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Reviews/Commentaries/ADA Statements

P O S I T I O N S T A T E M E N T

Exercise and Type 2 Diabetes


The American College of Sports Medicine and the American Diabetes
Association: joint position statement
SHERI R. COLBERG, PHD, FACSM1 RICHARD R. RUBIN, PHD6 disease (CVD), blindness, kidney and
RONALD J. SIGAL, MD, MPH, FRCP(C)2 LISA CHASAN-TABER, SCD, FACSM7 nerve disease, and amputation (261). Al-
BO FERNHALL, PHD, FACSM3 ANN L. ALBRIGHT, PHD, RD8 though regular physical activity (PA) may
JUDITH G. REGENSTEINER, PHD4 BARRY BRAUN, PHD, FACSM9 prevent or delay diabetes and its compli-
BRYAN J. BLISSMER, PHD5 cations (10,46,89,112,176,208,259,294),
most people with type 2 diabetes are not
active (193).
Although physical activity (PA) is a key element in the prevention and management of type 2 In this article, the broader term
diabetes, many with this chronic disease do not become or remain regularly active. High-quality physical activity (defined as bodily
studies establishing the importance of exercise and fitness in diabetes were lacking until recently, movement produced by the contraction
but it is now well established that participation in regular PA improves blood glucose control and
of skeletal muscle that substantially in-
can prevent or delay type 2 diabetes, along with positively affecting lipids, blood pressure,
cardiovascular events, mortality, and quality of life. Structured interventions combining PA and creases energy expenditure) is used in-
modest weight loss have been shown to lower type 2 diabetes risk by up to 58% in high-risk terchangeably with exercise, which is
populations. Most benefits of PA on diabetes management are realized through acute and chronic defined as a subset of PA done with the
improvements in insulin action, accomplished with both aerobic and resistance training. The intention of developing physical fitness
benefits of physical training are discussed, along with recommendations for varying activities, (i.e., cardiovascular [CV], strength, and
PA-associated blood glucose management, diabetes prevention, gestational diabetes mellitus, flexibility training). The intent is to rec-
and safe and effective practices for PA with diabetes-related complications. ognize that many types of physical move-
ment may have a positive effect on
Diabetes Care 33:e147 e167, 2010 physical fitness, morbidity, and mortality
in individuals with type 2 diabetes.
INTRODUCTION
Diagnosis, classification, and

D
iabetes has become a widespread tes, a condition in which blood glucose etiology of diabetes
epidemic, primarily because of the (BG) levels are above normal, thus greatly Currently, the American Diabetes Associ-
increasing prevalence and inci- increasing their risk for type 2 diabetes ation (ADA) recommends the use of any
dence of type 2 diabetes. According to the (261). Lifetime risk estimates suggest that of the following four criteria for diagnos-
Centers for Disease Control and Preven- one in three Americans born in 2000 or ing diabetes: 1) glycated hemoglobin
tion, in 2007, almost 24 million Ameri- later will develop diabetes, but in high- (A1C) value of 6.5% or higher, 2) fasting
cans had diabetes, with one-quarter of risk ethnic populations, closer to 50% plasma glucose 126 mg/dl (7.0 mmol/
those, or six million, undiagnosed (261). may develop it (200). Type 2 diabetes is a l), 3) 2-h plasma glucose 200 mg/dl
Currently, it is estimated that almost 60 significant cause of premature mortality (11.1 mmol/l) during an oral glucose tol-
million U.S. residents also have prediabe- and morbidity related to cardiovascular erance test using 75 g of glucose, and/or
4) classic symptoms of hyperglycemia
From the 1Human Movement Sciences Department, Old Dominion University, Norfolk, Virginia; the 2De- (e.g., polyuria, polydipsia, and unex-
partments of Medicine, Cardiac Sciences, and Community Health Sciences, Faculties of Medicine and plained weight loss) or hyperglycemic cri-
Kinesiology, University of Calgary, Calgary, Alberta, Canada; the 3Department of Kinesiology and Com- sis with a random plasma glucose of 200
munity Health, University of Illinois at Urbana-Champaign, Urbana, Illinois; the 4Divisions of General
Internal Medicine and Cardiology and Center for Womens Health Research, University of Colorado mg/dl (11.1 mmol/l) or higher. In the ab-
School of Medicine, Aurora, Colorado; the 5Department of Kinesiology and Cancer Prevention Research sence of unequivocal hyperglycemia, the
Center, University of Rhode Island, Kingston, Rhode Island; the 6Departments of Medicine and Pediatrics, first three criteria should be confirmed by
The Johns Hopkins University School of Medicine, Baltimore, Maryland; the 7Division of Biostatistics and repeat testing (4). Prediabetes is diag-
Epidemiology, University of Massachusetts, Amherst, Massachusetts; the 8Division of Diabetes Transla-
tion, Centers for Disease Control and Prevention, Atlanta, Georgia; and the 9Department of Kinesiology, nosed with an A1C of 5.7 6.4%, fasting
University of Massachusetts, Amherst, Massachusetts. plasma glucose of 100 125 mg/dl (5.6
Corresponding author: Sheri R. Colberg, scolberg@odu.edu. 6.9 mmol/l; i.e., impaired fasting glucose
This joint position statement is written by the American College of Sports Medicine and the American [IFG]), or 2-h postload glucose of 140
Diabetes Association and was approved by the Executive Committee of the American Diabetes Association
in July 2010. This statement is published concurrently in Medicine & Science in Sports & Exercise and
199 mg/dl (7.8 11.0 mmol/l; i.e., im-
Diabetes Care. Individual name recognition is stated in the ACKNOWLEDGMENTS at the end of the paired glucose tolerance [IGT]) (4).
statement. The major forms of diabetes can be
The findings and conclusions in this report are those of the authors and do not necessarily represent the categorized as type 1 or type 2 (4). In type
official position of the Centers for Disease Control and Prevention. 1 diabetes, which accounts for 510% of
DOI: 10.2337/dc10-9990
2010 by the American Diabetes Association. Readers may use this article as long as the work is properly
cases, the cause is an absolute deficiency
cited, the use is educational and not for profit, and the work is not altered. See http://creativecommons. of insulin secretion resulting from auto-
org/licenses/by-nc-nd/3.0/ for details. immune destruction of the insulin-
See accompanying article, p. 2692. producing cells in the pancreas. Type 2

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Exercise and type 2 diabetes

diabetes (90 95% of cases) results from a mobilization of alternate fuels, such as 5-AMPactivated protein kinase
combination of the inability of muscle free fatty acids (FFAs) (250,268). (198,293). Insulin-stimulated GLUT4
cells to respond to insulin properly (insu- Several factors influence exercise fuel translocation is generally impaired in type
lin resistance) and inadequate compensa- use, but the most important are the inten- 2 diabetes (96). Both aerobic and resis-
tory insulin secretion. Less common sity and duration of PA (9,29,47,83,111, tance exercises increase GLUT4 abun-
forms include gestational diabetes melli- 133,160,181,241). Any activity causes a dance and BG uptake, even in the presence
tus (GDM), which is associated with a shift from predominant reliance on FFA at of type 2 diabetes (39,51,204,270).
40 60% chance of developing type 2 di- rest to a blend of fat, glucose, and muscle Evidence statement. Insulin-stimulated
abetes in the next 510 years (261). Dia- glycogen, with a small contribution BG uptake into skeletal muscle predomi-
betes can also result from genetic defects from amino acids (15,31). With in- nates at rest and is impaired in type 2
in insulin action, pancreatic disease, sur- creasing exercise intensity, there is a diabetes, while muscular contractions
gery, infections, and drugs or chemicals greater reliance on carbohydrate as long stimulate BG transport via a separate ad-
(4,261). as sufficient amounts are available in ditive mechanism not impaired by insulin
Genetic and environmental factors muscle or blood (21,23,47,133). Early resistance or type 2 diabetes. ACSM evi-
are strongly implicated in the develop- in exercise, glycogen provides the bulk dence category A.
ment of type 2 diabetes. The exact genetic of the fuel for working muscles. As gly-
defects are complex and not clearly de- cogen stores become depleted, muscles Postexercise glycemic control/BG
fined (4), but risk increases with age, obe- increase their uptake and use of circu- levels
sity, and physical inactivity. Type 2 lating BG, along with FFA released from Aerobic exercise effects. During mod-
diabetes occurs more frequently in popu- adipose tissue (15,132, 271). Intramus- erate-intensity exercise in nondiabetic
lations with hypertension or dyslipide- cular lipid stores are more readily used persons, the rise in peripheral glucose up-
mia, women with previous GDM, and during longer-duration activities and take is matched by an equal rise in hepatic
non-Caucasian people including Native recovery (23,223,270). Glucose pro- glucose production, the result being that
Americans, African Americans, Hispanic/ duction also shifts from hepatic glyco- BG does not change except during pro-
Latinos, Asians, and Pacific Islanders. genolysis to enhanced gluconeogenesis longed, glycogen-depleting exercise. In
as duration increases (250,268). individuals with type 2 diabetes perform-
Treatment goals in type 2 diabetes Evidence statement. PA causes increased ing moderate exercise, BG utilization by
The goal of treatment in type 2 diabetes is glucose uptake into active muscles bal- muscles usually rises more than hepatic
to achieve and maintain optimal BG, anced by hepatic glucose production,
glucose production, and BG levels tend to
lipid, and blood pressure (BP) levels to with a greater reliance on carbohydrate to
decline (191). Plasma insulin levels nor-
prevent or delay chronic complications of fuel muscular activity as intensity in-
mally fall, however, making the risk of
diabetes (5). Many people with type 2 di- creases. The American College of Sports
exercise-induced hypoglycemia in any-
abetes can achieve BG control by follow- Medicine (ACSM) evidence category A (see
one not taking insulin or insulin secreta-
ing a nutritious meal plan and exercise Tables 1 and 2 for explanation).
program, losing excess weight, imple- Insulin-independent and insulin- gogues very minimal, even with
menting necessary self-care behaviors, dependent muscle glucose uptake dur- prolonged PA (152). The effects of a sin-
and taking oral medications, although ing exercise. There are two well-defined gle bout of aerobic exercise on insulin ac-
others may need supplemental insulin pathways that stimulate glucose uptake tion vary with duration, intensity, and
(261). Diet and PA are central to the man- by muscle (96). At rest and postprandi- subsequent diet; a single session in-
agement and prevention of type 2 diabe- ally, its uptake by muscle is insulin de- creases insulin action and glucose toler-
tes because they help treat the associated pendent and serves primarily to replenish ance for more than 24 h but less than
glucose, lipid, BP control abnormalities, muscle glycogen stores. During exercise, 72 h (26,33,85,141). The effects of
as well as aid in weight loss and mainte- contractions increase BG uptake to sup- moderate aerobic exercise are similar
nance. When medications are used to plement intramuscular glycogenolysis whether the PA is performed in a single
control type 2 diabetes, they should aug- (220,227). As the two pathways are dis- session or multiple bouts with the same
ment lifestyle improvements, not replace tinct, BG uptake into working muscle is total duration (14).
them. normal even when insulin-mediated up- During brief, intense aerobic exercise,
take is impaired in type 2 diabetes plasma catecholamine levels rise mark-
ACUTE EFFECTS OF (28,47,293). Muscular BG uptake re- edly, driving a major increase in glucose
EXERCISE mains elevated postexercise, with the production (184). Hyperglycemia can re-
contraction-mediated pathway persist- sult from such activity and persist for up
Fuel metabolism during exercise ing for several hours (86,119) and insulin- to 12 h, likely because plasma catechol-
Fuel mobilization, glucose production, mediated uptake for longer (9,33,141, 226). amine levels and glucose production do
and muscle glycogenolysis. The main- Glucose transport into skeletal mus- not return to normal immediately with
tenance of normal BG at rest and during cle is accomplished via GLUT proteins, cessation of the activity (184).
exercise depends largely on the coordina- with GLUT4 being the main isoform in Evidence statement. Although moderate
tion and integration of the sympathetic muscle modulated by both insulin and aerobic exercise improves BG and insulin ac-
nervous and endocrine systems (250). contractions (110,138). Insulin activates tion acutely, the risk of exercise-induced hy-
Contracting muscles increase uptake of GLUT4 translocation through a complex poglycemia is minimal without use of
BG, although BG levels are usually main- signaling cascade (256,293). Contrac- exogenous insulin or insulin secretagogues.
tained by glucose production via liver gly- tions, however, trigger GLUT4 transloca- Transient hyperglycemia can follow intense
cogenolysis and gluconeogenesis and tion at least in part through activation of PA. ACSM evidence category C.

