Comparison of Substrate Oxidation and Energy Expenditure During Acute Aerobic Exercise With Moderate and High Intensity in Patients With Type 2 Diabetes


Hamed Rezaei Nasab 1 , * , Rouhollah Ranjbar 1 , Abdolhamid Habibi 1 , Saeed Shakerian 1

1 Department Of Exercise Physiology, Faculty of Physical Education and Sport Sciences, Shahid Chamran University, Ahvaz, IR Iran

How to Cite: Rezaei Nasab H, Ranjbar R, Habibi A, Shakerian S. Comparison of Substrate Oxidation and Energy Expenditure During Acute Aerobic Exercise With Moderate and High Intensity in Patients With Type 2 Diabetes, Jentashapir J Cell Mol Biol. 2015 ; 6(5):e24160. doi: 10.17795/jjhr-24160.


Jentashapir Journal of Health Research: 6 (5); e24160
Published Online: September 30, 2015
Article Type: Research Article
Received: September 29, 2014
Revised: April 11, 2015
Accepted: April 22, 2015


Background: Type 2 diabetes and obesity are related to other metabolic disorders such as insulin resistance, high blood pressure, visceral obesity increase and metabolic syndrome with high danger of cardiovascular disease expansion.

Objectives: This study aimed to determine whether in patients with type 2 diabetes, substrate oxidation and energy expenditure were affected by the type of intensity of acute aerobic exercise they were provided.

Materials and Methods: Nine men with type 2 diabetes (Mean ± SD; age 52.6 ± 0.36 years, Body Mass Index (BMI) = 30.3 ± 2.4) and 9 obese control group (Mean ± SD; age 49.1 ± 1.4 years, BMI = 31.3 ± 1.8) were participated in this study. In the first session, anthropometric measurements, body composition and maximum oxygen uptake (VO2 peak) were measured in all subjects. In the next sessions, subjects completed two acute aerobic exercises on separate days in a crossover design. The two exercise trials performed at intensity of 60% and 80% VO2 peak after fasting for at least 10 hours. Means of volume of oxygen (VO2) and Volume of Carbon dioxide (VCO2) were calculated during 30 minutes for measuring the rates of fat oxidation, carbohydrate oxidation and energy expenditure at each intensity.

Results: The results showed that substrate oxidation and energy expenditure were lower in the diabetic group (P < 0.05) compared to the control one. Also, the results revealed that carbohydrate oxidation and energy expenditure were statistically increased by providing high intensity rather than moderate intensity; however, fat oxidation was statistically increased by providing moderate intensity rather than high intensity (P < 0.05).

Conclusions: According to the results of the present study, aerobic exercise at moderate intensity and proper time can be considered as a special treatment to prevent diabetes complications and related disorders, particularly obesity.

1. Background

Type 2 diabetes and obesity are related to other metabolic disorders such as insulin resistance, high blood pressure, visceral obesity increase and metabolic syndrome with high danger of cardiovascular disease expansion (1). In this regard, a regular exercise program with proper intensity and time as well as an ideal diet can reduce metabolic disorders related to type 2 diabetes and also reduces the weight and improving insulin sensitivity (2). However, changes in fat and carbohydrate metabolism in skeletal muscles in obese and patients with type 2 diabetes are important. Previous studies have shown that fat oxidation and absorption in type 2 diabetic patients’ skeletal muscles has decreased in post-absorptive state (3) and during β-adrenergic stimulation (3, 4). Schenk et al. (2007) revealed that fat oxidation induced from physical exercise improves fatty acids induced insulin sensitivity disorders (5). Fat and carbohydrates are main sources to use during rest and physical activity which may change their contribution in providing energy considering the time and intensity of that physical activity, previous fitness, ingredients used in the days before activity, muscle glycogen, exercise and environmental conditions (6). Meanwhile, the intensity and duration of exercise is always one of the main factors in fat and carbohydrates oxidation (6, 7). Changes in the substrate take place with increasing exercise intensity. Different intensities of exercise have different effects on the fuel (6, 8). The amount of energy is related to the intensity and duration of activity (9). Generally, the duration and intensity of exercise required to produce a change in fat oxidation are not clear exactly (7). In spite of the fact that the fat utilization pattern among the healthy volunteers during physical activities has been properly investigated (10), little attention has been paid to study the fat utilization in type 2 diabetes during exercise. Kelly et al. (11, 12) demonstrated that obese individuals with type 2 diabetes show an increase in the whole-body fat and carbohydrate utilization as compared to the body fat-matched control individuals with moderate intensity exercise whereas the utilization of the plasma glucose increases and the muscle glycogen oxidation decreases. However, a study on lean individuals with type II diabetes showed an increase in the amount of carbohydrate while the exercise-induced fat oxidation decreased (13).

