Determining the role of calcium in weight control

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Recently, an anti-obesity effect of dietary calcium has been postulated (for reviews see Teegarden (2003), Zemel (2002) and Zemel and Miller (2004a)). Although first observations in rats and men showing an inverse relation between calcium intake, adipocyte intracellular calcium and obesity had already been published at the end of the 1980s (Draznin et al., 1988), this idea has never been more popular in the scientific community since the publication of the papers of Zemel and colleagues (Xue et al., 1998, 2001, Zemel et al. 1995, 2000). These publications were based to a major extent on investigations on obese and insulin-resistant mutant mice ('agouti mouse') and led to an intensive re-examination and extended interpretation of data from several epidemiological studies.

11.2.1 Epidemiological and intervention studies showing a role for calcium in weight management

Data from the US NHANES III (Third National Health and Nutrition Examination Survey), the CSFII study (Continuing Survey of Food Intake by Individuals), the CARDIA study, the Quebec Family Study and the HERITAGE (Health, Risk Factors, Exercise, Training and Genetics) Family Study showed accordingly a significant inverse relationship between calcium consumption and body weight, body mass index (BMI; BMI = body weight/ body length, kg/m2), body fat distribution and the prevalence of obesity respectively (Table 11.1).

Zemel and co-workers (2000), who re-examined data from 380 women (of about 7000) from the NHANES III study, found less body fat and a lower risk for obesity in people with the highest calcium intake after controlling for energy intake and physical activity, and the risk of being in the highest BMI quartile was reduced by 85% at the highest quartile of calcium intake. The anti-obesity effect of calcium has been demonstrated in black and in white people of both sexes, although in the HERITAGE Family Study the strongest effects occurred in white women and black men (Loos et al., 2004): the former exhibited a significant inverse relationship between calcium and BMI, percentage body fat and total abdominal fat, the latter between calcium intake and leanness.

An inverse relationship between BMI and dietary calcium or consumption of milk and dairy products was also found in adult women when the data from the CSFII study (Albertson et al., 2003), as well as data in a sample of the cross-sectional Portuguese Health Interview Survey 19981999 (Marques-Vidal et al., 2005), were re-examined. Two other long-term observational studies examined the effect of milk consumption on body composition and also on several physiological parameters. In the Quebec Family Study, abdominal circumference was negatively associated with dairy products consumption (Drapeau et al., 2004, Jacqmain et al., 2003), whereas in the prospective CARDIA study, an inverse relation-

Table 11.1 Human studies showing significant anti-obesity effects of increased calcium intake

Subjects

Period

Verum group

Results

References

Ol 3

1 if

A. Re-examination of earlier epidemiological studies

Table 11.1 Human studies showing significant anti-obesity effects of increased calcium intake

A. Re-examination of earlier epidemiological studies

Inverse association between:

NHANES III

c-s

calcium intake and risk of being in the highest BMI quartile

Zemel et al., 2000

HERITAGE Family Study

c-s

calcium intake and BMI, % body fat and (black men) obesity

Loos et al., 2004

CSFII study

c-s

intake of dairy calcium and BMI

Albertson et al., 2003

Portuguese Health

c-s

dairy intake and BMI

Marques-Vidal. et al.,

Interview Survey

2006

Quebec Family Study

c-s

dairy consumption and abdominal circumference

Jacqmain et al., 2003

CARDIA study

10 years

dairy intake and obesity

Pereia et al., 2002

B. Re-examination of prior observation and intervention studies with skeletal endpoints

Significant inverse relationship between: calcium intake and BMI

150 + 198 women 19-26 years c-s

(2 cohorts)

70 + 216 midlife women 8 years/ (2 cohorts) 21 years

216 women >65 years

Young healthy women, 19-26 years

4 years 3 years

+1.2 g/day Ca; same energy intake +1.5 g/day Ca calcium intake and midlife weight gain

