormone (PTH)3 and 1,25dihydroxyvitamin D [1,25(OH)2D] (Fig. 2). With low dietary calcium intakes, serum calcium is reduced, and this reduction stimulates the release of PTH. PTH acts to activate renal 1
-hydroxylase which converts 25-hydroxyvitamin D (25OHD) to the active metabolite, 1,25(OH)2D. 25OHD is the best indicator of vitamin D status. PTH and 1,25(OH)2D coordinately act on the intestine, kidneys, and bone to increase the levels of serum calcium.
In addition to these classical functions of PTH and 1,25(OH)2D to maintain serum calcium homeostasis, a variety of other functions have been credited to these hormones. Increased concentrations of fasting PTH are hypothesized to influence increased levels of body fat mass (23). Serum PTH concentrations in fasting subjects correlated positively with body fat mass at baseline (n = 155) and the change in serum PTH predicted the change in body fat mass over 1 y in a cohort of normal weight young women (24). Another link between serum PTH concentrations and body composition was shown in a study of 302 mixed-race, obese and nonobese adults in which PTH positively correlated with BMI and body fat mass (25). Serum PTH levels were higher in obese than in nonobese young adults (26). In addition, hyperparathyroid postmenopausal women have a greater fat mass with a more android pattern of fat distribution compared with age-matched controls (27). After a 1-y dairy product intervention in young women, the change in PTH correlated with the change in fat oxidation, independently of control or dairy product intervention group assignment (28), suggesting that another factor also regulates fasting concentrations of PTH and that PTH may regulate energy metabolism. These results suggest that there is substantial evidence, albeit associative, that serum PTH concentrations may play a role in regulating body fat levels.
More direct evidence to link dietary calcium and hormonal regulation of body composition is provided in studies employing the agouti mouse model for diet-induced adult onset obesity (4). Increased dietary calcium intake in this model caused reduced fat mass accumulation with reduced activity and expression of fatty acid synthase, as well as increased lipolysis in fat tissue. 1,25(OH)2D and PTH stimulated increased intracellular calcium in adipocytes, and changes in intracellular calcium in turn regulated fatty acid synthase (4). Further, 1,25(OH)2D inhibited lipolysis in cultured human adipocytes (4). The regulation of these hormones by dietary calcium may play a role in the response at the level of the adipocyte after dietary intervention.
Although the adipocyte is the primary storage tissue for fat, it is important to determine the effect of the dietary calcium-regulated hormones on energy metabolism in the appropriate tissues such as muscle. This is particularly true in light of evidence demonstrating a role of calcium in regulating lipid oxidation because muscle is the most highly oxidative tissue. Several studies in rats with chronic renal failure (which are hyperparathyroid) support a direct role for PTH in suppressing lipid oxidation in muscle, potentially by reducing the activity of carnitine palmitoyl tranferase-1, the mitochondrial transfer protein that is the rate-limiting step in mitochondrial ß-oxidation (29). PTH may be a mediator of regulation of lipid oxidation by dietary calcium, but we cannot eliminate a role for 1,25(OH)2D.
Other Dairy Product Components. Dairy products contain components in addition to calcium that are proposed to alter energy balance. For example, the amino acid composition, in particular the abundance of leucine may have a positive effect on protein synthesis and maintenance of lean mass (30,31). Stimulation of protein synthesis may lead to a repartitioning of energy from fat mass into lean mass. The use of whey protein, compared with red meat, in a high-protein, high-fat diet in rats reduced weight gain by 4%, suggesting that the composition of whey protein promotes a less positive energy balance than the composition of red meat (32). Further, whey protein was shown to enhance calcium absorption in rats (33), and increasing the bioavailability of calcium may enhance its effect on body composition. Another component of dairy products, conjugated linoleic acid, may also affect body weight. However, the studies in mice (4,34) that showed an enhanced effect of dairy product on changes in body weight were completed with a nonfat dairy source (nonfat dry milk powder) and thus were devoid of conjugated linoleic acid.
The results in humans suggest that vitamin D status may have effects that oppose those of PTH in regulating fat mass. For example, both the biomarker of vitamin D status, 25OHD, and 1,25(OH)2D correlated negatively with BMI and body fat mass in the study by Parikh (25). In addition, in a randomized 12-wk weight loss study in which overweight and obese subjects were assigned to low-calcium, calcium supplementation, and dairy product intake groups (13), baseline serum 25OHD levels correlated with the change in the thermic effect of a meal, independently of group assignment (21). It is clear that a key regulator of serum PTH concentrations in fasting subjects is the improvement in vitamin D status (35). Thus, it is intriguing to consider that the suppression of PTH levels by improved vitamin D status may also contribute to regulating fat mass accumulation. Thus, dairy product components other than calcium may affect body weight, but more evidence is required to support an independent or synergistic effect of these components on the regulation of fat mass.
Summary. Thus, substantial evidence exists for an association between dietary calcium or dairy product intakes and lower body fat or waist circumference. Few data are available in randomized clinical trials in which the prevention of fat mass gain was tested specifically. Long-term trials are required for these investigations because changes in fat mass due to dietary calcium may be too small to be detectable given the other potentially influential variables. The results of randomized clinical weight loss trials demonstrate predominantly that dairy products enhance weight and fat mass loss, but the results for dietary calcium are contradictory. The number of conflicting results suggests that if there is an effect, multiple factors, such as total energy intake, protein amount and source, and/or vitamin D status, may act synergistically to regulate energy balance to promote reduction or prevent gain of body fat. Other critical factors implicated in the ability of calcium or dairy products to mediate reductions in body fat mass include initial body fat mass status, exercise levels, and changing energy balance status (weight loss/weight gain). It is important to recognize that, unlike pharmacology, nutrients are likely to have small, but in the long term, substantial effects on human health. Finally, it is critical that we gain a better understanding of the underlying mechanisms so that effective recommendations can be developed for specific populations and situations. Thus, if current recommendations for calcium intake were met through food sources in the promotion of optimal bone health, this might also help to reduce the incidence and development of overweight and obesity.
FOOTNOTES
1 Manuscript received 28 July 2005. 
3 Abbreviations used: 1,25(OH)2D, 1,25-dihydroxyvitamin D; 25OHD, 25-hydroxyvitamin D; PTH, parathyroid hormone.
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