Buscar en
Atención Primaria
Toda la web
Inicio Atención Primaria Dietary program and physical activity impact on biochemical markers in patients ...
Información de la revista
Compartir
Compartir
Descargar PDF
Más opciones de artículo
Visitas
5793
Original article
Open Access
Dietary program and physical activity impact on biochemical markers in patients with type 2 diabetes: A systematic review
Programa de dietas e impacto de la actividad física sobre marcadores bioquímicos en pacientes con diabetes tipo 2: una revisión sistemática
Visitas
5793
Eduarda Barreiraa,
Autor para correspondencia
edubarreira4@hotmail.com

Corresponding author.
, André Novoa,b, Josiana A. Vaza,c, Ana M.G. Pereiraa
a Health School, Polytechnic Institute of Bragança, Bragança, Portugal
b CINTESIS-Research Center on Health Technologies and Services, Porto, Portugal
c CIMO-Mountain Research Centre, Polytechnic Institute of Bragança, Campus de Santa Apolónia, Bragança, Portugal
Este artículo ha recibido

Under a Creative Commons license
Recibido 16 febrero 2017. Aceptado 13 junio 2017
Información del artículo
Resumen
Texto completo
Bibliografía
Descargar PDF
Estadísticas
Figuras (215)
Mostrar másMostrar menos
Tablas (2)
Table 1. Risk of bias for each study included in the analysis.
Table 2. General description of the included trials in this review per intervention and continent.
Mostrar másMostrar menos
Abstract
Objectives

Evaluate the effectiveness of the implementation of independently or combined dietary and physical activity programs on the blood glucose values and lipid profile in patients with type 2 diabetes, including participants aged 60 years and over.

Design

Systematic review.

Data source

PubMed/Medline database, with language restrictions. Papers published between 2010 and 2016 were included.

Study selection

A total of 30 randomised controlled trials were included that focused on physical activity and dietary interventions in patients with type 2 diabetes mellitus and include participants aged 60 years and over.

Results

The selected articles have shown that the implementation of physical activity programs (aerobic, resistance, flexibility and combined exercises), and programs based on a higher intake of vegetables, grains, legumes, fruits, unsaturated fatty acids, as well as consumption of foods with low glycaemic index, calorie restriction, intake of probiotics, vitamin D supplementation and educational sessions about diabetes improves blood glucose levels, as well as the lipid profile, in patients with type 2 diabetes.

Conclusions

Physical activity and dietary programs are fundamental in the treatment and metabolic control of type 2 diabetes mellitus.

Keywords:
Nutrition
Physical exercise
Glycemic control
Dyslipidemia
Resumen
Objetivos

Evaluar la efectividad de la implementación de programas de actividad física y dietética independientemente o combinados en los valores de glucosa en sangre y perfil lipídico en pacientes con diabetes tipo 2, incluyendo participantes de 60 años y más.

Diseño

Revisión sistemática.

Fuentes de datos

PubMed/Medline, con restricciones de idioma. Se incluyeron artículos publicados entre 2010 y 2016.

Selección de estudios

Se incluyeron 30 estudios controlados aleatorios, centrados en la actividad física e intervenciones dietéticas en pacientes con diabetes tipo 2 que incluían sujetos de 60 años y más.

Resultados

Los artículos seleccionados han demostrado que la implementación de programas de actividad física (ejercicios aeróbicos, resistencia, flexibilidad y ejercicios combinados) y programas basados en una mayor ingesta de vegetales, granos, legumbres, frutas, ácidos grasos insaturados, el consumo de alimentos con bajo índice glucémico, restricción calórica, ingesta de probióticos, suplementos de vitamina D y sesiones educativas sobre la diabetes mejoran los niveles glucémicos, así como el perfil lipídico en pacientes con diabetes tipo 2.

Conclusiones

Los programas de actividad física y dietéticos son fundamentales en el tratamiento y control metabólico de la diabetes mellitus tipo 2.

Palabras clave:
Nutrición
Ejercicio físico
Control glucémico
Dislipidemia
Texto completo
Introduction

Diabetes mellitus is a metabolic disorder characterized by the presence of chronic hyperglycemia with disturbance of carbohydrates, protein and fat metabolism. Results of insufficient secretion of insulin by pancreatic cells and/or an incomplete action of produced insulin, to which are related a serial of macrovascular and microvascular complications that affect quality of life.1–7 It is a chronic disorder with major expansion worldwide. It is estimated that the number of diabetes sufferers increase rapidly in the coming decades due to the population ageing, poor diet, lack of physical activity and obesity.8–10 Worldwide, in 2015, it is estimated that there were 415 million people with diabetes, and this number is expected to reach 642 million by 2040. In the same year, this disease was responsible for 5 million deaths. The World Health Organization projects diabetes as the 7th leading cause of death in 2030.9,11 Clinical manifestation of different variants of the disease, type 2 diabetes has been suffering a major increase worldwide representing 90–95% of all cases of diabetes mellitus.1,9 Its prevalence increases with age,9,12–16 and is directly related to bad eating habits, abdominal and visceral obesity, sedentary lifestyles.1,7,9,16–19 People with diabetes have an increased risk to have cardiovascular disease than non-diabetics, which can be 2–4 times greater.6,16,20–22 Dyslipidemia and insulin resistance are risk factors for cardiovascular disease dyslipidemia and insulin resistance are risk factors for cardiovascular disease.16,21,23–28 This disease is a major cause of morbidity and reduced life expectancy in patients with diabetes.29,30 It is estimated that at least 68% of diabetic patients over 65 years old die from heart disease and 16% due to stroke.31

A balanced and healthy diet is an essential component for the prevention and selfcontrol of type 2 diabetes. It contributes to a harmonious growth and development, also reflected in the patterns of acquired diseases, that is, it has a profound impact on the individual's health in all its dimensions (social, physical and mental). For this, the diet must respect the nutritional recommendations, namely hours and quality of meals.32–34 The nutrition intervention emphasizing the promotion of healthy eating has been shown to be an important point in diabetes mellitus treatment since promotes a better glycemic control and lipid profile. Diets rich in whole grains, fruits, vegetables, nuts, whit a moderate alcohol intake, a lower intake of red meat, processed refined foods, sweets, dairy products with high fat and soft drinks have been correlated with a reduced risk of diabetes, better glycemic control and lipid profile in patients with diabetes.1,35–41 Physical activity can be described as any body movement that which requires muscular use and more energy expenditure than at rest.42 Is widely recommended as an essential non-pharmacological therapeutic strategy to the prevention and metabolic control of type 2 diabetes.1,9,41

International organizations recommend a weekly accumulation of a minimum of 150min of aerobic moderate exercise (50–70% the maximum heart rate), 75min of vigorous intensity, or a combination of both types, distributed over a minimum of 3 days per week, with no more than 2 consecutive days without exercise.1,43

The objective of this systematic review is evaluate the effectiveness of the implementation of independently or combined dietary and physical activity programs on the blood glucose values and lipid profile in patients with type 2 diabetes, including participants aged 60 and more years. Given the high aging rate and the prevalence of type 2 diabetes of the population, we choose to conduct an analysis of several publications on this topic.

MethodsData sources

A comprehensive search was performed in the international scientific database:

PubMed/Medline, using the descriptors “Diabetes AND ((food habits) OR BMI OR obesity OR (physical activity) OR exercise OR glucose OR HbA1c OR (total cholesterol) OR HDL OR LDL OR VLDL OR triglycerides OR apoA OR apoB OR apoC OR apoD OR apoE)”.

Study selection, selection criteria and quality assessment

The research and study selection was performed independently by two reviewers. If there were uncertainty regarding eligibility, their inclusion or not was jointly decided by the four reviewers. Were considered eligible for the purposes of this review only randomized clinical trials comparing physical activity or dietary interventions with control group in type 2 diabetes, that include participants with 60 and more years, published between 2010 and 2015, available in full text, with evaluation of the proposed intervention and published in Portuguese, Spanish, English or French. Were excluded studies that did not recruit elderly patients with type 2 diabetes, opinion articles, and with no final assessment of the proposed intervention. The following PICO (Population, Intervention, Comparator, Outcome) methodology was used: Population: patients with type 2 diabetes, age ≥60 years; Implementation/Indicator: Dietary program and physical activity; Comparator: control program; Outcome: Impact on the blood glucose values and lipid profile in patients with type 2 diabetes.

The included articles were assessed for the risk of bias using the recommendations for judging the risk of bias, provided in Chapter 8 of the Cochrane Handbook,44 since the selected studies were randomized. Such studies are very prone to bias due to the arbitrariness of researchers in sample selection, assessment of the variables analyzed and difficulty in control of external variables that can influence the results.45

The evaluation consists of two parts, where the risk of bias is assessed in seven areas: Random sequence generation, allocation concealment, blinding of participants and researchers, blinding of outcome assessment, incomplete outcome data, selective reporting and other sources of bias. The first makes an analysis to what is described in that study and analyzed in order to be able to classify the risk of bias. In the second part is made the classification of the risk of bias in one of three categories: low risk of bias, high risk of bias or uncertain risk of bias, for each of the analyzed domains.44 The general description and an overall assessment of risk of bias of the included trials in this review are shown in Table 1 and Figure 1.