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Colberg and Associates

Table 1Evidence categories for ACSM and evidence-grading system for clinical practice recommendations for ADA

I. ACSM evidence categories


Evidence
category Source of evidence Definition
A Randomized, controlled trials (overwhelming data) Provides a consistent pattern of findings with substantial studies
B Randomized, controlled trials (limited data) Few randomized trials exist, which are small in size, and results are inconsistent
C Nonrandomized trials, observational studies Outcomes are from uncontrolled, nonrandomized, and/or observational studies
D Panel consensus judgment Panels expert opinion when the evidence is insufficient to place it in categories
AC

II. ADA evidence-grading system for clinical practice recommendations


Level of
evidence Description
A Clear evidence from well-conducted, generalizable, randomized, controlled trials that are adequately powered, including the
following:
Evidence from a well-conducted multicenter trial
Evidence from a meta-analysis that incorporated quality ratings in the analysis
Compelling nonexperimental evidence, i.e., the all-or-none rule developed by the Centre for Evidence-Based Medicine at
Oxford
Supportive evidence from well-conducted, randomized, controlled trials that are adequately powered, including the following:
Evidence from a well-conducted trial at one or more institutions
Evidence from a meta-analysis that incorporated quality ratings in the analysis
B Supportive evidence from well-conducted cohort studies, including the following:
Evidence from a well-conducted prospective cohort study or registry
Evidence from a well-conducted meta-analysis of cohort studies
Supportive evidence from a well-conducted case-control study
C Supportive evidence from poorly controlled or uncontrolled studies, including the following:
Evidence from randomized clinical trials with one or more major or three or more minor methodological flaws that could
invalidate the results
Evidence from observational studies with high potential for bias (such as case series with comparison to historical controls)
Evidence from case series or case reports
Conflicting evidence with the weight of evidence supporting the recommendation
E Expert consensus or clinical experience

Resistance exercise effects. The acute Any increase in muscle mass that may re- (286,291), although others have not
effects of a single bout of resistance train- sult from resistance training could con- (159,257). One study suggested that yo-
ing on BG levels and/or insulin action in tribute to BG uptake without altering the gas benefits on fasting BG, lipids, oxida-
individuals with type 2 diabetes have not muscles intrinsic capacity to respond to tive stress markers, and antioxidant status
been reported. In individuals with IFG insulin, whereas aerobic exercise en- are at least equivalent to more conven-
(BG levels of 100 125 mg/dl), resistance hances its uptake via a greater insulin ac- tional forms of PA (98). However, a meta-
exercise results in lower fasting BG levels tion, independent of changes in muscle analysis of yoga studies stated that the
24 h after exercise, with greater reduc- mass or aerobic capacity (51). However, limitations characterizing most studies,
tions in response to both volume (multi- all reported combination training had a such as small sample size and varying
ple- vs. single-set sessions) and intensity greater total duration of exercise and ca- forms of yoga, preclude drawing firm
of resistance exercise (vigorous compared loric use than when each type of training
conclusions about benefits to diabetes
with moderate) (18). was undertaken alone (51,183,238).
management (117).
Evidence statement. The acute effects of Mild-intensity exercises such as tai chi
resistance exercise in type 2 diabetes have and yoga have also been investigated for Evidence statement. A combination of
not been reported, but result in lower fast- their potential to improve BG manage- aerobic and resistance exercise training
ing BG levels for at least 24 h after exercise ment, with mixed results (98,117,159, may be more effective in improving BG
in individuals with IFG. ACSM evidence 257,269,286,291). Although tai chi may control than either alone; however, more
category C. lead to short-term improvements in BG studies are needed to determine if total
Combined aerobic and resistance and levels, effects from long-term training caloric expenditure, exercise duration, or
other types of training. A combination (i.e., 16 weeks) do not seem to last 72 h exercise mode is responsible. ACSM evi-
of aerobic and resistance training may be after the last session (257). Some studies dence category B. Milder forms of exercise
more effective for BG management than have shown lower overall BG levels with (e.g., tai chi, yoga) have shown mixed re-
either type of exercise alone (51,238). extended participation in such activities sults. ACSM evidence category C.

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Exercise and type 2 diabetes

Table 2Summary of ACSM evidence and ADA clinical practice recommendation statements

ACSM evidence category


(A, highest; D, lowest)/
ADA level of evidence
ACSM evidence and ADA clinical practice recommendation statements (A, highest; E, lowest)
Acute effects of exercise PA causes increased glucose uptake into active muscles balanced by hepatic glucose A/*
production, with a greater reliance on carbohydrate to fuel muscular activity as intensity
increases.
Insulin-stimulated BG uptake into skeletal muscle predominates at rest and is impaired A/*
in type 2 diabetes, while muscular contractions stimulate BG transport via a separate,
additive mechanism not impaired by insulin resistance or type 2 diabetes.
Although moderate aerobic exercise improves BG and insulin action acutely, the risk of C/*
exercise-induced hypoglycemia is minimal without use of exogenous insulin or insulin
secretagogues. Transient hyperglycemia can follow intense PA.
The acute effects of resistance exercise in type 2 diabetes have not been reported, but C/*
result in lower fasting BG levels for at least 24 h postexercise in individuals with IFG.
A combination of aerobic and resistance exercise training may be more effective in B/*
improving BG control than either alone; however, more studies are needed to
determine whether total caloric expenditure, exercise duration, or exercise mode is
responsible.
Milder forms of exercise (e.g., tai chi, yoga) have shown mixed results. C/*
PA can result in acute improvements in systemic insulin action lasting from 2 to 72 h. A/*
Chronic effects of Both aerobic and resistance training improve insulin action, BG control, and fat B/*
exercise training oxidation and storage in muscle.
Resistance exercise enhances skeletal muscle mass. A/*
Blood lipid responses to training are mixed but may result in a small reduction in LDL C/*
cholesterol with no change in HDL cholesterol or triglycerides. Combined weight loss
and PA may be more effective than aerobic exercise training alone on lipids.
Aerobic training may slightly reduce systolic BP, but reductions in diastolic BP are less C/*
common, in individuals with type 2 diabetes.
Observational studies suggest that greater PA and fitness are associated with a lower C/*
risk of all-cause and CV mortality.
Recommended levels of PA may help produce weight loss. However, up to 60 min/day C/*
may be required when relying on exercise alone for weight loss.
Individuals with type 2 diabetes engaged in supervised training exhibit greater B/*
compliance and BG control than those undertaking exercise training without
supervision.
Increased PA and physical fitness can reduce symptoms of depression and improve B/*
health-related QOL in those with type 2 diabetes.
PA and prevention of At least 2.5 h/week of moderate to vigorous PA should be undertaken as part of A/A
type 2 diabetes lifestyle changes to prevent type 2 diabetes onset in high-risk adults.
PA in prevention and Epidemiological studies suggest that higher levels of PA may reduce risk of developing C/*
control of GDM GDM during pregnancy.
RCTs suggest that moderate exercise may lower maternal BG levels in GDM. B/*
Preexercise evaluation Before undertaking exercise more intense than brisk walking, sedentary persons with C/C
type 2 diabetes will likely benefit from an evaluation by a physician. ECG exercise
stress testing for asymptomatic individuals at low risk of CAD is not recommended but
may be indicated for higher risk.
Recommended PA Persons with type 2 diabetes should undertake at least 150 min/week of moderate to B/B
participation for vigorous aerobic exercise spread out during at least 3 days during the week, with no
persons with type 2 more than 2 consecutive days between bouts of aerobic activity.
diabetes In addition to aerobic training, persons with type 2 diabetes should undertake B/B
moderate to vigorous resistance training at least 23 days/week.
Supervised and combined aerobic and resistance training may confer additional health B/C
benefits, although milder forms of PA (such as yoga) have shown mixed results.
Persons with type 2 diabetes are encouraged to increase their total daily unstructured
PA. Flexibility training may be included but should not be undertaken in place of
other recommended types of PA.
(continued)

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Table 2Continued

ACSM evidence category


(A, highest; D, lowest)/
ADA level of evidence
ACSM evidence and ADA clinical practice recommendation statements (A, highest; E, lowest)
Exercise with Individuals with type 2 diabetes may engage in PA, using caution when exercising with C/E
nonoptimal BG BG levels exceeding 300 mg/dl (16.7 mmol/l) without ketosis, provided they are
control feeling well and are adequately hydrated.
Persons with type 2 diabetes not using insulin or insulin secretagogues are unlikely to C/C
experience hypoglycemia related to PA. Users of insulin and insulin secretagogues are
advised to supplement with carbohydrate as needed to prevent hypoglycemia during
and after exercise.
Medication effects on Medication dosage adjustments to prevent exercise-associated hypoglycemia may be C/C
exercise responses required by individuals using insulin or certain insulin secretagogues. Most other
medications prescribed for concomitant health problems do not affect exercise, with
the exception of -blockers, some diuretics, and statins.
Exercise with long-term Known CVD is not an absolute contraindication to exercise. Individuals with angina C/C
complications of classified as moderate or high risk should likely begin exercise in a supervised cardiac
diabetes rehabilitation program. PA is advised for anyone with PAD.
Individuals with peripheral neuropathy and without acute ulceration may participate B/B
in moderate weight-bearing exercise. Comprehensive foot care including daily
inspection of feet and use of proper footwear is recommended for prevention and early
detection of sores or ulcers. Moderate walking likely does not increase risk of foot
ulcers or reulceration with peripheral neuropathy.
Individuals with CAN should be screened and receive physician approval and possibly C/C
an exercise stress test before exercise initiation. Exercise intensity is best prescribed
using the HR reserve method with direct measurement of maximal HR.
Individuals with uncontrolled proliferative retinopathy should avoid activities that D/E
greatly increase intraocular pressure and hemorrhage risk.
Exercise training increases physical function and QOL in individuals with kidney C/C
disease and may even be undertaken during dialysis sessions. The presence of
microalbuminuria per se does not necessitate exercise restrictions.
Adoption and Efforts to promote PA should focus on developing self-efficacy and fostering social B/B
maintenance of support from family, friends, and health care providers. Encouraging mild or moderate
exercise by persons PA may be most beneficial to adoption and maintenance of regular PA participation.
with diabetes Lifestyle interventions may have some efficacy in promoting PA behavior.
*No recommendation given.

Insulin resistance (21,64,95), more prolonged or intense PA aerobic training seems to be related to gains
Acute changes in muscular insulin re- acutely enhances insulin action for longer in peripheral, not hepatic, insulin action
sistance. Most benefits of PA on type 2 periods (9,29,75,111,160,238). (146,282). Such training not resulting in
diabetes management and prevention are Acute improvements in insulin sensi- overall weight loss may still reduce hepatic
realized through acute and chronic im- tivity in women with type 2 diabetes have lipid content and alter fat partitioning and
provements in insulin action (29,46, been found for equivalent energy expen- use in the liver (128).
116,118,282). The acute effects of a re- ditures whether engaging in low-intensity Evidence statement. PA can result in
cent bout of exercise account for most of or high-intensity walking (29) but may be acute improvements in systemic insulin
the improvements in insulin action, with affected by age and training status action lasting from 2 to 72 h. ACSM evi-
most individuals experiencing a decrease (24,75,100,101,228). For example, mod- dence category A.
in their BG levels during mild- and mod- erate- to heavy-intensity aerobic training
erate-intensity exercise and for 272 h af- undertaken three times a week for 6 CHRONIC EFFECTS OF
terward (24,83,204). months improved insulin action in both EXERCISE TRAINING
BG reductions are related to the dura- younger and older women but persisted Metabolic control: BG levels and insu-
tion and intensity of the exercise, preex- only in the younger group for 72120 h. lin resistance. Aerobic exercise has been
ercise control, and state of physical Acute changes in livers ability to pro- the mode traditionally prescribed for dia-
training (24,26,47,238). Although previ- cess glucose. Increases in liver fat con- betes prevention and management. Even
ous PA of any intensity generally exerts its tent common in obesity and type 2 diabetes 1 week of aerobic training can improve
effects by enhancing uptake of BG for gly- are strongly associated with reduced he- whole-body insulin sensitivity in individ-
cogen synthesis (40,83) and by stimulat- patic and peripheral insulin action. En- uals with type 2 diabetes (282). Moderate
ing fat oxidation and storage in muscle hanced whole-body insulin action after and vigorous aerobic training improve in-

