REVISIÓN

Dairy products consumption versus type 2 diabetes prevention and treatment; a review of recent findings from human studies

Consumo de los productos lácteos versus prevención y tratamiento de la diabetes tipo 2; una revisión de los resultados recientes de estudios en humanos

Tadeu Silva Ton and Rita de Cássia Gonçalves Alfenas

Nutrition and Health Department. Federal University of Viçosa. Brazil

To CAPES for the master's scholarship grant and to FAPEMIG for the support (CDS-APQ-01677-10).

ABSTRACT

Introduction: It has been claimed that the appropriate consumption of dairy products can be beneficial for the prevention and treatment of type 2 diabetes mellitus (T2DM).
Objective: The objective of this review is to critically analyze the main scientific evidence about this topic.
Methods: MEDLINE, PubMEd, Science Direct, SCIELO and LILACS were searched for studies published over the past 12 years exploring the effects of the consumption of dairy products or its components (calcium, vitamin D and magnesium) on T2DM.
Results and discussion: Epidemiological studies indicate that consumption of at least three servings of low-fat dairy products per day as a part of a healthy diet is crucial to reduce the risk of developing T2DM. The majority of the analyzed intervention studies reported beneficial effects of increased calcium and vitamin D ingestion on insulin sensitivity improvement and T2DM prevention.
Conclusions: Although the impact of dairy consumption to treat T2DM needs further investigation, the consumption of low-fat dairy products may be an important strategy to prevent and control T2DM.

Key words: Dairy products. Milk. Calcium. Vitamin D. Diabetes. Insulin resistance.

RESUMEN

Palabras clave: Productos lácteos. Leche. Calcio. Vitamina D. Diabetes. Resistencia a la insulina.

Introduction

Type 2 diabetes mellitus (T2DM), which is partially characterized by insulin resistance (IR), is one of the most common chronic diseases in the world. IR is a pathological condition in which insulin becomes less effective at lowering blood glucose levels. T2DM occurs when the functional expansion of islet Β-cells fails to compensate for the degree of IR.¹ The worldwide prevalence of this disease among adults is estimated to increase from 285 million cases (6.4% of the population) in 2010 to 439 million (7.7%) in 2030. It is believed that this increase will be especially prominent in developing countries (69% increase compared to an increase of 20% in developed countries).²

The rapid increase in the incidence of T2DM indicates a low correlation with genetic causes and a strong correlation with lifestyle and/or environmental factors.^3,4Accordingly, body weight reduction, increased physical activity, and good dietary habits are effective strategies for reducing the incidence of IR and T2DM^5-7as well as for treating these disorders.^8,9 With regard to dietary habits, the influence of dairy intake on the prevention and treatment of T2DM deserves special attention.¹⁰

The objective of this study was to critically analyze the major scientific evidence regarding the role of dairy products and their components in the prevention and management of T2DM. We believe this is an important step to stimulate the conductance of scientific studies on this topic, favoring the establishment of public policies that can lead to health benefits to the world's populations.

Methods

We searched the MEDLINE, PubMEd, Science Direct, Scientific Electronic Library Online (SCIELO), and Latin American and Caribbean Health Sciences Literature-LILACS electronic databases to identify studies published within the last 12 years regarding the effects of consuming dairy products or their components (calcium, vitamin D and magnesium) on T2DM. For epidemiological studies, the prevalence and risks of T2DM and/or insulin resistance syndrome (IRS) were considered regarding dairy products, calcium and vitamin D consumption. For intervention studies, a minimum of 4 weeks intervention was considered regarding dairy products consumption, supplementation level (minimum) of vitamin D (400 IU) and calcium (500 mg), in which fasting glycemia and insulinemia, glycated hemoglobin, Homeostasis Model Assessment (HOMA) index, HOMA of insulin resistance (HOMA-IR), HOMA of insulin sensitivity (HOMA-%S); HOMA of β-cell function (HOMA-%B), quantitative insulin sensitivity check index (QUICKI) and intraplatelet calcium were assessed.