Moreover, patients with type 2 diabetes may observe a change in fat and carbohydrate oxidation and eventually their energy during physical exercise because of some special metabolic disorders (14). These changes have an effect on energy balance and metabolism of these kinds of patients.

No research has been done so far comparing the effects of moderate and high intensities of acute exercise on substrate oxidation and energy expenditure of male patients with type 2 diabetes. Therefore, the current study aimed to determine whether substrate oxidation and energy expenditure would be influenced by moderate- and high- intensity aerobic exercise in patients with type 2 diabetes.

2. Objectives

This study aimed to determine whether in patients with type 2 diabetes, substrate oxidation and energy expenditure were affected by the type of intensity of acute aerobic exercise they were provided.

3. Materials and Methods

The present study was performed on 9 male subjects with type 2 diabetes and 9 male obese control subjects. All the diabetic individuals followed a normal diet. Except for their diabetes, the considered subjects had no other serious health problems. Moreover, the subjects were withheld from the blood glucose-lowering medication for two days before the conduction of the experiment. Subject characteristics are indicated in Table 1. It should be noted that the related protocol was in compliance with the medical ethical review committee and the subjects gave a written informed consent.

Table 1. Mean ± Standard Deviation of Physical Properties a
Physical PropertiesObese SubjectsSubjects With Type 2 Diabetes
Age, y49.1 ± 1.452.6 ± 0.36
Height, m173.8 ± 5.3171.3 ± 6.7
Weight, kg93.7 ± 4.388.5 ± 4.7
BMI, kg/m231.3 ± 1.830.3 ± 2.4
Body fat, %31.2 ± 1.329.4 ± 2.09
VO2 peak, L/min2.8 ± 1.682.4 ± 0.36
VO2 peak, mL/kg/min41.3 ± 1.034.6 ± 3.93

a Abbreviation: BMI, body mass index.

3.1. Experimental Design

After determination of body composition and maximal aerobic power on a separate occasion, all subjects participated after fasting for at least 12 hours in a crossover design with participation in three supervised exercise sessions per week, 30 minutes at 60% of whole body peak oxygen uptake VO2 peak (moderate intensity) and 80% of VO2 peak (high intensity) the subjects were exposed to treadmill running test during two sessions with 1 week in between.

3.2. Body Composition

Subjects’ body compositions were measured using the bioelectric impedance method (Olympia 3.3, Jawn, Korean, 2000)

3.3. Maximal Aerobic Capacity

Before the measurements of maximal oxygen uptake (VO2 peak), subjects were informed about the test and instructed to exercise to their maximum limit. Familiarization with the treadmill (h/p/cosmos, Saturn, Germany), the warm up, and the VO2 max ramp procedure have been described in detail. Then VO2 peak was measured by the Bruce modified test (15).

3.4. Determination of Substrate Oxidation and Energy Expenditure

Breath-by-breath measurements were taken throughout the exercise using an automated gas-analysis system (GANSHORN, Germany). The gas analyzers were calibrated with a 4.95% CO2 -95.05% N2 gas mixture (BOC Gases, Surrey, UK), and the volume transducer was calibrated with a 1-liter calibration syringe (GANSHORN, Germany). Heart rate was recorded continuously by telemetry using a heart-rate monitor (Polar Vantage NV, Polar Electro Oy, Kempele, Finland).

Means of VO2 and VCO2 were calculated during each 30-minute protocol. With this method, the expired air was sampled for 1 minute at the 3, 10, 20 and 30 minutes time-points of each session to determine the rate of fat and carbohydrate oxidation across the duration of each constant load test. Then the amount of fat and carbohydrate oxidation was calculated using the following stoichiometric equation (16), and the amount of energy expenditure was calculated during each 30-minute protocol by equation of “Volpe and Bar-Or” (17). Assuming that the urinary nitrogen excretion rate was negligible.