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sulin sensitivity (9,75,83,111), albeit for that aerobic training decreases total and (175,238,283). Carefully designed RCTs
only a period of hours to days (141), but a LDL cholesterol and raises HDL choles- using increasing levels of PA also failed to
lesser intensity may also improve insulin terol (130,229). One larger RCT found show any change in BP despite substan-
action to some degree (111). Training can decreases in total cholesterol with both tially increased PA (6,258).
enhance the responsiveness of skeletal aerobic and yoga training but no changes Evidence statement. Aerobic training
muscles to insulin with increased expres- in HDL cholesterol or LDL cholesterol may slightly reduce systolic BP, but re-
sion and/or activity of proteins involved (98), although most have found no effect ductions in diastolic BP are less common,
in glucose metabolism and insulin signal- of any form of exercise training on lipids in individuals with type 2 diabetes. ACSM
ing (39,110,204,270). Moderate training (6,175,178,238,258,267). RCTs de- evidence category C.
may increase glycogen synthase activity signed to increase PA also had no effect on Mortality and CV risk. Higher levels of
and GLUT4 protein expression but not the cholesterol profile in type 2 diabetes, physical fitness and PA are associated
insulin signaling (39). Fat oxidation is with most also finding no change in trig- with lower CV risk and mortality in both
also a key aspect of improved insulin ac- lycerides (6,175,238,258,267). A meta- healthy and clinical populations (19,
tion, and training increases lipid storage analysis of training effects on blood lipids 153,164,207). Increases in PA and phys-
in muscle and fat oxidation capacity in adults with type 2 diabetes found, how- ical fitness are also associated with re-
(64,95,136,223). ever, that LDL cholesterol may be reduced duced early mortality in both populations
An individuals training status will af- by 5% (136). as well (19,42,153,163,164,186,272).
fect the use of carbohydrate during an aer- Lipid profiles may benefit more from All-cause and CV mortality risk was 1.7
obic activity. Aerobic training increases concomitant exercise training and weight 6.6 times higher in low-fit compared with
fat utilization during a similar duration reduction. Some studies using intensive high-fit men with type 2 diabetes, with
bout of low- or moderate-intensity activ- diet and aerobic exercise interventions re- the fittest men exhibiting the lowest risk
ity done after training, which spares mus- ported large reductions in total choles- (42,43). A work capacity 10 METs
cle glycogen and BG and results in a lesser terol and triglycerides but failed to (where 1 MET is defined as the equivalent
acute decrease in BG (28,83,223). Type 2 include controls (12,13). In the Look of resting metabolic rate) carries the low-
diabetes may be associated with a de- AHEAD (Action for Health in Diabetes) est risk, independent of obesity
crease in lipid oxidation and shift toward study, intensive lifestyle participants ex- (42,153,186). No RCT data on the effects
greater carbohydrate oxidation at all exer- hibited greater decreases in triglycerides of changes in physical fitness on mortality
cise intensities (87). and increases in HDL cholesterol than the in diabetes exist.
Resistance exercise training also ben- control group, while both the intensive Evidence statement. Observational
efits BG control and insulin action in type lifestyle and usual care groups decreased studies suggest that greater PA and fitness
2 diabetes (46,65,115,116,118,246). In a LDL cholesterol (218). Most lifestyle in- are associated with a lower risk of all-
randomized controlled trial (RCT), twice- terventions have been accompanied by an cause and CV mortality. ACSM evidence
weekly progressive resistance training for approximate 5-kg weight loss. category C.
16 weeks by older men with newly diag- Evidence statement. Blood lipid re- Body weight: maintenance and loss.
nosed type 2 diabetes resulted in a 46.3% sponses to training are mixed but may result The most successful programs for long-
increase in insulin action, a 7.1% reduc- in a small reduction in LDL cholesterol with term weight control have involved com-
tion in fasting BG levels, and significant no change in HDL cholesterol or triglycer- binations of diet, exercise, and behavior
loss of visceral fat (116). An increase in ides. Combined weight loss and PA may be modification (281). Exercise interven-
muscle mass from resistance training may more effective than aerobic exercise training tions undertaken with volumes typically
contribute to BG uptake from a mass ef- alone on lipids. ACSM evidence category C. recommended to improve BG control and
fect, and heavy weight training in partic- Hypertension. Hypertension is a com- reduce CVD risk (e.g., 150 min/week of
ular may reverse or prevent further loss of mon comorbidity affecting more than brisk walking) are usually insufficient for
skeletal muscle due to disuse and aging 60% of individuals with type 2 diabetes major weight loss (24), likely because
(34,276). In another RCT, all 20 men (201,249). The risk of vascular complica- obese and older people frequently have
with type 2 diabetes who participated in tions in hypertensive individuals with difficulty performing sufficient exercise to
either resistance or aerobic exercise thrice type 2 diabetes is 66 100% higher than create a large energy deficit and can easily
weekly for 10 weeks improved their over- with either condition alone (103,195). counterbalance expenditures by eating
all BG control, but those doing resistance Both aerobic and resistance training can more (281). However, in RCTs, about 1 h
training had significantly lower A1C val- lower BP in nondiabetic individuals, with of daily moderate aerobic exercise pro-
ues (32). Diabetic women undergoing 12 slightly greater effects observed with the duces at least as much fat loss as equiva-
weeks of low-intensity training with resis- former (49,134,135,137). Most observa- lent caloric restriction, with resultant
tance bands had gains in strength and tional studies show that both exercises greater insulin action (231,232).
muscle mass and loss of fat mass but had lower BP in diabetic individuals (35, The optimal volume of exercise to
no change in insulin sensitivity (157). 46,78,208,267). Several RCTs have achieve sustained major weight loss is
Evidence statement. Both aerobic and shown reductions in systolic BP (4 8 probably much larger than the amount
resistance training improve insulin ac- mmHg), but only one reported a slightly required to achieve improved BG control
tion, BG control, and fat oxidation and lower diastolic BP (11,130,140,176). The and CV health (24,217). In observational
storage in muscle. ACSM evidence category Look AHEAD trial found reductions in studies (234,235,274), individuals who
B. Resistance exercise enhances skeletal both systolic and diastolic BP with exer- successfully maintained large weight loss
muscle mass. ACSM evidence category A. cise and weight loss (218), but several during at least a year typically engaged in
Lipids and lipoproteins. Small RCTs studies have reported no changes in BP 7 h/week of moderate- to vigorous-
involving type 2 diabetes have reported with training in type 2 diabetes intensity exercise (62). Two RCTs found

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that higher exercise volumes (2,000 and psychological well-being was signifi- min of strenuous, or 5 min of very stren-
2,500 kcal/week) produced greater and cantly improved among individuals who uous exercise one to two times a day) re-
more sustained weight loss than 1,000 exercised for disease prevention, it dete- duced diabetes risk by 46% (compared
kcal/week of exercise (123,124). riorated significantly when undertaken with 42% for diet plus exercise and 31%
Evidence statement. Recommended lev- for management of CVD, end-stage renal for diet alone). The Finnish Diabetes Pre-
els of PA may help produce weight loss. disease, pulmonary disease, neurological vention Study (74,260) and the U.S. Dia-
However, up to 60 min/day may be re- disorders, and cancer (90). These find- betes Prevention Program (DPP) (149)
quired when relying on exercise alone for ings suggest that benefits may vary, with included intensive, lifestyle modifications
weight loss. ACSM evidence category C. those with fewer existing complications with both diet and increased PA. In the
Supervision of training. Exercise inter- benefiting the most. former, 522 middle-aged, overweight
vention studies showing the greatest ef- Meta-analyses of clinically depressed adults with IGT completed either lifestyle
fect on BG control have all involved men and women of all age-groups found modifications of at least 30 min of daily,
supervision of exercise sessions by quali- substantial decreases in depressive symp- moderate PA, or no change in behavior
fied exercise trainers (34,65,196,238). toms after both short and long courses of (74,260). The DPP randomized 3,234
The most direct test of the incremental exercise (50) and clinical depression and men and women with IGT or IFG into
benefits of supervised training was the depressive symptoms among the aged control, medication (metformin), or life-
Italian Diabetes and Exercise Study (11). (243). Potential mechanisms of exercise style modification groups, composed of
In this 1-year trial, all 606 participants with include psychological factors, such as in- dietary and weight loss goals and 150 min
type 2 diabetes (both intervention and con- creased self-efficacy, a sense of mastery, of weekly aerobic activity (149). Lifestyle
trol) received high-quality exercise counsel- distraction, and changes in self-concept, modification in both studies reduced in-
ing that increased self-reported PA as well as physiological factors such as in- cident diabetes by 58% and, in the DPP,
substantially. The intervention group also creased central norepinephrine transmis- had a greater effect than metformin
received supervised, facility-based com- sion, changes in the hypothalamic (31%). Weight loss was the dominant
bined aerobic and resistance exercise adrenocortical system (63), serotonin predictor of a lower incidence, but in-
training twice weekly, resulting in greater synthesis and metabolism (61), and en- creased PA reduced risk of type 2 diabetes
improvements in overall BG control, BP, dorphins. Regular PA may improve psy- even when weight loss goals were not
BMI, waist circumference, HDL choles- chological well-being, health-related achieved (104,158,173). PA seems to
terol, and estimated 10-year CVD risk. A QOL, and depression in individuals with play a role in preventing type 2 diabetes
recent systematic review of 20 resistance type 2 diabetes, among whom depression across ethnic groups and in both sexes
training studies on type 2 diabetes (97) is more common than in the general pop- (154,224).
found that supervised training of varying ulation (73). Data show that moderate exercise
volume, frequency, and intensity im- Evidence statement. Increased PA and such as brisk walking reduces risk of type
proved BG control and insulin sensitivity, physical fitness can reduce symptoms of 2 diabetes (108,113,114,154,224), and
but that when supervision was removed, depression and improve health-related all studies support the current recom-
compliance and BG control both QOL in those with type 2 diabetes. ACSM mendation of 2.5 h/week of a moderate
deteriorated. evidence category B. aerobic activity or typically 30 min/day
Evidence statement. Individuals with for 5 days/week for prevention. A meta-
type 2 diabetes engaged in supervised PA AND PREVENTION OF analysis of 10 cohort studies (125) that
training exhibit greater compliance and TYPE 2 DIABETES Participation assessed the preventive effects of moder-
BG control than those undertaking exer- in regular PA improves BG control and ate-intensity PA found that risk reduction
cise training without supervision. ACSM can prevent or delay onset of type 2 dia- for type 2 diabetes was 0.70 (0.58 0.84)
evidence category B. betes (64,104,149,158, 170,260). Pro- for walking on a regular basis (typically
Psychological effects. Exercise likely spective cohort and cross-sectional briskly for 2.5 h/week). The preventive
has psychological benefits for persons observational studies that assessed PA effects of resistance training have not been
with type 2 diabetes, although evidence with questionnaires showed that higher studied.
for acute and chronic psychological ben- PA levels are associated with reduced risk Type 2 diabetes is also increasing in
efits is limited. In the Look AHEAD trial, for type 2 diabetes, regardless of method prevalence in children and adolescents,
participants in the intensive lifestyle inter- of activity assessment, ranges of activity with increasingly sedentary behavior and
vention attempted to lose more than 7% categories, and statistical methods obesity as key contributors. No RCTs
of their initial weight and increase mod- (108,113,182). Both moderate walking have been completed that address
erately intense PA to greater than 175 and vigorous activity have been associ- whether PA or exercise prevents type 2
min/week. They had improvements in ated with a decreased risk, and greater diabetes in youth. However, limited stud-
health-related (SF-36 physical compo- volumes of PA may provide the most pre- ies suggest that, to prevent and manage
nent scores) quality of life (QOL) and de- vention (113). Observational studies have type 2 diabetes, goals for youth should
pression symptoms after 12 months that reported that greater fitness is associated include limiting daily screen time (televi-
were mediated by enhanced physical fit- with a reduced risk of developing type 2 sion, computer, or video game) to less
ness (280). diabetes (251,273), even if only moder- than 60 min/day and doing at least 60
However, it seems that individuals ate-intensity exercise is undertaken. min/day of PA (188). A multicenter trial
who undertake exercise to prevent a The Da Qing study in China (211) (the TODAY study) is currently underway
chronic disease fare better than those who included an exercise-only treatment arm to assess the role of PA as part of a behav-
undertake it to manage an existing one. A and reported that even modest changes in ioral lifestyle intervention aimed at pre-
recent meta-analysis found that while exercise (20 min of mild or moderate, 10 venting type 2 diabetes in youth (254).

care.diabetesjournals.org DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 e153
Exercise and type 2 diabetes

Evidence statement. At least 2.5 h/week changes (239). For individuals desiring to for previously sedentary individuals with
of moderate to vigorous PA should be un- participate in low-intensity PA such as diabetes who want to undertake activity
dertaken as part of lifestyle changes to walking, health care providers should use more intense than brisk walking. The goal
prevent type 2 diabetes onset in high-risk clinical judgment in deciding whether to is to more effectively target individuals at
adults. ACSM evidence category A. ADA A recommend preexercise testing (3). Con- higher risk for underlying CVD (239).
level recommendation. ducting exercise stress testing before The UKPDS Risk Engine (http://www.
walking is unnecessary. No evidence sug- dtu.ox. ac.uk/riskengine/download.htm)
PA AND PREVENTION AND gests that it is routinely necessary as a (248) can also be used to calculate ex-
CONTROL OF GDM As the prev- CVD diagnostic tool, and requiring it may pected 10-year CV risk based on age, sex,
alenceofdiabetescontinuestoriseworldwide, create barriers to participation. smoking, A1C, diabetes duration, lipids,
it becomes increasingly important to identify For exercise more vigorous than brisk BP, and race.
high-risk populations and to implement strat- walking or exceeding the demands of ev- In general, electrocardiogram (ECG)
egies to delay or prevent diabetes onset. eryday living, sedentary and older dia- stress testing may be indicated for indi-
Women diagnosed with GDM are at substan- betic individuals will likely benefit from viduals matching one or more of these
tially increased risk of developing type 2 dia- being assessed for conditions that might criteria:
betes; therefore, PA may be considered a tool be associated with risk of CVD, contrain- Age 40 years, with or without CVD
to prevent both GDM and possibly type 2 di- dicate certain activities, or predispose to risk factors other than diabetes
abetes at a later date (70). Prepregnancy PA injuries, including severe peripheral neu- Age 30 years and
has been consistently associated with a re- ropathy, severe autonomic neuropathy, Type 1 or type 2 diabetes of 10
duced risk of GDM (57,58,69,206, 290). and preproliferative or proliferative reti- years in duration
Studies during pregnancy are sparse, with nopathy (240). Before undertaking new Hypertension
only one case-control study (57), one retro- higher-intensity PA, they are advised to Cigarette smoking
spective study (174), and one study of a co- undergo a detailed medical evaluation Dyslipidemia
hort of Hispanic women (37) observing and screening for BG control, physical Proliferative or preproliferative reti-
significant protective effects of PA, while oth- limitations, medications, and macrovascu- nopathy
ers have not (58,69,206). lar and microvascular complications (3). Nephropathy including microalbu-
Engaging in 30 min of moderate- This assessment may include a graded minuria
intensity PA (e.g., brisk walking) during exercise test depending on the age of the Any of the following, regardless of age
most days of the week (e.g., 2.5 h/week) person, diabetes duration, and the pres- Known or suspected CAD, cerebro-
has been adopted as a recommendation ence of additional CVD risk factors vascular disease, and/or peripheral
for pregnant women without medical or (3,240). The prevalence of symptomatic artery disease (PAD)
obstetrical complications (222). How- and asymptomatic coronary artery dis- Autonomic neuropathy
ever, few primary prevention studies have ease (CAD) is greater in individuals with Advanced nephropathy with renal
examined whether making a change in PA type 2 diabetes (72,155), and maximal failure
reduces risk of developing GDM. In 2006, graded exercise testing can identify a
a meta-analysis reviewed four RCTs on small proportion of asymptomatic per- Use of these criteria does not exclude
GDM in which pregnant women in their sons with severe coronary artery obstruc- the possibility of conducting ECG stress
third trimester exercised on a cycle or arm tion (52). testing on individuals with a low CAD risk
ergometer or performed resistance train- Most young individuals with a low or those who planning to engage in less
ing three times a week for 20 45 min CAD risk may not benefit from preexer- intense exercise (248). In the absence of
compared with doing no specific program cise stress testing. In the Look AHEAD contraindications to maximal stress test-
(36). The women involved in exercise had trial, although exercise-induced abnor- ing, it can still be considered for anyone
better BG control, lower fasting and post- malities were present in 1,303 (22.5%) with type 2 diabetes. Although clinical ev-
prandial glucose concentrations, and im- participants, only older age was associ- idence does not definitively determine
proved cardiorespiratory fitness, ated with increased prevalence of all ab- who should undergo such testing, poten-
although frequency of prescription of in- normalities during maximal testing (52). tial benefits should be weighed against the
sulin to control BG did not differ from A systematic review of the U.S. Preventive risk associated with unnecessary proce-
nonexercisers, and pregnancy outcomes Services Task Force (USPSTF) concluded dures for each individual (155,239).
were unchanged. that stress testing should not be routinely In individuals with positive or non-
Evidence statement. Epidemiological recommended to detect ischemia in specific ECG changes in response to exer-
studies suggest that higher levels of PA asymptomatic individuals with a low cise, or with nonspecific ST- and T-wave
may reduce risk of developing GDM dur- CAD risk (10% risk of a cardiac event changes at rest, follow-up testing may be
ing pregnancy. ACSM evidence category C. more than 10 years) because the risks performed (236). However, the DIAD
RCTs suggest that moderate exercise may from invasive testing done after a false- trial involving 1,123 individuals with
lower maternal BG levels in GDM. ACSM positive test outweigh the benefits of its type 2 diabetes and no symptoms of CAD
evidence category B. detection (79,262). The lower the CAD found that screening with adenosine-
risk, the higher the chance of a false pos- stress radionuclide myocardial perfusion
PREEXERCISE EVALUATION itive (79,248). imaging for myocardial ischemia more
Safe exercise participation can be compli- Current guidelines attempt to avoid than 4.8 years did not alter rates of cardiac
cated by the presence of diabetes-related automatic inclusion of lower-risk individ- events (288); thus, the cost-effectiveness
health complications such as CVD, hyper- uals with type 2 diabetes, stating that ex- and diagnostic value of more intensive
tension, neuropathy, or microvascular ercise stress testing is advised primarily testing remains in question.

