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Nutrición Hospitalaria
versión On-line ISSN 1699-5198versión impresa ISSN 0212-1611
Nutr. Hosp. vol.27 no.6 Madrid nov./dic. 2012
https://dx.doi.org/10.3305/nh.2012.27.6.5977
Calcium ingestion and obesity control
Ingesta de calcio y control de la obesidad
D. M. de Oliveira Freitas, H. Stampini Duarte Martino, S. Machado Rocha Ribeiro, R. de C. Gonçalves Alfenas
Department of Nutrition and Health, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil.
Acknowledgements to CAPES for the master's scholarship grant and to FAPEMIG for the support (CDS-APQ-01677-10).
ABSTRACT
Introduction: Obesity is a risk factor for other nontransmissible chronic diseases. It has been suggested calcium intake helps to control obesity, but there is no consensus about this.
Objective: Analyze the studies published on this topic in order to highlight issues to be further explored in future studies.
Methods: A literature review was conducted using the PUBMED, Science Direct, Scielo, Scopus, Medline and CAPES electronic scientific basis. Studies, which evaluated the effect of calcium ingestion in energy metabolism, body weight, and body composition, published from 2000 through 2011, were analyzed.
Results and discussion: The results of most of the interventional studies selected suggest that calcium ingestion may favor the reduction of the anthropometric measures and improve body composition. The discrepancy in the results of the observational studies is probably due to methodological differences. It seems that the benefits are only detected when a low calcium habitual ingestion (≈ 700 mg/day or lower) is increased to about 1,200-1,300 mg/day.
Conclusion: When assessing the effect of calcium derived from supplements, the investigators should test higher bioavailability compounds. If the calcium source is the dairy product, it is necessary that to consider and isolate the impact of other nutrients present in these foods. Longer term studies should be conducted to assess the effect of calcium on energy metabolism.
Key words: Calcium. Energy metabolism. Body weight. Body composition.
RESUMEN
Introducción: La obesidad es un factor de riesgo para otras enfermedades crónicas no transmisibles. Se ha sugerido que el consumo de calcio ayuda a controlar la obesidad, pero no hay un consenso al respecto.
Objetivo: Analizar los estudios publicados sobre este tema con el fin de destacar los aspectos a investigar en estudios futuros.
Métodos: Se realizó una revisión bibliográfica utilizando las bases de datos electrónicas PUBMED, Science Direct, Scielo, Scopus, Medline y CAPES. Se analizaron los estudios que evaluaban el efecto de la ingesta de calcio sobre el metabolismo energético, el peso corporal y la composición corporal, publicados desde 2000 a 2011.
Resultados y discusión: Los resultados de la mayoría de los estudios intervencionistas seleccionados sugieren que la ingesta de calcio podría favorecer la reducción de las medidas antropométricas y mejorar la composición corporal. La discrepancia de los resultados de los estudios observacionales probablemente sea debida a diferencias metodológicas. Parece que los beneficios sólo se detectan cuando una ingesta habitual de calcio baja (~ 700 mg/día o menor) se incrementa hasta cerca de 1.200-1.300 mg/día.
Conclusión: Cuando se evalúa el efecto del calcio derivado de los suplementos, los investigadores deberían evaluar la biodisponibilidad de los preparados. Si la fuente de calcio son los productos lácteos, es necesario que consideren y aíslen el impacto de otros nutrientes presentes en estos alimentos. Deberían realizarse estudios a largo plazo para evaluar el efecto del calcio sobre el metabolismo energético.
Palabras clave: Calcio, Metabolismo energético, Peso corporal, Composición corporal.
Abbreviations
NTSD = Non-Transmissible Chronic Diseases.
PTH = Parathyroid Hormone.
RDA = Recommended Dietary Allowance.
NHANES = National Health and Nutrition Examination Survey.
FAS = Fatty Acid Synthase.
UCP2 = Uncoupling protein 2.
BMI = Body Mass Index.
WC = Waist Circumference.
EAR = Estimated Average Requirement.
DEXA = Dual Energy X Ray Absorptiometry.
Introduction
Non-transmissible chronic diseases (NTSD) are a global health problem.1 It causes serious impacts on health, leading to several adverse effects on life quality of people, favoring the occurrence of premature deaths and high costs for society.2 Cardiovascular diseases, cancer, chronic respiratory diseases and diabetes are responsible for 60% of deaths around the world.3 If effective prevention and control measures are not taken, it is estimated that 41 million people will die from a NTSD by 2015.2
Obesity stands out among the NTSD because it is a risk factor for other diseases such as dyslipidemia, cardiovascular diseases, diabetes, hypertension, cancer.1,2,4-6 Overweight and obesity are responsible for 2.6 million deaths per year.2 Regardless of its complex and multifactorial etiology,7 the decrease in the levels of physical activity and the increase in energy intake are strong environmental determinants for this situation.2,7,8 Many researchers have focused on the identification of the combination of macronutrients capable of regulating body weight, but the effect of micronutrients still needs to be further explored.9-12 Minerals participate in the energy metabolism and in the secretion and action of insulin,13 and may interfere in the control of obesity.
Calcium, the most abundant mineral in the human body, is involved in various physiological processes: muscle contraction, cell adhesion, hormones and neurotransmitters release, glycogen metabolism, cell proliferation and differentiation, blood clotting, nerve or synapthetic impulse transmission and structural support of the skeleton.14,15 In addition, it has been suggested that it may assist body weight control. Two possible mechanisms of action have been proposed to explain this effect. It seems that when high quantities of calcium is consumed, it binds to dietary fat forming insoluble compounds, reducing fat absorption and hence the amount of calories generated from this absorption.16,17 Calcium ingestion is also important to maintain normal blood calcium levels, preventing the increase of 1,25(OH)2D3 and parathyroid hormone (PTH), which in turn can promote increased levels of intracellular Ca2+, activating lipogenic routes.18
However, there is no consensus in the results of studies evaluating the effects of calcium intake on body weight and body composition,11,19-29 and in energy metabolism.11,17,30-32 It is possible that the outcomes may be affected by the source of calcium tested. Although the results of some studies suggest that calcium originated from the supplements has no effect,20,22,24,27,29 others demonstrate positive effects in controlling obesity.21,33,34 It has been suggested that dairy products may have a stronger effect than supplements.18,33 However, exact the reason why this occurs is not known.17,27,35,36
The new recommendation for calcium intake (Recommended Dietary Allowance (RDA) = 1000 mg/day) is based on its effects on bone health, since there is no consensus on its effects on NTSD.38 According to some authors, to obtain the beneficial effects on body weight and NTSD calcium intake should range from 1,000 to 1,200 mg/day.39 It is unclear whether the effects are dose dependent, but the knowledge of the minimal dosage capable of resulting in positive effects is important to improve adherence and effectiveness in response to the mineral intake and to minimize the costs with NTSD.29
Due to the increase in obesity prevalence, the effect of diet in its etiology and the limited number of longitudinal clinical studies publish about this topic so far, it is necessary to conduct well-designed studies to assess the effect of high calcium intake on resting energy expenditure, body weight, and body fat control.12,19 Therefore, the purpose of this review is to highlight issues to be further explored in future studies to clarify the possible effect of calcium intake on anthropometry, body composition and energy metabolism.
