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American Journal of Clinical Nutrition, Vol. 88, No. 5, 1248-1255, November 2008
© 2008 American Society for Nutrition

ORIGINAL RESEARCH COMMUNICATION

Dairy consumption and 6-y changes in body weight and waist circumference in middle-aged French adults1,2,3

Anne-Claire Vergnaud, Sandrine Péneau, Stacie Chat-Yung, Emmanuelle Kesse, Sébastien Czernichow, Pilar Galan, Serge Hercberg and Sandrine Bertrais

1 From INSERM U557, INRA U1125, CNAM EA3200, Paris 13 University, and the Research Unit on Nutritional Epidemiology, CRNH IdF, Bobigny, France

2 Supported by a grant from the Direction Générale de la Santé (French National Health Ministry).

3 Reprints not available. Address correspondence to A-C Vergnaud, UMR INSERM U557/INRA U1125/CNAM/PARIS 13, Centre de Recherche en Nutrition Humaine d'Ile de France, UFR SMBH, Faculty of Medicine, 74 rue Marcel Cachin, 93017 Bobigny Cedex, France. E-mail: ac.vergnaud{at}uren.smbh.univ-paris13.fr.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Some studies have shown an inverse relation between calcium intake and body weight or fat mass.

Objective: We aimed to investigate the relations of dairy consumption and calcium intake with 6-y changes in body weight and waist circumference (WC).

Design: Multivariate analysis of variance according to dairy consumption or calcium intake quartile was presented, stratified by sex and body weight status at baseline, in 2267 middle-aged French adults.

Results: The associations between dairy products and anthropometric changes differed according to sex and overweight status at baseline. In overweight men only, 6-y changes in weight and WC were inversely associated with the consumption of dairy products—especially that of milk (P = 0.02 for both weight and WC changes) and yogurt (P = 0.01 and 0.03 for weight and WC changes, respectively). No relation was observed with cheese and calcium intake. Positive relations were found between milk consumption and WC change in overweight women and between yogurt consumption and weight change in normal-weight women. Multivariate analyses showed a trend toward increases in weight with high dairy calcium intakes in normal-weight women.

Conclusions: The relation of dairy products and calcium intake with changes in weight and WC may differ according to sex, initial body-weight status, and type of dairy products. The negative association between dairy products and anthropometric changes observed in overweight men was not explained by dairy calcium intakes, which suggests that other components of dairy products or specific dietary patterns associated with dairy consumption may help to explain the observed associations.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Controversy has emerged in the literature with respect to the relation among dairy product consumption, calcium intakes, and body weight regulation (1-3). Several (4, 5) but not all (6-11) epidemiologic studies have shown that dairy consumption is inversely related to body weight or obesity. Others have reported different associations, depending on the type of dairy products and initial body mass status (12, 13). Dairy foods are an important source of nutrients (14), including calcium, which has also been shown to be inversely related to body weight or fat mass in numerous observational and clinical studies (15-23). However, several studies have found no such association with dietary calcium (7-10, 24, 25).

Most intervention studies to date have measured such effects over a relatively short term (≤1 y), and few epidemiologic studies have examined the relation between calcium or dairy intake and long-term weight changes in adults (10, 12, 13, 26). The Health Professionals Follow-up Study, which investigated the relation of calcium and dairy intakes with 12-y weight change, found no associations after adjustment for lifestyle and intake confounders (10). In a study in young US adults from the Coronary Artery Risk Development in Young Adults (CARDIA) study (12), total dairy intake was inversely related to obesity 10 y later only in subjects who had been overweight at baseline. Among the various types of consumed dairy products studied in a large prospective study in middle-aged Swedish women, the consumption of cheese and whole or sour milk was associated with lower weight change after 9 y in normal-weight women only (13). Furthermore, data on long-term relations with regional body fat distribution are scarce.