e154 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.org
Colberg and Associates

There is no evidence available to de- analysis (25) showed that exercise lute intensity for less time and achieve the
termine whether preexercise evaluation intensity predicts improvements in over- same benefits.
involving stress testing is necessary or all BG control to a greater extent than ex- Mode. Any form of aerobic exercise (in-
beneficial before participation in anaero- ercise volume, suggesting that those cluding brisk walking) that uses large
bic or resistance training. At present, most already exercising at a moderate intensity muscle groups and causes sustained in-
testing centers are equipped for maximal should consider undertaking some vigor- creases in HR is likely to be beneficial
stress testing but not for an alternate form ous PA to obtain additional BG (and likely (114), and undertaking a variety of modes
of testing involving resistance exercise. CV) benefits. of PA is recommended (217).
Moreover, coronary ischemia is less likely Duration. Individuals with type 2 diabe- Rate of progression. At present, no
to occur during resistance compared with tes should engage in a minimum of 150 study on individuals with type 2 diabetes
aerobic exercise eliciting the same heart min/week of exercise undertaken at mod- has compared rates of progression in ex-
rate (HR), and some doubt exists as to erate intensity or greater. Aerobic activity ercise intensity or volume. Gradual pro-
whether resistance exercise induces isch- should be performed in bouts of at least gression of both is advisable to minimize
emia (77,88). A review of 12 studies of 10 min and be spread throughout the the risk of injury, particularly if health
resistance exercise in men with known week. Around 150 min/week of moder- complications are present, and to en-
CAD found no angina, ST depression, ab- ate-intensity exercise is associated with hance compliance.
normal hemodynamics, ventricular dys- reduced morbidity and mortality in ob- Body weight loss and maintenance.
rhythmias, or other complications during servational studies in all populations The most successful weight control pro-
such exercise (275). (217). The average weekly duration in grams involve combinations of exercise,
Evidence statement. Before undertaking meta-analyses of exercise interventions in diet, and behavior modification. People
exercise more intense than brisk walking, type 2 diabetes (24,246,255), including who successfully maintain a large weight
sedentary persons with type 2 diabetes higher-intensity aerobic exercise (196), loss report exercising about 7 h/week
will likely benefit from an evaluation by a has been in a similar range. Recent joint (62,212,234,235,274).
physician. ECG exercise stress testing for ACSM/American Heart Association Evidence statement. Persons with type 2
asymptomatic individuals at low risk of guidelines (105,202) recommended 150 diabetes should undertake at least 150
CAD is not recommended but may be in- min of moderate activity (30 min, 5 days/ min/week of moderate to vigorous aero-
dicated for higher risk. ACSM evidence cat- week) or 60 min of vigorous PA (20 min bic exercise spread out during at least 3
egory C. ADA C level recom- days during the week, with no more than
on 3 days) for all adults, whereas recent
mendation. 2 consecutive days between bouts of aer-
U.S. federal guidelines (217) recom-
obic activity. ACSM evidence category B.
mended 150 min of moderate or 75 min
RECOMMENDED PA ADA B level recommendation.
of vigorous activity, or an equivalent com-
PARTICIPATION FOR
bination, spread throughout each week.
PERSONS WITH TYPE 2 Resistance exercise training
The U.S. federal guidelines (217) sug-
DIABETES Just 39% of adults with Frequency. Resistance exercise should
diabetes are physically active compared gest that an exercise volume of 500 be undertaken at least twice weekly on
with 58% of other American adults (193). 1,000 MET min/week (MET equivalent nonconsecutive days (1,105,202,217,
However, for most people with type 2 di- of PA number of minutes) is optimal 239,240), but more ideally three times a
abetes, exercise is recommended for dia- and can be achieved, for example, with week (65,246), as part of a PA program
betes management and can be 150 min/week of walking at 6.4 km/h (4 for individuals with type 2 diabetes, along
undertaken safely and effectively. mph; intensity of 5 METs) or 75 min of with regular aerobic activities.
jogging at 9.6 km/h (6 mph; 10 METs). Intensity. Training should be moderate
Aerobic exercise training Unfortunately, most people with type 2 (50% of 1-repetition maximum [1-RM])
Frequency. Aerobic exercise should be diabetes do not have sufficient aerobic ca- or vigorous (75 80% of 1-RM) for opti-
performed at least 3 days/week with no pacity to jog at 9.6 km/h for that weekly mal gains in strength and insulin action
more than 2 consecutive days between duration, and they may have orthopedic (1,97,239,240,263). Home-based resis-
bouts of activity because of the transient or other limitations. In a meta-analysis, tance training following supervised, gym-
nature of exercise-induced improvements the mean maximal aerobic capacity in di- based training may be less effective for
in insulin action (26,141). Most clinical abetic individuals was only 22.4 ml/kg/ maintaining BG control but adequate for
trials evaluating exercise interventions in min, or 6.4 METs (25), making 4.8 METs maintaining muscle mass and strength
type 2 diabetes have used a frequency of (75% of maximal) the highest sustainable (66).
three times per week (24,238,246,255), intensity. Therefore, most diabetic indi- Duration. Each training session should
but current guidelines for adults generally viduals will require at least 150 min of minimally include 510 exercises involv-
recommend five sessions of moderate ac- moderate to vigorous aerobic exercise per ing the major muscle groups (in the upper
tivity (105,202,217). week to achieve optimal CVD risk reduc- body, lower body, and core) and involve
Intensity. Aerobic exercise should be at tion. Some CV and BG benefits may be completion of 10 15 repetitions to near
least at moderate intensity, correspond- gained from lower exercise volumes (a fatigue per set early in training (1,
ing approximately to 40 60% of VO2max minimum dose has not been established), 97,239,240,263), progressing over time to
(maximal aerobic capacity). For most whereas further benefit likely results from heavier weights (or resistance) that can be
people with type 2 diabetes, brisk walking engaging in durations beyond recom- lifted only 810 times. A minimum of one set
is a moderate-intensity exercise. Addi- mended amounts. Individuals with of repetitions to near fatigue, but as many as
tional benefits may be gained from vigor- higher aerobic capacities (10 METs) three to four sets, is recommended for optimal
ous exercise (60% of VO2max). A meta- may be able to exercise at a higher abso- strength gains.

care.diabetesjournals.org DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 e155
Exercise and type 2 diabetes

Mode. Resistance machines and free Daily movement (unstructured have shown mixed results. Persons with
weights (e.g., dumbbells and barbells) activity) type 2 diabetes are encouraged to increase
can result in fairly equivalent gains in Individuals with type 2 diabetes are en- their total daily unstructured PA. Flexibil-
strength and mass of targeted muscles couraged to increase their total daily, un- ity training may be included but should
(66). Heavier weights or resistance may structured PA to gain additional health not be undertaken in place of other rec-
be needed for optimization of insulin ac- benefits. Nonexercise activity thermogen- ommended types of PA. ACSM evidence
tion and BG control (276). esis (i.e., energy expending for activities category B. ADA C level recommendation.
Rate of progression. To avoid injury, of daily living) can create a large daily ca-
progression of intensity, frequency, and loric deficit to prevent excessive weight EXERCISE WITH
duration of training sessions should occur gain (168,169). In an observational NONOPTIMAL BG CONTROL
slowly. In most progressive training, in- study, obese individuals sat for about Hyperglycemia. While hyperglycemia
creases in weight or resistance are under- 2.5 h more and walked an average of 3.5 can be worsened by exercise in type 1 di-
taken first and only once when the target miles/day or less than their lean counter- abetic individuals who are insulin defi-
parts do. Most of the lean subjects greater cient and ketotic (due to missed or
number of repetitions per set can consis-
activity came from walks of short dura- insufficient insulin), very few persons
tently be exceeded, followed by a greater
tion (15 min) and low velocity (1 with type 2 diabetes develop such a pro-
number of sets and lastly by increased mph) (168). found degree of insulin deficiency. There-
training frequency. Progression for 6 Moreover, use of objective measures fore, individuals with type 2 diabetes
months to thrice-weekly sessions of three such as step counters may enhance reach- generally do not need to postpone exer-
sets of 8 10 repetitions done at 75 to 80% ing daily goals. A meta-analysis of 26 cise because of high BG, provided that
of 1-RM on 8 10 exercises may be an op- studies with a total of 2,767 (primarily they are feeling well. If they undertake
timal goal (65). nondiabetic) participants (8 RCTs and 18 strenuous physical activities with elevated
Evidence statement. In addition to aero- observational studies) found that pedom- glucose levels (300 mg/dl or 16.7
bic training, persons with type 2 diabetes eter users increased PA by 26.9% over mmol/l), it is prudent to ensure that they
should undertake moderate to vigorous baseline in studies having an average in- are adequately hydrated (3). If hypergly-
resistance training at least 23 days/week. tervention of 18 weeks (30). An impor- cemic after a meal, individuals with type 2
ACSM evidence category B. ADA B level tant predictor of increased PA was the use diabetes will still likely experience a re-
recommendation. of a goal, such as to take 10,000 steps per duction in BG during aerobic work be-
day (30). cause endogenous insulin levels will
likely be higher at that time (221).
Supervised training Flexibility training Evidence statement. Individuals with
Initial instruction and periodic supervi- Flexibility training may be included as type 2 diabetes may engage in PA, using
sion by a qualified exercise trainer is rec- part of a PA program, although it should caution when exercising with BG levels
ommended for most persons with type 2 not substitute for other training. Older exceeding 300 mg/dl (16.7 mmol/l) with-
diabetes, particularly if they undertake re- adults are advised to undertake exercises out ketosis, provided they are feeling well
sistance exercise training, to ensure opti- that maintain or improve balance and are adequately hydrated. ACSM
mal benefits to BG control, BP, lipids, and (202,217), which may include some flex- evidence category C. ADA E level
CV risk and to minimize injury risk (11). ibility training, particularly for many recommendation.
older individuals with type 2 diabetes Hypoglycemia: causes and prevention.
with a higher risk of falling (194). Al- Of greatest concern to many exercisers is
Combined aerobic and resistance though flexibility exercise (stretching) the risk of hypoglycemia. In individuals
and other types of training has frequently been recommended as a whose diabetes is being controlled by life-
Inclusion of both aerobic and resistance means of increasing joint range of motion style alone, the risk of developing hypo-
exercise training is recommended. Com- (ROM) and reducing risk of injury, two glycemia during exercise is minimal,
bined training thrice weekly in individu- systematic reviews found that flexibility making stringent measures unnecessary
exercise does not reduce risk of exercise- to maintain BG (239). Glucose monitor-
als with type 2 diabetes may be of greater
induced injury (237,287). A small RCT ing can be performed before and after PA
benefit to BG control than either aerobic
found that ROM exercises modestly de- to assess its unique effect. Activities of
or resistance exercise alone (238). How-
creased peak plantar pressures (94), but longer duration and lower intensity
ever, the total duration of exercise and no study has directly evaluated whether generally cause a decline in BG levels but
caloric expenditure was greatest with such training reduces risk of ulceration or not to the level of hypoglycemia
combined training in all studies done to injury in type 2 diabetes. However, flexi- (9,29,75,111,160). While very intense
date (51,183,238), and both types of bility exercise combined with resistance activities can cause transient elevations in
training were undertaken together on the training can increase ROM in individuals BG (156,252,253), intermittent high-
same days. No studies have yet reported with type 2 diabetes (109) and allow in- intensity exercise done immediately after
whether daily, but alternating, training is dividuals to more easily engage in activi- breakfast in individuals treated with diet
more effective or the BG effect of isoca- ties that require greater ROM around only reduces BG levels and insulin secre-
loric combinations of training. Milder joints. tion (160).
forms of PA, such as yoga and tai chi, may Evidence statement. Supervised and In insulin or insulin secretagogue us-
benefit control of BG (98,117,269, combined aerobic and resistance training ers, who frequently have the effects of
286,291), although their inclusion is not may confer health additional benefits, al- both exercise and insulin to increase glu-
supported conclusively at this time. though milder forms of PA (such as yoga) cose uptake, PA can complicate diabetes