Methodology
Articles published from 2000 to 2011, in which the effects/association of calcium intake on/with body weight, body composition and energy metabolism were selected. A literature review was conducted in order to find articles in the electronic databases PUBMED, Science Direct, Scielo, Scopus, Medline and CAPES Journals.
Using the following indexing terms in English or in Portuguese: "calcium intake and obesity", "calcium intake and weight control", "calcium intake and weight loss", "calcium intake and body composition", "calcium intake and energy metabolism," "calcium intake and fat oxidation", "calcium intake and energy intake".
Possible mechanisms through which calcium may favor obesity control
The inverse relationship between calcium intake and body weight was observed since the 1st National Health and Nutrition Examination Survey (NHANES) in 1984.40 However, due to the lack of a possible mechanism of action to explain this association made this topic was not explored at that time. Today, the mechanisms by which calcium may control body weight and the magnitude of this effect are not well understood.22 However, two possible mechanisms of action have been suggested. These mechanisms will be presented below.30,41,42
Increased fat excretion
It has been postulated that the interaction of calcium with fatty acids forming insoluble soaps can reduce the absorption and increase the excretion of these fatty acids, contributing to body weight reduction.16,17,43
In a crossover study, the effect of two treatment types on fat excretion in adult men was assessed. One of the treatments contained ≈ 410 mg/day of dietary calcium. The other contained 1,800 mg of calcium citrate malate plus 400 mg/day of dietary calcium (total of ≈ 2,200 mg/day). Calcium citrate malate, a soluble form of calcium, was administered together with fatty acids. Saturated fatty acids excretion doubled after the high calcium treatment compared to the low content one.43 In another study, the effect of the consumption of a diet containing calcium-free chocolate (≈ 950 mg/day) and of another containing chocolate supplemented with calcium (calcium carbonate) was compared (≈ 1,855 mg/day). Once again, the excretion of saturated fatty acids was increased approximately two times after the consumption of the chocolate supplemented diet.16 The results of these last two studies suggest that fatty acids should be consumed with calcium in the same meal so that fat excretion increase can take place.
Fecal fat excretion was 2.5 times higher after the consumption of a diet containing 1,800 mg/day of calcium and 15% protein compared to two other test diets (500 mg/day of calcium + 15% of protein and 1,800 mg/day of calcium + 23% of protein). According to the authors, a higher protein intake may favor calcium binding to phosphorylated proteins. Therefore, fatty acids would be free to be absorbed in the intestine, reducing the effects of calcium intake on fat excretion.17
The results of these studies suggest that calcium consumption > 1,800 mg/day may be effective to reduce fat absorption, and that the joint ingestion of that mineral with fatty acids is important for that effect to occur. It should be noted, however, that this amount is higher than the recommended daily intake of calcium.38 It has been shown that in some populations calcium intake is less than what is recommended.41,42,44-48
It should be emphasized that in two of the previously mentioned studies17,43 there was an increase in urinary calcium excretion in response to the higher calcium intake, suggesting that the amount of the ingested calcium capable of increasing fat excretion may be lower than the ones tested. However, in one of these studies,17 the higher urinary excretion was observed only when the high calcium intake was associated with high protein intake (1,800 mg/day + 23% protein). It has been demonstrated that an increase in protein consumption may increase calcium urinary excretion.49
Increased levels of intracellular Ca2+
Some authors suggest that the effect in response to calcium consumption would be small to explain the magnitude of the observed effects on body weight and body composition. Besides that the amount to be consumed to possibly lead to these effects is very high.33,50 Therefore, the mechanism proposed by Zemel et al. (2000)18 (fig. 1) has been pointed out as the more consistent one to explain how low calcium intake would contribute to excess weight.42
The analysis of human adiposities indicated that the levels of 1,25(OH)2D3 and PTH can increase the intracellular levels of Ca2+ and inhibit lipolysis.18 The results of human adipose tissue culture studies showed that the treatment with 1,25(OH)2D3 induced an increase of intracellular Ca2+ in a dose dependent form, increased by 40% the activity of fatty acid synthase (FAS), increased from 2 to 2.5 times the expression of mRNA FAS and inhibited the lipolysis in 35%,51 reducing in 40% the expression of mRNA of uncoupling protein (UCP2), which is involved in the regulation of thermogenesis and energy metabolism and the levels of UCP2 in 50%.52
On the other hand, a higher consumption of calcium is capable of preventing weight gain, reducing body fat and increasing thermogenesis. These effects were observed in an animal study, which ate one of the four types of diet. 1) 0.4% of calcium diet, 2) 1.2% of calcium (0.4% dietary calcium + 0.8% from CaCO3 supplement), 3) 1.2% of calcium (0.4% non-dairy source + 0.8% derived from dairy) and 4) 2.4% (0.4% non-dairy source + 2% derived from dairy). Although in terms of quality the effects of calcium from supplement were equivalent to dairy, the effects of calcium from dairy were stronger.18
Animal studies also support this evidence.35,53,54 The consumption of a low calcium (0.4%), high fat, and sucrose diet doubled the concentration of intracellular Ca2+. On the other hand, the consumption of diets containing 1.2 and 2.4% of calcium reduced the concentration to 50%, besides leading to greater reduction on body weight, body fat, mRNA FAS expression, FAS activity, and increased lipolysis, UCP2 expression, and body temperature. A greater increase body temperature, and a greater reduction in body weight, body fat, activity and expression of FAS was observed in response to the consumption of dairy calcium compared to calcium carbonate.35 Parra et al. (2008)54 verified that the consumption of a calcium supplemented diet reduced body weight and body fat in laboratory animals. But no changes were observed in the levels of UCP2. The effect of the consumption of a diet enriched with milk serum protein, calcium and vitamin D to that of a diet with low content of these nutrients were tested. Both test diets had high fat and sucrose content. Although food intake and body weight were not affected, it was observed that the animals that were fed the enriched diets had less body fat, and there was an increase in lean body mass.53 However, the results of this study cannot be attributed to any specific nutrient (protein, vitamin D or calcium).