The aim of the present prospective study was to investigate the relations of dairy and calcium intakes with 6-y changes in body weight and body fat distribution, as assessed by waist circumference (WC), in a large sample of middle-aged French men and women.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
Subjects were participants of the Supplementation en Vitamines et Mineraux Antioxidants (SU.VI.MAX) Study, a randomized, double-blind, placebo-controlled primary-prevention trial initially designed to evaluate the effect of daily antioxidant supplementation at nutritional doses (120 mg vitamin C, 30 mg {alpha}-tocopherol, 6 mg β-carotene, 100 µg Se, and 20 mg Zn) on the 8-y incidence of cancer and ischemic heart disease. Details of the rationale, design, and methods of the study and of the subjects' baseline characteristics were provided elsewhere (27, 28). Briefly, 13 017 subjects (5141 men 45–60 y old, 7876 women 35–60 y old) from all over France were recruited in 1994 and 1995 by a large national media campaign via television, radio, and newspapers. To be eligible, volunteers had to return a signed informed-consent form and a completed screening questionnaire. Further eligibility criteria were lack of any disease likely to hinder active participation or to threaten 5-y survival; acceptance of the possibility of being given a placebo and acceptance of the constraints of participation; lack of previous regular supplementation with any of the vitamins or minerals in the supplement provided; and absence of extreme beliefs or behavior regarding diet. During follow-up, subjects were invited regularly to a medical visit involving either biochemical sampling (in 1994–1995, 1996–1997, 1998–1999, and 2001–2002) or clinical examination, including anthropometric measurements (in 1995–1996, 1997–1998, and 2001–2002). Subjects were also encouraged to provide dietary data in the form of 24-h dietary records every 2 mo after enrollment in 1994 and 1995.

For the present study, we included only those subjects who had completed at least six 24-h dietary records during the first 18 mo of follow-up and who had available anthropometric measurements at the first (1995–1996) and last (2001–2002) clinical examinations. In addition, we excluded persons who had a major health event during the follow-up and those with any missing value for covariates. A final sample of 2267 subjects (1022 F, 1245 M) >45 y old at inclusion was included in the present study. The general characteristics of the study population are shown in Table 1Go.


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  		TABLE 1. Baseline characteristics by sex1

 
The SU.VI.MAX study was approved by the Regional Ethics Committee for Studies with Human Subjects of Paris-Cochin Hospital (CCPPRB no. 706) and by the Commission Nationale de l'Informatique et des Libertés (CNIL no. 334641), which advocates that all medical information remain confidential and anonymous.

Dietary assessment
Dietary data were collected by using the Minitel Telematic Network (France Telecom, Paris, France). The Minitel is a small terminal that was widely used as an adjunct to the telephone in France at the beginning of the SU.VI.MAX Study. At enrollment, participants received free of charge a tiny central processing unit that was specifically developed for the study; it contained specialized software that allowed subjects to fill out the computerized dietary record offline and to transmit data during brief telephone connections. Subjects were assisted by the conversational features of the software and were given an instruction manual for coding of foods, including photographs for estimating portion or glass sizes that had previously been validated in a pilot study of 780 subjects. Diet at baseline was estimated from the 24-h dietary records completed during the first 18 mo of follow-up of each subject. For the present analyses, we selected only the subjects who completed at least six 24-h dietary records during those 18 mo. To account for potential seasonal and weekly variations, all nutrient and dietary values reported here are based on the average of these 24-h dietary records for each subject. Total dairy products were considered, as were 3 specific dairy products—milk, cheese, and yogurt (including cottage cheese, small individual containers of cream cheese, and regular yogurt)—and expressed in servings per day. We used the following amounts per serving: 225 g for milk, 30 g for cheese, 100 g for cottage cheese, 60 g for a small individual container of cream cheese, and 125 g for yogurt. The nutritional values of the diet, including calcium, were estimated by using a French computerized food-composition table developed for the SU.VI.MAX Study. In addition, calcium intakes from dairy and nondairy products were studied separately.

To take into account the confounding effect of diet quality in our analyses, we used the mean adequacy ratio index (MARi) as an indicator of nutritional quality. Although multiple versions of this index exist, MARi has repeatedly been shown to be positively associated with other indexes of diet quality (29, 30). The adaptation of MARi used in these analyses was based on the mean percentage of the recommended intakes for 23 key nutrients and was calculated by using the following equation (31):

Formula 1(1)
where intakep is the daily intake of each nutrient p, and RDAp is the French Recommended Dietary Allowance for that nutrient. As in the past, each ratio of intakep to RDAp was truncated at 1, so that a low intake of one nutrient could not compensate for a high intake of another nutrient (32).

Body weight, height, and waist measurements
Weight, height, and WC were measured by using standardized procedures. Weight was measured by using an electronic scale while subjects were wearing indoor clothing and no shoes. Height was measured under the same conditions to the nearest 0.5 cm by using a wall-mounted stadiometer. Body mass index (BMI; in kg/m2) was calculated, and overweight was defined as a BMI ≥ 25. Using an inelastic tape, WC was measured as the circumference midway between the lower ribs and the iliac crest. Changes in weight and WC were calculated, in absolute terms, as the difference between the last and the first measures.