e156 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.org
Colberg and Associates

management (138,198,230,293). For dosing before (and possibly after) exercise exception of -blockers, some diuretics,
preexercise BG levels of less than 100 (83,161). Before planned exercise, short- and statins. ACSM evidence category C.
mg/dl (5.5 mmol/l), ADA recommends acting insulin doses will likely have to be ADA C level recommendation.
that carbohydrate be ingested before any reduced to prevent hypoglycemia.
PA (3), but this applies only to individuals Newer, synthetic, rapid-acting insulin an- EXERCISE WITH LONG-
taking insulin or the secretagogues more alogs (i.e., lispro, aspart, and glulisine) in- TERM COMPLICATIONS OF
likely to cause hypoglycemia (e.g., sulfo- duce more rapid decreases in BG than DIABETES
nylureas such as glyburide, glipizide, and regular human insulin. Individuals will Vascular disease. Individuals with an-
glimepiride, as well as nateglinide and re- need to monitor BG levels before, occa- gina and type 2 diabetes classified as mod-
paglinide) (161,230). If controlled with sionally during, and after exercise and erate or high risk should preferably
diet or other oral medications, most indi- compensate with appropriate dietary exercise in a supervised cardiac rehabili-
viduals will not need carbohydrate sup- and/or medication regimen changes, par- tation program, at least initially (245).
plements for exercise lasting less than an ticularly when exercising at insulin peak Diabetes accelerates the development of
hour. Insulin users should likely consume times. If only longer-acting insulins such atherosclerosis and is a major risk factor
up to 15 g of carbohydrate before exercise as glargine, detemir, and NPH are being for CVD and PAD. Individuals with type
for an initial BG level of 100 mg/dl or absorbed from subcutaneous depots dur- 2 diabetes have a lifetime risk of CAD
lower, with the actual amount dependent ing PA, exercise-induced hypoglycemia is that includes 67% of women and 78% of
on injected insulin doses, exercise dura- not as likely (219), although doses may men and is exacerbated by obesity
tion and intensity, and results of BG mon- need to be reduced to accommodate reg- (22,80,165). Moreover, some individuals
itoring. Intense, short exercise requires ular participation in PA. Doses of select who have an acute myocardial infarction
lesser or no carbohydrate intake (156). oral hypoglycemic agents (glyburide, may not experience chest pain, and up to
Later-onset hypoglycemia is a greater glipizide, glimepiride, nateglinide, and a third may have silent myocardial isch-
concern when carbohydrate stores (i.e., repaglinide) may also need to be lowered emia (45,180).
muscle and liver glycogen) are depleted in response to regular exercise training if For individuals with PAD, with and
during an acute bout of exercise. In par- the frequency of hypoglycemia increases without intermittent claudication and
ticular, high-intensity exercise (e.g., re- (161,230). pain in the extremities during PA, low-to-
peated interval or intense resistance Diabetic individuals are often pre- moderate walking, arm-crank, and cycling
training) can result in substantial deple- scribed a variety of medications for co- exercise have all been shown to enhance
tion of muscle glycogen, thereby increas- morbid conditions, including diuretics, mobility, functional capacity, exercise pain
ing risk for postexercise hypoglycemia in -blockers, ACE inhibitors, aspirin, lipid- tolerance, and QOL (214,295). Lower ex-
users of insulin or insulin secretagogues lowering agents, and more. These medi- tremity resistance training also improves
(161). In such cases, the consumption of cations generally do not affect exercise functional performance measured by tread-
530 g of carbohydrate during and within responses, with some notable exceptions. mill walking, stair climbing ability, and
30 min after exhaustive, glycogen- -Blockers are known to blunt HR re- QOL measures (187).
depleting exercise will lower hypoglyce- sponses to exercise and lower maximal Vascular alterations are common in
mia risk and allow for more efficient exercise capacity to 87% of expected via diabetes, even in the absence of overt vas-
restoration of muscle glycogen (31,247). negative inotropic and chronotropic cular disease. Endothelial dysfunction
Evidence statement. Persons with type 2 effects (241). They may also block adren- may be an underlying cause of many as-
diabetes not using insulin or insulin ergic symptoms of hypoglycemia, in- sociated vascular problems (45,54). In
secretagogues are unlikely to experience creasing the risk of undetected addition to traditional risk factors, hyper-
hypoglycemia related to PA. Users of in- hypoglycemia during exercise. However, glycemia, hyperinsulinemia, and oxida-
sulin and insulin secretagogues are ad- -blockers may increase exercise capacity tive stress contribute to endothelial
vised to supplement with carbohydrate as in those with CAD, rather than lowering damage, leading to poor arterial function
needed to prevent hypoglycemia during it, by reducing coronary ischemia during and greater susceptibility to atherogenesis
and after exercise. ACSM evidence category activity (53). Diuretics, however, may (45,82,289). Both aerobic and resistance
C. ADA C level recommendation. lower overall blood and fluid volumes re- training can improve endothelial function
sulting in dehydration and electrolyte im- (46,294), but not all studies have shown
balances, particularly during exercise in posttraining improvement (283).
MEDICATION EFFECTS ON the heat. Statin use has been associated Evidence statement. Known CVD is not
EXERCISE RESPONSES Current with an elevated risk of myopathies (my- an absolute contraindication to exercise. In-
treatment strategies promote combina- algia and myositis), particularly when dividuals with angina classified as moderate
tion therapies to address the three major combined with use of fibrates and niacin or high risk should likely begin exercise in a
defects in type 2 diabetes: impaired pe- (203). An extended discussion on medi- supervised cardiac rehabilitation program.
ripheral glucose uptake (liver, fat, and cations can be found in the Handbook of PA is advised for anyone with PAD. ACSM
muscle), excessive hepatic glucose release Exercise in Diabetes (2002) (84). evidence category C. ADA C level
(with glucagon excess), and insufficient Evidence statement. Medication dosage recommendation.
insulin secretion. Medication adjust- adjustments to prevent exercise- Peripheral neuropathy. Mild to moder-
ments for PA are generally necessary only associated hypoglycemia may be required ate exercise may help prevent the onset of
with use of insulin and other insulin by individuals using insulin or certain in- peripheral neuropathy (10). Individuals
secretagogues (161,230). To prevent hy- sulin secretagogues. Most other medica- without acute foot ulcers can undertake
poglycemia, individuals may need to re- tions prescribed for concomitant health moderate weight-bearing exercise, al-
duce their oral medications or insulin problems do not affect exercise, with the though anyone with a foot injury or open

care.diabetesjournals.org DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 e157
Exercise and type 2 diabetes

sore or ulcer should be restricted to non cise with maximal HR directly measured, croalbumin in urine. Resistance exercise
weight-bearing PA. All individuals should rather than estimated, for better accuracy training is especially effective in improv-
closely examine their feet on a daily basis (48,265). ing muscle function and activities of daily
to prevent and detect sores or ulcers early Approximately 22% of those with living, which are normally severely af-
and follow recommendations for use of type 2 diabetes have CAN, but most ex- fected by later-stage kidney disease (126).
proper footwear. Previous guidelines hibit alterations in autonomic function Before initiation of PA, individuals with
stated that persons with severe peripheral (292). The presence of CAN doubles the overt nephropathy should be carefully
neuropathy should avoid weight-bearing risk of mortality (48,265) and indicates screened, have physician approval, and
activities to reduce risk of foot ulcerations more frequency of silent myocardial isch- possibly undergo stress testing to detect
(102,264). However, recent studies indi- emia (265), orthostatic hypotension, or CAD and abnormal HR and BP responses
cated that moderate walking does not in- resting tachycardia (76,177). CAN also (1,27). Exercise should be begun at a low
crease risk of foot ulcers or reulceration in impairs exercise tolerance and lowers intensity and volume because aerobic ca-
those with peripheral neuropathy maximal HR (131,265). Although both pacity and muscle function are substan-
(166,167). sympathetic and parasympathetic dys- tially reduced, and avoidance of the
Peripheral neuropathy affects the ex- functions can be present, vagal dysfunc- Valsava maneuver or high-intensity exer-
tremities, particularly the lower legs and tion usually occurs earlier. Slower HR cise to prevent excessive increases in BP is
feet. Hyperglycemia causes nerve toxicity, recovery after PA is associated with mor- advised (1). Supervised, moderate aero-
leading to nerve damage and apoptosis tality risk (38,265). bic exercise undertaken during dialysis
(242,244), which causes microvascular Evidence statement. Individuals with sessions, however, has been shown to be
damage and loss of perfusion. Symptoms CAN should be screened and receive phy- effective as home-based exercise and may
manifest as neuropathic pain and/or loss sician approval and possibly an exercise improve compliance (126,151).
of sensation that, coupled with poor stress test before exercise initiation. Exer- Diabetic nephropathy develops in
blood flow, increase the risk of foot inju- cise intensity is best prescribed using the 30% of individuals with diabetes and is
ries and ulcerations (45,244). Up to 40% HR reserve method with direct measure- a major risk factor for death in those with
of diabetic individuals may experience ment of maximal HR. ACSM evidence cat- diabetes (20,45). Microalbuminuria, or
peripheral neuropathy, and 60% of lower egory C. ADA C level recommendation. minute amounts of albumin in the urine,
extremity amputations in Americans are Retinopathy. In diabetic individuals is common and a risk factor for overt ne-
related to diabetes (166,199,216). with proliferative or preproliferative reti- phropathy (45) and CV mortality (91).
Evidence statement. Individuals with nopathy or macular degeneration, careful Tight BG and BP control may delay pro-
peripheral neuropathy and without acute screening and physician approval are rec- gression of microalbuminuria (127,148),
ulceration may participate in moderate ommended before initiating an exercise along with exercise and dietary changes
weight-bearing exercise. Comprehensive program. Activities that greatly increase (81,162). Exercise training delays the
foot care including daily inspection of feet intraocular pressure, such as high- progression of diabetic nephropathy in
and use of proper footwear is recom- intensity aerobic or resistance training animals (89,259), but few evidence is
mended for prevention and early detec- (with large increases in systolic BP) and available in humans.
tion of sores or ulcers. Moderate walking head-down activities, are not advised Evidence statement. Exercise training
likely does not increase risk of foot ulcers with uncontrolled proliferative disease, increases physical function and QOL in
or reulceration with peripheral neuropa- nor are jumping or jarring activities, all of individuals with kidney disease and may
thy. ACSM evidence category B. ADA B level which increase hemorrhage risk (1). Dia- even be undertaken during dialysis ses-
recommendation. betic retinopathy is the main cause of sions. The presence of microalbuminuria
Autonomic neuropathy. Moderate- blindness in developed countries and is per se does not necessitate exercise re-
intensity aerobic training can improve au- associated with increased CV mortality strictions. ACSM evidence category C. ADA
tonomic function in individuals with and (129,147). Individuals with retinopathy C level recommendation.
without CV autonomic neuropathy may receive some benefits, such as im-
(CAN) (112,176,208); however, im- proved work capacity, after low- to mod- ADOPTION AND
provements may only be evident after an erate-intensity exercise training (16,17). MAINTENANCE OF
acute submaximal exercise (78). Screen- While PA has been shown to be protective EXERCISE BY PERSONS
ing for CAN should include a battery of against development of age-related mac- WITH DIABETES Most American
autonomic tests (including HR variabil- ular degeneration (150), very little re- adults with type 2 diabetes or at highest risk
ity) that evaluate both branches of the au- search exists in type 2 diabetes. for developing it do not engage in regular
tonomic nervous system. Given the Evidence statement. Individuals with PA; their rate of participation is significantly
likelihood of silent ischemia, HR, and BP uncontrolled proliferative retinopathy below national norms (193). Additional
abnormalities, individuals with CAN should avoid activities that greatly in- strategies are needed to increase the adop-
should have physician approval and pos- crease intraocular pressure and hemor- tion and maintenance of PA.
sibly undergo stress testing to screen for rhage risk. ACSM evidence category D. One of the most consistent predictors
CV abnormalities before commencing ex- ADA E level recommendation. of greater levels of activity has been higher
ercise (265). Exercise intensity may be ac- Nephropathy and microalbuminuria. levels of self-efficacy (2,55,68), which re-
curately prescribed using the HR reserve Both aerobic and resistance training im- flect confidence in the ability to exercise
method (a percentage of the difference be- prove physical function and QOL in indi- (185). Social support has also been asso-
tween maximal and resting HR, added to viduals with kidney disease (126,209, ciated with greater levels of PA (93,
the resting value) to approximate oxygen 210), although BP increases during PA 190,215), supporting the role of social
consumption during submaximal exer- may transiently elevate levels of mi- networks in the spread of obesity (41).

e158 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.org
Colberg and Associates