The consumption of a calcium-rich diet by laboratory animals led to less body weight and body fat gain, increased UCP2 expression, higher lipolysis rates, and higher body temperature than those that consumed a diet with low calcium content. These results suggest that calcium and dairy products may modulate adiposity independently of caloric restriction. In quantitative terms, the consumption of the high calcium derived dairy products diet resulted in the greatest effects than the diet continuing calcium from fortified cereal.37
This is useful for explaining the effect of calcium in adiposities and in rodents, but there it is necessary to conduct studies involving human beings to test this mechanism.19 Although investigations in animals support this hypothesis, there is no homogeneity in the results of the studies in terms of some parameters assessed; for example the expression of UCP2.35,52,53,54 There is also a study involving animals in which body fat was not affected after the ingestion of diets with low, normal amount of calcium and supplemented with calcium.55
The reasons why the effects of dairy products could exert more striking effects, quantitatively, than calcium supplements are not clear.17,35,50 In animals similar effects were observed in reducing the concentration of intracellular Ca2+. It has been suggested that other dairy products components may act by a route independent of that concentration. However, neither the mechanism of action nor the responsible components of dairy products have been identified,35 and future studies are needed to determine the effect of these components.50
In human studies, the effects of calcium in body weight and body fat are not consistent either.32 If we think about the proposed mechanism18 it is important to find out not only the possible effects of calcium but also the role that PTH and 1,25(OH)2D3 may play in humans body weight and body fat regulation.11
Effect of vitamin D ingestion and serum levels
There is no consensus on the relationship between serum levels of vitamin D and adiposity. The results of an intervention study indicated that there is no difference between serum levels of vitamin D between obese and normal weight people.56 However, after being submitted to UV-B, obese subjects showed a more attenuated response to changes in the levels of 1,25(OH)2D3 than the normal weight subjects, regardless of the absence of a significant difference in the production of 1,25(OH)2D3.56 This result suggests that obese individuals release less vitamin D from the skin to the circulation.56 It has been claimed that vitamin D is stored in the adipose tissue, and that the higher the fatty tissue, the lower the serum levels of 25(OH)D.57 In the previously mentioned study,56 it was verified a negative correlation between body mass index (BMI) and serum levels of 1,25(OH)2D3 only after UV-B radiation treatment. Obese patients had lower serum levels of 25(OH)D. BMI was negatively correlated with 25(OH)D concentrations only after the ingestion of 50000 IU of that vitamin.56
These results have been corroborated in other studies. Parikh et al. (2004) verified lower levels of 25(OH)D and 1,25(OH)2D3 in obese compared to normal weight adults.36 Vitamin D deficiency (levels of 25(OH)D < 20 ng/ml) was considered a predictor of metabolic syndrome in obese patients with BMI > 40 kg/m2. It was observed a higher occurrence of deficiency between obese patients presenting metabolic syndrome.58 The levels of 25(OH)D were negatively correlated with body fat,57,59 BMI,59,60 waist circumference (WC) and skinfolds.59
These data contradict what has been claimed by Zemel et al. (2000),18 that is high serum levels of vitamin D would increase the body weight and adiposity. Therefore, further studies are needed to evaluate the influence of serum levels of vitamin D on body weight, body composition and energy metabolism.
Thus, there has also been evaluated the possible influence of the ingestion of this vitamin on body weight and body composition. In the fourth Tromso Study, the usual intake of vitamin D by adults was negatively correlated with BMI. The odds ratio for obesity was equivalent to 2.24 in men and 1.51 in women. These participants were in the lowest quartile of intake of the vitamin. However, the authors report that cod liver oil the cod fish itself were the highest source of vitamin D habitually consumed by the subjects of that study. Therefore, the effect observed may have been caused by other substances present in these foods.61 In the Women's Health Study, the usual intake of vitamin D was negatively associated with BMI and WC. However, this association was independent of calcium intake.62 These results suggest that habitual intake of vitamin D alone has little influence on body weight and body composition.
The effect of vitamin supplementation on body weight, body fat and anthropometric indicators was also evaluated. The addition of 400 IU/day of vitamin D and 1,200 mg/day of calcium associated with caloric restriction (700 kcal/day) did not affect BMI, body weight, body fat and WC in women with excess body weight and obese, which had a habitual calcium intake < 800 mg/day.63 However, when among women with habitual calcium intake < 600 mg/day, there was a reduction in body weight, BMI and body fat percentage.64
In women with lower calcium intake than the recommendations, it was verified that the supplementation with 400 IU of vitamin D associated with 1,000 mg of elemental calcium for seven years reduced the risk of body weight gain.65 However, weekly supplementation of 20,000 IU (≈ 2,857/day) and 40,000 IU (≈ 5,714/day) of vitamin D associated with 500 mg of calcium/day, did not promote a significant reduction of BMI, body weight, body fat percentage, waist circumference and hip circumference, compared to a placebo containing 500 mg of calcium/day.60 In another study, the supplementation of 2,000 IU of vitamin D for seven days did not change serum calcium levels, resting metabolic rate and the expression of genes related to lipogenic and lipolytic process such as FAS and UCP2.66 Despite the increased vitamin D serum levels and reduced PTH concentrations obtained as a result of the daily 3,332 IU vitamin D supplementation for 12 months associated with a body weight reduction program it did not affect the body weight compared to placebo.67
These results suggest that the supplementation in higher dosages than the RDA (600 IU)38 does not result in body weight control. However, the intake of vitamin D in amounts equivalent to the Estimated Average Requirement (EAR = 400 IU)38 may exert a beneficial effect when combined with calcium supplementation and applied to people with low habitual dietary calcium intake. This data raise questions about which nutrient would be responsible for such benefits (vitamin D or calcium). It is possible that the benefits are due to the combined effect of these nutrients and they are conditioned to the habitual intake of the population evaluated.
Human prospective intervention studies assessing the effect of the adequacy of vitamin D status for NTSD treatment and prevention are still scarce. Therefore, the impact of vitamin D nutritional status in these diseases should be evaluated in future studies.68
Effect of PTH serum levels
Some studies have shown higher levels of PTH in obese individuals compared to normal weight individuals.36,56,59,69 There has been observed a positive association between BMI and PTH levels, PTH and body fat in adults,37 and between PTH levels and body fat, BMI, waist circumference and skinfold sum in elderly.59 In the fifth Tromso Study it was observed that each increase of 1 pmol/l in PTH caused an increase of 0.17 kg/m2 in men and 0.26 kg/m2 in women in terms of BMI. The relative risk for obesity was 1.40 for men and 1.48 for women, who were in the highest PTH levels quartile.69 These studies are consistent with the mechanism proposed by Zemel et al. (2000).18
In adiposites and skeletal muscles PTH stimulates phospholipids C resulting in an increase in intracellular Ca2+. This increase can impair the ability of catecholamine to activate lipolysis and stimulates cAMP phosphodiesterase, which suppresses lipolysis. The increase in calcium concentration in adiposities can increase the expression of fatty acid synthase and increase lipogenesis.70
Although some studies show that both calcium and vitamin D intake and their serum levels may influence the levels of PTH,69,71 studies involving young adults in Brazil, showed no association between PTH levels versus serum calcium levels and 25(OH)D and calcium intake.72 Studies involving the supplementation of vitamin D (40,000 IU vitamin D + 500 mg of calcium)60 and dosage of 3,332 IU of that vitamin caused a reduction of PTH concentrations.67 These results highlight the controversy as to the triggering factor responsible for the increase in PTH levels. With respect to vitamin D, supplemented quantities capable of reducing the PTH levels are higher (40,000 IU) or close (3,332) to the upper intake levels for this vitamin (4,000 IU).38
Observational studies
The results of some studies have suggested the occurrence of possible effects and relationships dosage/effect of calcium intake on body weight and body composition. It has been claimed that calcium intake may explain 3 to 10% of body weight variation.73,74 Analyzing the data from NHANES III, it was observed that an increase in calcium intake from 400 mg to 1,000 mg for a year in obese American subjects caused a reduction of 4.9 kg.18 In middle aged women it was observed that the probability of overweight is reduce from 14.6% to 4.1% and of becoming obese reduces from 1.4 to 0.2%, when calcium intake increases from 10 to 20 mg calcium/g of protein. Besides that the weight gain/year reduces from 0.425 to -0.011 kg when the ingestion increases from 9 to 20 mg calcium/g of protein.74 According to Eagan et al. (2006), in young normal weight people it is expected a body fat gain of 1.26 kg in 18 months in response to the ingestion of 500 mg of calcium from dairy products/ day while in response to an ingestion of 1,200 mg/day it is expected a weight loss of 0.631 kg.57
The main features of these observational studies can be seen in table I. Despite the suggestions of the existence of a possible ratio dosage/effect previously mentioned, he analyses of a larger number of observational studies show a non-conclusive scenario in terms of: the existence of effects, dosages and source of calcium (dairy products or supplement). This can be attributed to methodological differences among these studies in term of how the anthropometric data, body composition, and dietary intake were obtained, and even with regards to types of analyses used in these studies.
