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DIABETES/METABOLISM RESEARCH AND REVIEWS REVIEW ARTICLE Diabetes Metab Res Rev 2009; 25(Suppl 1): S29–S33. Published online in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/dmrr.985 Physical activity/exercise training in type 2 diabetes. The role of the Italian Diabetes and Exercise Study S. Balducci 1,2 * S. Zanuso 3 F. Fernando 4 S. Fallucca 1 F. Fallucca 1 G. Pugliese 2 for the Italian Diabetes Exercise Study (IDES) Group 1 Metabolic Fitness Association, Monterotondo, Rome, Italy 2 Diabetes Division, S. Andrea Hospital and Department of Clinical Sciences, 2nd Medical School, ‘La Sapienza’ University, Rome, Italy 3 Department of Motor Science, Faculty of Medicine, University of Padua, Padua, Italy 4 Division of Sport Medicine, St. Andrea Hospital, Rome, Italy *Correspondence to: S. Balducci, Metabolic Fitness Association, Via Nomentana, 27 - 00015 Monterotondo (Rome), Italy. E-mail: [email protected] Received: Summary Cardiorespiratory fitness is inversely related to the development of type 2 diabetes and cardiovascular morbidity and mortality. Trials in individuals with impaired glucose tolerance have highlighted the role of physical activity/exercise in the prevention of type 2 diabetes. Moreover, physical activity and exercise training have been recognized as treatment options for patients with type 2 diabetes. Both aerobic and resistance training were shown to produce beneficial effects by reducing HbA 1c , inducing weight loss and improving fat distribution, lipid profile and blood pressure in patients with type 2 diabetes. Mixed aerobic and resistance training was recently shown to be more effective than either one alone in ameliorating HbA 1c . However, further research is needed to establish the volume, intensity and type of exercise that are required to reduce cardiovascular burden and particularly to define the best strategy for promoting long-term compliance and durable lifestyle changes in individuals with type 2 diabetes. The Italian Diabetes Exercise Study (IDES) is a prospective Italian multicentre randomized controlled trial, of larger size and longer duration than previously published trials. It has been designed to assess the combined effect of structured counselling and supervised mixed (aerobic plus resistance) exercise training, as compared with counselling alone, on HbA 1c and other cardiovascular risk factors as well as fitness parameters in individuals with type 2 diabetes and the metabolic syndrome. This study was also aimed at testing a sustainable strategy for promoting and maintaining a sufficient level of physical activity among individuals with type 2 diabetes to be implemented at the population level. Copyright 2009 John Wiley & Sons, Ltd. Keywords type 2 diabetes; metabolic syndrome; physical activity; exercise; exercise counselling It has been shown that cardiorespiratory fitness is inversely related to the development of type 2 diabetes [1] and cardiovascular morbidity and mortality [2]. Therefore, physical activity has been proposed as a valuable approach for the prevention and treatment of type 2 diabetes by ameliorating insulin sensitivity and the modifiable cardiovascular risk factors. The 1996 report of the US Surgeon General on ‘Physical Activity and Health’ [3] distinguished the terms ‘physical activity’ and ‘exercise’ as two different types of ‘movement’. Physical activity was defined as any bodily movement produced by the contraction of skeletal muscle that requires energy expen- diture in excess of resting energy expenditure; and exercise as a subset of physical activity: planned, structured, and repetitive bodily movements per- formed to improve or maintain one or more components of physical fitness. Copyright 2009 John Wiley & Sons, Ltd.