The studies were searched using the following main terms: dairy product, milk, diabetes, IR, glucose intolerance, impaired glucose, calcium, vitamin D, dairy products consumption, and serum vitamin D.

The effects of dairy intake on T2DM prevention and treatment

Evidence from epidemiological studies

The results of several epidemiological studies substantiate the existence of an inverse correlation between the consumption of dairy products, calcium, and/or vitamin D and T2DM^{11-15,17-22,24} or irs.^{12,17,18,20,23-26}

It is noteworthy that the best effects were associated with the consumption of low-fat dairy products.^11,13,21,22 No beneficial effects were verified for subjects who consumed the high-fat ones.^21,22 It was observed that while the consumption of one dairy portion daily resulted in an average reduction of 5% in the risk of T2DM in both males and females, the consumption of one portion of low-fat dairy products was associated with a 10% reduction.²² In postmenopausal women, an average daily intake of at least 1.5 low-fat dairy portions reduced the risk of T2DM compared to those with a daily intake of < 0.5 portions, especially among women with a higher BMI.²¹

In contrast, the authors of a recent study did not observe any beneficial effect of dairy consumption on T2DM prevention, regardless of its fat content. A total of 4,526 men and women were involved in that 10-year prospective study.³³ However, the data obtained in that study was analyzed after being divided into tertiles instead of quintiles as it has been done in other studies. Due to that the small variation in the dairy intake among groups (difference of 329 g/day between the medians of the first and third tertiles) may have impaired the detection of significant correlations. In addition, the average values of dairy (246 g/day) and calcium (935 ± 321 mg/day) intake in the group with the lowest intake level were still relatively high. It seems that the increased risk of T2DM occurs mainly when dairy consumption is lower than those reported in the aforementioned study.²⁴

The beneficial effects of calcium and vitamin D intakes on the risk of developing T2DM were assessed in three prospective studies.^14,15,19 The authors of two of these studies did not identify significant effects of calcium¹⁹ or vitamin D¹⁴ consumption, although Pittas et al.¹⁴ and Van Dan et al.¹⁵reported that calcium alone did have an effect. In the latter study, this effect was observed before adjusting for magnesium intake. Magnesium acts as a cofactor of enzymes involved in glucose metabolism. Low magnesium intake has been associated with an increased risk of T2DM.³⁴ Since dairy products are good sources of magnesium, this element may be implicated in the benefits associated with dairy consumption. Vitamin D was shown to play an important role in reducing the T2DM risk only among the participants who used supplements of this vitamin.¹⁴ However, a high calcium intake significantly reduced the risk of developing T2DM in participants who consumed the greatest levels of dietary vitamin D.¹⁹ The intake of doses greater than 1,200 mg/day of calcium and 800 IU/day of vitamin D correlated with a 33% reduction (RR 0.67, CI, 0.49-0.90) in the risk of T2DM compared to doses of less than 600 mg/day and 400 IU/day, respectively.²⁴ Such results are surprising from a clinical perspective due to the magnitude of the reduction of the risks.

The effects of the consumption of dairy products or their components on T2DM and IRS was investigated in two meta-analyses.^18,24 The results of these studies confirmed the protective effect of dairy product, calcium, and vitamin D intake. The authors of the first study¹⁸ reported 10% (RR 0.92; CI, 0.86-0.97) and 25% (RR 0.74; CI, 0.64-0.84) reductions in the probability of developing T2DM and IRS, respectively, with highest intake of milk or dairy products. In the second study,²⁴ the consumption of 3 to 5 portions of dairy products per day reduced the probability of developing T2DM (OR 0.86; CI, 0.79-0.93) and IRS (OR 0.71; CI 0.57-0.89) compared to the intake of less than 1.5 portions per day.