Assessment of covariates
Level of education was obtained from a questionnaire at baseline and was coded in 3 categories according to the highest level completed (ie, primary school, high school, or university or equivalent). Data on smoking status (current smoker, previous smoker, or nonsmoker), overall physical activity level (irregular, low, or equivalent to ≥1 h walking/d), and menopausal status (yes or no) were collected by using the same questionnaire.

Statistical analysis
Quartiles of dairy food consumption and calcium intake were calculated by sex for the distributions of both consumers and nonconsumers. The sex x overweight status x milk consumption and sex x overweight status x yogurt consumption interactions were significant (P = 0.02 and 0.04, respectively), which indicated that the associations between weight change and the consumption of these dairy products differed according to both sex and initial weight status. Therefore, analyses were performed separately for normal-weight and overweight men and for normal-weight and overweight women. Associations of changes in body weight and WC over the 6-y follow-up with consumption of dairy products and dietary calcium intake were assessed by using analysis of covariance with adjustment for age. In the multivariate model, we further adjusted for other potential confounders at baseline, including energy, alcohol, MARi, intervention group, educational level, smoking status, physical activity level, baseline outcome value, and menopausal status (for women) (Tables 2Go and 3Go ). For each type of dairy product (ie, milk, cheese, or yogurt), we also controlled for the consumption of the other 2 dairy foods (Tables 2Go and 3Go). Accordingly, dairy and nondairy calcium intakes were adjusted for each other. Tests for linear trend were performed. Statistical significance was judged at {alpha} < 0.05. Statistical analyses were carried out by using SAS software (version 8; SAS Institute Inc, Cary, NC).


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  		TABLE 2. Changes in weight and waist circumference in men by baseline weight status and quartile (Q) dairy consumption

 

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  		TABLE 3. Changes in weight and waist circumference in women according to baseline weight status and quartile (Q) dairy consumption

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Compared with women, men were, on average, older, more highly educated, and more physically active, and they were likely to have been more frequent smokers in the past. At the first clinical examination, men had higher mean values for weight, BMI, and WC than did women; 50.1% of men and 25.3% of women were overweight (BMI ≥ 25). Weight increased over the 6-y follow-up by a mean (± SD) of 1.97 ± 3.96 kg in men and by 1.77 ± 4.13 kg in women; WC increased by 1.14 ± 5.33 cm in men and 2.20 ± 6.34 cm in women (data not shown). Daily intakes of alcohol and calories (excluding alcohol) were significantly higher in men than in women. The macronutrient balance was similar in both sexes, but the MARi was significantly higher in men than in women. Men consumed more dairy products, especially more cheese, but less yogurt than did women. Milk consumption did not differ significantly between the sexes. The mean proportions of milk and yogurt consumed in dairy products were 39.9 ± 33.5% and 31.8 ± 27.4% for men and 37.7 ± 31.9% and 43.9 ± 28.3% for women. The contribution of cheese to total dairy product consumption was on average 28.4 ± 26.8% in men and 18.4 ± 19.8% in women (data not presented).

Analyses of anthropometric changes and dairy consumption
The relations between dairy consumption and changes in body weight and WC in men are shown in Table 3Go. In multivariate analyses, negative (borderline significant) associations between changes in both weight and WC over the 6-y period and total dairy product consumption were found only in men who were overweight at baseline (P for trend = 0.06 and 0.09, respectively). When dairy products were analyzed by categories, these inverse relations in overweight men were strengthened for milk (P for trend = 0.02 for both weight and WC changes) and yogurt consumption (P for trend = 0.01 and 0.03 for weight and WC changes, respectively) and disappeared for cheese consumption.

As was the case in men, we did not find any significant associations with 6-y changes in body weight and WC in normal-weight women except a positive association between yogurt consumption and weight change (P for trend = 0.04) (Table 1Go). In overweight women, the relation between milk consumption and WC change was not significant (but almost so). When models were further adjusted for site region (the southeast, northeast, southwest, or northwest of France or the Paris area), this association became significant (P for trend = 0.045). Further adjustment for the percentage of lipid intakes in total energy intakes did not modify the results.

Analyses of anthropometric changes and calcium intake
Total, dairy, and nondairy calcium intakes were not related to anthropometric changes in men who were overweight at the beginning of follow-up or in men who were not (data not shown). After adjustment for age, body-weight gain tended to be higher in normal-weight women with higher dairy calcium intake (quartile 4: 2.00 ± 0.25 kg compared with quartile 1: 1.45 ± 0.25 kg; P for trend = 0.04), but this relation was no longer significant in the multivariate-adjusted model (P for trend = 0.08). No results were modified when models were further adjusted for site or for percentage of lipid intakes.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this large sample of middle-aged French adults, total dairy consumption, especially milk and yogurt, was inversely associated with 6-y changes in weight and WC only in men who were initially overweight. These associations were not explained by calcium intakes. In contrast, a positive relation was observed between weight change and yogurt consumption in normal-weight women, whereas a positive relation between milk consumption and WC change was observed in overweight women.