Fat oxidation = 1.67 VO2 - 1.67 VCO2, carbohydrate oxidation = 4.55 VCO2 - 3.21 VO2, energy expenditure = 4.184 VO2. (1.23 RER + 3.815), where VO2 and VCO2 are reported as l minutes-1 and oxidation rate as g minutes-1, where energy expenditure is reported as k.j minutes-1. Energy expenditure was measured in kilo joules, but the data were reported in terms of calories.

3.5. Statistical Analysis

First, the normality of the data and the homoscedasticity were checked. The sphericity assumption was also tested using the Mauchly’s sphericity test. (Fat oxidation: Mauchly’s W = 0.63, P = 0.84 and carbohydrate oxidation: Mauchly’s W = 0.98, P = 0.92 and energy expenditure: Mauchly’s W = 0.89, P = 0.57). The data showed that the normality and sphericity were not violated; thus, parametrical statistical tests could be used. Fat oxidation, carbohydrate oxidation and energy expenditure were analyzed in a 2 (group) x (the crosshairs) 2 (intensity) analysis of variance (ANOVA) with repeated measures on the second factor. Also, independent t-test was used to compare two groups in different intensity and dependent variables. Statistical significance was set at P < 0.05.

4. Results

Means (±SD) of fat oxidation, carbohydrate oxidation and energy expenditure measures in different intensity for obese and type 2 diabetic individuals are listed in Table 2.

Table 2. Means ± Standard Deviations of Fat Oxidation, Carbohydrate Oxidation and Energy Expenditure Measures During Different Intensity in Obese and Type 2 Diabetic Subjects
Group/ IntensityFat Oxidation, g/minCarbohydrate Oxidation, g/minEnergy Expenditure, kg/min
60% VO2 peak0.37 ± 0.061.04 ± 0.28213.96 ± 22.08
80% VO2 peak0.11 ± 0.022.93 ± 0.51329.14 ± 50.02
Type 2 diabetes
60% VO2 peak0.29 ± 0.030.84 ± 0.28197.34 ± 16.28
80% VO2 peak0.08 ± 0.022.22 ± 0.56284.99 ± 31.43

4.1. Fat Oxidation

Fat oxidation was analyzed using a 2 X 2 (group X intensity) ANOVA with repeated measures on the second factor. This analysis indicated a significant main effect for groups, F (1, 16) = 5.16, p = 0.037, η2 = 0.244. The intensity main effect was also significant, F (16) = 75.60, p = 0.000, η2 = 0.825. Independent t-test was indicated that there was a significant difference between groups in fat oxidation in 60% intensity, t (16) = 3.36, P = 0.004, η2 = 0.41, and the fat oxidation rate was significantly superior in the obese individuals (M = 0.37, SD = 0.06) than the type 2 diabetic individuals (M = 0.29, SD = 0.03), but there was no significant difference between groups in fat oxidation in 80% intensity, t (16) = 0.69, P = 0.495, η2 = 0.03. The interaction of group X intensity was not significant, F (1, 16) = 0.881, P = 0.362, η2 = 0.052 (Figure 1).

4.2. Carbohydrate Oxidation

A two-way repeated-measure of variance on the intensity factor indicated that there were significant differences between groups (F (1, 16) = 7.85, P = 0.013, η2 = 0.329) and intensity (F (1, 16) = 172.21, P = 0.000, η2 = 0.915). The carbohydrate oxidation rate was higher during 80% intensity in obese individuals (M = 2.93, SD = 0.51) compared to individuals with type 2 diabetes (M = 2.22, SD = 0.56) (t (16) = 2.77, P = 0.014, η2 = 0.325), but during 60% intensity was not significant (t (16) = 1.48, P = 0.156, η2 = 0.122). The interaction of group x intensity was not significant F (1, 16) = 4.23, P = 0.056, η2 = 0.209 (Figure 2).