Table 1.

Risk of bias for each study included in the analysis.

  Random sequence generation (selection bias)  Allocation concealment (selection bias)  Blinding of participants and researchers (performance bias)  Blinding of outcome assessment (detection bias)  Incomplete outcome data (attrition bias)  Selective reporting (reporting bias)  Other bias 
Gavin et al. (2010)55 
 
 
 
 
 
 
 
Okada et al. (2010)46 
 
 
 
 
 
 
 
Church et al. (2010)47 
 
 
 
 
 
 
 
Wong et al. (2010)65 
 
 
 
 
 
 
 
De Greef et al. (2011)61 
 
 
 
 
 
 
 
Ariza Copado et al. (2011)62 
 
 
 
 
 
 
 
Jorge et al. (2011)48 
 
 
 
 
 
 
 
Larose et al. (2011)49 
 
 
 
 
 
 
 
Ferrer-García et al. (2011)17 
 
 
 
 
 
 
 
Cohen and Johnston (2011)37 
 
 
 
 
 
 
 
Sharma et al. (2011)73 
 
 
 
 
 
 
 
Kahleova et al. (2011)67 
 
 
 
 
 
 
 
Andrews et al. (2011)69 
 
 
 
 
 
 
 
Balducci et al. (2012)50 
 
 
 
 
 
 
 
Balducci et al. (2012)51 
 
 
 
 
 
 
 
Swift et al. (2012)54 
 
 
 
 
 
 
 
Soric (et al. 2012)75 
 
 
 
 
 
 
 
Breslavsky et al. (2013)78 
 
 
 
 
 
 
 
Strobel et al. (2014)76 
 
 
 
 
 
 
 
Kampmann et al. (2014)77 
 
 
 
 
 
 
 
Ryu et al. (2014)79 
 
 
 
 
 
 
 
Yuan et al. (2014)63 
 
 
 
 
 
 
 
Asemi et al. (2014)93 
 
 
 
 
 
 
 
Li et al. (2014)72 
 
 
 
 
 
 
 
Stenvers et al. (2014)70 
 
 
 
 
 
 
 
Vinetti et al. (2015)52 
 
 
 
 
 
 
 
Motahari-Tabari et al. (2015)53 
 
 
 
 
 
 
 
Ostadrahimi et al. (2015)94 
 
 
 
 
 
 
 
Hove et al. (2015)95 
 
 
 
 
 
 
 
Tonucci et al. (2015)96 
 
 
 
 
 
 
 

: low risk of bias;
: high risk of bias;
: unclear risk of bias.

Figure 1.

Percentage of risk of bias for each study included in the analysis.

(0,14MB).

In Table 2, are reported the general description of the included trials in this review per intervention and continent. In this table, taking into account the type of intervention, the articles were grouped in six categories: physical activity; dietary program; physical activity and dietary program; educational sessions; educational sessions whit physical activity; and educational sessions, physical activity and dietary program. Each study has the year and place of development, number of participants, description of the intervention, its duration and the principal results

Table 2.

General description of the included trials in this review per intervention and continent.