Physical activity/exercise training in type 2 diabetes. The role of the Italian Diabetes and Exercise Study

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DIABETES/METABOLISM RESEARCH AND REVIEWS R E V I E W A R T I C L EDiabetes Metab Res Rev 2009; 25(Suppl 1): S29–S33.Published online in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/dmrr.985

Physical activity/exercise training in type 2diabetes. The role of the Italian Diabetesand Exercise Study

S. Balducci1,2*S. Zanuso3

F. Fernando4

S. Fallucca1

F. Fallucca1

G. Pugliese2 for the ItalianDiabetes Exercise Study(IDES) Group

1Metabolic Fitness Association,Monterotondo, Rome, Italy2Diabetes Division, S. AndreaHospital and Department of ClinicalSciences, 2nd Medical School, ‘LaSapienza’ University, Rome, Italy3Department of Motor Science,Faculty of Medicine, University ofPadua, Padua, Italy4Division of Sport Medicine, St.Andrea Hospital, Rome, Italy

*Correspondence to: S. Balducci,Metabolic Fitness Association, ViaNomentana, 27 - 00015Monterotondo (Rome), Italy.E-mail: [email protected]

Received:

Summary

Cardiorespiratory fitness is inversely related to the development of type 2diabetes and cardiovascular morbidity and mortality. Trials in individualswith impaired glucose tolerance have highlighted the role of physicalactivity/exercise in the prevention of type 2 diabetes. Moreover, physicalactivity and exercise training have been recognized as treatment options forpatients with type 2 diabetes. Both aerobic and resistance training were shownto produce beneficial effects by reducing HbA1c, inducing weight loss andimproving fat distribution, lipid profile and blood pressure in patients withtype 2 diabetes. Mixed aerobic and resistance training was recently shownto be more effective than either one alone in ameliorating HbA1c. However,further research is needed to establish the volume, intensity and type ofexercise that are required to reduce cardiovascular burden and particularlyto define the best strategy for promoting long-term compliance and durablelifestyle changes in individuals with type 2 diabetes.

The Italian Diabetes Exercise Study (IDES) is a prospective Italianmulticentre randomized controlled trial, of larger size and longer durationthan previously published trials. It has been designed to assess the combinedeffect of structured counselling and supervised mixed (aerobic plus resistance)exercise training, as compared with counselling alone, on HbA1c and othercardiovascular risk factors as well as fitness parameters in individuals withtype 2 diabetes and the metabolic syndrome. This study was also aimed attesting a sustainable strategy for promoting and maintaining a sufficient levelof physical activity among individuals with type 2 diabetes to be implementedat the population level. Copyright 2009 John Wiley & Sons, Ltd.

Keywords type 2 diabetes; metabolic syndrome; physical activity; exercise;exercise counselling

It has been shown that cardiorespiratory fitness is inversely related tothe development of type 2 diabetes [1] and cardiovascular morbidity andmortality [2]. Therefore, physical activity has been proposed as a valuableapproach for the prevention and treatment of type 2 diabetes by amelioratinginsulin sensitivity and the modifiable cardiovascular risk factors.

The 1996 report of the US Surgeon General on ‘Physical Activity and Health’[3] distinguished the terms ‘physical activity’ and ‘exercise’ as two differenttypes of ‘movement’. Physical activity was defined as any bodily movementproduced by the contraction of skeletal muscle that requires energy expen-diture in excess of resting energy expenditure; and exercise as a subset ofphysical activity: planned, structured, and repetitive bodily movements per-formed to improve or maintain one or more components of physical fitness.

Copyright 2009 John Wiley & Sons, Ltd.

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S30 S. Balducci et al.

Table 1. Summary of the three major randomized controlled trials on the effects of lifestyle modification programs on the incidenceof type 2 diabetes

Study population Mean BMI Arms Diabetes incidencea RRR NNT

Diabetes Prevention Program (atotal of 3234 primary carepatients, both sexes, mixedethnic backgrounds, variousages)

34 Control 11.0 Baseline Baseline

Finnish Diabetes PreventionStudy (a total of 522 patients)

31 Metformin 7.8 31% 14 (over 7 years)

Intensive lifestylemodification

4.8 58% 7 (over 7 years)

Da Qing IGT and Diabetes Study(a total of 577 primary carepatients, men and women aged<25 years).