Anthropometric and body composition data have been obtained by self-reports, electrical bioimpedance and anthropometry (weight, height, BMI, WC), computed tomography and dual energy x ray absorptiometry (DEXA). It is clear that the use of some of these methodologies may affect the accuracy of the measurements. It has been shown, for example, that self-report data may differ from the measured data, which may interfere in the nutritional status classification.75,76 Some authors have reported that bio-impendence may underestimate body fat percentage compared to DEXA in overweight people.77,78 These methods have different capabilities and applicability of measuring body fat and its distribution.79
Food intake data have been obtained through dietary recalls and food frequency questionnaires. The number of recalls and frequency in which they were used vary between studies. The 24-hour recall and food record only represent the habitual diet if applied for several nonconsecutive days.80,81 The accuracy of these methods depends on the number of days in which they are repeated. According to Willett et al. (1998),80 these dietary recalls should be applied from 3 to 10 times.
Another important factor to be considered is the need to adjust the statistical analyses regarding the consumption of nutrients such as proteins and vitamin D that may affect results.23,37,64,82-88
Nevertheless, the results of these studies suggest that calcium derived from dairy products or from supplements and even the dairy products themselves are associated with body weight and body composition, and that a low calcium intake (≈ 600-700 mg/day) is related to a higher body weight and adiposity. Due to methodological differences and to the fact that observational studies do not prove causality it is necessary to analyze the results obtained in the existing intervention studies.
Intervention studies
Effect of calcium intake on anthropometry and body composition
The characteristics of some intervention studies on the effect of calcium on body weight and body composition are shown in table II. The results of sudies that evaluated the effects of the calcium intake derived from the supplements,20,22,27 mostly suggest that calcium does not affect body weight and body composition. However, there are some common points in these studies that need to be better explored. It is observed that the tested dosage of the supplements was higher than 1,000 mg/day, which added to the habitual food intake lead to a daily ingestion higher than the recommendation.38 If calcium affects anthropometry and body composition, there may be a threshold level after which this effect does not occur. Another issue is that in these studies the average habitual intake of the participants was higher than 800 mg/day and results of observational studies19,25 suggest that there is a strong association when the habitual intake is lower than ≈ 700 mg/day. Therefore, there must be a lower intake threshold where the association can be detected. The administration different forms of supplements can also interfere in the results. According to one of the proposed mechanisms of action of calcium, the ingestion of supplement in association with food is important for the mineral to cause the expected effect.16,43 Furthermore, the ingestion in association with certain types of foods may increase the calcium bioavailability.49
The results of intervention studies28,33,83 reinforce the assumption that when participants have low habitual intake < ≈ 700 mg/day, calcium seems to really affect body weight and body composition.19,25 In the study conducted by Kabrnova-Hlavata et al. (2008)84 there was no significant effect of calcium. However, in the treatment groups fat free mass was preserved compared to placebo. Furthermore, it is likely that the absence of effects may be attributed to the amount of calcium consumed (850 mg/day), which was lower than the RDA (1,000 mg),38 or to the short duration of the study.
In a study conducted by Zemel et al. (2004),33 the effect of calcium derived from dairy products was quantitatively higher than that derived from calcium supplements. The possible reason for this possible superiority remains unexplained. This difference may be due to the bioavailability of the mineral in the supplement. Therefore, it becomes interesting to conduct studies to test the effect of supplements having higher bioavailability such as calcium citrate.49,89,90 It is also necessary to consider the way in which the supplement is administrated, that is if it is administrated in association with food or not.
Some authors attribute the stronger observed effect to other nutrients present in dairy products such as vitamin D64 and proteins (branched chain amino acids, such as leucine).23,37,82-88 It has been claimed that proteins could increase satiation, thermogenesis and avoid muscular mass loss.
Leucine would lead to greater fat mass loss, would stimulate the recovery of muscle protein synthesis thus reducing the loss of lean body mass.85-88 In the culture of cells, leucine stimulated fat oxidation in muscular cells and inhibited FAS in adiposites.82 On the other hand, in the elderly, the ingestion of 1g of protein /kg of body weight, containing 7.5 g of leucine/day did not change body composition.91
In general, it is suggested that a high protein intake is required to exert the effect. In a recent review study it was shown that in most studies, there is a reduction in energy intake when 30% or more of total energy intake derives from protein.87 The comparison of the effect of the consumption of isocaloric and isoglycidic diets containing 15% and 30% of protein showed no difference in adults resting metabolic rate. However, there was a reduction in hunger sensation and energy intake, and an increase in satiety in the group that consumed the diet containing 30% of protein.92 In contrast, in another study, obese subjects consumed diets containing 30% of protein (1,600 mg of calcium) x 15% of protein (600 mg calcium) and the same fat content (30%). There was no difference in energy intake, body weight and body composition. Only in women who consumed 1.4 g of protein/kg body weight lean body mass was preserved. Furthermore, in the group that consumed 30% of protein there was lower ingestion of fiber and higher ingestion of cholesterol. One cannot distinguish if the observed effects are related to increased intake of protein, calcium or reducing carbohydrate ingestion.93 Similarly, in studies in which there is great change in the percentage of macronutrients, the effects can perhaps be attributed to these changes.
Besides confirming the effectiveness of increased protein intake on obesity control, future studies should assess how this type of dietary intervention effects renal function, calcium balance, cardiovascular diseases risk and other adverse effects associated with chronic high protein consumption before high protein diets are recommended for weight loss,87,92 once there is currently no Tolerable Upper Intake Level for protein.85
These facts can lead to discussion about the most appropriate distribution of macronutrients to maintain healthy body weight. The current recommended distribution of macronutrients considering the total energy expenditure is: protein - 10 to 15%, carbohydrate - 45 to 65%; fat - 20 to 35%.94 The distribution of macro nutrients tested by some authors, that is (protein: 16%, fat: 35%, carbohydrates: 49%),33 (protein: 25,3%, fat: 28,7%, carbohydrate: 46%),84 and (protein:18%, fat: 27%, carbohydrate: 55%)83 differ from the current healthy diet recommendations and the ones recommended for weight loss (protein: 15%, fat: 30%, carbohydrate: 55%).5,95-97 Therefore, the effect of increased calcium ingestion associated with the consumption of a diet presenting the recommended macronutrient distribution is not known.
The results of these intervention studies suggest that a daily intake of about 1,200-1,300 mg/day can affect body weight and body composition.57 On the other hand, the results of the studies that assessed the association between increased fat excretion versus body composition and anthropometry it seems that the ingestion of large quantities of calcium has no effect, suggesting the existence of an upper threshold quantity capable of controlling obesity.