In the verum compared with the placebo group: significantly more weight loss over 4 years less fat/more lean body mass

Davies et al., 2000

Davies et al., 2000 Barger-Lux et al., 2001

Table 11.1 Continued

Subjects

Period

Verum group

Results

References

C. Observation/intervention studies relating nutrient (or especially calcium) intake to body composition

Significant inverse relationship

54 normal weight women, 2 years 18-30 years

Midlife Caucasian women c-s

Midlife African American c-s women

Puerto Rican children c-c

53 white preschool children, until 8 years initially 2 years old

African-American women c-s

80 obese, 10-14 years; Ca c-s below recommendations

African-American 1 year hypertensive males + NIDD

32 obese adults 24 weeks

+2 servings yoghurt/day

Standard diet (450 mg/day Ca, 500 kcal/day deficit) + 800 mg/day Ca supplement between:

energy-adjusted Ca intake and change in weight/fat calcium intake in midlife and

BMI/body fat* no calcium effect dairy product (~ calcium) intake and obesity calcium intake and body fat accumulation*

calcium intake and BMI

calcium intake and overweight/obesity

Ca intake is positively associated with fat oxidation** In the verum compared with the placebo group: 4.5 kg less body fat (p < 0.01)*

Lin et al., 2000 Lovejoy et al., 2001

Tanasecu et al., 2000

Carruth and Skinner, 2001

Skinner et al., 2003 Buchowski et al., 2002 Lelovics, 2004

Melanson et al., 2003

Zemel et al., 1990 Zemel and Miller, 2004

* % or kg body fat were assessed by dual energy x-ray absorptiometry (DEXA); ** measured by whole-room indirect calorimetry.

c-s = cross-sectional, c-c = case control, NIDD = non-insulin dependent diabetic.

ship was found between milk and dairy products intake and several parameters associated with insulin resistance, including obesity (Pereia et al., 2002).

Although positive results were independent of whether calcium intake itself was estimated in the respective study or whether milk was taken as a measure of calcium intake, the approach for assessing calcium intake may be criticised, as calcium was not the prime test parameter in the studies mentioned. This criticism is, however, weakened by the fact that evidence also came from studies relating nutrient intake to body composition and from the re-analysis of clinical observational studies and controlled intervention trials, with the primary focus on the calcium effect on bone mass or blood pressure respectively (Table 11.1). By reverting to the same pool of studies with skeletal endpoints, Davies and colleagues (2000) and Heaney (2003) re-examined data from 780 women of young, middle and older age (four observational studies and one randomised controlled trial) or from 348 young women (19-26 years) from two cohorts respectively. Overall the authors found a significant negative association between calcium intake and body weight. The weight increase per year of women of middle age was also negatively associated with calcium consumption (Heaney, 2003). Young women at the lower (25%) quartile of calcium intake had a 15% prevalence to overweight, whereas a high calcium intake according to the recommended dietary intake (RDA) was associated only with a 4% prevalence (Heaney, 2003), and the odds ratio (OR) for being overweight was 2.25 when calcium intake was below the median (Davies et al., 2000). Davies et al. also calculated from the results of the intervention studies, that the daily consumption of a 1500 mg calcium supplement would reduce body weight significantly as compared with a placebo group and that 3% of the weight change can be explained by the level of calcium intake, whereby an increase of calcium intake by 1 g accounts for a weight reduction of 8 kg. The re-examination of further clinical studies (six observational studies and three clinical trials, with skeletal or circulation endpoints) by the same group confirmed the above-mentioned results in terms of quality and quantity (Heaney et al., 2002).

Despite these, overall, quite consistent results, it must be stated explicitly that re-examination of previous studies and, in particular, of observational studies provides, for several reasons, not the strongest evidence for an anti-obesity effect of calcium.