25.8 Control 23 Baseline Baseline

Intensive lifestylemodification

11 58% 5 (over 5 years)

Control 15 Baseline BaselineDiet 10 31% 17Exercise 8 46% 14Diet + exercise 9.5 42% 16

aIncidence of diabetes per 100 person-year.BMI, body mass index; IGT, impaired glucose tolerance; NNT, number needed to treat; RRR, relative risk reduction.

Table 2. Summary of the effects of aerobic, resistance and mixed exercise training in type 2 diabetic patients

Exercise type Effects Higlights

Aerobic exercise Improves glycemic control; assists inlipoproteins/lipids control; helps in bodyweight control; increases insulin sensitivity

More vigorous aerobic exercise programsare better than those of low-to-moderateintensity

Resistance exercise Improves glycemic control; increases insulinsensitivity; increases lean body mass;increases overall functionality

Resistance exercise offers the same benefitsas aerobic exercise

Mixed aerobic and resistance exercise Improves glycemic control more thanaerobic or resistance alone

Mixed training offers incrementaladvantages

Even though these terms are properly utilized inthe context of exercise science, they are not alwaysoperationally well defined and often used interchangeablyin studies involving patients with impaired glucosetolerance (IGT) or diabetes.

Physical activity and exercise in theprevention of type 2 diabetes

In recent years, clinical trials and cohort studies havehighlighted the role of physical activity in the preventionof type 2 diabetes. Most of the studies focused onindividuals at high risk for developing type 2 diabetes,such as those with IGT, who were received a ‘lifestyleintervention’ consisting of diet, physical activity andexercise, either separately or in combination.

The most relevant randomized clinical trials publishedin the literature are the ‘Da Qing IGT and Diabetes Study’[4], the ‘Diabetes Prevention Study’ [5] and the ‘DiabetesPrevention Program’ [6], which evaluated the effect ofdiet and/or physical activity/exercise in IGT subjects. Inthe ‘Da Qing IGT and Diabetes Study’, diet, exercise, anddiet plus exercise interventions were associated with 31%,

46%, and 42% decreases in risk of developing diabetes,respectively, [4] whereas, in the other two trials, riskreduction was 58% with combined intervention [5,6](Table 1).

In a meta-analysis and systematic review of pharmaco-logical and lifestyle interventions to prevent or delay type2 diabetes in IGT subjects [7], the authors concluded thatlifestyle interventions seem to be at least as effective asdrug treatment, but wondered whether lifestyle shouldreally be treated as a lifelong course of medication. Thus,as compliance is the key to the success of lifestyle interven-tions, strategies to assist compliance need to be carefullyconsidered and implemented.

Current actions to implementdiabetes prevention programs intoclinical practice

Currently, numerous prevention management conceptsexist in the various European countries which can beimplemented into clinical practice. Finland is the pioneerand has started with the Program for the Preventionof Type 2 Diabetes [8] and is testing in practice the

Copyright 2009 John Wiley & Sons, Ltd. Diabetes Metab Res Rev 2009; 25(Suppl 1): S29–S33.DOI: 10.1002/dmrr

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translation of the findings of the Diabetes PreventionStudy into strategies, facilitating and supporting theimplementation of preventive activities in primary healthcare centres and occupational (employer-provided) healthcare units in Finland.

In Germany, an intensive implementation process hasstarted and it is currently the largest and most practicalimplementation concept. It is a standardized structuredconcept considering scientific evidence and application topractical requirements during implementation [9].

In Europe, some strategic focused actions are goingon, funded by the European Union in the public healthsector. One European Union public health research project‘Diabetes in Europe – Prevention using Lifestyle, PhysicalActivity and Nutritional intervention’ [10] is developingstructures of a European prevention management conceptand is testing it in pilot projects funded by the Commissionof the European Communities.

In addition, the European Union currently started aproject for the ‘Development and Implementation of aEuropean Guideline and Training Standards for DiabetesPrevention’ [11]. The ‘Development and Implementationof a European Guideline and Training Standards forDiabetes Prevention’ project will develop a Europeanpractice-orientated guidelines for the primary preventionof type 2 diabetes.