4.3. Energy Expenditure

There was a significant difference between groups (F (16) = 4.84, P = 0.043, η2 = 0.232) and intensity (F (1, 16) = 228.61, P = 0.000, η2 = 0.935) in energy expenditure rate. The energy expenditure rate was higher during 80% intensity in obese individuals (M = 329.14, SD = 50.02) compared to those with type 2 diabetes (M = 284.99, SD = 31.43) (t (16) = 2.24, P = 0.039, η2 = 0.239), but during 60% intensity was not significant (t (16) = 1.81, P = 0.088, η2 = 0.171). The interaction of group × intensity was not significant F (1, 16) = 4.21, P = 0.057, η2 = 0.208 (Figure 3).

5. Discussion

The results of the present study showed that the rate of fat oxidation in moderate intensity (60% vo2peak) compared to high intensity (80% Vo2peak) in type 2 male diabetic patients and the control group have been higher as well as the rate of carbohydrate oxidation of energy expenditure in high intensity compared to moderate intensity in type 2 male diabetic patients and the control group have been higher. Previous studies revealed that the absolute rate of carbohydrate oxidation has a positive correlation with the physical activity, while the fatty acid oxidation in healthy subjects has increased from resting state to almost 60% VO2max then gradually decreased to reach VO2max (18). Absolute and relative contributions of these fuels can be affected by nutrition, muscle glycogen content, exercise intensity, time and status (6).

Figure 1. The Rate of Fat Oxidation in Patients With Type 2 Diabetes and Obese Subjects in Moderate and High Intensity Acute Aerobic Exercise
Figure 2. The Rate of Carbohydrate Oxidation in Patients With Type 2 Diabetes and Obese Subjects in Moderate and High Intensity Acute Aerobic Exercise
Figure 3. The Rate of Energy Expenditure in Patients With Type 2 Diabetes and Obese Subjects in Moderate and High Intensity Acute Aerobic Exercise

The use of substrates can be rationalized by their availability. As it has been shown in healthy subjects, the increase of availability of blood sugar causes the increase of carbohydrate oxidation compared to fat oxidation (19) as well as the fat availability causes the increase of fat compared to carbohydrate (19).

Since fat is the main fuel in low and moderate intensities, the high rate of fat oxidation in moderate intensity compared to high intensity in type 2 diabetic patients in the present study can be explained (6, 7, 18, 20, 21); this is the same in carbohydrate oxidation in high intensity of physical activity. Also, because the time of activity was similar in both, the energy expenditure is higher considering the fact that material metabolism is higher in high rates (9, 22).

However, in moderate rate activities, the lipolysis speed triples because of the increase of beta-adrenergic stimulation (epinephrine) and decrease of insulin (23). Also, Re-esterified for example, the Re-Esterified triglycerides decreases (24) and the amount of adipose tissue blood flow increases which eventually causes the increase of the availability of fatty acids in plasma (23). Parallel to this study, Schenk et al. (2007) have shown that the fat oxidation of the physical activity improves the disorders of fatty acid-induced insulin sensitivity (5).

Since the high rate of available systematic fatty acids absorbed by skeletal muscle acts as a key mediator for insulin resistance in obesity and diabetes (25-27). Also, resistance to insulin induced by fatty acids is largely determined by extra fatty acid detachment in muscle cells for intracellular fatty acid metabolites’ saving, oxidation or aggregation (27-29). Resistance to insulin induced of fat increase in diabetic patients can decrease by such a physical activity in which fat oxidation occurs in a high rate (5, 30, 31).

Previous studies have shown that the fat oxidation increase due to physical activity (32) can improve insulin sensitivity (29, 33). Moderate physical activity causes pyruvate dehydrogenase activity’s decrease which increases fat oxidation (34). Recent researches have revealed that low capacity of fat oxidation may be the main reason for increase of insulin resistance (35, 36). Generally, the results of this study showed that moderate physical activity causes an increase in the rate of fat oxidation in patients with type 2 diabetes, which decreases insulin resistance.

The other results of this study showed that the rate of fat and carbohydrate oxidation and energy expenditure in moderate and high intensities in patients with type 2 diabetes is lower than the control group (fat subjects). However, the rate of carbohydrate oxidation and energy expenditure in moderate intensity between the two groups showed no significant difference. The results of this study are partly similar to those of Ghanassia et al. (2006) (37).

Some of the previous studies have not observed any significant difference between diabetic subjects and obese subject in substrate oxidation rate, which differ from the results of this study (38-40). The reason of this difference can be related to the type of exercise protocol and its intensity. It should be mentioned that the previous studies had different subjects in case of age, gender and weight.

Muscle contraction and the production of catecholamines are those mechanisms that cause metabolic adaptation during physical activity (41). These mechanisms cause decrease in insulin secretion and increase in glucagon production via afferent which enhances the available energy substrates by EPG increase and glucose absorption.

Meanwhile lipolysis in adipose tissue of insulin-induced decreases (42, 43). Impaired insulin secretion and glucose specific to type 2 diabetes can affect the use of substrate during physical activity (44).

Considering metabolic disorders in patients with type 2 diabetes (14) and the equality of all the subjects of this study in terms of age, gender and weight, the decrease of the fat and carbohydrate oxidation and energy expenditure in moderate and high intensity in patients with type 2 diabetes compared to the control group can be related to diabetic metabolic disorders (37). Metabolic disorders can reduce substrate consumption in patients with type 2 diabetes compared to healthy subjects. Small sample size was one of the limitations of this study. In the present study it should be noted that due to the considered criteria for inclusion of the tested in this experiment (a given age limit, blood sugar limit, duration of diabetes, lack of cardiovascular diseases, lack of muscular diseases, etc.), it was not possible to select a wide range of samples in terms of the above-mentioned criteria used in the this study. It has been suggested to do the same study with a larger sample sizes.

Generally, with control of type 2 diabetic patients’ blood sugar, some of the neuropathic and micro angiopathic effects may be prevented which causes the reduction of some cardiovascular diseases in such patients. Also, obesity can cause some metabolic disorders such as poor glucose tolerance and cardiovascular disease in patients with type 2 diabetes. Therefore, physical activity with proper intensity and time may be considered as an adjunctive treatment to prevent these effects and disorders.




  • 1.

    Klein S, Burke LE, Bray GA, Blair S, Allison DB, Pi-Sunyer X, et al. Clinical implications of obesity with specific focus on cardiovascular disease: a statement for professionals from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism: endorsed by the American College of Cardiology Foundation. Circulation. 2004; 110(18) : 2952 -67 [DOI][PubMed]

  • 2.

    Ishii T, Yamakita T, Sato T, Tanaka S, Fujii S. Resistance training improves insulin sensitivity in NIDDM subjects without altering maximal oxygen uptake. Diabetes Care. 1998; 21(8) : 1353 -5 [PubMed]

  • 3.

    Kelley DE, Simoneau JA. Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest. 1994; 94(6) : 2349 -56 [DOI][PubMed]

  • 4.

    Blaak EE, Wagenmakers AJ, Glatz JF, Wolffenbuttel BH, Kemerink GJ, Langenberg CJ, et al. Plasma FFA utilization and fatty acid-binding protein content are diminished in type 2 diabetic muscle. Am J Physiol Endocrinol Metab. 2000; 279(1) : E146 -54 [PubMed]

  • 5.

    Schenk S, Horowitz JF. Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest. 2007; 117(6) : 1690 -8 [DOI][PubMed]

  • 6.

    Venables MC, Achten J, Jeukendrup AE. Determinants of fat oxidation during exercise in healthy men and women: a cross-sectional study. J Appl Physiol (1985). 2005; 98(1) : 160 -7 [DOI][PubMed]

  • 7.

    Achten J, Jeukendrup AE. Optimizing fat oxidation through exercise and diet. Nutrition. 2004; 20(7-8) : 716 -27 [DOI][PubMed]

  • 8.

    Coyle EF. Substrate utilization during exercise in active people. Am J Clin Nutr. 1995; 61(4 Suppl) : 968S -79S [PubMed]

  • 9.

    Brooks GA, Fahey TD. Exercise Physiology: Human Bioenergetics and Its Applications. 2001;

  • 10.

    Spriet LL. Regulation of fat/carbohydrate interaction in human skeletal muscle during exercise. Adv Exp Med Biol. 1998; 441 : 249 -61 [PubMed]

  • 11.

    Kang J, Kelley DE, Robertson RJ, Goss FL, Suminski RR, Utter AC, et al. Substrate utilization and glucose turnover during exercise of varying intensities in individuals with NIDDM. Med Sci Sports Exerc. 1999; 31(1) : 82 -9 [PubMed]

  • 12.

    Colberg SR, Hagberg JM, McCole SD, Zmuda JM, Thompson PD, Kelley DE. Utilization of glycogen but not plasma glucose is reduced in individuals with NIDDM during mild-intensity exercise. J Appl Physiol (1985). 1996; 81(5) : 2027 -33 [PubMed]

  • 13.

    Martin IK, Katz A, Wahren J. Splanchnic and muscle metabolism during exercise in NIDDM patients. Am J Physiol. 1995; 269(3 Pt 1) : E583 -90 [PubMed]

  • 14.

    Perez-Martin A, Raynaud E, Mercier J. Insulin resistance and associated metabolic abnormalities in muscle: effects of exercise. Obes Rev. 2001; 2(1) : 47 -59 [PubMed]

  • 15.

    Bruce RA, Kusumi F, Hosmer D. Maximal oxygen intake and nomographic assessment of functional aerobic impairment in cardiovascular disease. Am Heart J. 1973; 85(4) : 546 -62 [PubMed]

  • 16.

    Frayn KN. Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol Respir Environ Exerc Physiol. 1983; 55(2) : 628 -34 [PubMed]

  • 17.

    Volpe Ayub B, Bar-Or O. Energy cost of walking in boys who differ in adiposity but are matched for body mass. Med Sci Sports Exerc. 2003; 35(4) : 669 -74 [DOI][PubMed]

  • 18.

    Lima-Silva AE, Bertuzzi RC, Pires FO, Gagliardi JF, Barros RV, Hammond J, et al. Relationship between training status and maximal fat oxidation rate. J Sports Sci Med. 2010; 9(1) : 31 -5 [PubMed]

  • 19.

    Horowitz JF, Mora-Rodriguez R, Byerley LO, Coyle EF. Lipolytic suppression following carbohydrate ingestion limits fat oxidation during exercise. Am J Physiol. 1997; 273(4 Pt 1) : E768 -75 [PubMed]

  • 20.

    Riddell MC, Jamnik VK, Iscoe KE, Timmons BW, Gledhill N. Fat oxidation rate and the exercise intensity that elicits maximal fat oxidation decreases with pubertal status in young male subjects. J Appl Physiol (1985). 2008; 105(2) : 742 -8 [DOI][PubMed]

  • 21.

    Venables MC, Jeukendrup AE. Endurance training and obesity: effect on substrate metabolism and insulin sensitivity. Med Sci Sports Exerc. 2008; 40(3) : 495 -502 [DOI][PubMed]

  • 22.

    Gore CJ, Withers RT. The effect of exercise intensity and duration on the oxygen deficit and excess post-exercise oxygen consumption. Eur J Appl Physiol Occup Physiol. 1990; 60(3) : 169 -74 [PubMed]

  • 23.

    Wolfe RR, Klein S, Carraro F, Weber JM. Role of triglyceride-fatty acid cycle in controlling fat metabolism in humans during and after exercise. Am J Physiol. 1990; 258(2 Pt 1) : E382 -9 [PubMed]

  • 24.

    Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E, et al. Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol. 1993; 265(3 Pt 1) : E380 -91 [PubMed]

  • 25.

    Boden G, Lebed B, Schatz M, Homko C, Lemieux S. Effects of acute changes of plasma free fatty acids on intramyocellular fat content and insulin resistance in healthy subjects. Diabetes. 2001; 50(7) : 1612 -7 [PubMed]

  • 26.

    Bachmann OP, Dahl DB, Brechtel K, Machann J, Haap M, Maier T, et al. Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes. 2001; 50(11) : 2579 -84 [PubMed]

  • 27.

    Itani SI, Ruderman NB, Schmieder F, Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes. 2002; 51(7) : 2005 -11 [PubMed]

  • 28.

    Lee JS, Pinnamaneni SK, Eo SJ, Cho IH, Pyo JH, Kim CK, et al. Saturated, but not n-6 polyunsaturated, fatty acids induce insulin resistance: role of intramuscular accumulation of lipid metabolites. J Appl Physiol (1985). 2006; 100(5) : 1467 -74 [DOI][PubMed]

  • 29.

    Todd MK, Watt MJ, Le J, Hevener AL, Turcotte LP. Thiazolidinediones enhance skeletal muscle triacylglycerol synthesis while protecting against fatty acid-induced inflammation and insulin resistance. Am J Physiol Endocrinol Metab. 2007; 292(2) : E485 -93 [DOI][PubMed]

  • 30.

    Ropelle ER, Pauli JR, Prada PO, de Souza CT, Picardi PK, Faria MC, et al. Reversal of diet-induced insulin resistance with a single bout of exercise in the rat: the role of PTP1B and IRS-1 serine phosphorylation. J Physiol. 2006; 577(Pt 3) : 997 -1007 [DOI][PubMed]

  • 31.

    Oakes ND, Bell KS, Furler SM, Camilleri S, Saha AK, Ruderman NB, et al. Diet-induced muscle insulin resistance in rats is ameliorated by acute dietary lipid withdrawal or a single bout of exercise: parallel relationship between insulin stimulation of glucose uptake and suppression of long-chain fatty acyl-CoA. Diabetes. 1997; 46(12) : 2022 -8 [PubMed]

  • 32.

    Votruba SB, Atkinson RL, Hirvonen MD, Schoeller DA. Prior exercise increases subsequent utilization of dietary fat. Med Sci Sports Exerc. 2002; 34(11) : 1757 -65 [DOI][PubMed]

  • 33.

    Pinnamaneni SK, Southgate RJ, Febbraio MA, Watt MJ. Stearoyl CoA desaturase 1 is elevated in obesity but protects against fatty acid-induced skeletal muscle insulin resistance in vitro. Diabetologia. 2006; 49(12) : 3027 -37 [DOI][PubMed]

  • 34.

    Kimber NE, Heigenhauser GJ, Spriet LL, Dyck DJ. Skeletal muscle fat and carbohydrate metabolism during recovery from glycogen-depleting exercise in humans. J Physiol. 2003; 548(Pt 3) : 919 -27 [DOI][PubMed]

  • 35.

    Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med. 2004; 350(7) : 664 -71 [DOI][PubMed]

  • 36.

    Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003; 34(3) : 267 -73 [DOI][PubMed]

  • 37.

    Ghanassia E, Brun JF, Fedou C, Raynaud E, Mercier J. Substrate oxidation during exercise: type 2 diabetes is associated with a decrease in lipid oxidation and an earlier shift towards carbohydrate utilization. Diabetes Metab. 2006; 32(6) : 604 -10 [DOI][PubMed]

  • 38.

    Blaak EE, van Aggel-Leijssen DP, Wagenmakers AJ, Saris WH, van Baak MA. Impaired oxidation of plasma-derived fatty acids in type 2 diabetic subjects during moderate-intensity exercise. Diabetes. 2000; 49(12) : 2102 -7 [PubMed]

  • 39.

    Borghouts LB, Wagenmakers AJ, Goyens PL, Keizer HA. Substrate utilization in non-obese Type II diabetic patients at rest and during exercise. Clin Sci (Lond). 2002; 103(6) : 559 -66 [PubMed]

  • 40.

    Zakrzewski JK, Tolfrey K. Comparison of fat oxidation over a range of intensities during treadmill and cycling exercise in children. Eur J Appl Physiol. 2012; 112(1) : 163 -71 [DOI][PubMed]

  • 41.

    Viru A. Plasma hormones and physical exercise. Int J Sports Med. 1992; 13(3) : 201 -9 [DOI][PubMed]

  • 42.

    Frayn KN. The glucose-fatty acid cycle: a physiological perspective. Biochem Soc Trans. 2003; 31(Pt 6) : 1115 -9 [PubMed]

  • 43.

    Kiens B. Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev. 2006; 86(1) : 205 -43 [DOI][PubMed]

  • 44.

    Riddell MC, Bar-Or O, Wilk B, Parolin ML, Heigenhauser GJ. Substrate utilization during exercise with glucose and glucose plus fructose ingestion in boys ages 10--14 yr. J Appl Physiol (1985). 2001; 90(3) : 903 -11 [PubMed]

  • Copyright © 2015, Ahvaz Jundishapur University of Medical Sciences. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.