Physical activity: American continent
Author Reference  Year, Country  Group, number of patients  Description of intervention  Length of program  Results 
Gavin et al.552010, Canada  Aerobic training group, 60  Aerobic training supervised, three times per week on a treadmill or cycle ergometer.  6 monthsTriglycerides (TG) were reduced in resistance combined and aerobic exercise group, p=0.02/0.001/p>0.05. Apo B48 decreased in resistance and combined exercise group, p<0.05/p>0.05. In the aerobic exercise group increased, p>0.05.
  Resistance exercise, 64  2–3 sets the resistance exercise supervised on weight machines, 2–3 days per week 
  Combined exercise, 64  Full aerobic plus the full resistance program. 
  Control, 63  Revert to their level of activity at baseline and to maintain this level 
Church et al.472010, USA  Aerobic exercise, 72  Aerobic exercise supervised at 50%–80% of maximum oxygen consumption with an energy expenditure of 12kcal/kg per week  9 monthsCompared with the control group, the HbA1c decrease 0.34% in the combined exercise group, 0.16% in resistance exercise group, and 0.24% in aerobic exercise group, p=0.03/032/0.14.
In diabetes patients with HbA1c7 and compared with the control group, the combined exercise reduces HbA1c 0.53%, the aerobic exercise 0.50%, and 0.33% the resistance exercise, p=0.008/0.01/0.10.
  Resistance exercise, 73  Resistance exercise supervised 3 days per week 
  Combination exercise, 76  2 resistance training sessions per week and aerobic exercise supervised with energy expenditure of 10kcal/kg per week 
  Control, 41  Stretching and relaxation classes supervised. And was asked to maintain current activity during the study period 
Jorge et al.482011, Brazil  Aerobic, 12  60min of aerobic exercise (cycling) 3 days per week  12 weeksIt has been found in 4 groups a reduction of fasting and postprandial glucose, p<0.05.
The HbA1c and insulin resistance decreased in the aerobic, resistance and combined exercise group and increased in the control group, p>0.05.
It was found in 4 groups decrease the TC and TG, p<0.05.
The HDL cholesterol had a decreased in the aerobic, resistance and control group, p<0.05.
  Resistance, 12  60min of resistance exercise supervised 3 days per week 
  Combined, 12  Aerobic and resistance exercise interchanged at the same intensity and half the volume of the aerobic and resistance group 
  Control, 12  Stretching exercises designed to provide participative involvement but not to elicit changes in muscle strength or cardiovascular fitness 
Larose et al.492011, Canada  Aerobic, 60  45min of aerobic exercise supervised (treadmill or cycle ergometer) 3 days per week  6 monthsAerobic exercise and resistance reduced HbA1c (0.51/0.38%, p=0.007/0.037) compared with the control group.
In the group that practiced exercise combined the reduction was 0.46%, p=0.014 compared to the group that practiced aerobic exercise and 0.59%, p=0.001 compared to the group that performed resistance exercise.
  Resistance, 64  45min of resistance exercise supervised on weight machines, 2–3 days per week 
  Combined, 64  Aerobic and resistance exercise supervised 
  Control, 63  Subsequent to the run-in phase, were asked to revert to their level of activity at baseline and to maintain this level for the remainder of the study 
Swift et al.542012, USA  Aerobic exercise, 50  Aerobic training supervised by study staff in exercise training laboratory.  9 monthsThere was a reduction in HbA1c from the group practiced combined exercise (0.34%, p<0.05) compared with the control group (+0.24%). In the group aerobic exercise and resistance is also reduced (0.15/0.16%, p>0.05). The increased fasting glucose in the 4 groups (aerobic exercise: 2.96mg/dl; resistance: 4.76mg/dl; combined: 0.46mg/dl; control: 7.54mg/dl) and fasting insulin decreased (aerobic exercise: 1.53pmol/l resistance: 1.89pmol/l; combined: 2.05pmol/l; Control: 3.61pmol/l, p>0.05).
  Resistance exercise, 58  Resistance training supervised in exercise training laboratory 3 days per week 
  Combination exercise, 59  Combination of resistance and aerobic training in exercise training laboratory. 
  Control, 37  Stretching and relaxation classes and was asked to maintain their current activity during the study period. 
Physical activity: Asiatic continent
Author reference  Year, country  Group, number of patients  Description of intervention  Length of program  Results 
Okada et al.462010, Japan  Exercise, 21  Aerobic and resistance exercise program from 3 to 5 days per week, supervised by physiotherapist.  3 monthsThe HbA1c was decreased in the exercise and control group, p<0.01. Fasting blood glucose levels in plasma in the exercise group increased and decreased in the control group, p>0.05. There was a decreased in both group the TC, p>0.05, LDL cholesterol (exercise: p<0.01; control: p<0.05) and TG, p>0.05. The HDL cholesterol increased (exercise: p<0.01; control: p<0.05)
  Control, 17  Without exercise training 
Motahari-Tabari et al.532015, Iran  Exercise, 27  Aerobic exercise 3 times a week  8 weeksThe fasting glucose was reduced in the exercise group and increased in the control group, p=0.06. These changes were not statistically significant between groups, p=0.06. Plasma insulin was reduced in both groups throughout the study p=0.002. These changes were statistically significant between groups, p=0.007. Insulin resistance was lower in the exercise group compared with the control group. These changes were statistically significant throughout the study and between groups, p=0.004/0.007
  Control, 26  Without exercise training 
Physical activity: European continent
Author reference  Year, country  Group, number of patients  Description of intervention  Length of program  Results 
Ferrer-García et al.172011, SpainIntervention, 44  45min of combined physical exercise program (aerobic and anaerobic exercises) from 3 to 5 days per week, and conventional treatment for diabetes  24 weeksHbA1c decreased in the experimental and control group, p<0.05. The fasting glucose decreased in the intervention group, p=0.002, and increased in the control group, p=0.10. In the experimental group TG, TC and LDL decreased and HDL increased after 6 months (p=0.138/0.046/0.217/0.226). In the control group TC, LDL and HDL were reduced and increased TG (p=0.624/0.220/0.460/0.032).
Control, 40  Conventional treatment for diabetes 
Balducci et al.502012, ItalyExercise moderate-to-high intensity (HI), 152  Aerobic and resistance exercise supervised the moderate to high intensity 2 days per week and recommendations on both types of exercise every 3 months  12 monthsThere were lower HbA1c, fasting blood glucose, plasma insulin, insulin resistance in the LI group (p=0.005/0.030/0.009) and the HI group (p<0.001/=0.003/=0.03/=0.003). In the LI group, TG and HDL cholesterol increased (p=0.010/<0.001), the TC and LDL cholesterol decreased (p<0.001).
In the HI group, there was a decrease of TG, TC and LDL, the HDL cholesterol increased (p=0.51/<0.001/<0.001/<0.001).
Exercise low-to-moderate intensity (LI), 136  Aerobic and resistance exercise supervised the low to moderate intensity 2 days per week and recommendations on both types of exercise every 3 months 
Control, 303  Exercise counseling 
Balducci et al.512012, ItalyExercise group, 36  75min day of aerobic and resistance exercise supervised twice weekly. All participants received structured exercise counseling, encouraging any type of leisure-time physical activity  12 monthsIn the exercise group there were lower HbA1c, TC, and LDL cholesterol (p<0.001/=0.20/=0.04). TG and HDL cholesterol increased (p=0.80/0.25). In the control group HbA1c, TC, HDL and LDL cholesterol decreased (p=0.16/0.74/0.18/0.75) and increased TG (p=0.035).
Control group, 34  Structured exercise counseling, encouraging any type of leisure-time physical activity 
Vinetti et al.522015, ItalyIntervention, 10  Aerobic, resistance and flexibility exercise supervised by personal trainers and hospital-based setting  12 monthsThe fasting plasma glucose decreased in intervention/control groups (p=0.32/0.26). HbA1c decreased in the experimental group and increased in the control group (p=0.08/0.25,these changes were not statistically significant between groups, p=0.75/0.05). The same is observed with the fasting insulin (p=0.01/0.42, these alterations were statistically significant between groups, p=0.02), insulin resistance (p=0.02/p<0.05), TC (p=0.03/0.52, these changes were not statistically significant between groups, p=0.05), LDL cholesterol (p=0.04/>0.05) and TG (p=0.11/0.33. These changes were statistically significant between groups, p=0.06). HDL cholesterol decreased in the 2 groups (p=0.79/0.20). This reduction was not statistically significant between the groups p=0.29.
Control, 10  Standard medical care only 
Dietary program: American continent
Author reference  Year, country  Group, number of patients  Description of intervention  Length of program  Results 
Cohen and Johnston.372011, USAAlmond, 7  28g almond ingestion 5 day/week  12 weeksThe consumption of almond decreased the HbA1c, p=0.045, glucose concentration, p=0.305 and TG, p>0.05.
The fasting insulin increased in groups 2, p=0.610.
The TC and LDL increased consumption almond group and decreased in the control group, p>0.05.
Control, 6  2 cheese sticks ingestion 5 day/week 
Soric et al.752012, USAVitamin D, 19  2000IU vitamin D3 (cholecalciferol) daily by mouth  12 weeksThe HbA1c decreased in Vitamin D group and increased in control group, p=0.16. In the subgroup analysis, diabetic patients with baseline HbA1c>9% who had received vitamin D, have a largest decline in HbA1c (−1.4%, p=0.013) compared to those with values between 8 and 8.9% (+0.3, p=0.90) and between 7 and 7.9% (+0.1%, p=0.50).
Vitamin C (control), 18  500mg vitamin C daily by mouth. 
Toinucci et al.962015, BrazilProbiotic, 23  120g/daily of fermented milk fermented milk containing Lactobacillus acidophilus La-5 and Bifidobacterium animalis subsp lactis BB-12  6 weeksHbA1c decreased in the probiotic group and increased in the placebo group, p=0.06/0.82. These changes were statistically significant between groups p=0.02. The fasting glucose increased in 2 groups p=0.14/0.65, no statistically significant differences between groups, p=0.48. The same is observed with insulin resistance, p=0.41/0.7; between groups: p=0.77, and TG, p=0.16/0.08, between groups: p=0.62.
Insulin decreased in the 2 groups, p=0.73/0.95, no statistically significant differences between groups, p=0.72.
The TC, LDL and HDL cholesterol were reduced in the probiotic p=0.52; p=0.31; p=0.50, and increased in the placebo group, p=0.01, p=0.004; p=0.59. These changes were statistically significant differences between groups for the TC/LDL values, p=0.04/0.03, but not HDL cholesterol, p=0.38.
Placebo, 22  Conventional fermented milk. 
Dietary program: Asian continent
Author reference  Year, Country  Group, number of patients  Description of intervention  Length of program  Results 
Wong et al.652010, ChinaFish oil, 49  Fish-oil (4g/day) supplements  12 weeksThe consumption of fish oil reduced the serum TG, p<0.01, TC, p=0.08, LDL cholesterol, p=0.53, HDL cholesterol, p=0.65 and fasting glucose, p=0.08.