A beneficial effect of dairy products on weight has been suggested by a substantial body of literature (1-3). Zemel (33) and Zemel et al (34) reported that isocaloric substitution of dairy products in the diet of obese adults resulted in a reduction of body fat mass. However, intervention studies did not find consistent results. Of 9 randomized dairy product supplementation trials reviewed by Barr (35), 7 found no significant difference in body-weight change between groups, and 2 studies conducted in older adults observed significantly greater weight gain in the dairy product groups. In a intervention study performed in healthy young women, a greater intake of dairy products does not alter body weight or fat mass over 1 y (36). In agreement with 3 previous prospective studies (12, 13, 37), our results suggest that the inverse association of dairy products with changes in weight differs according to body mass status.

The issue of the possible link between calcium intakes and weight change remains controversial. Several observational studies, most of which had a cross-sectional design, did not find an inverse association between calcium intake and adiposity (7-10, 25). Results from a retrospective US study in free-living adults suggested that dietary calcium intake was not related to weight change, but that dietary calcium intake from supplements was negatively associated with 10-y weight gain (24). In contrast, Lorenzen et al (38) found an inverse relation between body fat and habitual calcium intake but no association between body fat and calcium supplementation. As for dairy supplementation, intervention studies did not find consistent results. Of the 17 randomized trials reviewed by Barr (35) in which calcium intakes were supplemented, only 1 study found greater weight loss in the calcium-supplemented group than in the control group. Bowen et al (39) found no difference in weight loss in obese subjects following a high-dairy protein, high-calcium (2400 mg Ca/d) diet and those following a mixed-protein, low-calcium (500 mg Ca/d) diet. Shapses et al (40) found only a nonsignificant trend for increased weight loss in women supplemented with calcium.

Few studies have investigated the relations between dairy consumption (7, 12, 22, 37) or calcium intake (7, 13, 17, 19, 22, 41) and abdominal obesity, and even fewer have used a prospective design (12, 22, 37, 41). As for weight change, results are controversial. Pereira et al (12) found a significant inverse association between dairy consumption and WC only in overweight subjects, but, contrary to our results, no interaction with sex was mentioned. In 301 healthy 63-y-old men, the significant relations between dairy fat or calcium intake and sagittal abdominal diameter observed in the wall sample were weaker or disappeared when underreporters were excluded (13). Rosell et al suggested that these inverse relations could exist only in obese subjects, who were more likely to be in the underreporter group in their study. In an intervention study conducted in 32 obese adults, trunk region fat loss was significantly higher in subjects following a high-calcium diet and even higher in those following a high-dairy diet than in those following a standard diet (22). In participants from the Hoorn Study, it was shown that dairy consumption was significantly associated with an increase in WC only in subjects with a BMI of <25 at baseline (37). Therefore, it seems that dairy consumption could have a beneficial effect on abdominal obesity only in overweight subjects, but other confounders may be involved (12, 19).

The present study showed that some differences according to sex exist in the relations between dairy consumption or calcium intakes and anthropometric changes. Sex differences were also reported in the Health, Risk Factors, Exercise, and Genetics (HERITAGE) Family Study (19), in which energy-adjusted calcium intake tended to be positively related to BMI, WC, and the prevalence of obesity and overweight in black women, whereas inverse associations were observed between calcium intake and adiposity in black men and white women. In the Québec Family Study (17) and in the third National Health and Nutrition Examination Survey (21), such inverse associations were found in women, but no relation was found in men. The large prospective cohort Health Professionals Follow-up study (10) of US men similarly found no associations between dairy or supplemented calcium intakes and weight changes after adjustment for potential confounders. Differences in diet and lifestyle between men and women may explain sex differences and inconsistent results between dairy products and calcium.

We found no significant association between calcium intakes (total, from dairy or nondairy sources) and anthropometric changes, except a borderline significant relation in normal-weight women, between 6-y gain in weight and dairy calcium intake. The literature suggests that dairy sources of calcium exert stronger effects than do nondairy sources (15, 22). Lin et al (18) reported that the ratio of dietary calcium to energy and the ratio of dairy calcium to energy negatively predicted changes in both body weight and body fat. These effects appeared to be specific to dairy sources, because nondairy calcium was not a predictor of change in body composition. It is therefore important to identify other components of dairy products that may be responsible for these additional effects. Possible components include the high branched-chain amino acid content of dairy protein and the angiotensin-converting enzyme inhibitory activity contained in whey protein (33).