The original goal of these studies was not to investigate the effects of calcium on weight loss, therefore the study design and, in particular, the choice of the independent variables and primary study parameters are often not optimised for the problem of interest. Another problem is that some of the studies are included and re-used in various combinations for several re-examinations and meta-analyses of the calcium effect, which leads only to an apparently increased statistical power. Finally, if associations are derived from observational studies, no evidence of causality can be ascertained, even if the data allow for control of possible confounding factors such as energy intake or physical activity. A high or low intake of dairy products (and thus of calcium) could, for example, be simply the consequence of a lifestyle that favours a lower or higher body weight.

Therefore it is particularly important that, in recent years, some studies have been published that test explicitly the effect of calcium on body weight, body fat and the efficacy of weight-reduction diets. An epidemio-logical, population-based, cross-sectional observation study in 357 male and 470 female Tehranian adults aged 18-74 years showed an inverse association between milk, cheese and yoghurt consumption (assessed with the use of a 168-item semi-quantitative food-frequency questionnaire) and parameters of the metabolic syndrome - including waist circumference and obesity (Azadbakht et al2005). Subjects in the highest compared with the lowest quartile of dairy intake had lower odds of having enlarged waist circumference (OR = 0.63 vs. 1; p < 0.001) and a lower prevalence of obesity (17 vs. 23%; p < 0.04). The ratios became weaker after adjustment for calcium intake, indicating that the effect of dairy consumption on waist girth and obesity is only partly mediated by dietary calcium.

Numerous smaller observational studies of recent years, with between 35 and 80 participating subjects and observation periods of between 2 months and 8 years, relating nutrient or especially calcium intake to body composition, consistently revealed that a high calcium intake from the regular diet in childhood and adulthood as well as supplemental calcium is associated with a lower body weight (or BMI), less body fat due to a shift from fat to lean body mass and less age-dependent weight gain in midlife (Table 11.1). Moreover, calcium increased the efficacy of energy-reduced weight-reduction diets.

There are only a small number of (prospective) intervention trials in humans using calcium supplementation and body weight gain as independent and dependent study variables. In an earlier, placebo-controlled intervention trial in diabetic African-American males, the intake of ~300 mg/day calcium as yoghurt (two servings per day) throughout 1 year also increased body fat loss significantly by 4.5 kg (Zemel and Zemel, 1990). Zemel and co-workers (2004) also reported significantly greater weight loss (-10.9%) in subjects on a standard energy-deficient diet plus dairy products compared with subjects on the same standard diet alone or plus calcium supplements from other sources (-8.6% or -6.4% respectively; p < 0.01, n = 32, 24 weeks). Consumption of calcium and milk products enhanced particularly truncal fat loss, as shown in a randomised controlled study on 34 obese adults (Zemel et al., 2005). Addition of three servings per day of calcium-fortified low-fat yoghurt to an energy-reduced (-500 cal/day) low-calcium diet over 12 weeks increased weight loss by 22%, body fat loss by 61% and central fat loss by 81 %.