Control, 48  Olive-oil, with equivalent calories of fish-oil supplements 
Sharma et al.732011, IndiaExperimental, 20  9g brewer's yeast (42μg chromium) daily. 3 capsules after breakfast, lunch and dinner with either milk or water  3 monthsThere was a reduction in the experimental group/control in the HbA1c, p<0.001/<0.01, TC, p<0.02/<0.08, LDL cholesterol, p<0.001/<0.04 and VLDL cholesterol, p<0.04/<0.02. The TG decreased in the experimental group and increased in the control group, p<0.05/<0.09. HDL cholesterol increased in the experimental group, and decreased in the control group, p<0.5/<0.06.
Control, 20  Received yeast devoid of chromium 
Breslavsky et al.782013, IsraelGroup 1, 24  Oral daily supplementation with vitamin D (1000U/day)  12 monthsIn group 1, fasting glucose, HbA1c, insulin, and insulin resistance increased, p>0.05. The same was found with TC, HDL and LDL cholesterol, p>0.05. Only the TG decreased, p>0.05. In group 2 only registered lower HbA1c, p>0.05. The fasting glucose, insulin, insulin resistance, TC, HDL cholesterol, LDL cholesterol and TG increased, p>0.05.
Group 2 (control), 23  Placebo capsules 
Ryu et al.792014, KoreaVitamin D, 40  Cholecalciferol 2000IU/day and calcium 200mg/day  24 weeksHbA1c, insulin resistance and TG increased in the vitamin D group and decreased in placebo group, p=0.280/0.981/0.682.
The fasting blood glucose increased 3.2±27.5mg/dl in vitamin D group and 28.2±3.9mg/dl in the placebo group, p=0.891.
The CT, LDL and HDL cholesterol increased in the vitamin D group and in the placebo group, p=0.248/0.092/0.998.
Placebo, 41  Calcium 200mg/day 
Asemi et al.932014, IranSynbiotic food, 31  27×107UFC L. sporogenes and 1.08g inulin each day.  6 weeksThe consumption of probiotic compared with the control resulted in a decrease in serum insulin levels, p=0.03. The fasting plasma glucose also decreased in the probiotic group and increased in the control group. The same is observed with insulin resistance. The serum levels of TG, TC and LDL cholesterol increased in 2 groups. The HDL cholesterol increased in the group that consumed probiotic, and decreased in the control group. All these changes were not statistically significant, p>0.05.
Control food, 31  Same substance without probiotic bacteria and insulin 
Li et al.722014, ChinaBreakfast replacement, 36  75g of the low glycemic index multi-nutrient supplement (provides 346kcal energy) in place of breakfast  12 weeksIn breakfast replacement group showed a decrease in HbA1c, glycated protein in the serum, p<0.01 and insulin, p>0.05. The fasting glucose and insulin resistance increase, p>0.05. In the control group there was an increase in fasting blood glucose, HbA1c, insulin resistance, p<0.05 and insulin, p>0.05. Glycated serum protein decreased, p<0.05. In the breakfast replacement group TG, TC, HDL cholesterol, Apo A1 and Apo B increased, p>0.05. In the control group there was a decrease of TG, TC and LDL cholesterol, p<0.05) and increased HDL-cholesterol, Apo A1, p>0.05 and Apo B, p<0.005.
Control, 18  Healthy breakfast 
Ostadrahimi et al.942015, IranIntervention, 30  600ml fermented milk (kefir) containing probiotics twice a day (in lunch and dinner)  8 weeksThere was a decrease in serum glucose in both groups (intervention: p=0.05; placebo: p>0.05, this decrease was statistically significant between groups, p=0.03. HbA1c decreased in the intervention group and increased placebo group, p=0.001/p>0.05, these changes were statistically significant between groups, p=0.02. The TC, LDL cholesterol and TG levels decreased in both, p>0.05. The HDL cholesterol decreased in the intervention group and increased in the placebo group, p>0.05.
Placebo, 30  600ml conventional fermented milk (dough) twice a day (in lunch and dinner) 
Dietary program: European continent
Author reference  Year, country  Group, number of patients  Description of intervention  Length of program  Results 
Strobel et al.762014, GermanyVerum, 40  20 drops vigantol oil once a week, corresponding to a daily dose of 1904IU/day  6 monthsThe fasting glucose and HbA1c decreased in the 2 groups (verum, p=0.282/0.245; control: p=0.85/0.064). Insulin increased in the 2 groups, p=0.492/0.013. The decreased insulin resistance in verum group and increasing in the control group, p=0.954/0.030. The HbA1c value was lowest at baseline and after intervention in diabetic patients with levels of 25-hydroxy-vitamin D>20ng/ml, p=0.008/0.009.
Placebo, 40  Placebo oil consisting of medium chain triglycerides 
Kampmann et al.772014, DenmarkVitamin D, 7  Colecalciferol (280μg daily for 2 weeks, 140μg daily for 10 weeks)  12 weekHbA1c decreased in vitamin D group, and placebo group, p=0.79/0.07. Glucose increased in 2 groups, p=0.78/0.73; none of these changes was statistically significant between groups, p=0.13/0.89. Insulin in serum increased in the vitamin D group and decreased in the placebo group, p=0.087/0.95, and insulin secretion increased in the 2 groups, p=0.22/0.25. None of these changes was statistically significant between groups, p=0.28/0.34. The TC (p=0.90/0.61) and LDL (p=1.00/0.16) increased in vitamin D and placebo group, and HDL decreased in the 2 groups, p=0.65/0.92. None of these changes was statistically significant between groups, p=0.71/0.28/0.78.
Placebo, 8  Identical placebo tablets 
Stenvers et al.702014, NederlandsLow glycaemic response (GR), 9  103ml of Glucerna SR  3 monthsIn the low glycaemic response group there was a decrease in fasting glucose, TC, LDL and HDL cholesterol. Fasting insulin increase, and HbA1c was maintained.
In the control group increased fasting glucose, HbA1c, fasting insulin, LDL and HDL cholesterol, and decreased TC. None of these changes was statistically significant, p>0.05.
Control, 11  Free-choice breakfast 
Hove et al.952015, DenmarkCardi04 yogurt, 23  300ml milk fermented with L. helveticus (Cardi04 yogurt)  12 weeksHbA1c increased in the Cardi04 yogurt group and placebo group, p=0.740. Compared to placebo group, the plasma glucose and insulin resistance decreased in the Cardi04 yogurt group, p=0.525/0.022. The C-peptide, insulin, CT and LDL cholesterol increased, p=0.616/0.628/0.835/0.851. HDL cholesterol and proinsulin decreased, p=0.092/0.035. The TG showed the same value. In the control group, TC, LDL, HDL, TG and proinsulin increased. The C-peptide and insulin decreased, p<0.05.
Placebo, 18  300ml artificially acidified milk (placebo yogurt) 
Physical activity and dietary program: European continent
Kahleova et al.672011, Czech RepublicExperimental, 37  12 weeks of vegetarian diet. The second 12 weeks of the diet were combined with aerobic exercise.  24 weeksThe HbA1c and fasting glucose were reduced in the experimental group to 3/6 months, p<0.001. In control group HbA1c decreased to 3/6 months, p<0.001/p=0, 370. The fasting plasma glucose decreased to 3/6 months, p<0.01/p=0.420. The fasting plasma insulin decreased at 3/6 months in the experimental group, p<0.05/0.001 and experimental group, p=0.780.
In experimental group to 3/6 months decreased the TC, TG, LDL and HDL cholesterol, p=0.730/p=0.120/p<0.05/p=0.070.
In the control group at 3 months increased TC and decreased at 6 months, p=0.730. HDL cholesterol increased, p=0.70/p<0.05, LDL cholesterol was reduced, p=0.050 and increased TG, p=0.12.
Control, 37  12 weeks of conventional diabetic diet. The second 12 weeks of the diet were combined with aerobic exercise 
Andrews et al.692011, EnglandDietary Intervention, 248  Intensive diet intervention to lose 5–10% of their initial bodyweight and to maintain this loss throughout the study. Plus dietary consultation every 3 months with monthly nurse support.  12 mothsCompared with the control group, HbA1c decreased in dietary intervention group and physical activity and dietary intervention group, p=0.005/0.027. The same is observed with glucose, p<0.0001/p=0.01, and fasting insulin, p=0.001/0.022.
Insulin resistance decreased in the diet intervention group and dietary intervention and physical activity, p=0.0001/0.011. The insulin secretion decreased in the dietary intervention group diet and dietary intervention and physical activity group, p>0.05.
The TC decreased in the dietary intervention group and dietary intervention and physical activity, p>0.05. The LDL and HDL cholesterol decreased in the dietary intervention group and increased in dietary intervention and physical activity group. TG increased in the dietary group and decreased in dietary intervention and physical activity group, p>0.05.
Dietary intervention and physical activity, 246  Intensive diet intervention plus a pedometer-based physical activity program. 
Control, 99  Initial dietary consultation and follow-up every 6 months 
Educational sessions: European continent
Author reference  Year, country  Group, number of patients  Description of intervention  Length of program  Results 
De Greef et al.612011, BelgiumIndividual consultation, 22  Physical activity individual counseling by a general practitioner  12 weeksThe participants of individual, counseling/group and control group had a decrease in HbA1c value, p0.05. The fasting glucose also decreased, p<0.05, and increased in the control group, p>0.05. The TC increased in the 3 groups, p>0.05.
Group counseling, 21  Physical activity group counseling by a general practitioner 
Control, 24  General care from their general practitioner 
Educational sessions and physical activity European continent
Author reference  Year, country  Group, number of patients  Description of intervention  Length of program  Results 
Ariza Copado et al.622011, Spain1: diabetes education, 27  Educational sessions with basic content on diabetes mellitus  6 monthsCompared with the control group, HbA1c decreased in 3 groups (Group 1: −1.00; Group 2: −1.93, Group 3: −1.56%). The same is true of glucose (−1.00, −1.45, −1.48mg/dl), TC (−1.08; 1.48; −1.20mg/dl), LDL (−1.44, 1.82, 1, 27mg/dl), TG (−1.08; −1.04; −1.04mg/dl). HDL cholesterol increased in the 3 groups (+1.00, +1.17, +1.11).
2: diabetes education and physical, exercise, 28  Educational sessions with basic content on diabetes mellitus and 3–4 sections/week of aerobic exercise of moderate intensity with a duration of 60–90min each. 
3: physical exercise, 26  3–4 sections/week of aerobic exercise of moderate intensity with duration of 60–90min each. 
4: control, 27  It was followed in normal diabetes consultations. 
Educational sessions, physical activity and dietary program: Asiatic continent
Author reference  Year, country  Group, number of patients  Description of intervention  Length of program  Results 
Yuan et al.632014, JapanIntervention, 44  8-week education on self-management of diabetes mellitus and subsequent 4 weeks of practice of the self-management guidelines  3-monthHbA1c levels decreased in the intervention group and increased in the control group, p=0.039/0.102, the same was found with fasting glucose, p=0.238/0.427 and TG, p=0.626/0.850. In both groups there was a decrease in TC, p=0.034/<0.001, LDL, p=0.005/<0.001). The HDL cholesterol increased in intervention group and decreased in the control group, p=0.160/0.303).
Control, 44  Standard advice on medical nutrition therapy 
Results and discussion