Fortunately, those same social dynamics ing type 2 diabetes (279,284,285). The
References
may be exploited to increase the effects of results have been mixed, with some 1. Albright A, Franz M, Hornsby G, et al.
interventions beyond the target individ- showing increased PA (67,120,145,171) American College of Sports Medicine.
ual (8,99) and potentially can help spread and others showing no effect Position Stand: exercise and type 2 dia-
PA behavior. Counseling delivered by (142,143,189). Effective short-term pro- betes. Med Sci Sports Exerc 2000;32(7):
health care professionals may be a mean- grams have used print (67), phone 1345 60
ingful source of support and effective (44,144,233), in-person (120,139), or 2. Aljasem LI, Peyrot M, Wissow L, Rubin
source for delivery (7,144). Physicians Internet (92,171) delivery. Long-term ef- RR. The impact of barriers and self-efficacy
vary in counseling their patients to exer- fectiveness of such interventions has not on self-care behaviors in type 2 diabetes.
cise: on average, advice or referral related been assessed (197). Diabetes Educ 2001;27(3):393 404
to exercise occurred at 18% of office visits Evidence statement. Efforts to promote 3. American Diabetes Association. Physical
activity/exercise and diabetes. Diabetes
among diabetic patients (213), and 73% PA should focus on developing self-
Care 2004;27(90001):S58 S62
of patients reported receiving advice at efficacy and fostering social support from 4. American Diabetes Association. Diagno-
some point to exercise more (192). The family, friends, and health care providers. sis and classification of diabetes mellitus.
availability of facilities or pleasant and Encouraging mild or moderate PA may be Diabetes Care 2010;33(1 Suppl.):S629
safe places to walk may also be important most beneficial to adoption and mainte- 5. American Diabetes Association. Stan-
predictors of regular PA (59). nance of regular PA participation. Life- dards of medical care in diabetes 2010.
When prescribing PA for the preven- style interventions may have some Diabetes Care 2010;33(Suppl. 1):S11
tion or control of type 2 diabetes, the ef- efficacy in promoting PA behavior. ACSM S61
fects of the dose of the prescription on evidence category B. ADA B level 6. Araiza P, Hewes H, Gashetewa C, Vella
adherence are small (225). Therefore, recommendation. CA, Burge MR. Efficacy of a pedometer-
practitioners are encouraged to use fac- based physical activity program on
parameters of diabetes control in type 2
tors such as choice and enjoyment in CONCLUSIONS Exercise plays a diabetes mellitus. Metabolism 2006;
helping determine specifically how an in- major role in the prevention and control 55(10):13827
dividual would meet recommended par- of insulin resistance, prediabetes, GDM, 7. Armit CM, Brown WJ, Marshall AL, et al.
ticipation. Affective responses to exercise type 2 diabetes, and diabetes-related Randomized trial of three strategies to
may be important predictors of adoption health complications. Both aerobic and promote physical activity in general
and maintenance, and encouraging activ- resistance training improve insulin ac- practice. Prev Med 2009;48(2):156 63
ity at intensities below the ventilatory tion, at least acutely, and can assist with 8. Bahr DB, Browning RC, Wyatt HR, Hill
threshold may be most beneficial the management of BG levels, lipids, BP, JO. Exploiting social networks to miti-
(172,277,278). Many individuals with, or CV risk, mortality, and QOL, but exercise gate the obesity epidemic. Obesity 2009;
at risk of developing, type 2 diabetes pre- 17(4):723 8
must be undertaken regularly to have 9. Bajpeyi S, Tanner CJ, Slentz CA, et al.
fer walking as an aerobic activity (190), continued benefits and likely include reg- Effect of exercise intensity and volume
and pedometer-based interventions can ular training of varying types. Most per- on persistence of insulin sensitivity dur-
be effective for increasing aerobic activity sons with type 2 diabetes can perform ing training cessation. J Appl Physiol
(30,205,258). Finally, the emerging im- exercise safely as long as certain precau- 2009;106(4):1079 85
portance of sedentary behaviors in deter- tions are taken. The inclusion of an exer- 10. Balducci S, Iacobellis G, Parisi L, et al.
mining metabolic risk (106,107) suggests cise program or other means of increasing Exercise training can modify the natural
that future interventions may also benefit overall PA is critical for optimal health in history of diabetic peripheral neuropa-
from attempting to decrease sitting time individuals with type 2 diabetes. thy. J Diabetes Complications 2006;
and periods of extended sedentary 20(4):216 23
activity. 11. Balducci S, Zanuso S, Nicolucci A, et al.
Large-scale trials such as the DPP and Acknowledgments The authors have no fi- Effect of an intensive exercise interven-
Look AHEAD provide some insight into nancial support or professional conflicts of in- tion strategy on modifiable cardiovascu-
terest to disclose related to the articles lar risk factors in type 2 diabetic
successful lifestyle interventions that help
content. subjects. A randomized controlled trial:
promote PA by incorporating goal setting, The Italian Diabetes and Exercise Study
This joint position statement was written by
self-monitoring, frequent contact, and ACSM and ADA. ACSM: Sheri R. Colberg, (IDES). Arch Intern Med. In press
stepped-care protocols (56,60,71,266). PhD, FACSM (Chair); Ann L. Albright, PhD, 12. Barnard RJ, Lattimore L, Holly RG,
Delivering these programs requires exten- RD; Bryan J. Blissmer, PhD; Barry Braun, PhD, Cherny S, Pritikin N. Response of non
sive access to resources, staff, and space, FACSM; Lisa Chasan-Taber, ScD, FACSM; insulin-dependent diabetic patients to
although they are cost-effective overall and Bo Fernhall, PhD, FACSM. ADA: Judith G. an intensive program of diet and exer-
(121,122). Regensteiner, PhD; Richard R. Rubin, PhD; cise. Diabetes Care 1982;5(4):370 4
These large studies are multifactorial, and Ronald J. Sigal, MD, MPH, FRCP(C). 13. Barnard RJ, Ugianskis EJ, Martin DA.
targeting several behaviors that include This pronouncement was reviewed by the The effects of an intensive diet and exer-
PA, but include multiple behavior inter- ACSM Pronouncements Committee, ADA cise program on patients with non-
Professional Practice Committee, and by Greg- insulin-dependent diabetes mellitus. J Car-
ventions that also require changes in diet
ory D. Cartee, PhD, FACSM; Peter A. Farrell, diopulm Rehabil 1992;12:194201
and focusing on weight loss or manage- PhD, FACSM; Laurie J. Goodyear, PhD, 14. Baynard T, Franklin RM, Goulopoulou
ment (179). Therefore, strategies for PA FACSM; and Andrea M. Kriska, PhD, FACSM. S, Carhart R Jr, Kanaley JA. Effect of a
intervention in weight management are This joint position statement replaces the single vs multiple bouts of exercise on
highly relevant to this population (62). 2000 ACSM Position Stand Exercise and type glucose control in women with type 2
Fewer RCTs solely targeted PA behavior 2 Diabetes (Med Sci Sports Exerc diabetes. Metabolism 2005;54(8):989
in individuals with or at risk of develop- 2000;32:13451360). 94

care.diabetesjournals.org DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 e159
Exercise and type 2 diabetes

15. Bergman BC, Butterfield GE, Wolfel EE, 29. Braun B, Zimmermann MB, Kretchmer 42. Church TS, Cheng YJ, Earnest CP, et al.
Casazza GA, Lopaschuk GD, Brooks GA. N. Effects of exercise intensity on insulin Exercise capacity and body composition as
Evaluation of exercise and training on sensitivity in women with noninsulin- predictors of mortality among men with
muscle lipid metabolism. Am J Physiol dependent diabetes mellitus. J Appl diabetes. Diabetes Care 2004;27(1):83 8
1999;276(1 Pt 1):E106 E17 Physiol 1995;78(1):300 6 43. Church TS, LaMonte MJ, Barlow CE,
16. Bernbaum M, Albert SG, Cohen JD. Ex- 30. Bravata DM, Smith-Spangler C, Blair SN. Cardiorespiratory fitness and
ercise training in individuals with dia- Sundaram V, et al. Using pedometers to body mass index as predictors of cardio-
betic retinopathy and blindness. Arch increase physical activity and improve vascular disease mortality among men
Phys Med Rehabil 1989;70(8):60511 health: a systematic review. JAMA 2007; with diabetes. Arch Intern Med 2005;
17. Bernbaum M, Albert SG, Cohen JD, 298(19):2296 304 165(18):2114 20
Drimmer A. Cardiovascular condition- 31. Burke LM, Hawley JA. Carbohydrate 44. Clark M, Hampson SE, Avery L, Simp-
ing in individuals with diabetic retinop- and exercise. Curr Opin Clin Nutr son R. Effects of a tailored lifestyle self-
athy. Diabetes Care 1989;12(10):740 2 Metab Care 1999;2(6):51520 management intervention in patients
18. Black LE, Swan PD, Alvar BA. Effects of 32. Bweir S, Al-Jarrah M, Almalty AM, et al. with type 2 diabetes. Br J Health Psychol
intensity and volume on insulin sensitiv- Resistance exercise training lowers 2004;9(Pt 3):36579
ity during acute bouts of resistance train- HbA1c more than aerobic training in 45. Coccheri S. Approaches to prevention of
ing. J Strength Cond Res 2010;24(4): adults with type 2 diabetes. Diabetol cardiovascular complications and events
1109 16 Metab Syndr 2009;1:27 in diabetes mellitus. Drugs 2007;67(7):
19. Blair SN, Kohl HW 3rd, Barlow CE, 33. Cartee GD, Young DA, Sleeper MD, Zier- 9971026
Paffenbarger RS Jr, Gibbons LW, Macera ath J, Wallberg-Henriksson H, Holloszy 46. Cohen ND, Dunstan DW, Robinson C,
CA. Changes in physical fitness and all- JO. Prolonged increase in insulin-stimu- Vulikh E, Zimmet PZ, Shaw JE. Im-
cause mortality. A prospective study of lated glucose transport in muscle after proved endothelial function following a
healthy and unhealthy men. JAMA exercise. Am J Physiol 1989;256(4 Pt 1): 14-month resistance exercise training
1995;273(14):1093 8 E494 E499 program in adults with type 2 diabetes.
20. Bo S, Ciccone G, Rosato R, et al. Renal 34. Castaneda C, Layne JE, Munoz-Orians L, Diabetes Res Clin Pract 2008;79(3):
damage in patients with type 2 diabetes: et al. A randomized controlled trial of 40511
a strong predictor of mortality. Diabet resistance exercise training to improve 47. Colberg SR, Hagberg JM, McCole SD,
Med 2005;22(3):258 65 glycemic control in older adults with Zmuda JM, Thompson PD, Kelley DE.
21. Boon H, Blaak EE, Saris WH, Keizer HA, type 2 diabetes. Diabetes Care 2002; Utilization of glycogen but not plasma
Wagenmakers AJ, van Loon LJ. Sub- 25(12):2335 41 glucose is reduced in individuals with
strate source utilisation in long-term di- 35. Cauza E, Hanusch-Enserer U, Strasser B, NIDDM during mild-intensity exer-
agnosed type 2 diabetes patients at rest et al. The relative benefits of endurance cise. J Appl Physiol 1996;81(5):
and during exercise and subsequent re- and strength training on the metabolic 202733
covery. Diabetologia 2007;50(1):10312 factors and muscle function of people 48. Colberg SR, Swain DP, Vinik AI. Use of
22. Booth GL, Kapral MK, Fung K, Tu JV. with type 2 diabetes mellitus. Arch Phys heart rate reserve and rating of perceived
Recent trends in cardiovascular compli- Med Rehabil 2005;86(8):152733 exertion to prescribe exercise intensity
cations among men and women with 36. Ceysens G, Rouiller D, Boulvain M. Ex- in diabetic autonomic neuropathy. Dia-
and without diabetes. Diabetes Care ercise for diabetic pregnant women. Co- betes Care 2003;26(4):986 90
2006;29(1):327 chrane Database Syst Rev. 2006;3: 49. Cornelissen VA, Fagard RH. Effect of re-
23. Borghouts LB, Wagenmakers AJ, Goyens CD004225 sistance training on resting blood pres-
PL, Keizer HA. Substrate utilization in 37. Chasan-Taber L, Schmidt MD, Pekow P, sure: a meta-analysis of randomized
non-obese Type II diabetic patients at et al. Physical activity and gestational di- controlledtrials.JHypertens2005;23(2):
rest and during exercise. Clin Sci (Lond) abetes mellitus among Hispanic women. 2519
2002;103(6):559 66 J Womens Health (Larchmt) 2008;17(6): 50. Craft LL, Perna FM. The benefits of ex-
24. Boule NG, Haddad E, Kenny GP, Wells 999 1008 ercise for the clinically depressed. Prim
GA, Sigal RJ. Effects of exercise on gly- 38. Cheng YJ, Lauer MS, Earnest CP, et al. Care Companion J Clin Psychiatry 2004;
cemic control and body mass in type 2 Heart rate recovery following maximal 6(3):104 11
diabetes mellitus: a meta-analysis of con- exercise testing as a predictor of cardio- 51. Cuff DJ, Meneilly GS, Martin A, Ignasze-
trolledclinicaltrials.JAMA2001;286(10): vascular disease and all-cause mortality wski A, Tildesley HD, Frohlich JJ. Effec-
1218 27 in men with diabetes. Diabetes Care tive exercise modality to reduce insulin
25. Boule NG, Kenny GP, Haddad E, Wells 2003;26(7):20527 resistance in women with type 2 diabetes.
GA, Sigal RJ. Meta- analysis of the effect 39. Christ-Roberts CY, Pratipanawatr T, Diabetes Care 2003;26(11):297782
of structured exercise training on cardio- Pratipanawatr W, et al. Exercise training 52. Curtis JM, Horton ES, Bahnson J, et al.
respiratory fitness in type 2 diabetes mel- increases glycogen synthase activity and Prevalence and predictors of abnormal
litus. Diabetologia 2003;46(8):107181 GLUT4 expression but not insulin sig- cardiovascular responses to exercise
26. Boule NG, Weisnagel SJ, Lakka TA, et naling in overweight non- diabetic and testing among individuals with type 2
al. Effects of exercise training on glucose type 2 diabetic subjects. Metabolism diabetes: the Look AHEAD (Action for
homeostasis: the HERITAGE family 2004;53(9):1233 42 Health in Diabetes) study. Diabetes Care
study. Diabetes Care 2005;28(1):10814 40. Christ-Roberts CY, Pratipanawatr T, 2010;33(4):9017
27. Braden C. Nephropathy: advanced. In Pratipanawatr W, Berria R, Belfort R, 53. de Muinck ED, Lie KI. Safety and effi-
The Health Professionals Guide to Diabetes Mandarino LJ. Increased insulin recep- cacy of beta-blockers in the treatment
and Exercise. Alexandria (VA): American tor signaling and glycogen synthase ac- of stable angina pectoris. J Cardiovasc
Diabetes Association 1995. p. 177 80 tivity contribute to the synergistic effect Pharmacol 1990;16(Suppl. 5):S123S128
28. Braun B, Sharoff C, Chipkin SR, Beau- of exercise on insulin action. J Appl 54. Deckert T, Feldt-Rasmussen B, Borch-
doin F. Effects of insulin resistance on Physiol 2003;95(6):2519 29 Johnsen K, Jensen T, Kofoed-Enevold-
substrate utilization during exercise in 41. Christakis NA, Fowler JH. The spread of sen A. Albuminuria reflects widespread
overweight women. J Appl Physiol obesity in a large social network over 32 vascular damage. The Steno hypothesis.
2004;97(3):9917 years. N Engl J Med 2007;357(4):370 9 Diabetologia 1989;32(4):219 26

e160 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.org
Colberg and Associates