In overweight men, the present study showed an inverse association between weight and the consumption of both milk and yogurt. Similar relations were observed for WC. In normal-weight women, a positive relation was observed between weight change and yogurt consumption only, whereas, in overweight women, a positive relation was observed between WC change and milk consumption only. Generally, only an overall effect of total dairy products has been assessed in the literature, but dairy products present different nutritional compositions—eg, fat content. Zemel et al (23) observed a beneficial effect of yogurt intake on fat loss and central adiposity in obese subjects during energy restriction. Others found an inverse association between obesity and milk intake and no effect of yogurt or cheese (12). A beneficial effect of milk on weight was also found by others (4, 26). In Swedish women aged 40–55 y at baseline, whole milk and sour milk intakes in overweight persons and cheese intakes in both overweight and normal-weight persons were inversely associated with 9-y weight gain (13). Thus, it is not clear that the same benefit could be derived from different dairy products, and results from recent studies examining this question remain inconclusive.

Until recently, little was known about the mechanisms by which calcium intake could affect body composition. It has been hypothesized that a low dietary calcium intake stimulates high concentrations of parathyroid hormone and 1,25-hydroxyvitamin D, which, in turn, activates high concentrations of intracellular calcium in adipocytes, thus stimulating lipogenesis and inhibiting lipolysis (3). It has also been proposed that high calcium intake leads to the formation of indigestible calcium soaps in the gastrointestinal tract, which makes fat unavailable for absorption and thereby reduces calorie intake (42). High dietary calcium intakes have been shown to increase fat oxidation (43, 44) and fecal fat excretion (45). However, those studies either lacked sufficient power to detect any appreciable changes in body weight or fat mass (43) or measured only short-term changes, so that effects of habitual calcium intake were not observed (46). In addition, it should be noted that larger doses of calcium (1800 mg Ca/d) were required to produce a relatively small (fecal) energy loss. Thus, this mechanism does not entirely explain observed antiobesity effects of calcium (3).

One limitation of the present study was that it was not primarily designed to examine the effects of calcium intake on weight and WC changes. Subjects were participants in a nutritional intervention study, and they may therefore have a healthier lifestyle than does the general population. Indeed, calcium intakes in the present study were higher than those observed in some (7, 10) but not all (12, 19) other observational studies. More research is needed to investigate the relation between calcium intake and adiposity, as well as the connections of this relation with dietary patterns, which may play an important role in obesity (26, 47). We also did not separate high-fat from low-fat dairy products in this study, but we did control for the effect of fat intake. The relations between high- and low-fat dairy products and changes in body weight remain unclear. Indeed, some authors reported an inverse association between both low-fat and high-fat dairy products and obesity (12). However, Rajpathak et al (10) found a positive association with total and high-fat dairy intake and weight gain, but not with low-fat dairy intake. Finally, we could not assess the relation between dairy products or calcium intakes and changes in body composition. However, WC has been shown to be closely related to visceral obesity (48), a major cardiovascular disease risk factor (49, 50). Strengths of the present study include the large number of subjects, which provided sufficient statistical power to detect small changes in weight. In addition, the longitudinal design allowed us to compare 6-y changes in weight and WC across dairy and calcium categories from at least six 24-h dietary records.

In conclusion, our data suggest that the relations of dairy products and calcium intake to change in weight and WC may differ according to sex, initial body weight status, and type of dairy products. Dietary patterns, which may related differently to dairy consumption according to country, sex, and body mass status, could in part explain the interaction in the present study and the inconsistent results observed the literature. Further studies are needed to learn how the relations observed between dairy consumption and weight change are mediated by other dietary habits.


   ACKNOWLEDGMENTS
 
We thank all staff members of our institutions who contributed to this study and especially Nathalie Arnault for her management of the dietary database.

The authors' responsibilities were as follows—AC: performed the analyses and wrote the manuscript; SB: designed the study and supervised and assisted with study analyses, interpretation of the findings, and writing of the manuscript; PG and SH (the national coordinators of the SU.VI.MAX Study): were involved in the original data collection; and PG, SH, SP, SCY, EK, and SC: assisted in the writing of the manuscript and approved the final version. None of the authors had a personal or financial conflict of interest.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication August 1, 2007. Accepted for publication July 22, 2008.





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