In the initial search were identified 230.825 studies through the PubMed/Medline database, of which 224.146 studies were excluded due to lack of relevancy and 6.679 were selected. Of these publications, 6.581 were excluded and 98 were initially selected based on title and abstract. Of these publications, 68 articles we excluded after full text reading; in the end 30 met the inclusion criteria and were considered for this systematic review. The flowchart for the selection of trials is shown in Figure 2.

Figure 2.

Flowchart depicting the study selection procedure.

(0,15MB).

Results of several studies confirm that physical exercise is a key tool in glycemic control and lipid profile in type 2 diabetic patients. The practice of physical activity programs is correlated with better glycemic control and lipid profile since it decreases glycated hemoglobin levels (HbA1c),17,46–52 fasting glucose17,46,48,50,52,53 and postprandial levels,48 insulin resistance48,50,52,53 and fasting plasma insulin levels.50,52–54 It is also observed a decrease in TG,17,48,50,52,55 TC,17,46,48,50–52 LDL,17,46,50,52 Apo B 4855 an increase in HDL-cholesterol.17,46,48,50,51

Regarding the mode of exercise, it was found in three studies47,54,55 that combined exercise, compared to individual aerobic or resistance exercise, has better benefits to people with diabetes. The intensity of the exercise influences the lipid profile because a moderate to low aerobic exercise does not reduce TG.50

In two studies48,52 it was found that aerobic resistance and flexibility exercise decreases HDL cholesterol. The fasting glucose increased in one study.54

In summary, with respect to changes caused by exercise in the different continents where the various studies were conducted it is demonstrated reduction of HbA1c, glucose, insulin, TG, TC, LDL cholesterol, Apo B 48, lower insulin resistance and HDL cholesterol increase. According with studies performed by Nojima et al.,56 Kasumov et al.,57 De Filippis et al.,58 Lazarevic et al.59 and Hordern et al.,60 where it has also found that physical exercise is essential in the metabolic control of type 2 diabetes. The implementation of educational sessions that address the practice of physical activity and healthy eating were addressed in three of the studies analyzed. It can be seen that educational sessions that address the importance of physical activity and an healthy diet in diabetes control, in conjunction with aerobic exercise of moderate intensity, correlates with lower HbA1c,61–63 glucose,61,62 TC, LDL cholesterol, TG and increased HDL cholesterol.62,63 Similar results were observed in a systematic review with meta-analysis performed by Steinsbekk et al. where the self-management education promotes better control of type 2 diabetes.64

A healthy and balanced nutrition is an essential component for the prevention and selfmanagement of type 2 diabetes.1 A correct intake of the various food components, namely avoiding the excessive consumption of saturated fat and carbohydrates are important for obtaining a good glycemic and lipid control. A dietary program with emphasis on greater consumption of polyunsaturated fatty acids is correlated with lower levels of fasting glucose, TG, TC and LDL cholesterol.65 This is in agreement with the results of the study of Lee et al.66

The intake of almonds reduces fasting blood glucose, HbA1c and increases fasting insulin. Regarding the lipid profile, there is an increase of TC and HDL cholesterol and a reduction of TG.37

The increased consumption of grains, fruit and vegetables alone (vegetarian diet) or in combination with supervised aerobic exercise correlates with decrease of HbA1c, glucose and fasting insulin, TG, TC and LDL. HDL cholesterol also decreases.67 Given these results, the vegetarian diets may be beneficial for people with type 2 diabetes, as they induce glycemic and lipid control. However, we consider that is needed to be cautious in this matter as is also needed to carry out further studies in this field. According to the study of Takahashi et al., the consumption of vegetables is correlated with improved control of HbA1c and TG levels in elderly type 2 diabetes.68 Modifying the amount of macronutrients may improve glycemic and lipid control in patients with type 2 diabetes. Low-calorie, low-fat and low-GI diets correlate with lower levels of HbA1c, fasting glucose and insulin, insulin resistance, TC, LDL and HDL cholesterol. TG had a slightly increase. When this type of diet is combined with physical activity, the results obtained are similar.69 When uncontrolled type 2 diabetes ingest a low glycemic index liquid breakfast, rich in polyunsaturated fatty acids, fiber and fructose, reduces fasting glucose, TC, LDL, HDL cholesterol and increase the fasting insulin.70 Since participants had uncontrolled DM2, replacement of breakfast alone as well as the intervention period may not have been sufficient to provide long term glycemic control. Thus, further investigations should be conducted in this population over a longer period of time, replacing not only breakfast but other meals. The consumption of low glycemic foods at breakfast decreased the HbA1c, glycated serum protein and insulin. There was an increase of glucose, insulin resistance, TG, TC, LDL, HDL cholesterol, Apo A1 and Apo B.71 Results of the systematic review and meta-analysis of Ajala et al.72 they demonstrated that low-carbohydrate, low glycemic index, Mediterranean, and high-protein diets are effective in controlling the glycemic and lipid profile and should be part of the management of type 2 diabetes.

The effectiveness of the consumption of chromium, vitamin D and probiotics supplements were also studied in some articles selected for this revision.73–82 The chromium supplementation for 3 months provides a reduction in HbA1c. And has also beneficial effects on dyslipidemia, since decrease TC, LDL cholesterol, VLDL cholesterol and TG levels, and increase HDL cholesterol.73 The same is verified in a systematic review with meta-analysis performed by Suksomboon et al.83

Five of the studies analyzed the effectiveness of vitamin D supplementation in patients with type 2 diabetes.74–78 The consumption of these supplements decrease the HbA1c,74–76 glucose, insulin resistance75 and increased insulin secretion.76 Glucose increased in 3 studies,76–78 such as HbA1c and insulin resistance.77,78 Given this, it can be seen that vitamin D supplementation provides a blood glucose control in the short and long term only in studies in the American and European continent. In Asia it was not found relation to benefits. This may be due to different lifestyles and eating habits of each region.

The lipid level results were not favorable because there was an increase in total cholesterol, LDL, HDL,77,78 TG increased in one study78 in another decreased.77 This discrepancy may be due to the fact that vitamin D administered was not the same in all studies, as well as the duration of treatment, of serum levels of vitamin D of the participants could be different, researchers may not have taken into account the sun exposure of the participants in the studies. Some scientific evidence has suggested that vitamin D may play a causal role in the development of diabetes and its complications. Deficiency of this vitamin is associated with increased risk of cardiovascular disease, obesity, diabetes mellitus, dyslipidemia and hypertension. High serum vitamin D concentrations have a protective effect on glucose intolerance, insulin resistance and the risk of developing DM2. The use of supplements of this vitamin in glycemic control, insulin resistance and lipid profile is not yet clear, although some studies have shown beneficial effects.84–96 Four studies have analyzed the influence of the consumption of probiotics in patients with type 2 diabetes.79,82 It was found a decrease in glucose,79–81 HbA1c,80,82 insulin79,82 and insulin resistance.79,81 Glucose and insulin resistance only increased in one study,82 as well as HbA1c.81 The consumption of probiotics in studies conducted in Asia translates into control of the short and long term blood sugar. On the European continent there was only a blood glucose control of short term and on the American continent the control was long-term.

There was a decrease in TC, LDL and TG in two studies,80,82 and increased in two other studies.79,81The HDL cholesterol increased only in one study79 and decreased in the remaining.80–82 It may also be noted that only the administration of probiotics containing Lactobacillus acidophilus and Bifidobacterium provided lipid control. This discrepancy results may be due to five facts: the probiotic used, the amount administered, the time of administration, the duration of the treatment was not the same, as well as the continent where the studies were conducted (different dietary habits and lifestyles).

Since not all studies replicate positive results after taking vitamin D supplements and probiotics, the association between this supplementation and glycemic and lipid profile in type 2 diabetic elderly patients had a somewhat uncertain development. To provide more evidence is necessary to perform further studies to confirm the potentially beneficial relationship between supplementation with vitamin D and probiotics on glycemic and lipid profile in patients with type 2 diabetes.

Regarding the evaluation of the quality of the selected studies, as can be seen in the Figure 1, it was found that most of the articles feature uncertain selection bias because they do not describe in detail the method used to generate the random sequence and to hide this sequence; half of the articles do not describe what measures used to blind outcome assessors in relation to knowledge of the intervention provided to each participant and the results according to what has been proposed. With regard to attrition and reporting bias, all studies are at low risk since all describe the sample size at the beginning and at the end of the study. If any participant was deleted or abandoned the study that fact is referenced as well the reasons for that.

Our study shows, however, some limitations that should be considered when interpreting the results, such as the intensity and type of exercise and different diet plans may affect the outcome; different duration of the programs, and the population studied in the various articles are also heterogeneous. The exercise and usual practice of physical activity and eating habits may be over underestimated, lack of monitoring of patients after program to evaluate the persistence of potential long-term benefits and unclear risk of bias in the included studies.

Another of the limitations is the fact that pharmacological treatment for diabetes is not taken into account as well as the use of dietary supplements or other treatments, particularly to lose weight. All this makes it difficult to compare the studies and their results.

Although, some articles do not show favorable results regarding the implementation of dietary programs, and prevails a greater number of articles that highlights the importance of nutrition education, physical activity and healthy eating on glycemic control and lipid profile in patients with type 2 diabetes. We understand therefore that it is appropriate to continue to perform this type of intervention, since they have lower cost if compared with pharmacological treatments, but in a longer period of time in order to prove the long-term results.

Conclusions

Given the high prevalence of type 2 diabetes in the population, particularly in the elderly population, and considering that this pathology tends to increase with age, it becomes crucial to change behaviors in activities of daily living, promoting more active and healthy lifestyles throughout life. Physical activity, dietary programs and health education sessions regarding the importance of changing lifestyles according to scientifically valid information are revealed as complementary therapeutic strategies in treatment and metabolic control of type 2 diabetes.