Effect of calcium intake on energy expenditure and substrate oxidation
The main characteristics of the studies that evaluated the effect of calcium on energy expenditure and substrate oxidation are presented in table III. Although the results of the studies indicate that the highest consumption of calcium or dairy products might increase lipid oxidation, this topic is still controversial.34
In the study conducted by Teegarden et al. (2008),34 there was an increase in fat oxidation only in the group treated with supplement. The authors report that other components of dairy products might prevent the increase in fat oxidation induced by calcium. In that study,34 the protein content was higher (16% SEV) than the recommendations.5,94-97 The results of that study34 contradicts the idea that protein could increase thermogenesis and lipid oxidation.85,86,88,98 In other studies, the consumption of diets containing 20%30 and 23%17 of total energy intake derived from proteins did not affect energy expenditure and fat oxidation. But this aspect should be further explored because in two other studies17,32 the consumption of a diet containing 15% of protein did not change such parameters. However, in that second study, the percentage of carbohydrate in the diet (60% of total energy intake) may have inhibited fat oxidation, since the carbohydrate is the preferred source of energy.99 This reinforces the importance to assess how the distribution of macronutrients affects the results of such studies.
In terms of the effects of calcium intake on body weight and body composition a minimum and maximum consumption seems to be necessary for the effects to be detected. It is not known whether these assumptions can be extrapolated in terms of the effects on energy expenditure and substrate oxidation. It has been observed that there is an increase in calcium urinary excretion in participants that are used to consuming that mineral above the RDA (1,000 mg),17,30 which start consuming a higher calcium dose.31,32 In a study conducted by Jacobsen et al. (2005),17 it was observed an increase in urinary excretion of calcium only when the diet was high in protein content (23%). However, Farnsworth et al. (2003)93 did not detect differences in excretion when comparing the effect of the consumption of a diet containing 30% of protein (1,600 mg calcium) versus a 15% of protein (600 mg calcium) diet. Data available in the literature are insufficient to define the minimum amount of dietary calcium required to induce a change in energy expenditure and substrate utilization.32
The number of human studies in which energy expenditure and substrate oxidation was assessed is small and the duration of these studies is short compared to the number of studies that anthropometry and body composition were evaluated. For example, Boon et al. (2005)30 tested the effect of the consumption of 1,200-1,300 mg of calcium /day for a period of seven days. On the other hand, it has been suggested that acute changes in calcium ingestion can modify fat oxidation rates. However, these modifications tend revert within a relatively short period of time.32
Thinking about the relationship between the effects of calcium intake and study duration, Melanson et al. (2003)9 and Gunther et al. (2005)11 obtained different results. In the first study,9 the authors observed that an acute increase in calcium intake leads to an increase in fat oxidation, whereas if the usual intake of calcium is already high that parameter is not affected. According to Gunther et al. (2005),11 fat oxidation is only affected when a higher calcium ingestion occurs for longer periods of time. The duration of these two studies and the usual ingestion of the participants were quite different. In addition, both involved normal weight participants. It is not known if the response would differ in overweight people. It has been argued that in normal weight people, the increase in calcium ingestion may cause alter substrate oxidation, without, however, affecting energy expenditure. That would happen as a mechanism to maintain body weight and prevent excessive weight loss due to the increase in fat oxidation.11
Final considerations
The results of the studies published so far suggest that the consumption of calcium derived from supplements and dairy products can reduce the anthropometric measurements and favor the achievement of an adequate body composition. However, there is no homogeneity in the results of the observational studies probably due to the differences in the methodologies used. It appears that the benefits of calcium ingestion are only detected in individuals with low habitual consumption of the mineral, and there may be an upper threshold amount of calcium from which this effect is no longer observed. Further studies are needed to confirm this fact and to determine what these values are. It should be emphasized that higher availability supplements should be tested and the administration form must be considered. In the case of dairy products, it is necessary to isolate the effect of other nutrients also present in these foods. It should also be taken into consideration the interference of the distribution of macronutrients in the possible effects of calcium. To better understand the consequences of calcium intake on energy expenditure and substrate oxidation in addition to these factors, longer duration studies should be conducted.
References
1. Schmidt MI, Duncan BB, Azevedo e Silva G, Menezes AM, Monteiro CA, Barreto SM, Chor D, Menezes PR. Doenças crônicas não transmissíveis no Brasil: carga e desafios atuais. The Lancet Saúde no Brasil 2011; Saúde no Brasil 4, Maio : 61-74. [ Links ]
2. World Health Organization. Preventing Chronic Diseases a vital investment. 2005. [ Links ]
3. World Health Organization. 2008-2013 Action Plan for the Global Strategy for the Prevention and Control of Noncommunicable Diseases. 2009. [ Links ]
4. Sociedad Española para el Estudio de la Obesidad (SEEDO). Consenso SEEDO 2007 para la evaluación del sobrepeso y la obesidad y el establecimiento de criterios de intervención terapéutica Revista Española de Obesidad. Marzo 2007. [ Links ]
5. Sociedade Brasileira de Cardiologia. I Diretriz Brasileira de Diagnóstico e Tratamento da Síndrome Metabólica. Arq Bras Cardiol 2005; 84, Suplemento I, Abril. [ Links ]
6. Sociedade Brasileira de Cardiologia. VI Diretrizes Brasileiras de Hipertensão. Arq Bras Cardiol 2010; 95 (1 Suppl. 1): 1-51. [ Links ]