55. Delahanty LM, Conroy MB, Nathan DM. 67. Dutton GR, Provost BC, Tan F, Smith D. improves post-exercise cardiac auto-
Psychological predictors of physical ac- A tailored print-based physical activity nomic modulation in obese women with
tivity in the Diabetes Prevention Pro- intervention for patients with type 2 di- and without type 2 diabetes. Eur J Appl
gram. J Am Diet Assoc 2006;106(5): abetes. Preventive Medicine 2008;47(4): Physiol 2007;100(4):437 44
698 705 409 11 79. Fowler-Brown A, Pignone M, Pletcher
56. Delahanty LM, Nathan DM. Implica- 68. Dutton GR, Tan F, Provost BC, Sorenson M, Tice JA, Sutton SF, Lohr KN. Exercise
tions of the Diabetes Prevention Pro- JL, Allen B, Smith D. Relationship be- tolerance testing to screen for coronary
gram and Look AHEAD clinical trials for tween self-efficacy and physical activity heart disease: a systematic review for the
lifestyle interventions. J Am Diet Assoc among patients with type 2 diabetes. J technical support for the U.S. Preventive
2008;108(4 Suppl. 1):S66 S72 Behav Med 2009;32(3):270 7 Services Task Force. Ann Intern Med
57. Dempsey JC, Butler CL, Sorensen TK, et 69. Dyck R, Klomp H, Tan LK, Turnell RW, 2004;140(7):W9 W24
al. A case-control study of maternal rec- Boctor MA. A comparison of rates, risk 80. Fox CS, Pencina MJ, Wilson PW, Payn-
reational physical activity and risk of factors, and outcomes of gestational di- ter NP, Vasan RS, DAgostino RB Sr. Life-
gestational diabetes mellitus. Diabetes abetes between aboriginal and non-ab- time risk of cardiovascular disease
Res Clin Pract 2004;66(2):20315 original women in the Saskatoon health among individuals with and without di-
58. Dempsey JC, Sorensen TK, Williams district. Diabetes Care 2002;25(3): abetes stratified by obesity status in the
MA, et al. Prospective study of gesta- 48793 Framingham heart study. Diabetes Care
tional diabetes mellitus risk in relation to 70. Dyck RF, Sheppard MS, Cassidy H, 2008;31(8):1582 4
maternal recreational physical activity Chad K, Tan L, Van Vliet SH. Preventing 81. Fredrickson SK, Ferro TJ, Schutrumpf
before and during pregnancy. Am J Epi- NIDDM among aboriginal people: is ex- AC. Disappearance of microalbuminuria
demiol 2004;159(7):66370 ercise the answer? Description of a pilot in a patient with type 2 diabetes and the
59. Deshpande AD, Baker EA, Lovegreen SL, project using exercise to prevent gesta- metabolic syndrome in the setting of an
Brownson RC. Environmental correlates tional diabetes. Int J Circumpolar Health intense exercise and dietary program
of physical activity among individuals 1998;57(Suppl. 1):375 8 with sustained weight reduction. Diabe-
with diabetes in the rural midwest. Dia- 71. Eakin EG, Reeves MM, Lawler SP, et al. tes Care 2004;27(7):1754 5
betes Care 2005;28(5):1012 8 The Logan Healthy Living Program: a 82. Gaede P, Vedel P, Larsen N, Jensen GV,
60. Diabetes Prevention Program (DPP) Re- cluster randomized trial of a telephone- Parving HH, Pedersen O. Multifactorial
search Group. The Diabetes Prevention delivered physical activity and dietary intervention and cardiovascular disease
Program (DPP): description of lifestyle behavior intervention for primary care in patients with type 2 diabetes. N Engl
intervention.DiabetesCare2002;25(12): patients with type 2 diabetes or hyper- J Med 2003;348(5):38393
216571 tension from a socially disadvantaged 83. Galbo H, Tobin L, van Loon LJ. Re-
61. Dishman RK, Renner KJ, Youngstedt SD, communityrationale, design and re- sponses to acute exercise in type 2 dia-
et al. Activity wheel running reduces es- cruitment. Contemp Clin Trials 2008; betes, with an emphasis on metabolism
cape latency and alters brain mono- 29(3):439 54 and interaction with oral hypoglycemic
amine levels after footshock. Brain Res 72. Eddy DM, Schlessinger L, Heikes K. The agents and food intake. Appl Physiol
Bull 1997;42(5):399 406 metabolic syndrome and cardiovascular Nutr Metab 2007;32(3):56775
62. Donnelly JE, Blair SN, Jakicic JM, risk: implications for clinical practice. 84. Ganda O. Patients on various drug ther-
Manore MM, Rankin JW, Smith BK, Int J Obes (Lond) 2008;32(Suppl. 2): apies. In Ruderman N DJ, Schenider SH,
American College of Sports Medicine. S5S10 Kriska A, Eds. Handbook of Exercise in
Position Stand: appropriate physical ac- 73. Egede LE, Zheng D. Independent factors Diabetes. Alexandria (VA): American Di-
tivity intervention strategies for weight associated with major depressive disor- abetes Association; 2002. p. 58799
loss and prevention of weight regain for der in a national sample of individuals 85. Garcia-Roves PM, Han DH, Song Z,
adults. Med Sci Sports Exerc 2009; with diabetes. Diabetes Care 2003;26(1): Jones TE, Hucker KA, Holloszy JO. Pre-
41(2):459 71 10411 vention of glycogen supercompensation
63. Droste SK, Gesing A, Ulbricht S, Muller 74. Eriksson J, Lindstrom J, Valle T, et al. pro- longs the increase in muscle GLUT4
MB, Linthorst AC, Reul JM. Effects of Prevention of type II diabetes in subjects after exercise. Am J Physiol Endocrinol
long-term voluntary exercise on the with impaired glucose tolerance: the Di- Metab 2003;285(4):E729 E736
mouse hypothalamicpituitaryadreno- abetes Prevention Study (DPS) in Fin- 86. Garetto LP, Richter EA, Goodman MN,
cortical axis. Endocrinology 2003;144(7): land. Study design and 1-year interim Ruderman NB. Enhanced muscle glu-
301223 report on the feasibility of the lifestyle cose metabolism after exercise in the rat:
64. Duncan GE, Perri MG, Theriaque DW, intervention programme. Diabetologia the two phases. Am J Physiol 1984;
Hutson AD, Eckel RH, Stacpoole PW. 1999;42(7):793 801 246(6 Pt 1):E471E475
Exercise training, without weight loss, 75. Evans EM, Racette SB, Peterson LR, Vil- 87. Ghanassia E, Brun JF, Fedou C, Raynaud
increases insulin sensitivity and post- lareal DT, Greiwe JS, Holloszy JO. Aero- E, Mercier J. Substrate oxidation during
heparin plasma lipase activity in previ- bic power and insulin action improve in exercise: type 2 diabetes is associated
ously sedentary adults. Diabetes Care response to endurance exercise training with a decrease in lipid oxidation and an
2003;26(3):557 62 in healthy 77 87 yr olds. J Appl Physiol earlier shift towards carbohydrate utili-
65. Dunstan DW, Daly RM, Owen N, et al. 2005;98(1):40 5 zation. Diabetes Metab 2006;32(6):
High-intensity resistance training im- 76. Ewing DJ, Clarke BF. Diabetic auto- 604 10
proves glycemic control in older patients nomic neuropathy: present insights and 88. Ghilarducci LE, Holly RG, Amsterdam
with type 2 diabetes. Diabetes Care future prospects. Diabetes Care 1986; EA. Effects of high resistance training in
2002;25(10):1729 36 9(6):648 65 coronary artery disease. Am J Cardiol
66. Dunstan DW, Daly RM, Owen N, et al. 77. Featherstone JF, Holly RG, Amsterdam 1989;64(14):866 70
Home-based resistance training is not EA. Physiologic responses to weight lift- 89. Ghosh S, Khazaei M, Moien-Afshari F,
sufficient to maintain improved glyce- ing in coronary artery disease. Am J Car- et al. Moderate exercise attenuates
mic control following supervised train- diol 1993;71(4):28792 caspase-3 activity, oxidative stress, and
ing in older individuals with type 2 78. Figueroa A, Baynard T, Fernhall B, Car- inhibits progression of diabetic renal
diabetes. Diabetes Care 2005;28(1):39 hart R, Kanaley JA. Endurance training disease in db/db mice. Am J Physiol Renal

care.diabetesjournals.org DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 e161
Exercise and type 2 diabetes

Physiol 2009;296(4):F700 F708 103. Grossman E, Messerli FH, Goldbourt U. 116. Ibanez J, Izquierdo M, Arguelles I, et al.
90. Gillison FB, Skevington SM, Sato A, High blood pressure and diabetes melli- Twice-weekly progressive resistance
Standage M, Evangelidou S. The effects tus: are all antihypertensive drugs cre- training decreases abdominal fat and im-
of exercise interventions on quality of ated equal? Arch Intern Med 2000; proves insulin sensitivity in older men
life in clinical and healthy populations; a 160(16):244752 with type 2 diabetes. Diabetes Care
meta-analysis. Soc Sci Med 2009;68(9): 104. Hamman RF, Wing RR, Edelstein SL, et 2005;28(3):6627
1700 10 al. Effect of weight loss with lifestyle in- 117. Innes KE, Vincent HK. The influence of
91. Gimeno Orna JA, Boned Juliani B, Lou tervention on risk of diabetes. Diabetes yoga-based programs on risk profiles in
Arnal LM, Castro Alonso FJ. Microalbu- Care 2006;29(9):21027 adults with type 2 diabetes mellitus: a
minuria and clinical proteinuria as the 105. Haskell WL, Lee IM, Pate RR, et al. Phys- systematic review. Evid Based Comple-
main predictive factors of cardiovascular ical activity and public health: updated ment Alternat Med 2007;4(4):469 86
morbidity and mortality in patients with recommendation for adults from the 118. Ishii T, Yamakita T, Sato T, Tanaka S,
type 2 diabetes [in Spanish]. Rev Clin American College of Sports Medicine Fujii S. Resistance training improves
Esp 2003;203(11):526 31 and the American Heart Association. insulin sensitivity in NIDDM subjects
92. Glasgow RE, Nutting PA, King DK, et al. Med Sci Sports Exerc 2007;39(8):142334 without altering maximal oxygen up-
Randomized effectiveness trial of a com- 106. Healy GN, Dunstan DW, Salmon J, et al. take. Diabetes Care 1998;21(8):
puter-assisted intervention to improve Breaks in sedentary time: beneficial as- 13535
diabetes care. Diabetes Care 2005;28(1): sociations with metabolic risk. Diabetes 119. Ivy JL, Holloszy JO. Persistent increase
339 Care 2008;31(4):661 6 in glucose uptake by rat skeletal muscle
93. Gleeson-Kreig J. Social support and 107. Healy GN, Wijndaele K, Dunstan DW, et following exercise. Am J Physiol 1981;
physical activity in type 2 diabetes: a so- al. Objectively measured sedentary time, 241(5):C200 C203
cial-ecologic approach. Diabetes Educ physical activity, and metabolic risk: the 120. Jackson R, Asimakopoulou K, Scammell
2008;34(6):1037 44 Australian Diabetes, Obesity and Life- A. Assessment of the transtheoretical
94. Goldsmith JR, Lidtke RH, Shott S. The style Study (AusDiab) Diabetes Care model as used by dietitians in promoting
effects of range-of-motion therapy on 2008;31(2):369 71 physical activity in people with type 2
the plantar pressures of patients with di- 108. Helmrich SP, Ragland DR, Leung RW, diabetes. J Hum Nutr Diet 2007;20(1):
abetes mellitus. J Am Podiatr Med Assoc Paffenbarger RS Jr. Physical activity and 2736
2002;92(9):48390 reduced occurrence of noninsulin-de- 121. Jacobs-van der Bruggen MA, Bos G, Be-
95. Goodpaster BH, Katsiaras A, Kelley DE. pendent diabetes mellitus. N Engl J Med melmans WJ, Hoogenveen RT, Vijgen
Enhanced fat oxidation through physical 1991;325(3):14752 SM, Baan CA. Lifestyle interventions are
activity is associated with improvements 109. Herriott MT, Colberg SR, Parson HK, cost-effective in people with different
in insulin sensitivity in obesity. Diabetes Nunnold T, Vinik AI. Effects of 8 weeks levels of diabetes risk: results from a
2003;52(9):21917 of flexibility and resistance training in modeling study. Diabetes Care
96. Goodyear LJ, Kahn BB. Exercise, glucose older adults with type 2 diabetes. Diabe- 2007;30(1):128 34
transport, and insulin sensitivity. Annu tes Care 2004;27(12):2988 9 122. Jacobs-van der Bruggen MA, van Baal
Rev Med 1998;49:235 61 110. Holten MK, Zacho M, Gaster M, Juel C, PH, Hoogenveen RT, et al. Cost-effec-
97. Gordon BA, Benson AC, Bird SR, Fraser Wojtaszewski JF, Dela F. Strength train- tiveness of lifestyle modification in dia-
SF. Resistance training improves meta- ing increases insulin-mediated glucose betes patients. Diabetes Care 2009;32(8):
bolic health in type 2 diabetes: a system- uptake, GLUT4 content, and insulin sig- 14538
atic review. Diabetes Res Clin Pract naling in skeletal muscle in patients with 123. Jakicic JM, Marcus BH, Gallagher KI,
2009;83(2):15775 type 2 diabetes. Diabetes 2004;53(2): Napolitano M, Lang W. Effect of exercise
98. Gordon LA, Morrison EY, McGrowder 294 305 duration and intensity on weight loss in
DA, et al. Effect of exercise therapy on 111. Houmard JA, Tanner CJ, Slentz CA, overweight, sedentary women: a ran-
lipid profile and oxidative stress indica- Duscha BD, McCartney JS, Kraus WE. domized trial. JAMA 2003;290(10):
tors in patients with type 2 diabetes. Effect of the volume and intensity of ex- 132330
BMC Complement Altern Med 2008; ercise training on insulin sensitivity. 124. Jeffery RW, Wing RR, Sherwood NE,
8:21 J Appl Physiol 2004;96(1):101 6 Tate DF. Physical activity and weight
99. Gorin AA, Wing RR, Fava JL, et al. 112. Howorka K, Pumprla J, Haber P, Koller- loss: does prescribing higher physical
Weight loss treatment influences un- Strametz J, Mondrzyk J, Schabmann A. activity goals improve outcome? Am J
treated spouses and the home environ- Effects of physical training on heart rate Clin Nutr 2003;78(4):684 9
ment: evidence of a ripple effect. Int J variability in diabetic patients with vari- 125. Jeon CY, Lokken RP, Hu FB, van Dam
Obes 2008;32(11):1678 84 ous degrees of cardiovascular autonomic RM. Physical activity of moderate inten-
100. Goulet ED, Melancon MO, Aubertin-Le- neuropathy. Cardiovasc Res 1997;34(1): sity and risk of type 2 diabetes: a system-
heudre M, Dionne IJ. Aerobic training 206 14 atic review. Diabetes Care 2007;30(3):
improves insulin sensitivity 72120 h 113. Hu FB, Sigal RJ, Rich-Edwards JW, et al. 744 52
after the last exercise session in younger Walking compared with vigorous phys- 126. Johansen KL. Exercise and chronic kid-
but not in older women. Eur J Appl ical activity and risk of type 2 diabetes in ney disease: current recommendations.
Physiol 2005;95(23):146 52 women: a prospective study. JAMA Sports Med 2005;35(6):48599
101. Goulet ED, Melancon MO, Dionne IJ, 1999;282(15):14339 127. John L, Rao PS, Kanagasabapathy AS.
Aubertin-Leheudre M. No sustained ef- 114. Hu FB, Stampfer MJ, Solomon C, et al. Rate of progression of albuminuria in
fect of aerobic or resistance training on Physical activity and risk for cardiovas- type II diabetes. Five-year prospective
insulin sensitivity in nonobese, healthy cular events in diabetic women. Ann In- study from south India. Diabetes Care
older women. J Aging Phys Act 2005; tern Med 2001;134(2):96 105 1994;17(8):888 90
13(3):314 26 115. Ibanez J, Gorostiaga EM, Alonso AM, et 128. Johnson NA, Sachinwalla T, Walton
102. Graham C, Lasko-McCarthey P. Exercise al. Lower muscle strength gains in older DW, et al. Aerobic exercise training re-
options for persons with diabetic com- men with type 2 diabetes after resistance duces hepatic and visceral lipids in
plications. Diabetes Educ 1990;16(3): training. J Diabetes Complications 2008; obese individuals without weight loss.
21220 22(2):112 8 Hepatology 2009;50(4):110512