Among the studies that assessed the effect of dairy products on T2DM and IRS,^{12,20,23,25,35} two reported protective effects against T2DM and IRS,^12,20 two observed this effect only for IRS,^23,25 and one reported that dairy consumption did not affect the risk of either T2DM or IRS.³⁵ Among the studies that investigated only the effect of dairy products on IRS,^17,26,36,37 the authors of three of these studies found a protective effect^17,26,36 and one did not.³⁷ However, the study conducted by Snijder et al.³⁷ only assessed dairy intake at baseline. Therefore, one cannot guarantee that the dietary patterns of the participants remained the same during the 6.4 years of follow-up. It should be noted also that the study population was relatively healthy, which might have contributed to the lack of correlations.

The conflicting results of an additional study also deserve discussion. Lawlor et al.³⁵ reported lower HOMA scores, triglyceride concentrations, BMI values, and high-density lipoprotein (HDL) levels among women who reported that they never drank milk compared to those that did. This study included 4,024 British postmenopausal women aged 60 to 79 years old. The probability of developing IRS was 45% lower among women who never drank milk compared to those who did (OR 0.55; CI, 0.33-0.94), even after adjusting for interfering variables. The authors of that study emphasize the need to establish whether there is causal relationship between the investigated variables and discuss the possibility that a biological variable, such as lactose intolerance, may have interfered with the results. Non-diabetic individuals are more prone to lactose intolerance and thus exclude dairy products from their diet. Therefore, the protective effect associated with the non-consumption of dairy products verified in their study may have been related with a lower genetic susceptibility to T2DM. In that case, the results obtained in that study would not indicate the lack of a protective effect of dairy intake.

Although the results of most studies indicate the existence of an inverse correlation between T2DM and dairy consumption, the results of some studies are conflicting.^23,25,35,37 Factors that may have interfered with the magnitude of the obtained correlations include gender, age range, ethnicity, BMI, and the amount and type of dairy products consumed. In some prospective studies,^{13,15,19,25,33,37} dietary intake was not monitored throughout the study. In other studies,^18,21,26 the exact amounts of dairy products and/or calcium and vitamin D consumed were not described or adjustments were not consistently performed among the assessed groups to account for confounding variables. The main characteristics and results from epidemiological studies in which the effect of the consumption of dairy products, calcium, and/or vitamin D on the development of T2DM and IRS are described in table I and table II, respectively.

Evidence from intervention studies

The causal relationship between the consumption of dairy products or their components and the development and treatment of T2DM can only be evaluated by intervention studies. There is only one clinical trial where dairy foods have been used as the experimental variable with respect to the treatment of T2DM in humans.³⁸ The remaining eight studies used supplements (pills or powders) containing nutrients like calcium and/or vitamin D found in dairy products (table III).

The combined effects of calcium and vitamin D supplements were studied in four intervention studies.^16,38,42,43 In a factorial clinical trial,³⁸ individuals with T2DM consumed yogurt-based beverages with different levels of calcium and vitamin D over 12 weeks. The participants were randomly allocated to 3 groups that drank one of the following beverages: plain yogurt without vitamin D₃ and with 150 mg Ca/250 mL (PY), yogurt fortified with 500 IU vitamin D₃ and 150 mg Ca/250 mL (DY), and yogurt fortified with 500 IU vitamin D₃ and 250 mg Ca/250 mL (DCY). Vitamin D₃ serum levels were significantly increased in the DY and DCY groups. HOMA-IR scores and fasting glycemia were significantly decreased in both groups compared with PY, but were lower in the DY group. However, the insulinemia and HbA1c levels did not differ between the groups.

The results of the previously mentioned study³⁸suggest that the daily intake of vitamin D₃-fortified yogurt with or without the addition of calcium may improve insulin sensitivity (HOMA-IR) and reduce fasting glycemia in diabetic individuals. However, it is not known whether the changes observed during the 12 week-study would persist if the beverages were consumed for a longer period of time. It should be noted that since the yogurt was not consumed in the laboratory, it is impossible to confirm whether the study treatments were actually consumed by subjects. Regardless, the results suggest that increased vitamin D intake may be beneficial in preventing and controlling T2DM.