7. Associação Brasileira para o Estudo da Obesidade e da Síndrome Metabólica (Abeso). Diretrizes Brasileiras de Obesidade. 3 ed; Itapevi, SP: AC Farmacêutica, 2009. [ Links ]
8. Brasil. Ministério da Saúde. Secretaria de Atenção à Saúde. Departamento de Atenção Básica. Obesidade. Brasília: Ministério da Saúde 2006; Cadernos de Atenção Básica, n. 12 Sèrie A. Normas e Manuais Técnicos: 108 p. [ Links ]
9. Melanson EL, Sharp TA, Schneider J, Donahoo WT, Grunwald GK, Hill JO. Relation between calcium intake and fat oxidation in adult humans. Int J Obes 2003; 27: 196-203. [ Links ]
10. Loos RJF, Rankinen T, Leon AS, Skinner JS, Wilmore JH, Rao DC, Bouchard C. Calcium Intake Is Associated with Adiposity in Black and White Men and White Women of the HERITAGE Family Study. J Nutr 2004; 134: 1772-8. [ Links ]
11. Gunther CW, Lyle RM, Legowski PA, James JM, McCabe LD, McCabe GP, Peacock M, Teegarden D. Fat oxidation and its relation to serum parathyroid hormone in young women enrolled in a 1-y dairy calcium intervention. Am J Clin Nutr 2005; 82: 1228-34. [ Links ]
12. Gunther CW, Legowski PA, Lyle RM, McCabe GP, Eagan MS, Peacock M, Teegarden D. Dairy products do not lead to alterations in body weight or fat mass in young women in a 1-y intervention. Am J Clin Nutr 2005; 81: 751-6. [ Links ]
13. Cominetti C, Marreiro DDN, Cozzolino SMF. Minerais e Obesidade In Cozzolino, SMF. Biodisponibilidade de nutrientes 3 ed. Barueri, SP: Manole; 2009, pp. 811-841. [ Links ]
14. World Health Organization and Food and Agriculture Organization of the United Nations Guidelines. Zinc, folate, vitamin B 12 and other B vitamins, vitamin C, vitamin D, calcium, selenium and fluoride. In: World Health Organization and Food and Agriculture Organization of the United Nations Guidelines on food fortification with micronutrients. 2006. [ Links ]
15. Pereira GAP, Genaro PS, Pinheiro MM, Szenjnfeld VL, Martini LA. Calcio dietético - estratégias para otimizar o consumo. Rev Bras Reumatol 2009; 49 (2): 164-80. [ Links ]
16. Shahkhalili Y, Murset C, Meirim I, Duruz E, Guinchard S, Cavadini C, Acheson K. Calcium supplementation of chocolate: effect on cocoa butter digestibility and blood lipids in humans. Am J Clin Nutr 2001; 73: 246-52. [ Links ]
17. Jacobsen R, Lorenzen J, Toubro S, Krog-Mikkelsen I, Astrup A. Effect of short- term high dietary calcium intake on 24-h energy expenditure, fat oxidation, and fecal fat excretion. Int J Obes 2005; 29: 292-301. [ Links ]
18. Zemel MB, Shi H, Greer B, Dirienzo D, Zemel PC. Regulation of adiposity by dietary calcium. FASEB J 2000; 14: 1132-8. [ Links ]
19. Jacqmain M, Doucet E, Després J, Bouchard C, Tremblay A. Calcium intake, body composition, and lipoprotein-lipid concentrations in adults. Am J Clin Nutr 2003; 77: 1448-52. [ Links ]
20. Reid IR, Horne A, Mason B, Ames R, Bava U, Gamble GD. Effects of Calcium Supplementation on Body Weight and Blood Pressure in Normal Older Women: A Randomized Controlled Trial. J Clin Endocrinol Metab 2005; 90: 3824-9. [ Links ]
21. Gonzalez AJ, White E, Kristal A, Littman AJ. Calcium Intake and 10-Year Weight Change in Middle-Aged Adults. J Am Diet Assoc 2006; 106: 1066-73. [ Links ]
22. Shapses SA, Heshka S, Heymsfield SB. Effect of Calcium Supplementation on Weight and Fat Loss in Women. J Clin Endocrinol Metab 2004; 89: 632-7. [ Links ]
23. Azadbakht L, Mirmiran P, Esmaillzadeh A, Azizi F. Dairy consumption is inversely associated with the prevalence of the metabolic syndrome in Tehranian adults. Am J Clin Nutr 2005; 82: 523-30. [ Links ]
24. Rajpathak SN, Rimm EB, Rosner B, Willett WC, Hu FB. Calcium and dairy intakes in relation to long-term weight gain in US men. Am J Clin Nutr 2006; 83: 559-66. [ Links ]
25. Eilat-Adar S, Xu J, Loria C, Mattil C, Goldbourt U, Howard BV, Resnick HE. Dietary Calcium Is Associated with Body Mass Index and Body Fat in American Indians. J Nutr 2007; 137: 1955-60. [ Links ]
26. Vergnaud A, Péneau S, Chat-Yung S, Kesse E, Czernichow S, Galan P, Hercberg S, Bertrais S. Dairy consumption and 6-y changes in body weight and waist circumference in middleaged French adults. Am J Clin Nutr 2008; 88: 1248-55. [ Links ]
27. Yanovski JA, Parikh SJ, Yanoff LB, Denkinger BI, Calis KA, Reynolds JC, Sebring NG, McHugh T. Effects of Calcium Supplementation on Body Weight and Adiposity in Overweight and Obese Adults. Ann Intern Med 2009; 150: 821-829. [ Links ]
28. Wennersberg MH, Smedman A, Turpeinen AM, Retterstol K, Tengblad S, Lipre E, Aro A, Mutanen P, Seljeflot I, Basu S, Perdersen JI, Mutanen M, Vessby B. Dairy products and metabolic effects in overweight men and women: results from a 6-mo intervention study. Am J Clin Nutr 2009; 90: 960-8. [ Links ]
29. Reid IR, Ames R, Mason B, Bolland, Mark J: Bacon, CJ, Reid HE, Campbell K, Gamble GD, Grey A, Horne A. Effects of calcium supplementation on lipids, blood pressure, and body composition in healthy older men: a randomized controlled trial. Am J Clin Nutr 2010; 91: 131-9. [ Links ]
30. Boon N, Hul GB, Viguerie N, Sicard A, Langin D, Saris WHM. Effects of 3 diets with various calcium contents on 24-h energy expenditure, fat oxidation, and adipose tissue message RNA expression of lipid metabolism-related proteins. Am J Clin Nutr 2005; 82: 1244-52. [ Links ]
31. Bortolotti M, Rudelle S, Schneiter P, Vidal H, Loizon E, Tappy L. Dairy calcium supplementation in overweight or obese persons: its effect on markers of fat metabolism. Am J Nutr 2008; 88: 877-85. [ Links ]
32. Sampath V, Havel PJ, King JC. Calcium Supplementation Does Not Alter Lipid Oxidation or Lipolysis in Overweight/ Obese Women. Obesity 2008; 16: 2400-4. [ Links ]
33. Zemel MB, Thompson W, Milstead A, Morris K, Campbell P. Calcium and Dairy Acceleration of Weight and Fat Loss during Energy Restriction in Obese Adults. Obes Res 2004; 12: 582-90. [ Links ]
34. Teegarden D, White KM, Lyle RM, Zemel MB, Van Loan MD, Matkovic V, Craig BA, Schoeller DA. Calcium and Dairy Product Modulation of Lipid Utilization and Energy Expenditure. Obesity 2008; 16 (7): 1566-72. [ Links ]
35. Shi H, DiRienzo D, Zemel MB. Effects of dietary calcium on adipocyte lipid metabolism and body weight regulation in energy -restricted aP2-agouti transgenic mice. FASEB J 2001; 15 (2): 291-3. [ Links ]
36. Parikh SJ, Edelman M, Uwaifo GI, Freedman RJ, Semega-Janneh M, Reynolds J, Yanovski JA. The Relationship between Obesity and Serum 1,25-Dihydroxy Vitamin D Concentrations in Healthy Adults. JCEM 2004; 89 (3): 1196-9. [ Links ]