Conflict of interest statement

The authors state that they have no conflicts of interest.

References
[1]
ADA.
Standards of medical care in diabetes – 2016.
Diabetes Care, 39 (2016), pp. S1-S112
[2]
R. Goldenberg, Z. Punthakee.
Committee CDACPGE. Definition, classification and diagnosis of diabetes, prediabetes and metabolic syndrome.
Can J Diabetes, 37 (2013), pp. S8-S11
[3]
G. Smushkin, A. Vella.
What is type 2 diabetes?.
Medicine (Abingdon), 38 (2010), pp. 597-601
[4]
A. Vuica, L. Ferhatović Hamzić, K. Vukojević, M. Jerić, L. Puljak, I. Grković, et al.
Aging and a long-term diabetes mellitus increase expression of 1 α-hydroxylase and vitamin D receptors in the rat liver.
Exp Gerontol, 72 (2015), pp. 167-176
[5]
G.C. Camen, O. Caraivan, M. Olteanu, A. Camen, A. Bunget, F.C. Popescu, et al.
Inflammatory reaction in chronic periodontopathies in patients with diabetes mellitus. Histological and immunohistochemical study.
Rom J Morphol Embryol, 53 (2012), pp. 5560
[6]
K. Balasubramaniam, G.N. Viswanathan, S.M. Marshall, A.G. Zaman.
Increased atherothrombotic burden in patients with diabetes mellitus and acute coronary syndrome: a review of antiplatelet therapy.
Cardiol Res Pract, 2012 (2012), pp. 909154
[7]
OMS.
Global report on diabetes.
World Health Organization, (2016),
[8]
J. Ena, R. Gómez-Huelgas, D. Sánchez-Fuentes, M. Camafort-Babkowsk, F. Formiga, A. Michán-Doña, et al.
Management of patients with type 2 diabetes and multiple chronic conditions: a Delphi consensus of the Spanish Society of Internal Medicine.
Eur J Intern Med, 27 (2016), pp. 31-36
[9]
IDF.
Diabetes atlas.
7th ed., International Diabetes Federation, (2015),
[10]
S. Wild, G. Roglic, A. Green, R. Sicree, H. King.
Global prevalence of diabetes: estimates for the year 2000 and projections for 2030.
Diabetes Care, 27 (2004), pp. 104753
[11]
C.D. Mathers, D. Loncar.
Projections of global mortality and burden of disease from 2002 to 2030.
[12]
M.L. Basanta-Alario, J. Ferri, M. Civera, S. Martínez-Hervás, J.F. Ascaso, J.T. Real.
Diferencias en las características clínico-biológicas y prevalencia de complicaciones crónicas en relación con el envejecimiento de pacientes con diabetes tipo 2.
Endocrinol Nutr, 63 (2016), pp. 79-86
[13]
M.A. Fernández.
Tratamiento del anciano con diabetes.
[14]
F. Formiga, R. Gómez-Huelgas, L. Rodríguez Mañas.
Características diferenciales de la diabetes mellitus tipo 2 en el paciente anciano. Papel de los inhibidores de la dipeptidil peptidasa 4.
Rev Española Geriatr Gerontol, 51 (2016), pp. 44-51
[15]
R. Gómez Huelgas, J. Díez-Espino, F. Formiga, J. Lafita Tejedor, L. Rodríguez Mañas, E. González-Sarmiento, et al.
Tratamiento de la diabetes tipo 2 en el paciente anciano.
Med Clín, 140 (2013),
134.e1–e12
[16]
J.B. Halter, N. Musi, F. McFarland Horne, J.P. Crandall, A. Goldberg, L. Harkless, et al.
Diabetes and cardiovascular disease in older adults: current status and future directions.
Diabetes, 63 (2014), pp. 2578-2589
[17]
J.C. Ferrer-García, P. Sánchez López, C. Pablos-Abella, R. Albalat-Galera, L. ElviraMacagno, C. Sánchez-Juan, et al.
[Benefits of a home-based physical exercise program in elderly subjects with type 2 diabetes mellitus].
Endocrinol Nutr, 58 (2011), pp. 387-394
[18]
M.L. Ganz, N. Wintfeld, Q. Li, V. Alas, J. Langer, M. Hammer.
The association of body mass index with the risk of type 2 diabetes: a case-control study nested in an electronic health records system in the United States.
Diabetol Metab Syndr, 6 (2014), pp. 50
[19]
C.R. Hofe, L. Feng, D. Zephyr, A.J. Stromberg, B. Hennig, L.M. Gaetke.
Fruit and vegetable intake, as reflected by serum carotenoid concentrations, predicts reduced probability of polychlorinated biphenyl-associated risk for type 2 diabetes: National Health and Nutrition Examination Survey 2003–2004.
Nutr Res, 34 (2014), pp. 285-293
[20]
M.M. Alvarez.
Plano alimentar em algumas complicações metabólicas do diabetes mellitus: hiperglicémia. nefropatias e dislipidemias.
Manual de nutrição – profissional da Saúde, pp. 42-47
[21]
M.A. Miselli, E.D. Nora, A. Passaro, F. Tomasi, G. Zuliani.
Plasma triglycerides predict ten-years all-cause mortality in outpatients with type 2 diabetes mellitus: a longitudinal observational study.
Cardiovasc Diabetol, 13 (2014), pp. 135
[22]
A. Hormigo-Pozo, J. Mancera-Romero, M.P. Perez-Unanua, M. Alonso-Fernandez, F. Lopez-Simarro, J.J. Mediavilla-Bravo, et al.
[Consensus document on the treatment of dyslipidemia in diabetes].
[23]
D. Luksiene, A. Tamosiunas, M. Baceviciene, R. Radisauskas, V. Malinauskiene, A. Peasey, et al.
Trends in prevalence of dyslipidaemias and the risk of mortality in Lithuanian urban population aged 45–64 in relation to the presence of the dyslipidaemias and the other cardiovascular risk factors.
[24]
H. Pikhart, J.A. Hubáček, A. Peasey, R. Kubínová, M. Bobák.
Association between fasting plasma triglycerides, all-cause and cardiovascular mortality in Czech population. Results from the HAPIEE study.
Physiol Res, 64 (2015), pp. S355-S361
[25]
M. Miller, N.J. Stone, C. Ballantyne, V. Bittner, M.H. Criqui, H.N. Ginsberg, et al.
Triglycerides and cardiovascular disease: a scientific statement from the American Heart Association.
Circulation, 123 (2011), pp. 2292-2333
[26]
Y. Hirakawa, T.H. Lam, T. Welborn, H.C. Kim, S. Ho, X. Fang, et al.
The impact of body mass index on the associations of lipids with the risk of coronary heart disease in the Asia Pacific region.
Prev Med Rep, 3 (2016), pp. 79-82
[27]
I. Ramasamy.
Update on the molecular biology of dyslipidemias.
Clin Chim Acta, 454 (2016), pp. 143-185
[28]
N. Cortez-Dias, S. Robalo Martins, A. Belo, M. Fiúza.
VALSIM endIdE [Characterization of lipid profile in primary health care users in Portugal].
Rev Port Cardiol, 32 (2013), pp. 987-996
[29]
J. Hippisley-Cox, C. Coupland.
Development and validation of risk prediction equations to estimate future risk of heart failure in patients with diabetes: a prospective cohort study.
BMJ Open, 5 (2015), pp. e008503
[30]
IDF.
Global guideline for managing older people with type 2 diabetes.
International Diabetes Federation, (2013),
[31]
D. Mozaffarian, E.J. Benjamin, A.S. Go, D.K. Arnett, M.J. Blaha, M. Cushman, et al.
Heart disease and stroke statistics – 2015 update: a report from the American Heart Association.
Circulation, 131 (2015), pp. e29-e322
[32]
C. Calhau, A. Faria, E. Keating, F. Martel, I. Azevedo, M.J. Martins, et al.
Guias de saúde nutrição.
QUIDNOVI, (2011),
[33]
P. Graça, M.J. Gregório.
Estratégias para a Promoção da Alimentação Saudável em Portugal.
Portugal Saúde Núm, 4 (2015), pp. 37-41
[34]
B.G. Abellán, J.D.L.T. Hidalgo, J.R. Sotos, J.L.T. López, C.L.V. Jiménez.
Alimentación saludable y autopercepción de salud.
Atención Primaria, (2016),
[35]
S.H. Ley, O. Hamdy, V. Mohan, F.B. Hu.
Prevention and management of type 2 diabetes: dietary components and nutritional strategies.
Lancet, 383 (2014), pp. 19992007
[36]
J. Salas-Salvadó, M. Martinez-González, M. Bulló, E. Ros.
The role of diet in the prevention of type 2 diabetes.
Nutr Metab Cardiovasc Dis, (2011), pp. B32-B48
[37]
A.E. Cohen, C.S. Johnston.