Elderly volunteers with normal fasting glucose or impaired fasting glucose (IFG) were given calcium pills (500 mg calcium citrate) and vitamin D (700 IU vitamin D₃) or placebo for 3 years. The IFG group exhibited smaller increases in fasting glycemia (+0.02 ± 0.4 vs. + 0.34 ± 6.1 mmol/L, P = 0.042) and HOMA-IR scores (+0.05 vs. +0.91, P = 0.031) compared to the placebo group.¹⁶

De Boer et al.⁴² conducted a randomized doubleblind clinical trial involving the participation of 33,951 healthy women who were given daily supplements of calcium (1,000 mg calcium carbonate) and vitamin D₃ (400 IU) or placebo for seven years. The incidence of diabetes in the study population was 6.5%. Supplementation did not alter the fasting glycemia, insulinemia, or HOMA-IR scores. One caveat of this study is that the participants reported if they were diabetics or not. No test was done to confirm the occurrence of diabetes among the participants. T2DM can manifest many years prior to a formal diagnosis.⁴⁴ The lack of homogeneity in the health status of those participants at the beginning of the study may have impaired the results.

The effects of vitamin D supplementation with or without calcium over 16 weeks were assessed in a study involving 92 adults.⁴³ The participants were divided into two groups: one group was supplemented daily with vitamin D₃ (2,000 IU or 50 mcg), and the other group received a placebo. Half of each group also received calcium supplements (800 mg calcium carbonate). Insulin secretion and sensitivity increased in the group exclusively supplemented with vitamin D compared to the placebo. Calcium supplementation did not affect any of the measured parameters.

Two other double-blind studies tested the effect of vitamin D supplements were tested in non-diabetic, overweight subjects.^45,46 Postprandial insulin sensitivity significantly improved following the administration of 120,000 IU of vitamin D₃ every two weeks over a six-week period.⁴⁵ The authors of another study reported that improved insulin sensitivity and reduced fasting glycemia were observed in subjects who took daily supplements of 100 mcg (4,000 IU) of vitamin D₃ for six months.⁴⁶ These findings further confirm that vitamin D might be important in the prevention and control of T2DM.

Conversely, daily vitamin D₃ supplements (83.3 mcg/ 3,332 IU) for 12 months did not have any beneficial effect in overweight or obese subjects⁽⁴⁷⁾. A 6-month regimen of weekly vitamin D₃ supplementation of 40,000 IU (5,700 IU per day in capsule form) did not affect the fasting glycemia, insulin, HOMA-IR scores, or HbA1c levels in diabetic subjects.⁴⁸

All of the studies that assessed the effects of vitamin D^{16,38,42,43, 45-49} reported significant increases in 25(OH)D₃ serum levels, which may subsequently improve insulin sensitivity.^50-52 Nevertheless, the variation among the supplement doses (ranging from 400 to 8,000 IU/daily) and the amounts of vitamin D typically found in dairy products (40 to 100 IU/milk or yougurt serving, best described later) must be taken into account. Moreover, the previously mentioned studies focused on the effect of vitamin D supplements in Caucasians, and even after adjusting for ethnicity, the results cannot be extrapolated to darker skin people, in whom vitamin D synthesis is impaired by greater skin pigmentation.⁵³ In addition, the geographical locations where the studies were conducted play a role in the extent of solar exposure and skin synthesis of vitamin D. These variables make it difficult to apply the findings of this study to populations that live at different latitudes.

Although several authors have reported that calcium improves insulin sensitivity and glycemia,^16,39,42 others have reported the lack of such effect.^42,43 Therefore, additional intervention studies are needed to elucidate the effects of calcium on glycemic status and insulin sensitivity in both normoglycemic and diabetic individuals.