37. Sun X, Zemel MB. Calcium and Dairy Products Inhibit Weight and Fat Regain during Ad Libitum Consumption Following Energy Restriction in Ap2- Agouti Transgenic Mice. J Nutr 2004; 134: 3054-60. [ Links ]
38. Food and Nutrition Board. Dietary Reference Intakes for Calcium and Vitamin D. 2011: Disponivel em: <http://www.nap.edu/openbook.php?record_id=13050&page=1>; Accessed on 20/01/2011. [ Links ]
39. Rodríguez-Rodríguez E, Navia Lombán B, López-Sobaler AM, Ortega Anta RM. Review and future perspectives on recommended calcium intake. Nutr Hosp 2010; 25 (3): 366-74. [ Links ]
40. McCarron DA. Dietary calcium as an antihypertensive agent. Nutr Rev 1984; 42: 223-5. [ Links ]
41. Bueno MB, Cesar CLG, Martini LA, Fisberg RM. Dietary calcium intake and overweight: An epidemiologic view. Nutrition 2008; 24: 1110-5. [ Links ]
42. Silva PMC, Cabral Junior CR, Vasconcelos SML. Ingestão do cálcio na obesidade de mulheres atendidas pelo Sistema Único de Saúde. Rev Nutr 2010; 23 (3): 357-67. [ Links ]
43. Denke MA, Fox MM, Schulte MC. Short-Term Dietary Calcium Fortification Increases Fecal Saturated Fat Content and Reduces Serum Lipids in Men. J Nutr 1993; 123: 1047-53. [ Links ]
44. Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa de Orçamentos Familiares 2008-2009. Análise do Consumo Alimentar Pessoal no Brasil. Rio de Janeiro, RJ- Brasil; 2011. [ Links ]
45. Batista MCR, Priore SE, Rosado LEFPL, Tinôco ALA, Franceschini SCC. Avaliação Dietética dos Pacientes Detectados Com Hiperglicemia na "Campanha de Detecção de Casos Suspeitos de Diabetes" no Município de Viçosa, MG. Arq Bras Endocrinol Metab 2006; 50 (6): 1041-9. [ Links ]
46. Castro TG, Bertolino CN, Gimeno SGA, Cardoso MA. Mudanças no consumo alimentar de nipo-brasileiros residentes em Bauru, São Paulo, Brasil, 1993-2000. Cad Saúde Pública, Rio de Janeiro 2006; 22 (11): 2433-40. [ Links ]
47. Crispim SP, Ribeiro RCL, Panato E, Silva MMS, Rosado LEFP, Rosado GP. Validade relativa de um questionário de freqüência alimentar para utilização em adultos. Rev Nutr 2009; 22 (1): 81-95. [ Links ]
48. Esteves EA, Rodrigues CAA, Paulino ÉJ. Ingestão dietética de cálcio e adiposidade em mulheres adultas. Rev Nutr 2010; 23(4): 543-52. [ Links ]
49. Silva AGH, Cozzolino Silva M Franciscato. Cálcio In Cozzolino, SMF. Biodisponibilidade de nutrientes 3 ed. Barueri, SP: Manole; 2009, pp. 513-541. [ Links ]
50. Parikh SJ, Yanovski JA. Calcium intake and adiposity. Am J Clin Nutr 2003; 77: 281-7. [ Links ]
51. Shi H, Norman AW, Okamura WH, Sen A, Zemel MB. 1 alpha, 25-Dihydroxyvitamin D 3 modulates human adipocyte metabolism via nongenomic action. FASEB J 2001; express article 10.1096/fj.01-0584fje. Published online October 15. [ Links ]
52. Shi H, Norman AW, Okamura WH, Sen A, Zemel MB. 1 alpha, 25-dihydroxyvitamin D 3 inhibits uncoupling protein 2 expression in human adipocytes. FASEB J 2002; express article 10.1096/fj.02-0255fje. Published online September 5. [ Links ]
53. Siddiqui SMK, Chang E, Li J, Burlage C, Zou M, Buhman KK, Koser S, Donkin SS, Teegarden D. Dietary intervention with vitamin D, calcium, and whey protein reduced fat mass and increased lean mass in rats. Nutr Res 2008; 28: 783-90. [ Links ]
54. Parra P, Bruni G, Palou A, Serra F. Dietary calcium attenuation of body fat gain during high fat feeding in mice. J Nutr Biochem 2008; 19: 108-17. [ Links ]
55. Paradis s, Cabanac M. Calcium deficiency cannot induce obesity in rats. Physiol Behav 2005; 85: 259-64. [ Links ]
56. Wortsman J, Matsuoka LY, Chen TC, Lu Z, Holick MF. Decreased bioavailability of vitamin D in obesity. Am J Clin Nutr 2000; 72: 690-3. [ Links ]
57. Eagan MS, Lyle RM, Gunther CW, Peacock M, Teegarden D. Effect of 1- Year dairy Product Intervention on Fat Mass in Young Women: 6- Month Follow-up. Obesity 2006; 14 (12):2242-8. [ Links ]
58. Botella-Carretero JI, Alvarez-Blasco F, Villafruela JJ, Balsa JA, Vázquez C, Escobar-Morreale HF. Vitamin D deficiency is associated with the metabolic syndrome in morbid obesity. Clin Nutr 2007; 26: 573-80. [ Links ]
59. Snijder MB, Van Dam RM, Visser M, Deeg DJH, Dekker JM, Bouter LM, Seidell JC, Lips P. Adiposity in Relation to Vitamin D Status and Parathyroid Hormone Levels: A Population-Based Study in Older Men and Women. JCEM 2005; 90 (7): 4119-23. [ Links ]
60. Sneve M, Figenschau Y, Jorde R. Supplementation with cholecalciferol does not result in weight reduction in overweight and obese subjects. Eur J Endocrinol 2008; 159: 675-84. [ Links ]
61. Kamycheva E, Joakimsen RM, Jorde R. Intakes of Calcium and Vitamin D Predict Body Mass Index in the Population of Northern Norway. J Nutr 2002; 132: 102-6. [ Links ]
62. Liu S, Song Y, Ford ES, Manson JE, Buring JE, Ridker PM. Dietary Calcium, Vitamin D, and the Prevalence of Metabolic Syndrome in Middle-Aged and Older U.S. Women. Diabetes Care 2005; 28: 2926-32. [ Links ]
63. Major GC, Alarie F, Doré J, Phouttama S, Tremblay A. Supplementation with calcium + vitamin D enhances the beneficial effect of weight loss on plasma lipid and lipoprotein concentrations. Am J Clin Nutr 2007; 85: 54-9. [ Links ]
64. Major GC, Alarie FP, Doré J, Tremblay A. Calcium plus vitamin D supplementation and fat mass loss in female very low-calcium consumers: potential link with a calcium -specific appetite control. Brit J Nutr 2009; 101: 659-63. [ Links ]
65. Caan B, Neuhouser M, Aragaki A, Lewis CB, Jackson R, LeBoof MS, Margolis KL, Powell L, Uwaifo G, Whitlock E, Wylie- Rosett J, LaCroix A. Calcium Plus Vitamin D Supplementation and the Risk of Postmenopausal Weight Gain. Arch Intern Med 2007; 167: 893-902. [ Links ]
66. Boon N, Hul GBJ, Sicard A, Kole E, Van Den Berg ER, Viguerie N, Langin D, Saris WHM. The Effects of Increasing Serum Calcitriol on Energy and Fat Metabolism and Gene Expression. Obesity 2006; 14 (10): 1739-46. [ Links ]
67. Zittermann A, Frisch S, Berthold HK, Gotting C, Kuhn J, Kleesiek K, Stehle P, Koertke H, Koefer R. Vitamin D supplementation enhances the beneficial effects of weight loss on cardiovascular disease risk markers. Am J Clin Nutr 2009; 89:1321-7. [ Links ]
68. Schuch NJ, Garcia VC, Martini LA. Vitamina D e doenças endocrinometabólicas. Arq Bras Endocrinol Metab 2009; 53(5): 625-33. [ Links ]
69. Kamycheva E, Sundsfjord J, Jorde R. Serum parathyroid hormone level is associated with body mass index. The 5th Tromsø study. Eur J Endocrinol 2004; 151: 167-72. [ Links ]
70. McCarty MF, Thomas CA. PTH excess may promote weight gain by impeding catecholamine- induced lipolysis -implications for the impact of calcium, vitamin D, and alcohol on body weight. Med Hypotheses 2003; 61 (5-6): 535-42. [ Links ]
71. Saraiva GL, Cendoroglo MS, Ramos LR, Araújo LMQ, Vieira JGH, Maeda SS, Borba VZC, Kunii I, Hayashi LF, Lazaretti-Castro M. Prevalência da Deficiência, Insuficiência de Vitamina D e Hiperparatiroidismo Secundário em Idosos Institucionalizados e Moradores na Comunidade da Cidade de São Paulo, Brasil. Arq Bras Endocrinol Metab 2007; 51 (3): 437-42. [ Links ]
72. Maeda SS, Kunni IS, Hayashi L, Lazaretti-Castro M. The effect of sun exposure on 25- hydroxyvitamin D concentrations in young healthy subjects living in the city of São Paulo, Brazil. Bras J Med Biol Res 2007; 40 (12): 1653-9. [ Links ]
73. Davies KM, Heaney RP, Recker RR, Lappe JM, Barger-Lux MJ, Rafferty K, Hinders S. Calcium Intake and Body Weight. J Clin Endocrinol Metab 2000; 85: 4635-8. [ Links ]
74. Heaney RP. Normalizing Calcium Intake: Projected Population Effects for Body Weight. J Nutr 2003; 133: 268S-270S. [ Links ]
75. Danubio ME, Miranda G, Vinciguerra MG, Vecchi E, Rufo F. Comparison of self-reported and measured height and weight: Implications for obesity research among young adults. Econ Hum Biol 2008; 6: 181-90. [ Links ]
76. Pérez-Cueto FJA, Verbeke W. Reliability and validity of selfreported weight and height in Belgium. Nutr Hosp 2009; 24 (3): 366-7. [ Links ]
77. Sun G, French CR, Martin GR, Younghusband B, Green RC, Xie Y, Mathews M, Barron JR, Fitzpatrick DG, Gulliver W, Zhang H. Comparison of multifrequency bioelectrical impedance analysis with dual-energy X-ray absorptiometry for assessment of percentage body fat in a large, healthy population. Am J Clin Nutr 2005; 81: 74-8. [ Links ]
78. Völgyi E, Tylavsky FA, Lyytikäinen A, Suominen H, Alén M, Cheng S Assessing Body Composition With DXA and Bioimpedance: Effects of Obesity, Physical Activity, and Age. Obesity 2008; 16: 700-705. [ Links ]
79. Snijder MB, Van Dam RM, Visser M, Seidell JC. What aspects of body fat are particularly hazardous and how do we measure them? Int J Epidemiol 2006; 35: 83-92. [ Links ]
80. Willett W. 24-Hour Dietary Recall and Food Record Methods. In Willett W. Nutritional Epidemiology Oxford University Press: New York Oxford; 1998, pp. 50-73. [ Links ]
81. Fisberg RM, Martini LA, Slater B. Métodos de Inquéritos Alimentares. In Inquéritos Alimentares Métodos e bases científicos. Manole (Ed.); 2005; 1-29. [ Links ]
82. Sun X, Zemel MB. Leucine and Calcium Regulate Fat Metabolism and Energy Partitioning in Murine Adipocytes and Muscle Cells. Lipidis 2007; 42: 297-305. [ Links ]
83. Faghih S, Abadi AR, Hedayati M, Kimiagar S. Comparison of the effects of cows' milk, fortified soy milk, and calcium supplement on weight and fat loss in premenopausal over-weight and obese women. Nutr Metab Cardiovasc Dis 2011; 21: 499-503. [ Links ]
84. Kabrnová-Hlavatá K, Hainer V, Gojová M, Hlavaty P, Kopsky V, Nedvídková J, Kunesová M, Parizková J, Wagenknecht M, Hill M, Drbohlav J. Calcium Intake and the Outcome of Short-Term Weight Management. Physiol Res 2008; 57: 237-45. [ Links ]
85. Layman DK. The Role of Leucine in Weight Loss Diets and Glucose Homeostasis. J Nutr 2003; 133: 261S-267S. [ Links ]
86. Layman DK, Baum JI. Dietary Protein Impact on Glycemic Control during Weight Loss. J Nutr 2004; 134: 968S-973S. [ Links ]
87. Oliveira FCE, Abranches MV, Bressan J. Incretinas e proteínas: nova opção no manejo do diabetes mellitus e obesidade. Rev Bras Nutr Clin 2010; 25 (1): 66-72. [ Links ]
88. Acheson KJ, Blondel-Lubrano A, Oguey-Araymon S, Beaumont M, Emady-Azar S, Ammon-Zufferey C, Monnard I, Pinaud S, Nielsen-Moennoz C, Bovetto L. Protein choices targeting thermogenesis and metabolism. Am J Clin Nutr 2011; 93: 525-34. [ Links ]
89. Harvey JA, Zobitz MM, Pak CYC. Dose Dependency of Calcium Absorption: A Comparison of Calcium Carbonate and Calcium Citrate. J Bone Miner Res 1988; 3 (3): 253-8. [ Links ]
90. Hanzlik RP, Fowler SC, Fisher DH. Relative Bioavailability of Calcium from Calcium Formate, Calcium Citrate, and Calcium Carbonate. Journal Pharmacol Exp Ther 2005; 313 (3): 1217-22. [ Links ]
91. Verhoeven S, Vanschoonbeek K, Verdijk LB, Koopman R, Wodzig WK, Dendale P, Van Loon LJ. Long-term leucine supplementation does not increase muscle mass or strength in healthy elderly men. Am J Clin Nutr 2009; 89: 1468-75. [ Links ]
92. Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, Purnell JQ. A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr 2005; 82: 41-8. [ Links ]
93. Farnsworth E, Luscombe ND, Noakes M, Wittert G, Argyiou E, Clifton PM. Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women. Am J Clin Nutr 2003; 78: 31-9. [ Links ]
94. Institute of Medicine/Food and Nutrition Board. Dietary Reference Intakes for energy, carbohydrate, fiber, fatty acids, cholesterol, protein, and amino acids. Disponível em <http://www.nap.edu>. 2002; Washington, D.C.: The National Academy Press: pp. 697-736. [ Links ]
95. National Institutes of Health, National Heart, Lung, and Blood Institute, NHLBI Obesity Education Initiative & North American Association for the Study of Obesity. The Practical Guide Identification, Evaluation, and Treatment of Overweight and Obesity in Adults. 2000. [ Links ]
96. Sociedad Española para el Estudio de la Obesidad (SEEDO). Consenso SEEDO'2000 para la evaluación del sobrepeso y la obesidad y el establecimiento de criterios de intervención terapéutica. Med Clin (Barc) 2000; 115: 587-97. [ Links ]
97. World Health organization, International Association for the Study of Obesity (IASO) & International Obesity Taskforce. The Asia-Pacific perspective: Redefining obesity and its treatment, February 2000. [ Links ]
98. Frestedt JL, Zenk JL, Kuskowski MA, Ward LS & Bastian ED. A whey protein-supplement increase fat loss and spares lean muscle in obese subjects: a randomized human clinical study. Nutr Metab 2008; 5: 8. [ Links ]
99. Guyton AC, Hall JE. Metabolismo de las proteínas In Guyton, Arthur C; Hall, John E. Tratado de Fisiología Medica Décima Edición. México: Mc Graw-Hill Interamericana; 2004, pp. 953-959. [ Links ]
Correspondence:
Rita de Cássia Gonçalves Alfenas.
Departamento de Nutrição e Saúde.
Universidade Federal de Viçosa.
Avenida PH Rolfs, s/n.
36570-000 Viçosa, MG, Brazil.
E-mail: ralfenas@ufv.br
Recibido: 1-VI-2012.
Aceptado: 3-VII-2012.