Almond ingestion at mealtime reduces postprandial glycemia and chronic ingestion reduces hemoglobin A(1c) in individuals with wellcontrolled type 2 diabetes mellitus.
Metabolism, 60 (2011), pp. 1312-1317
[38]
D.J. Jenkins, C.W. Kendall, M.S. Banach, K. Srichaikul, E. Vidgen, S. Mitchell, et al.
Nuts as a replacement for carbohydrates in the diabetic diet.
Diabetes Care, 34 (2011), pp. 1706-1711
[39]
S.K. Nishi, C.W. Kendall, R.P. Bazinet, B. Bashyam, C.A. Ireland, L.S. Augustin, et al.
Nut consumption, serum fatty acid profile and estimated coronary heart disease risk in type 2 diabetes.
Nutr Metab Cardiovasc Dis, 24 (2014), pp. 845-852
[40]
F. Shidfar, N. Froghifar, M. Vafa, A. Rajab, S. Hosseini, S. Shidfar, et al.
The effects of tomato consumption on serum glucose, apolipoprotein B, apolipoprotein A-I, homocysteine and blood pressure in type 2 diabetic patients.
Int J Food Sci Nutr, 62 (2011), pp. 289-294
[41]
S.E. Inzucchi, R.M. Bergenstal, J.B. Buse, M. Diamant, E. Ferrannini, M. Nauck, et al.
Management of hyperglycemia in type 2 diabetes: a patient-centered approach: position statement of the American Diabetes Association (ADA) and the European Association for the Study of Diabetes (EASD).
Diabetes Care, 35 (2012), pp. 1364-1379
[42]
World Health Organization.
Global strategy on diet, physical activity and health.
[43]
OMS.
Global recommendations on physical activity for health.
World Health Organization, (2010),
[44]
J. Higgins, D. Altman, The Cochrane Collaboration.
Assessing risk of bias in included studies.
Cochrane handbook for systematic reviews of intervention version 510 (update March 2011),
[45]
A.P.V. Carvalho, V. Silva, A.J. Grande.
Avaliação do Risco de Viés de Ensaios Clínicos Randomizados pela Ferramenta da Colaboração Cochrane.
Diagn Tratamento, 18 (2013), pp. 33-44
[46]
S. Okada, A. Hiuge, H. Makino, A. Nagumo, H. Takaki, H. Konishi, et al.
Effect of exercise intervention on endothelial function and incidence of cardiovascular disease in patients with type 2 diabetes.
J Atheroscler Thromb, 17 (2010), pp. 828-833
[47]
T.S. Church, S.N. Blair, S. Cocreham, N. Johannsen, W. Johnson, K. Kramer, et al.
Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial.
JAMA, 304 (2010), pp. 2253-2262
[48]
M.L. Jorge, V.N. de Oliveira, N.M. Resende, L.F. Paraiso, A. Calixto, A.L. Diniz, et al.
The effects of aerobic, resistance, and combined exercise on metabolic control, inflammatory markers, adipocytokines, and muscle insulin signaling in patients with type 2 diabetes mellitus.
Metabolism, 60 (2011), pp. 1244-1252
[49]
J. Larose, R.J. Sigal, F. Khandwala, D. Prud’homme, N.G. Boulé, G.P. Kenny, et al.
Associations between physical fitness and HbA1c in type 2 diabetes mellitus.
Diabetologia, 54 (2011), pp. 93-102
[50]
S. Balducci, S. Zanuso, P. Cardelli, L. Salvi, A. Bazuro, L. Pugliese, et al.
Effect of high- versus low-intensity supervised aerobic and resistance training on modifiable cardiovascular risk factors in type 2 diabetes; the Italian Diabetes and Exercise Study (IDES).
[51]
S. Balducci, S. Zanuso, P. Cardelli, G. Salerno, S. Fallucca, A. Nicolucci, et al.
Supervised exercise training counterbalances the adverse effects of insulin therapy in overweight/obese subjects with type 2 diabetes.
Diabetes Care, 35 (2012), pp. 39-41
[52]
G. Vinetti, C. Mozzini, P. Desenzani, E. Boni, L. Bulla, I. Lorenzetti, et al.
Supervised exercise training reduces oxidative stress and cardiometabolic risk in adults with type 2 diabetes: a randomized controlled trial.
Sci Rep, 5 (2015), pp. 9238
[53]
N. Motahari-Tabari, M. Ahmad Shirvani, M. Shirzad-E-Ahoodashty, E. YousefiAbdolmaleki, M. Teimourzadeh.
The effect of 8 weeks aerobic exercise on insulin resistance in type 2 diabetes: a randomized clinical trial.
Glob J Health Sci, 7 (2015), pp. 115-121
[54]
D.L. Swift, N.M. Johannsen, C.P. Earnest, S.N. Blair, T.S. Church.
Effect of exercise training modality on C-reactive protein in type 2 diabetes.
Med Sci Sports Exerc, 44 (2012), pp. 1028-1034
[55]
C. Gavin, R.J. Sigal, M. Cousins, M.L. Menard, M. Atkinson, F. Khandwala, et al.
Resistance exercise but not aerobic exercise lowers remnant-like lipoprotein particle cholesterol in type 2 diabetes: a randomized controlled trial.
Atherosclerosis, 213 (2010), pp. 552-557
[56]
H. Nojima, H. Watanabe, K. Yamane, Y. Kitahara, K. Sekikawa, H. Yamamoto, et al.
Effect of aerobic exercise training on oxidative stress in patients with type 2 diabetes mellitus.
Metabolism, 57 (2008), pp. 170-176
[57]
T. Kasumov, T.P. Solomon, C. Hwang, H. Huang, J.M. Haus, R. Zhang, et al.
Improved insulin sensitivity after exercise training is linked to reduced plasma C14:0 ceramide in obesity and type 2 diabetes.
Obesity (Silver Spring), 23 (2015), pp. 1414-1421
[58]
E. De Filippis, K. Cusi, G. Ocampo, R. Berria, S. Buck, A. Consoli, et al.
Exerciseinduced improvement in vasodilatory function accompanies increased insulin sensitivity in obesity and type 2 diabetes mellitus.
J Clin Endocrinol Metab, 91 (2006), pp. 4903-4910
[59]
G. Lazarevic, S. Antic, T. Cvetkovic, P. Vlahovic, I. Tasic, V. Stefanovic.
A physical activity programme and its effects on insulin resistance and oxidative defense in obese male patients with type 2 diabetes mellitus.
Diabetes Metab, 32 (2006), pp. 58390
[60]
M.D. Hordern, L.M. Cooney, E.M. Beller, J.B. Prins, T.H. Marwick, J.S. Coombes.
Determinants of changes in blood glucose response to short-term exercise training in patients with Type 2 diabetes.
Clin Sci (Lond), 115 (2008), pp. 273-281
[61]
K. De Greef, B. Deforche, C. Tudor-Locke, I. De Bourdeaudhuij.
Increasing physical activity in Belgian type 2 diabetes patients: a three-arm randomized controlled trial.
Int J Behav Med, 18 (2011), pp. 188-198
[62]
C. Ariza Copado, V. Gavara Palomar, A. Muñoz Ureña, F. Aguera Mengual, M. Soto Martínez, J.R. Lorca Serralta.
Mejora en el control de los diabéticos tipo 2 tras una intervención conjunta: educación diabetológica y ejercicio físico.
Atención Primaria, 43 (2011), pp. 398-406
[63]
C. Yuan, C.W. Lai, L.W. Chan, M. Chow, H.K. Law, M. Ying.
The effect of diabetes self-management education on body weight, glycemic control, and other metabolic markers in patients with type 2 diabetes mellitus.
J Diabetes Res, 2014 (2014), pp. 789761
[64]
A. Steinsbekk, L. Rygg, M. Lisulo, M.B. Rise, A. Fretheim.
Group based diabetes self-management education compared to routine treatment for people with type 2 diabetes mellitus. A systematic review with meta-analysis.
BMC Health Serv Res, 12 (2012), pp. 213
[65]
C.Y. Wong, K.H. Yiu, S.W. Li, S. Lee, S. Tam, C.P. Lau, et al.
Fish-oil supplement has neutral effects on vascular and metabolic function but improves renal function in patients with Type 2 diabetes mellitus.
[66]
T.C. Lee, P. Ivester, A.G. Hester, S. Sergeant, L.D. Case, T. Morgan, et al.
The impact of polyunsaturated fatty acid-based dietary supplements on disease biomarkers in a metabolic syndrome/diabetes population.
Lipids Health Dis, 13 (2014), pp. 196
[67]
H. Kahleova, M. Matoulek, H. Malinska, O. Oliyarnik, L. Kazdova, T. Neskudla, et al.
Vegetarian diet improves insulin resistance and oxidative stress markers more than conventional diet in subjects with Type 2 diabetes.