Actual nutritional recommendations vs. scientific evidences regarding dairy consumption and T2DM

The new DRIs for calcium and vitamin D were published in 2011.²⁷ The greatest difference from the previous DRIs was a change from Adequate Intakes (AI) to Estimated Average Requirements (EAR), Recommended Dietary Allowance (RDA), and Tolerable Upper Intake Level (UL).⁵⁴ Based on recent scientific studies about effects of calcium and vitamin D on bone health, an expert panel established by the Institute of Medicine (IOM) defined the reference values for several age ranges. The EAR and RDA of calcium for individuals > 1 year old ranges from 500-1,100 mg/day and 700-1,300 mg/day, respectively. Vitamin D levels were determined assuming low solar exposure levels. The EAR for individuals > 1 year old corresponds to 400 IU/day. The vitamin D RDA values differ by age group, and are listed as 600 IU/day for people between 1 and 70 years old and 800 IU/day for those > 71 years old and older.²⁷

Dietary guidelines (DGs) are a primary nutritional educational tool with a pivotal role in translating nutrient recommendations into food intake recommendations for the general population.⁵⁵ DGs must comply with the RDA,⁵⁵ which meets the needs of 97.5% of the healthy population.²⁷ One dairy portion supplies an average of 300 mg of calcium. Therefore, the calcium recommendations for adults (1,000-1,300 mg/d) are not met when < 3 dairy portions per day are consumed per day, even when other dietary calcium sources are consumed. For this reason, the daily dairy intake recommendations were increased from 2-3 portions to at least 3.^55,56

The vitamin D content of dairy products depends on whether the products are fortified. Vitamin D is heat stable, and thus, its concentrations are usually not altered during dairy product processing.⁵⁷ However, the vitamin D contents of dairy product are considered low relative to other dietary sources, such as high-fat fish and bovine liver. Nevertheless, dairy-derived vitamin D is important because other sources are not regularly consumed by the populations of many countries, and other vitamin D sources may contain high levels of cholesterol.⁵⁸ Therefore, dairy products are the main dietary source of vitamin D in several countries and are commonly fortified with additional vitamin D.^58,59 In the United States, the maximum limits of vitamin D supplementation are approximately 100 IU/milk serving or 40-80 IU/yogurt serving.⁵⁸ Therefore, the consumption of the three recommended servings of dairy every day provides at most 300 IU of vitamin D, which is less than the current recommendation of 600 to 800 IU/day. This deficit should be satisfied by other dietary sources.

Although the DRI recommendations for calcium and vitamin D intake only considered the benefits for bone health, consuming ≥ 3 dairy portions every day, as recommended by the DG, also protects against T2DM and IRS.^{11-14,18-21,23,24,26,36} Thus, a dairy intake that meets the DG might provide benefits with respect to T2DM, provided that appropriate vitamin D levels are maintained by means of other dietary sources or adequate solar exposure.⁵⁸

According to the International Dairy Federation, the worldwide current estimated average consumption of dairy seems to be far from the recommendations.⁶⁰ This estimate is based on total milk production and not in its actual intake, which can lead to small variations in the values. The average per capita consumption of milk in 2009 was 103 L, corresponding to approximately 280 mL per day. Although in 2009 there was an increase of 8% in the estimated consumption compared to consumption in 2000, this amount is far below the recommended dietary allowances of at least three servings a day. It should also be considered that this consumption is not equally distributed among the different territories around the world.^56,61

Conclusions

The results of the epidemiological studies indicate that the consumption of at least 3 servings of low-fat dairy products as part of a healthy diet is crucial to reduce the risk of developing T2DM. There are few intervention studies that explored the effects of dairy or its components (calcium or vitamin D) on T2DM development and treatment. In some of them high doses of calcium and/or vitamin D were tested. Nevertheless, the majority of the analyzed intervention studies reported that the consumption of calcium and vitamin D may be beneficial in preventing and treating T2DM. Although this topic needs further investigation, the consumption of low-fat dairy consumption may be an important strategy to prevent and control T2DM, especially because of the low estimate values of dairy consumption by people from different parts of the world.

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Correspondence:
Flávia Galvão Cândido
Departamento de Nutrição e Saúde - CCB II
Avenida PH Rolfs, s/n ]]> 36570-000 Vicosa, MG. Brasil
E-mail: flaviagcandido@hotmail.com  /flavia.candido@ufv.br

Recibido: 4-X-2012
1.^a Revisión: 18-V-2013
Aceptado: 17-VI-2013