Physical activity and exercise in themanagement of type 2 diabetes

A consensus statement from the American DiabetesAssociation summarizes the most clinically relevant recentadvances related to individuals with type 2 diabetes andformulates the recommendations that follow from thesefindings [12].

Aerobic training

Available data indicate that aerobic exercise is effective inreducing blood glucose and body weight and improvingcardiovascular risk profile in patients with type 2 diabetes.These results have been analysed in three recent meta-analyses [13–15], which confirmed the beneficial effect ofaerobic exercise on HbA1c, the best indicator of glycaemiccontrol (Table 2).

Two of these meta-analyses [13,14] also addressedthe issue of exercise intensity, showing that it was abetter predictor than exercise volume of the differencein HbA1c and VO2 max between the intervention and thecontrol groups. Recently, three randomized controlledtrials [16–18] and a review article [19] analysed the effectof exercise intensity on insulin sensitivity and found thatintensity of aerobic training, independent of total energyexpenditure, is a major determinant of the improvementin insulin action induced by exercise.

Resistance training

Resistance training has been shown to be beneficial intype 2 diabetic patients in a number of studies. Erikssonet al. showed that 3 months of moderate intensity circuitresistance training significantly decreases HbA1c [20].The randomized controlled trials by Dunstan et al. [21]and Ishii et al. [22] reported a reduced plasma insulinresponse to glucose ingestion and an increased glucosedisposal rate during the hyperinsulinemic–euglycaemicclamp, respectively. However, these studies failed todetect a significant change in HbA1c, which most likelydepended on the small sample size and short trainingduration (8 and 6 weeks, respectively) or lack of sufficientintensity and/or volume of exercise.

More recent trials by Castaneda et al. [23], Dunstanet al. [24], and particularly Baldi et al. [25], which wereof larger size and longer duration and utilized a resistancetraining of higher intensity than previous studies, did infact show a significant reduction in HbA1c in the resistancetraining group, as compared with control. In these threestudies, a significant relationship was observed betweenreduction in HbA1c and increase in skeletal muscle mass[23–25], thus supporting the hypothesis that resistancetraining improves glycaemic control by increasing muscleglucose uptake. However, the increased glucose rate ofdisappearance might also be dependent on qualitativechanges in certain muscle functions. In addition, theextent of HbA1c reduction in these studies was comparableto that reported in the meta-analysis by Boule et al. [13],thus indicating that resistance training is as effective asaerobic exercise in improving glycaemic control.

Mixed aerobic and resistance training

A number of studies in individuals with type 2 diabeteshave showed that mixed aerobic and resistance trainingis effective in reducing HbA1c, inducing weight loss andimproving fat distribution, lipid profile and blood pressure[26–28].

The question whether combination of aerobic andresistance training induces additive or synergistic effectsas compared with either one alone has been addressed byCuff et al. [29] and, more recently, by Sigal et al. [30]. Inthe first report, a mixed aerobic and resistance traininggroup was compared with an aerobic-only training groupand a non-exercising control group. However, the resultsof this study did not show any significant differenceamong groups, probably due to the low baseline HbA1c

values (6.7% on average) and particularly by the smallsample size (nine to ten persons per group) [29]. Thesecond, much larger trial, called the Diabetes Aerobicand Resistance Exercise Study, compared three groups ofsubjects performing supervised training (mixed aerobicand resistance, aerobic alone and resistance alone) anda sedentary control group. At variance with the previousstudy, mixed aerobic and resistance exercise was found

Copyright 2009 John Wiley & Sons, Ltd. Diabetes Metab Res Rev 2009; 25(Suppl 1): S29–S33.DOI: 10.1002/dmrr

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to be more effective than either one alone in amelioratingHbA1c, but not on other cardiovascular risk factors [30].

Based on these results, resistance training is nowrecommended by the American Diabetes Association incombination with aerobic exercise, or as an alternativewhen the latter is limited or contraindicated, [12] andalso in subjects with the metabolic syndrome [31].

The role of the Italian Diabetesand Exercise Study (IDES)

As previously mentioned, a major issue in lifestyleinterventions comprising physical activity/exercise iscompliance and strategies aimed at promoting complianceinclude structured conselling and supervised exercisetraining sessions. Both approaches have been shown to beeffective in promoting leisure-time physical activity andexercise, respectively [14,32].

The IDES is a prospective multicentre, randomizedcontrolled trial, of larger size (606 subjects) and longerduration (12 months) than previously published trials indiabetic patients, conducted in 22 outpatients diabetesclinics, connected with 20 metabolic fitness centresnationwide. This study, the design and methods ofwhich were published in detail elsewhere [33], has beendesigned to assess the combined effect of structuredcounselling and supervised mixed exercise training, ascompared with counselling alone, in subjects with type2 diabetes and the metabolic syndrome. Thus, theIDES allowed to compare the combination of leisure-time physical activity, mainly aerobic, and a mixed(aerobic + resistance) training program with leisure-timeaerobic physical activity alone.

Moreover, this study has been designed not only toanswer a scientific question, but also to test a practical,sustainable and viable strategy for the promotionand maintenance of a sufficient amount of physicalactivity/exercise among subjects with type 2 diabetes tobe implemented at the population level. In fact, supervisedsessions were not individual, were held in standard fitnessfacilities and were limited to two per week, leaving timefor practising leisure-time physical activity.

Finally, end points were HbA1c (primary outcome),other modifiable cardiovascular risk factors and globalcardiovascular risk (secondary outcomes), in keepingwith the concept that increased cardiovascular burdenin diabetic patients is attributable not only to hyper-glycaemia, but also to other cardiovascular risk factorsclustering with impaired glucose metabolism in the set-ting of the metabolic syndrome. Secondary end pointsincluded also physical fitness, comprising cardiorespira-tory fitness, strength and flexibility, due to the well-knowninverse relationship of fitness with cardiovascular morbid-ity and mortality in the general population [2] as well asin diabetic patients [34].

Because adherence is a crucial point in a long-termtrial such as the IDES, 2 years prior to initiating the

study, physicians and exercise specialists participatingin the study received a specific training to providestructured counselling and prescribe exercise and tosupervise exercise sessions, respectively. This strategy wasalso aimed at increasing awareness of the importance ofexercise in type 2 diabetic subjects among physicians andtrainers.

Conclusions

Physical activity/exercise has been shown to be effectivein preventing type 2 diabetes in IGT subjects and toimprove both glycaemic control and other cardiovascularrisk factors in patients with type 2 diabetes. Both aerobicand resistance training were shown to produce beneficialeffects, though combination of the two seems to besynergistic. However, a major issue for the success oflifestyle interventions is adherence, especially in thelong-term period, and strategies based on structuredcounselling or supervised exercise sessions have beendesigned to improve compliance.

The IDES is a prospective Italian multicentre, random-ized controlled trial, of larger size and longer durationthan previously published trials, designed to assess thecombined effect of these two strategies versus counsellingalone on HbA1c and other cardiovascular risk factors aswell as fitness parameters in subjects with type 2 diabetesand the metabolic syndrome. It was also aimed at testinga sustainable strategy for promoting and maintaining asufficient level of physical activity among subjects withtype 2 diabetes.

Conflict of interest

None declared.

References

1. Wei M, Gibbons LW, Mitchell TL, Kampert JB, Lee CD, Blair SN.The association between cardiorespiratory fitness and impairedfasting glucose and type 2 diabetes mellitus in men. Ann InternMed 1999; 130: 89–96.

2. Myers J, Prakash M, Froelicher V, Do D, Partington S,Atwood JE. Exercise capacity and mortality among men referredfor exercise testing. N Engl J Med 2002; 346: 793–801.

3. U.S. Department of Health and Human Services. Physical Activityand Health. A Report of the Surgeon General. Atlanta, GA, U.S.Department of Health and Human Services, Centers for DiseaseControl and Prevention, National Center for Chronic DiseasePrevention and Health Promotion, 1996.

4. Pan XR, Li GW, Hu YH, et al. Effects of diet and exercise inpreventing NIDDM in people with impaired glucose tolerance.The Da Qing IGT and Diabetes Study. Diabetes Care 1997; 20:537–544.

5. Tuomilehto J, Lindstrom J, Eriksson JG, et al. Prevention of type2 diabetes mellitus by changes in lifestyle among subjectswith impaired glucose tolerance. N Engl J Med 2001; 344:1343–1350.

6. Knowler WC, Barrett-Connor E, Fowler SE, et al. Reduction inthe incidence of type 2 diabetes with lifestyle intervention ormetformin. N Engl J Med 2002; 346: 393–403.

Copyright 2009 John Wiley & Sons, Ltd. Diabetes Metab Res Rev 2009; 25(Suppl 1): S29–S33.DOI: 10.1002/dmrr

Page 5: Physical activity/exercise training in type 2 diabetes. The role of the Italian Diabetes and Exercise Study

Physical Activity/Exercise in Type 2 Diabetes S33

7. Gillies CL, Abrams KR, Lambert PC, et al. Pharmacological andlifestyle interventions to prevent or delay type 2 diabetes inpeople with impaired glucose tolerance: systematic review andmeta-analysis. BMJ 2007; 334: 299–302.

8. Saaristo T, Peltonen M, Keinanen-Kiukaanniemi S, et al.National type 2 diabetes prevention programme in Finland:FIN-D2D. Int J Circumpolar Health 2007; 66: 101–112.

9. Schwarz PE, Schwarz J, Schuppenies A, Bornstein SR, Schulze J.Development of a diabetes prevention management program forclinical practice. Public Health Rep 2007; 122: 258–263.

10. Schwarz PE, Lindstrom J, Kissimova-Scarbeck K, et al. TheEuropean perspective of type 2 diabetes prevention: diabetesin Europe – prevention using lifestyle, physical activity andnutritional intervention (DE-PLAN) project. Exp Clin EndocrinolDiabetes 2008; 116: 167–172.

11. Schwarz PE, Gruhl U, Bornstein SR, Landgraf R, Hall M,Tuomilehto J. The European Perspective on DiabetesPrevention: development and Implementation of A EuropeanGuideline and training standards for diabetes prevention(IMAGE). Diab Vasc Dis Res 2007; 4: 353–357.

12. Sigal RJ, Kenny GP, Wasserman DH, Castaneda-Sceppa C,White RD. Physical activity/exercise and type 2 diabetes: aconsensus statement from the American Diabetes Association.Diabetes Care 2006; 29: 1433–1438.

13. Boule NG, Haddad E, Kenny GP, Wells GA, Sigal RJ. Effects ofexercise on glycemic control and body mass in type 2 diabetesmellitus: a meta-analysis of controlled clinical trials. JAMA 2001;286: 1218–1227.

14. Boule NG, Kenny GP, Haddad E, Wells GA, Sigal RJ. Meta-analysis of the effect of structured exercise training oncardiorespiratory fitness in type 2 diabetes mellitus. Diabetologia2003; 46: 1071–1081.

15. Kelley GA, Kelley KS. Effects of aerobic exercise on lipids andlipoproteins in adults with type 2 diabetes: a meta-analysisof randomized-controlled trials. Public Health 2007; 121:643–655.

16. O’Donovan G, Kearney EM, Nevill AM, Woolf-May K, Bird SR.The effects of 24 weeks of moderate- or high-intensity exerciseon insulin resistance. Eur J Appl Physiol 2005; 95: 522–528.

17. Coker RH, Hays NP, Williams RH, et al. Exercise-inducedchanges in insulin action and glycogen metabolism in elderlyadults. Med Sci Sports Exerc 2006; 38: 433–438.

18. DiPietro L, Dziura J, Yeckel CW, Neufer PD. Exercise andimproved insulin sensitivity in older women: evidence of theenduring benefits of higher intensity training. J Appl Physiol2006,; 100: 142–149.

19. Gill JM. Physical activity, cardiorespiratory fitness and insulinresistance: a short update. Curr Opin Lipidol 2007; 18: 47–52.

20. Eriksson J, Taimela S, Eriksson K, Parviainen S, Peltonen J,Kujala U. Resistance training in the treatment of non-insulin-dependent diabetes mellitus. Int J Sports Med 1997; 18:242–246.

21. Dunstan DW, Puddey IB, Beilin LJ, Burke V, Morton AR,Stanton KG. Effects of a short-term circuit weight trainingprogram on glycaemic control in NIDDM. Diabetes Res ClinPract 1998,; 40: 53–61.

22. Ishii T, Yamakita T, Sato T, Tanaka S, Fujii S. Resistancetraining improves insulin sensitivity in NIDDM subjects withoutaltering maximal oxygen uptake. Diabetes Care 1998; 21:1353–1355.

23. Castaneda C, Layne JE, Munoz-Orians L, et al. A randomizedcontrolled trial of resistance exercise training to improveglycemic control in older adults with type 2 diabetes. DiabetesCare 2002; 25: 2335–2341.

24. Dunstan DW, Daly RM, Owen N, et al. High-intensity resistancetraining improves glycemic control in older patients with type 2diabetes. Diabetes Care 2002; 25: 1729–1736.

25. Baldi JC, Snowling N. Resistance training improves glycaemiccontrol in obese type 2 diabetic men. Int J Sports Med 2003; 24:419–423.

26. Maiorana A, O’Driscoll G, Cheetham C, et al. The effect ofcombined aerobic and resistance exercise training on vascularfunction in type 2 diabetes. J Am Coll Cardiol 2001; 38: 860–866.

27. Balducci S, Leonetti F, Di Mario U, Fallucca F. Is a long-termaerobic plus resistance training program feasible for andeffective on metabolic profiles in type 2 diabetic patients?Diabetes Care 2004; 27: 841–842.

28. Tokmakidis SP, Zois CE, Volaklis KA, Kotsa K, Touvra AM. Theeffects of a combined strength and aerobic exercise programon glucose control and insulin action in women with type 2diabetes. Eur J Appl Physiol 2004; 92: 437–442.

29. Cuff DJ, Meneilly GS, Martin A, Ignaszewski A, Tildesley HD,Frohlich JJ. Effective exercise modality to reduce insulinresistance in women with type 2 diabetes. Diabetes Care 2003;26: 2977–2982.

30. Sigal RJ, Kenny GP, Boule NG, et al. Effects of aerobic training,resistance training, or both on glycemic control in type 2diabetes: a randomized trial. Ann Intern Med 2007; 147:357–369.

31. Eriksson J, Taimela S, Koivisto VA. Exercise and the metabolicsyndrome. Diabetologia 1997; 40: 125–135.

32. Di Loreto C, Fanelli C, Lucidi P, et al. Validation of a counselingstrategy to promote the adoption and the maintenance ofphysical activity by type 2 diabetic subjects. Diabetes Care 2003;26: 404–408.

33. Balducci S, Zanuso S, Massarini M, et al. The Italian Diabetesand Exercise Study (IDES): design and methods for a prospectiveItalian multicentre trial of intensive lifestyle intervention inpeople with type 2 diabetes and the metabolic syndrome. NutrMetab Cardiovasc Dis 2008; 18: 585–595.

34. Wei M, Gibbons LW, Kampert JB, Nichaman MZ, Blair SN. Lowcardiorespiratory fitness and physical inactivity as predictors ofmortality in men with type 2 diabetes. Ann Intern Med 2000;132: 605–611.

Copyright 2009 John Wiley & Sons, Ltd. Diabetes Metab Res Rev 2009; 25(Suppl 1): S29–S33.DOI: 10.1002/dmrr