Diabet Med, 28 (2011), pp. 549-559
[68]
K. Takahashi, C. Kamada, H. Yoshimura, R. Okumura, S. Iimuro, Y. Ohashi, et al.
Effects of total and green vegetable intakes on glycated hemoglobin A1c and triglycerides in elderly patients with type 2 diabetes mellitus: the Japanese Elderly Intervention Trial.
Geriatr Gerontol Int, 12 (2012), pp. 50-58
[69]
R.C. Andrews, A.R. Cooper, A.A. Montgomery, A.J. Norcross, T.J. Peters, D.J. Sharp, et al.
Diet or diet plus physical activity versus usual care in patients with newly diagnosed type 2 diabetes: the early ACTID randomised controlled trial.
[70]
D.J. Stenvers, L.J. Schouten, J. Jurgens, E. Endert, A. Kalsbeek, E. Fliers, et al.
Breakfast replacement with a low-glycaemic response liquid formula in patients with type 2 diabetes: a randomised clinical trial.
Br J Nutr, 112 (2014), pp. 504-512
[71]
D. Li, P. Zhang, H. Guo, W. Ling.
Taking a low glycemic index multi-nutrient supplement as breakfast improves glycemic control in patients with type 2 diabetes mellitus: a randomized controlled trial.
Nutrients, 6 (2014), pp. 5740-5755
[72]
O. Ajala, P. English, J. Pinkney.
Systematic review and meta-analysis of different dietary approaches to the management of type 2 diabetes.
Am J Clin Nutr, 97 (2013), pp. 505-516
[73]
S. Sharma, R.P. Agrawal, M. Choudhary, S. Jain, S. Goyal, V. Agarwal.
Beneficial effect of chromium supplementation on glucose, HbA1C and lipid variables in individuals with newly onset type-2 diabetes.
J Trace Elem Med Biol, 25 (2011), pp. 14953
[74]
M.M. Soric, E.T. Renner, S.R. Smith.
Effect of daily vitamin D supplementation on HbA1c in patients with uncontrolled type 2 diabetes mellitus: a pilot study.
[75]
F. Strobel, J. Reusch, M. Penna-Martinez, E. Ramos-Lopez, E. Klahold, C. Klepzig, et al.
Effect of a randomised controlled vitamin D trial on insulin resistance and glucose metabolism in patients with type 2 diabetes mellitus.
Horm Metab Res, 46 (2014), pp. 54-58
[76]
U. Kampmann, L. Mosekilde, C. Juhl, N. Moller, B. Christensen, L. Rejnmark, et al.
Effects of 12 weeks high dose vitamin D3 treatment on insulin sensitivity, beta cell function, and metabolic markers in patients with type 2 diabetes and vitamin D insufficiency – a double-blind, randomized, placebo-controlled trial.
Metabolism, 63 (2014), pp. 1115-1124
[77]
A. Breslavsky, J. Frand, Z. Matas, M. Boaz, Z. Barnea, M. Shargorodsky.
Effect of high doses of vitamin D on arterial properties, adiponectin, leptin and glucose homeostasis in type 2 diabetic patients.
Clin Nutr, 32 (2013), pp. 970-975
[78]
O.H. Ryu, W. Chung, S. Lee, K.S. Hong, M.G. Choi, H.J. Yoo.
The effect of highdose vitamin D supplementation on insulin resistance and arterial stiffness in patients with type 2 diabetes.
Korean J Intern Med, 29 (2014), pp. 620-629
[79]
Z. Asemi, A. Khorrami-Rad, S.A. Alizadeh, H. Shakeri, A. Esmaillzadeh.
Effects of synbiotic food consumption on metabolic status of diabetic patients: a double-blind randomized cross-over controlled clinical trial.
Clin Nutr, 33 (2014), pp. 198-203
[80]
A. Ostadrahimi, A. Taghizadeh, M. Mobasseri, N. Farrin, L. Payahoo, Z. Beyramalipoor Gheshlaghi, et al.
Effect of probiotic fermented milk (kefir) on glycemic control and lipid profile in type 2 diabetic patients: a randomized double-blind placebo-controlled clinical trial.
Iran J Public Health, 44 (2015), pp. 228-237
[81]
K.D. Hove, C. Brøns, K. Færch, S.S. Lund, P. Rossing, A. Vaag.
Effects of 12 weeks of treatment with fermented milk on blood pressure, glucose metabolism and markers of cardiovascular risk in patients with type 2 diabetes: a randomised double-blind placebocontrolled study.
Eur J Endocrinol, 172 (2015), pp. 11-20
[82]
L.B. Tonucci, K.M. Olbrich Dos Santos, L. Licursi de Oliveira, S.M. Rocha Ribeiro, H.S. Duarte Martino.
Clinical application of probiotics in type 2 diabetes mellitus: a randomized, double-blind, placebo-controlled study.
Clin Nutr, (2015),
[83]
N. Suksomboon, N. Poolsup, A. Yuwanakorn.
Systematic review and metaanalysis of the efficacy and safety of chromium supplementation in diabetes.
J Clin Pharm Ther, 39 (2014), pp. 292-306
[84]
N.G. Forouhi, Z. Ye, A.P. Rickard, K.T. Khaw, R. Luben, C. Langenberg, et al.
Circulating 25-hydroxyvitamin D concentration and the risk of type 2 diabetes: results from the European Prospective Investigation into Cancer (EPIC)-Norfolk cohort and updated meta-analysis of prospective studies.
Diabetologia, 55 (2012), pp. 2173-2182
[85]
N.O. Nielsen, P. Bjerregaard, P.F. Rønn, H. Friis, S. Andersen, M. Melbye, et al.
Associations between Vitamin D status and type 2 diabetes measures among Inuit in Greenland may be affected by other factors.
PLOS ONE, 11 (2016), pp. e0152763
[86]
P. Knekt, M. Laaksonen, C. Mattila, T. Härkänen, J. Marniemi, M. Heliövaara, et al.
Serum vitamin D and subsequent occurrence of type 2 diabetes.
Epidemiology, 19 (2008), pp. 666-671
[87]
A.G. Pittas, J. Lau, F.B. Hu, B. Dawson-Hughes.
The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis.
J Clin Endocrinol Metab, 92 (2007), pp. 2017-2029
[88]
K.S. Aljabri, S.A. Bokhari, M.J. Khan.
Glycemic changes after vitamin D supplementation in patients with type 1 diabetes mellitus and vitamin D deficiency.
Ann Saudi Med, 30 (2010), pp. 454-458
[89]
G. Muscogiuri, G.P. Sorice, R. Ajjan, T. Mezza, S. Pilz, A. Prioletta, et al.
Can vitamin D deficiency cause diabetes and cardiovascular diseases? Present evidence and future perspectives.
Nutr Metab Cardiovasc Dis, 22 (2012), pp. 81-87
[90]
M.B. Davidson, P. Duran, M.L. Lee, T.C. Friedman.
High-dose vitamin D supplementation in people with prediabetes and hypovitaminosis D.
Diabetes Care, 36 (2013), pp. 260-266
[91]
M.M. Oosterwerff, E.M. Eekhoff, N.M. Van Schoor, A.J. Boeke, P. Nanayakkara, R. Meijnen, et al.
Effect of moderate-dose vitamin D supplementation on insulin sensitivity in vitamin D-deficient non-Western immigrants in the Netherlands: a randomized placebo-controlled trial.
Am J Clin Nutr, 100 (2014), pp. 152-160
[92]
E. Barengolts, B. Manickam, Y. Eisenberg, A. Akbar, S. Kukreja, I. Ciubotaru.
Effect of high-dose vitamin D repletion on glycemic control in African-American males with prediabetes and hypovitaminosis D.
Endocr Pract, 21 (2015), pp. 604-612
[93]
C. Dalgård, M.S. Petersen, P. Weihe, P. Grandjean.
Vitamin D status in relation to glucose metabolism and type 2 diabetes in septuagenarians.
Diabetes Care, 34 (2011), pp. 1284-1288
[94]
A. Talaei, M. Mohamadi, Z. Adgi.
The effect of vitamin D on insulin resistance in patients with type 2 diabetes.
Diabetol Metab Syndr, 5 (2013), pp. 8
[95]
J. Zhang, J. Ye, G. Guo, Z. Lan, X. Li, Z. Pan, et al.
Vitamin D status is negatively correlated with insulin resistance in Chinese type 2 diabetes.
Int J Endocrinol, 2016 (2016), pp. 1794894
[96]
I. González-Molero, G. Rojo-Martínez, S. Morcillo, C. Gutiérrez-Repiso, E. RubioMartín, M.C. Almaraz, et al.
Vitamin D and incidence of diabetes: a prospective cohort study.
Clin Nutr, 31 (2012), pp. 571-573
Copyright © 2017. Elsevier España, S.L.U.. All rights reserved
Opciones de artículo
Herramientas
es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?

Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos