Diabetes Care 25:445-452, 2002
© 2002 by the American Diabetes Association, Inc.
Clinical Care/Education/Nutrition Original Article |
Intensive Lifestyle Changes Are Necessary to Improve Insulin Sensitivity
A randomized controlled trial
Kirsten A. McAuley, MBCHB1,
Sheila M. Williams, BSC2,
Jim I. Mann, DM, PHD1,
Ailsa Goulding, PHD, FACN3,
Alex Chisholm, PHD1,
Noela Wilson, PHD4,
Gretchen Story, BPHED1,
Rebecca T. McLay, MSC1,
Michelle J. Harper, BSC1 and
Ianthe E. Jones, MSC3
1 Department of Human Nutrition, Otago University, Dunedin, New Zealand
2 Department of Preventive and Social Medicine, Otago University, Dunedin, New Zealand
3 Department of Medical and Surgical Sciences, Otago University, Dunedin, New Zealand
4 Life in New Zealand Activity and Health Research Unit, Otago University, Dunedin, New Zealand.
 |
ABSTRACT
|
|---|
OBJECTIVEThe extent to which lifestyle must be altered to improve insulin sensitivity has not been established. This study compares the effect on insulin sensitivity of current dietary and exercise recommendations with a more intensive intervention in normoglycemic insulin-resistant individuals.
RESEARCH DESIGN AND METHODSSeventy-nine normoglycemic insulin-resistant (determined by the euglycemic insulin clamp) men and women were randomized to either a control group or one of two combined dietary and exercise programs. One group (modest level) was based on current recommendations and the other on a more intensive dietary and exercise program. Insulin sensitivity was measured using a euglycemic insulin clamp, body composition was measured using dual-energy X-ray absorptiometry, and anthropometry and aerobic fitness were assessed before and after a 4-month intervention period. Four-day dietary intakes were recorded, and fasting glucose, insulin, and lipids were measured.
RESULTSOnly the intensive group showed a significant improvement in insulin sensitivity (23% increase, P=0.006 vs. 9% in the modest group, P=0.23). This was associated with a significant improvement in aerobic fitness (11% increase in the intensive group, P=0.02 vs. 1% in the modest group, P=0.94) and a greater fiber intake, but no difference in reported total or saturated dietary fat.
CONCLUSIONSCurrent clinical dietary and exercise recommendations, even when vigorously implemented, did not significantly improve insulin sensitivity; however, a more intensive program did. Improved aerobic fitness appeared to be the major difference between the two intervention groups, although weight loss and diet composition may have also played an important role in determining insulin sensitivity.
Abbreviations: DXA, dual-energy X-ray absorptiometry Gbw, glucose infused for total body weight Gffm, glucose infused for fat-free mass IGT, impaired glucose tolerance OGTT, oral glucose tolerance test VLCD, very lowcalorie diet
 |
INTRODUCTION
|
|---|
Lifestyle intervention reduces the risk of progression from impaired glucose tolerance (IGT) to type 2 diabetes (1). It is widely assumed that current advice regarding physical activity (2) and dietary modification (3) is sufficient (presumably mediated via an improvement in insulin sensitivity) to reduce the risk of type 2 diabetes. All the large intervention trials either underway or completed have focused on intervention in subjects with IGT (1,4,5). However, it appears that once abnormal glucose levels have developed, significant ß-cell dysfunction has already occurred, and there is less chance of improving insulin sensitivity (6).
Intervention before IGT has developed may offer the best opportunity to reduce progression to IGT and type 2 diabetes. Although increased physical activity and dietary modification have been shown to improve insulin sensitivity, there are no data that clearly show the extent of lifestyle change required. This study is the first to compare two levels of practical lifestyle intervention in normoglycemic insulin-resistant individuals on insulin sensitivity, one based on current recommendations (modest) and the other on a more intensive dietary and exercise program. This will help to answer the important question as to whether more aggressive lifestyle intervention is more beneficial. In this study, participants were randomized to either a control group or one of two intervention groups.
 |
RESEARCH DESIGN AND METHODS
|
|---|
Eligibility
A total of 440 volunteers responded to local advertisements. Participants were eligible to be screened if they met the following criteria: aged 2570 years, able and willing to take part in a dietary and exercise program (7), and no personal history of diabetes or any major medical condition, psychiatric illness, or drug or alcohol dependence. Those on warfarin or oral steroids were excluded, but those on other medications were included if they had been treated for >6 months and were unlikely to alter the medication during the intervention period. Screening involved measurement of fasting glucose, insulin, and triglycerides. Those with fasting glucose <6.1 mmol/l and poor insulin sensitivity (n=140) based on our published prediction equation (8) were eligible for a euglycemic insulin clamp. Those with an insulin sensitivity index 4.2 G · mU-1 · l-1 (G=glucose infused in mg · kg-1 · min-1) were invited to enter the intervention study. This cutoff represented the lowest 25th centile of a lean population (BMI <27 kg/m2). Seventy-nine Caucasian men and women were eligible and gave informed consent for the study, which was approved by the Otago Ethics Committee. Screening and recruitment occurred between February 1999 and August 2000. Participants were randomized to the three groups in blocks of nine (so that entry to the study could be staggered) after stratification for sex and degree of insulin sensitivity.
Dietary intervention
The modest dietary program was intended to reflect present dietary advice, and the intensive diet aimed to achieve an even lower total and saturated fat intake, lower dietary cholesterol, and a higher fiber intake. The modest program aimed to achieve a diet in which <32% of total energy was from fat, 11% was from saturated fat, 14% was from monounsaturated fat, 7% was from polyunsaturated fat, 50% was from carbohydrates, and 18% was from protein. Cholesterol targets were <200 mg per day and dietary fiber >25 g per day. The intensive diet aimed for <26% of total energy from fat, <6% from saturated fat, 13% from monounsaturated fat, 7% from polyunsaturated fat, 55% from carbohydrates, and 18% from protein. Cholesterol targets were <140 mg/day and dietary fiber >35 g/day. In addition to these macronutrient goals, foods rich in nutrients believed to enhance insulin sensitivity were specified for each diet (9); the modest and intensive groups were required to have three or seven such foods daily, respectively. Study foods included low glycemic index foods, fish, nuts, seeds, grains, pasta, rice, fruit, vegetables, legumes, and low-fat dairy foods. The diets were individually prescribed and based on each participants usual intake or an energy level designed to lead to gradual and sustained weight reduction. Compliance was assessed by a 4-day diet record at baseline, 2 months, and 4 months and by a daily record sheet, where type and amount of recommended foods were recorded. Diet records were analyzed using Diet Cruncher for Macintosh (Version 1.1.0; Marshall-Seeley, Dunedin, New Zealand), which used food composition data from the New Zealand Institute for Crop and Food Research (10). No modifications were made to the database. Foods not in the database were coded so that the same substitutions were made throughout, and participants were asked to supply recipes so that individual ingredients were entered and analyzed in the appropriate quantity. Some food was supplied free of charge (cereals, low fat spread, and canola oil), and all dietary information, including lists of suitable foods, sample eating plans, foods to be avoided, cooking and preparation advice, and recipes, was provided.
Exercise intervention
At baseline, assessment of recent participation in physical activity was based on the Life in New Zealand validated questionnaire (11). The individually designed exercise program was planned to incorporate 30 min of activity 5 days/week (at different intensities, depending on group) and took into account preferred activities. An exercise consultant exercised with each participant in an individual or group situation at least once per week to ensure that appropriate activities were chosen and that motivation and compliance were enhanced. The modest exercise intervention program was based on current health promotion recommendations for activity, which do not specify heart rate targets (2). The intense exercise intervention program aimed to meet the 1990 American College of Sports Medicine guidelines for developing and maintaining cardiorespiratory and muscular fitness (12). Participants were encouraged to train five times per week for at least 20 min per session at an intensity of 8090% of age-predicted maximum heart rate. A gym membership was provided for participants in the intensive program to encourage participation in vigorous activity and involvement in resistance training at least twice per week. Type and duration of physical activity was recorded by participants for both intervention groups on a daily sheet (collected weekly). The control group was asked to continue their usual diet and exercise during the 4-month experimental period.
Clinical visits
At the time of the euglycemic insulin clamp study, fasting blood samples were taken for lipid measurements, and anthropometry and blood pressure measurements were repeated. Participants were randomized to one of the three groups, and within 1 week, they had a dual-energy X-ray absorptiometry (DXA) scan and an exercise test. All of these measures constituted baseline data. Intervention was commenced as soon as all baseline measures were collected. Participants in the intervention groups were seen by the researchers weekly for a weight measurement and a brief dietary and exercise assessment. If participants did not attend, they were contacted by phone, their progress was discussed, and a further appointment was made. At each monthly interval, participants in the intervention groups had the following measurements: weight, waist, and hip measurements, blood pressure, a fasting blood test for glucose, an insulin and lipid profile, and a 1-mile walk test. No contact was made with the control group until the end of the 4-month period, when baseline measures were repeated on all participants.
Methodology for outcome measures
The procedure for measuring waist and hip circumference, blood pressure, fasting insulin, glucose, and lipids has been previously described (8). Weight was measured using the same set of calibrated electronic scales, and all participants were weighed without shoes or heavy clothing. The last 50% of participants recruited had an oral glucose tolerance test (OGTT), which involved ingestion of a solution containing 75 g dextrose after a 10-h overnight fast, followed by a venous blood glucose drawing at 120 min (13). Body composition was measured using DXA, which is a sensitive test to quantitate changes in lean and fat mass in vivo (14) and to assess regional fat distribution (15). Total body scans were obtained on the same Lunar DPXL (Lunar, Madison, WI) scanner at baseline and at the end of the study on all participants weighing <120 kg, using patient positioning and scan speeds recommended by the manufacturer. All scans were analyzed with software package l.35 (Lunar). Coefficients of variation were 2.6% for fat mass, 2.5% for total body fat percentage, <3% for regional fat measures, and 0.88% for lean mass (15).
Insulin sensitivity was measured using the euglycemic insulin clamp, infusing insulin (Actrapid) at 40 mU · m2 · min1 and maintaining the blood glucose levels as close to 4.5 mmol/l as possible (8). The extent to which adipose tissue contributes to glucose disposal is controversial; therefore, we have expressed the glucose infused (G) for total body weight (Gbw) and glucose infused for fat-free mass (Gffm) calculated from the DXA (Gffm=Gbw · weight1 · lean body mass1) in mg · kg1 · min1. Gbw and Gffm are reported alone and divided by the average insulin (i) level during the final 60 min of the test (Gbw/i and Gffm/i), in G · mU1 · l1. A V 2max· test was considered inappropriate in sedentary overweight adults; therefore, aerobic fitness was estimated using a submaximal walk test on a motorized treadmill (Quinton Series 90 Q65; Quinton Instrument, Seattle, WA) based on a modified Bruce protocol (16). The test was terminated when the target heart rate (75% of age-predicted maximum) was reached or exercise could not be continued. Those on ß-blocker medication were excluded. Minute ventilation (VE), oxygen consumption (V 2), and carbon dioxide production (VCO2) were measured by open spirometry/indirect calorimetry (Sensormedics Metabolic Cart 2900Z BXB; Sensormedics, Anaheim, CA). The gas analyzer was calibrated before each test with standard mixtures. The average heart rate and V 2 were calculated for the last minute of each 3-min stage. A stage was included if the subject completed >2 min. If heart rates were <100 bpm, then only stages in which heart rate increased at least 5 bpm compared with the previous stage were used in the estimated V 2max. Heart rate was plotted against V 2, and the predicted V 2max was determined by extrapolation to the estimated maximal heart rate. Exercise tests were excluded from this analysis if less than three stages had been completed or when there was incomplete gas collection.
Statistical methods
Sample size calculations were based on an estimate of the SD of the log-transformed insulin sensitivity index (Gffm/i), which was 0.25. Thus, a sample size of 25 in the three groups would give an 80% chance of detecting a 20% improvement in Gffm/i using the 5% level of significance. Regression analysis with the baseline measure as a covariate was used to compare the treatment groups with the control group. STATA statistical software Version 7.0 (Stata, College Station, Texas) was used. All major end points were assessed without knowledge of treatment groups.
 |
RESULTS
|
|---|
The age and sex of the groups are included in Fig. 1, which also shows the progress of participants through the trial, including dropouts and those not completing each outcome measure. Five subjects were smokers and continued to smoke over the 4-month intervention. Of those who had an OGTT, two had a 2-h glucose value 7.8 mmol/l.
Insulin sensitivity changed significantly in the intensive group only (Table 1). This occurred in parallel with reductions in weight, waist circumference, BMI, systolic and diastolic blood pressure (Table 2), total and truncal fat (Table 1), increased reported dietary fiber, and increased aerobic fitness (Table 3). Both groups reduced intakes of total energy, total fat, saturated fat, and cholesterol. Attendance to supervised exercise sessions was similar for both intervention groups (>70%), and compliance based on self-reported daily tick sheets was high, with both groups meeting the exercise targets of 5 days/week.
View this table:
[in this window]
[in a new window]
|
Table 1 Baseline and final measures for DXA and euglycemic insulin clamp measures for the control (C), modest (M), and intensive (I) intervention groups
|
|
View this table:
[in this window]
[in a new window]
|
Table 2 Baseline and final measures for clinical and biochemical variables for the control (C), modest (M), and intensive (I) intervention groups
|
|
View this table:
[in this window]
[in a new window]
|
Table 3 Baseline and final measures for dietary and exercise variables for the control (C), modest (M), and intensive (I) intervention groups
|
|
 |
CONCLUSIONS
|
|---|
Resistance to the action of insulin is an important precursor of IGT and type 2 diabetes (17). It is widely believed that current dietary and exercise recommendations will improve insulin sensitivity to an extent great enough to reduce the risk of type 2 diabetes. However, the evidence that such relatively modest lifestyle changes will improve insulin sensitivity is limited. We have compared the effect on insulin sensitivity of a modest lifestyle change (reflecting current public health promotion messages) with a more intensive program. The intensive program resulted in an appreciable improvement in insulin sensitivity when compared with the control group (23% when infused glucose was expressed for total body weight, 16% when expressed for lean mass). Indeed, the effect of the intervention may have been underestimated because insulin sensitivity tended to improve in the control group. In contrast, the tendency toward improved insulin sensitivity in the modest group did not differ appreciably from that of the control subjects. These findings have profound implications for public health because it appears that current advice, even when vigorously implemented, did not significantly influence a major underlying abnormality of type 2 diabetes in this study. When compared with the control group, participants in both the modest and the intensive group reduced total and truncal fat and waist circumference without reducing lean mass. These changes were accompanied by statistically significant reductions in systolic and diastolic blood pressure. Fasting insulin and triglyceride levels were also lower after the intervention, but not significantly so, perhaps because levels tended to also fall in the control group. HDL cholesterol was lower in both groups after the intervention, perhaps due to weight loss and restriction of dietary fat. Although the change in body composition, blood pressure, and metabolic variables was more marked in the intensive than the modest group, the differences were not striking and did not achieve statistical significance. Failure to demonstrate more marked differences in these measures between the two interventions groups may be due to the fact that the two groups made fairly similar dietary changes with regard to important dietary variables other than dietary fiber, which increased to a greater extent in the intensive group. On the other hand, measures of aerobic physical fitness (V 2max and heart rate) differed appreciably between the two intervention groups. The standard advice of exercise for 30 min at least five times weekly (with no specific advice regarding intensity) appeared to have little effect, whereas the advice given to the intensive group has appreciably influenced all measures of aerobic fitness. As this is the main aspect of the intervention program that appears to differ significantly between the two intervention groups, it seems likely that this is one of the major factors accounting for the improved insulin sensitivity observed among those in the intensive program.
There is no doubt that weight loss leads to a reduction in resistance to the action of insulin (18,19). However, in this study, the difference in weight loss on the two programs did not achieve statistical significance. Goodpaster et al. (18) achieved a 15-kg weight loss and a 24% increase in insulin sensitivity in 32 obese men and women maintained on a very lowcalorie diet (VLCD). However, such an approach is neither a practical option for widespread adoption, nor is it desirable. The VLCD was associated with a loss in lean body mass of 2.1 kg in women and 4.6 kg in men. Ross et al. (20) found either diet- or exercise-induced weight loss achieved a similar improvement in insulin sensitivity when the amount of total fat loss was also similar. Information regarding the effect of specific foods or nutrients independent of weight change is sparse. Saturated fatty acids (especially palmitic acid), reduced levels of -linolenic acid, a low ratio of n-3 to n-6 fatty acids, and a high proportion of dihomo linolenic acid have been shown to be positively correlated with insulin resistance (21,22). In the only carefully controlled intervention trial, Vessby et al. (232) found a 10% reduction in insulin sensitivity when monounsaturated fatty acids were replaced by saturated fatty acids. However, this effect appeared to operate only when total fat intake was <38% total energy.
Aerobic exercise has been shown to improve insulin sensitivity (23), but there is less information regarding the precise level or frequency required. Yamanouchi et al. (24) compared two groups of hospitalized obese people with diabetes, all of whom made similar dietary changes. One group walked 4,500 steps per day, the other 19,200 steps per day. The glucose infusion rate during a euglycemic insulin clamp did not improve in the modest exercise group but increased 34% in the group that walked further. Although the latter group also achieved greater weight reduction, multiple regression analysis showed that only the effect of walking was significant on measures of insulin action. Similar findings have been made earlier by Bogardus et al. (25), who demonstrated that obese diabetic subjects on diet only did not improve glucose infusion rates, but diet and exercise (at 75% V 2max) did. In this study, weight loss was the same for both groups. The Da Qing IGT and Diabetes Study found a similar reduction in those converting to diabetes on a diet only, exercise only, or combined program. They concluded that the efficacy of the diet was similar to that of exercise, and there was no additional benefit of combination therapy, despite a greater reduction in BMI (1). The recent results of the Finnish Diabetes Prevention Study showed that after a mean follow-up of 3.2 years, a combined diet and exercise program reduced conversion from IGT to type 2 diabetes from 23% in the control group to 11% in the intervention group (4). Thus, existing data do not enable us to determine the component of our intensive exercise program that accounted for the improvement in insulin sensitivity. However, our data do suggest that an intervention program that does not include a substantial increase in physical activity in addition to modest weight loss may not produce an appreciable improvement in insulin sensitivity. Furthermore, the level of physical activity required is greater than that currently recommended for the general population.
These data have important public health implications in countries with high rates of type 2 diabetes, and they have a bearing on intervention trials involving people with IGT. In those who have already developed IGT and are prescribed modest exercise as part of their program, it appears that a substantial number will still go on to develop type 2 diabetes (1). The greatest benefit of lifestyle intervention may be seen when instituted in insulin-resistant individuals who have not yet developed IGT and who have achieved an improved level of aerobic fitness.
 |
Acknowledgments
|
|---|
Acknowledgments
This study was funded by the Health Research Council, Otago University, and the Otago Diabetes Research Trust, New Zealand.
Many thanks to Maggie Oakley and Ashley Duncan for technical assistance.
 |
Footnotes
|
|---|
Address correspondence and reprint requests to Dr. Kirsten McAuley, Department of Human Nutrition, Otago University, P.O. Box 56, Dunedin, New Zealand. E-mail: kirsten.mcauley{at}stonebow.otago.ac.nz.
Received for publication 23 May 2001 and accepted in revised form 6 December 2001.
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.
 |
References
|
|---|
-
Pan X, Li G, Hu Y, Wang J, Yang W, An Z, Hu Z, Lin J, Xiao J, Cao H, Liu P, Jiang X, Jiang Y, Wang J, Zheng H, Zhang H, Bennett P, Howard B: Effects of diet and exercise in preventing NIDDM in people with impaired glucose tolerance: the Da Qing IGT and Diabetes Study. Diabetes Care 20:537544, 1997[Abstract]
-
Pate R, Pratt M, Blair SN, Haskell WL, Macera CA, Bouchard C, Buchner D, Ettinger W, Heath GW, King AC, et al.: Physical activity and public health: a recommendation from the Centres for Disease Control and Prevention and the American College of Sports Medicine. JAMA 273:402407, 1995[Abstract]
-
Krauss RM, Eckel RH, Howard B, Appel LJ, Daniels SR, Deckelbaum RJ, Erdman JW Jr, Kris-Etherton P, Goldberg IJ, Kotchen TA, Lichtenstein AH, Mitch WE, Mullis R, Robinson K, Wylie-Rosett J, St Jeor S, Suttie J, Tribble DL, Bazzarre TL: Revision 2000: a statement for healthcare professionals from the Nutrition Committee of the American Heart Association. J Nutr 131:132146, 2001[Free Full Text]
-
Tuomilehto J, Lindstrom J, Eriksson J, Valle T, Hamalainen H, Ilanne-Parikka P, Keinanen-Kiukaanniemi S, Laakso M, Louheranta A, Rastas M, Salminen V, Uusitupa M: Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 344:13431350, 2001[Abstract/Free Full Text]
-
The Diabetes Prevention Program Research Group: The Diabetes Prevention Program: design and methods for a clinical trial in the prevention of type 2 diabetes. Diabetes Care 22:623631, 1999[Abstract]
-
Proietto J, Andrikopoulos S, Rosella G, Thorburn A: Understanding the pathogenesis of type 2 diabetes. Can we get off the metabolic merry-go-rounds? Aust N Z J Med 25:870875, 1995[Medline]
-
Thomas S, Reading J, Shepard R: Revision of the physical activity readiness questionnaire (PAR-Q). Can J Sport Sci 1996:338345, 1996
-
McAuley K, Williams S, Mann J, Walker R, Lewis-Barned N, Temple L, Duncan A: Diagnosing insulin resistance in the general population. Diabetes Care 24:460464, 2001[Abstract/Free Full Text]
-
Riccardi G, Rivellese AA: Dietary treatment of the metabolic syndrome: the optimal diet. Br J Nutr 83 (Suppl. 1):S143S148, 2000
-
New Zealand Institute of Crop and Food Research: The New Zealand Food Composition Database. Palmerston North, New Zealand, New Zealand Institute of Crop and Food Research, 1993
-
Hopkins W, Wilson N, Russell D: Validation of the physical activity instrument for the Life in New Zealand national survey. Am J Epidemiol 133:7382, 1991[Abstract/Free Full Text]
-
American College of Sports Medicine Position Stand: The recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness in healthy adults. Med Sci Sports Exerc 22:265274, 1990[Medline]
-
Alberti K, Zimmet P: Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and Classification of Diabetes Mellitus Provisional Report of a WHO Consultation. Diabet Med 15:539553, 1998[Medline]
-
Going S: Detection of small changes in body composition by dual-energy X-ray absorptiometry. Am J Clin Nutr 57:845850, 1993[Abstract/Free Full Text]
-
Taylor R, Keil D, Gold E, Williams S, Goulding A: Body mass index, waist girth, and waist-to-hip ratio as indexes of total and regional adiposity in women: evaluation using receiver operating characteristic curves. Am J Clin Nutr 67:4449, 1998[Abstract]
-
McInnis K, Balady G: Comparison of submaximal exercise responses using the Bruce vs modified Bruce protocols. Med Sci Sports Exerc 26:103107, 1994[Medline]
-
DeFronzo R, Ferrannini E: Insulin resistance: a multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care 14:173194, 1991[Abstract]
-
Goodpaster BH, Kelley DE, Wing RR, Meier A, Thaete FL: Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 48:839847, 1999[Abstract]
-
Markovic T, Jenkins A, Campbell L, Furler S, Kraegen E, Chisholm D: The determinants of glycemic responses to diet restriction and weight loss in obesity and NIDDM. Diabetes Care 21:687694, 1998[Abstract]
-
Ross R, Dagnone D, Jones P, Smith H, Paddags A, Hudson R, Janssen I: Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men: a randomized, controlled trial. Ann Intern Med 133:92103, 2000[Abstract/Free Full Text]
-
Storlien L, Baur L, Kritetos A, Pan D, Cooney G, Jenkins A, Calvert G, Campbell L: Dietary fats and insulin action. Diabetologia 39:621631, 1996[Medline]
-
Vessby B, Tengblad S, Lithell H: Insulin sensitivity is related to the fatty acid composition of serum lipids and skeletal muscle phospholipids in 70 year old men. Diabetologia 37:10441050, 1994[Medline]
-
Borghouts L, Keizer H: Exercise and insulin sensitivity: a review. Int J Sports Med 21:112, 2000[Medline]
-
Yamanouchi K, Shinozaki T, Chikada K, Nishikawa T, Ito K, Shimizu S, Ozawa N, Suzuki Y, Maeno H, Kato K, Oshida Y, Sato Y: Daily walking combined with diet therapy is a useful means for obese NIDDM patients not only to reduce body weight but also to improve insulin sensitivity. Diabetes Care 18:775778, 1995[Abstract]
-
Bogardus C, Ravussin E, Robbins D, Wolfe R, Horton E, Sims E: Effects of physical training and diet therapy on carbohydrate metabolism in patients with glucose intolerance and non-insulin-dependent diabetes mellitus. Diabetes 33:311318, 1984[Abstract]

CiteULike Del.icio.us Digg Reddit Technorati What's this?
This article has been cited by other articles:

|
 |

|
 |
 
U. Riserus, J. Arnlov, and L. Berglund
Long-Term Predictors of Insulin Resistance: Role of lifestyle and metabolic factors in middle-aged men
Diabetes Care,
November 1, 2007;
30(11):
2928 - 2933.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Dansinger, A. Tatsioni, J. B. Wong, M. Chung, and E. M. Balk
Meta-analysis: The Effect of Dietary Counseling for Weight Loss
Ann Intern Med,
July 3, 2007;
147(1):
41 - 50.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. McAuley and J. Mann
Thematic review series: Patient-Oriented Research. Nutritional determinants of insulin resistance
J. Lipid Res.,
August 1, 2006;
47(8):
1668 - 1676.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. DiPietro, J. Dziura, C. W. Yeckel, and P. D. Neufer
Exercise and improved insulin sensitivity in older women: evidence of the enduring benefits of higher intensity training
J Appl Physiol,
January 1, 2006;
100(1):
142 - 149.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. B. Carr, K. M. Utzschneider, E. J. Boyko, P. J. Asberry, R. L. Hull, K. Kodama, H. S. Callahan, C. C. Matthys, D. L. Leonetti, R. S. Schwartz, et al.
A Reduced-Fat Diet and Aerobic Exercise in Japanese Americans With Impaired Glucose Tolerance Decreases Intra-Abdominal Fat and Improves Insulin Sensitivity but not {beta}-Cell Function
Diabetes,
February 1, 2005;
54(2):
340 - 347.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Yoo, T. Nicklas, T. Baranowski, I. F Zakeri, S.-J. Yang, S. R Srinivasan, and G. S Berenson
Comparison of dietary intakes associated with metabolic syndrome risk factors in young adults: the Bogalusa Heart Study
Am. J. Clinical Nutrition,
October 1, 2004;
80(4):
841 - 848.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. P. Trevino, Z. Yin, A. Hernandez, D. E. Hale, O. A. Garcia, and C. Mobley
Impact of the Bienestar School-Based Diabetes Mellitus Prevention Program on Fasting Capillary Glucose Levels: A Randomized Controlled Trial
Arch Pediatr Adolesc Med,
September 1, 2004;
158(9):
911 - 917.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L Cox, V. Burke, A. R Morton, L. J Beilin, and I. B Puddey
Independent and additive effects of energy restriction and exercise on glucose and insulin concentrations in sedentary overweight men
Am. J. Clinical Nutrition,
August 1, 2004;
80(2):
308 - 316.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Wolf, M. R. Conaway, J. Q. Crowther, K. Y. Hazen, J. L.Nadler, B. Oneida, and V. E. Bovbjerg
Translating Lifestyle Intervention to Practice in Obese Patients With Type 2 Diabetes: Improving Control with Activity and Nutrition (ICAN) study
Diabetes Care,
July 1, 2004;
27(7):
1570 - 1576.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Sato, M. Nagasaki, N. Nakai, and T. Fushimi
Physical Exercise Improves Glucose Metabolism in Lifestyle-Related Diseases
Experimental Biology and Medicine,
November 1, 2003;
228(10):
1208 - 1212.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|
|