11.2.2 Epidemiological and intervention studies showing no calcium effect

However, not all cell culture and animal experiments confirmed the mechanism of the calcium effect proposed by Zemel and co-workers, and not all epidemiological studies and intervention trials observed positive effects of calcium supplements and/or milk products on body weight. Feeding normal or energy-dense diets differing in calcium content (0.2-1.8%) to normal and obese rats and mice (Paradis and Cabanac, 2005, Zhang and Tordoff, 2004) had no significant effect on energy intake, body weight or body fat and did not show the inverse relationship between 1,25-dihydroxy-vitamin D3 or parathyroid hormone (PTH) and body weight that is propounded by Zemel and co-workers (Shi et al., 2001). In addition, the core of Zemel's hypothesis, that a diet-induced decrease of intracellular calcium concentration in the adipocytes would enhance lipolysis and decrease fat deposition in adipo-cytes could not be confirmed in any of these studies. For example, when intracellular calcium in white adipose tissue was increased artificially by adrenergic stimulation, this was even associated with enhanced lipolysis (Boschmann et al., 2002). This coincides with findings made by Barr and co-workers (2004). Repeating the analysis of Zemel et al. (2000), but using the data from 6878 instead of 380 women, as in the NHANES III study, they did not observe a significant association between a low calcium or milk product intake and the risk of being in the highest quartile for body fat. A lack of relationship between calcium intake and BMI was also found in an observational study on 65 adult and 78 infant Pima Indians (Venti et al., 2005). In this case the authors explain the negative study results with the fact that Pima Indians are genetically prone to becoming obese, and that this could conceal a weak calcium effect. The Fourth Tromso study, a Norwegian population study on 9252 men and 9662 women, even showed a positive association between calcium intake and BMI in men and an unexpected negative association between vitamin D intake and BMI in both sexes (Kamycheva et al., 2003). In addition, in a longitudinal observation study in 1200 adolescents weight gain over 3 years was even directly proportional to the number of dairy product servings per day (Berkey et al., 2005).

In two recently published randomised controlled intervention trials on obese adults, high-calcium, energy-restricted diets (2400 or 1400 mg/day calcium, mainly from dairy products) caused the same (Bowen et al., 2005) or a non-significantly higher (+20%; Thompson et al., 2005) loss of body weight and body fat, compared with the same energy-restricted diets containing 500 or 800 mg/day calcium respectively.

Furthermore, administration of 1 g/day 'extra calcium' did not promote postpartum loss of body weight and fat in lactating and non-lactating mothers (Wosje and Kalkwarf, 2004). The same calcium dose increased weight and fat loss in 100 pre- and postmenopausal women following an energy-restricted diet over 25 weeks; however, this increase was not significant (Shapses et al., 2004).

11.2.3 How to weigh up the differing study outcomes

All in all there is, at this point in time, some confusion about the extent and importance of the postulated role of supplemental calcium or dairy products in weight management. One comment (Clifton, 2005) concludes from the recently published studies that did not find a calcium effect, that this may be 'the beginning of the end for the dietary calcium and obesity hypothesis'. This is certainly not correct, as the author does not explain or consider otherwise the findings of the numerous studies with a positive outcome.

On the other hand it is still completely unclear how the different outcomes of the 'positive' and 'negative' studies come about. Erroneous estimates of calcium intake are certainly not the explanation, because in both fractions there are small and observational studies in which regular consumption of dairy products and other calcium sources was estimated according to food-frequency questionnaires, as well as controlled intervention trials with defined and controlled administration of supplemental calcium. Also, with respect to other factors - such as, ethnicity, age, the pre- or post-menopausal stage of women, weight or sex of the subjects, the energy provided (i.e. normocaloric or calorie-restricted diets) and the calcium content of the basal diet or the amount of supplemental calcium - the positive and negative studies do not differ completely. Other parameters such as the nutritional, calcium or vitamin D status of the study subjects, the bioavail-ability of calcium from different sources as well as the influence of other diet components (except for milk and dairy components) were usually not taken into consideration.

It seems rather likely that the influence of calcium on body weight and body fat is in any case rather small, and that therefore already small differences between studies concerning design, study population or other factors not included in the compilation of the results, could decide on whether an effect is apparent or even statistically significant. Beyond that, those studies that were originally designed to address other topics, and which were then re-analysed, need to be interpreted particularly cautiously. In addition, cross-sectional/observational studies are not usually suited to uncovering causal relationships, but show only associations.

In order to examine the role of dietary calcium in weight management, more well-designed longer-term intervention studies with a sufficient number of participants, defined endpoints and well-characterised target groups are required, as well as knowledge of the underlying mechanisms. It will be, after all, not so much a question of whether calcium has an anti-obesity effect or not (in reality there is mostly an 'under certain conditions yes, otherwise no'), but rather in which target group can calcium play a role in weight management, and to what extent, and how this impact is modified by other factors.

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