e162 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.org
Colberg and Associates

129. Juutilainen A, Lehto S, Ronnemaa T, lin action and glucose tolerance in mid- tion of type 2 diabetes by lifestyle inter-
Pyorala K, Laakso M. Retinopathy pre- dle-aged people. J Appl Physiol 1995; vention: a Japanese trial in IGT males.
dicts cardiovascular mortality in type 2 78(1):1722 Diabetes Res Clin Pract 2005;67(2):
diabetic men and women. Diabetes Care 142. Kinmonth AL, Wareham NJ, Hardeman 152 62
2007;30(2):2929 W, et al. Efficacy of a theory-based be- 155. Kothari V, Stevens RJ, Adler AI, et al.
130. Kadoglou NP, Iliadis F, Angelopoulou havioural intervention to increase phys- UKPDS 60: risk of stroke in type 2 dia-
N, et al. The anti-inflammatory effects of ical activity in an at-risk group in betes estimated by the UK Prospective
exercise training in patients with type 2 primary care (ProActive UK): a random- Diabetes Study risk engine. Stroke 2002;
diabetes mellitus. Eur J Cardiovasc Prev ised trial. Lancet 2008;371(9606):41 8 33(7):1776 81
Rehabil 2007;14(6):837 43 143. Kirk A, Barnett J, Leese G, Mutrie N. A 156. Kreisman SH, Halter JB, Vranic M, Marliss
131. Kahn JK, Zola B, Juni JE, Vinik AI. De- randomized trial investigating the 12- EB. Combined infusion of epinephrine
creased exercise heart rate and blood month changes in physical activity and and norepinephrine during moderate ex-
pressure response in diabetic subjects health outcomes following a physical ac- ercise reproduces the glucoregulatory re-
with cardiac autonomic neuropathy. Di- tivity consultation delivered by a person sponse of intense exercise. Diabetes 2003;
abetes Care 1986;9(4):389 94 or in written form in type 2 diabetes: 52(6):134754
132. Kang J, Kelley DE, Robertson RJ, et al. Time2Act. Diabet Med 2009;26(3): 157. Kwon HR, Han KA, Ku YH, et al. The
Substrate utilization and glucose turn- 293301 effects of resistance training on muscle
over during exercise of varying intensi- 144. Kirk A, Mutrie N, MacIntyre P, Fisher M. and body fat mass and muscle strength
ties in individuals with NIDDM. Med Sci Effects of a 12-month physical activity in type 2 diabetic women. Korean Dia-
Sports Exerc 1999;31(1):829 counselling intervention on glycaemic betes J 2010;34(2):10110
133. Kang J, Robertson RJ, Hagberg JM, et al. control and on the status of cardiovascu- 158. Laaksonen DE, Lindstrom J, Lakka TA,
Effect of exercise intensity on glucose lar risk factors in people with type 2 et al. Physical activity in the prevention
and insulin metabolism in obese indi- diabetes. Diabetologia 2004;47(5): of type 2 diabetes: the Finnish Diabetes
viduals and obese NIDDM patients. Di- 82132 Prevention Study. Diabetes 2005;54(1):
abetes Care 1996;19(4):3419 145. Kirk AF, Mutrie N, Macintyre PD, Fisher 158 65
134. Kelley GA, Kelley KA, Tran ZV. Aerobic MB. Promoting and maintaining physi- 159. Lam P, Dennis SM, Diamond TH, Zwar
exercise and resting blood pressure: a cal activity in people with type 2 diabe- N. Improving glycaemic and BP control
meta-analytic review of randomized, tes. Am J Prev Med 2004;27(4):289 96 in type 2 diabetes. The effectiveness of tai
controlled trials. Prev Cardiol 2001; 146. Kirwan JP, Solomon TP, Wojta DM, chi. Aust Fam Physician 2008;37(10):
4(2):73 80 Staten MA, Holloszy JO. Effects of 7 days 8847
135. Kelley GA, Kelley KS. Progressive resis- of exercise training on insulin sensitivity 160. Larsen JJ, Dela F, Madsbad S, Galbo H.
tance exercise and resting blood pres- and responsiveness in type 2 diabetes The effect of intense exercise on post-
sure: a meta-analysis of randomized mellitus. Am J Physiol Endocrinol Metab prandial glucose homeostasis in type II
controlled trials. Hypertension 2000; 2009;297(1):E151E156 diabetic patients. Diabetologia 1999;
35(3):838 43 147. Klein R, Klein BE, Moss SE. Epidemiol- 42(11):128292
136. Kelley GA, Kelley KS. Effects of aerobic ogy of proliferative diabetic retinopathy. 161. Larsen JJ, Dela F, Madsbad S, Vibe-Pe-
exercise on lipids and lipoproteins in Diabetes Care 1992;15(12):187591 tersen J, Galbo H. Interaction of sulfo-
adults with type 2 diabetes: a meta-anal- 148. Klein R, Klein BE, Moss SE. Prevalence nylureas and exercise on glucose
ysis of randomized-controlled trials. of microalbuminuria in older-onset dia- homeostasis in type 2 diabetic patients.
Public Health 2007;121(9):64355 betes. Diabetes Care 1993;16(10): Diabetes Care 1999;22(10):164754
137. Kelley GA, Sharpe Kelley K. Aerobic ex- 132530 162. Lazarevic G, Antic S, Vlahovic P, Djord-
ercise and resting blood pressure in 149. Knowler WC, Barrett-Connor E, Fowler jevic V, Zvezdanovic L, Stefanovic V.
older adults: a meta-analytic review of SE, et al. Reduction in the incidence of Effects of aerobic exercise on microalbu-
randomized controlled trials. J Gerontol type 2 diabetes with lifestyle interven- minuria and enzymuria in type 2 dia-
A Biol Sci Med Sci 2001;56(5):M298 tion or metformin. N Engl J Med 2002; betic patients. Ren Fail 2007;29(2):
M303 346(6):393 403 199 205
138. Kennedy JW, Hirshman MF, Gervino 150. Knudtson MD, Klein R, Klein BE. Phys- 163. Lee DC, Sui X, Church TS, Lee IM, Blair
EV, et al. Acute exercise induces GLUT4 ical activity and the 15-year cumulative SN. Associations of cardiorespiratory fit-
translocation in skeletal muscle of nor- incidence of age-related macular degen- ness and obesity with risks of impaired
mal human subjects and subjects with eration: the Beaver Dam Eye study. Br J fasting glucose and type 2 diabetes in
type 2 diabetes. Diabetes 1999;48(5): Ophthalmol 2006;90(12):14613 men. Diabetes Care 2009;32(2):257 62
11927 151. Koh KP, Fassett RG, Sharman JE, 164. Lee IM, Skerrett PJ. Physical activity and
139. Keyserling TC, Samuel-Hodge CD, Am- Coombes JS, Williams AD. Effect of in- all-cause mortality: what is the doser-
merman AS, et al. A randomized trial of tradialytic versus home-based aerobic esponse relation? Med Sci Sports Exerc
an intervention to improve self-care be- exercise training on physical function 2001;33(Suppl. 6):S459 S471; discus-
haviors of African-American women and vascular parameters in hemodialysis sion S93S94
with type 2 diabetes: impact on physical patients: a randomized pilot study. Am J 165. Legato MJ, Gelzer A, Goland R, et al.
activity. Diabetes Care 2002;25(9): Kidney Dis 2010;55(1):88 99 Gender-specific care of the patient with
1576 83 152. Koivisto V, Defronzo R. Exercise in the diabetes: review and recommendations.
140. Kim SH, Lee SJ, Kang ES, et al. Effects of treatment of type II diabetes. Acta Endo- Gend Med 2006;3(2):13158
lifestyle modification on metabolic pa- crinol (Copenh) 1984;262(Suppl.): 166. Lemaster JW, Mueller MJ, Reiber GE,
rameters and carotid intima-media 10716 Mehr DR, Madsen RW, Conn VS. Effect
thickness in patients with type 2 diabe- 153. Kokkinos P, Myers J, Nylen E, et al. Ex- of weight-bearing activity on foot ulcer
tes mellitus. Metabolism 2006;55(8): ercise capacity and all-cause mortality in incidence in people with diabetic pe-
10539 African American and Caucasian men ripheral neuropathy: feet first random-
141. King DS, Baldus PJ, Sharp RL, Kesl LD, with type 2 diabetes. Diabetes Care ized controlled trial. Phys Ther
Feltmeyer TL, Riddle MS. Time course 2009;32(4):623 8 2008;88(11):138598
for exercise-induced alterations in insu- 154. Kosaka K, Noda M, Kuzuya T. Preven- 167. Lemaster JW, Reiber GE, Smith DG,

care.diabetesjournals.org DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 e163
Exercise and type 2 diabetes

Heagerty PJ, Wallace C. Daily weight- complications in patients with type-2 di- chyan V, Sullivan PW. Physical activity
bearing activity does not increase the abetes mellitus and silent myocardial in U.S. adults with diabetes and at risk
risk of diabetic foot ulcers. Med Sci ischaemia: five-year follow-up [in Pol- for developing diabetes, 2003. Diabetes
Sports Exerc 2003;35(7):10939 ish]. Pol Arch Med Wewn 2004;112(6): Care 2007;30(2):2039
168. Levine JA, Lanningham-Foster LM, Mc- 1433 43 194. Morrison S, Colberg SR, Mariano M, Par-
Crady SK, et al. Interindividual variation 181. Manetta J, Brun JF, Perez-Martin A, Cal- son HK, Vinik AI. Balance training re-
in posture allocation: possible role in lis A, Prefaut C, Mercier J. Fuel oxidation duces falls risk in older individuals with
human obesity. Science 2005;307(5709): during exercise in middle-aged men: type 2 diabetes. Diabetes Care 33(4):
584 6 role of training and glucose disposal. 748 50
169. Levine JA, McCrady SK, Lanningham- Med Sci Sports Exerc 2002;34(3):4239 195. Mourad JJ, Le Jeune S. Blood pressure
Foster LM, Kane PH, Foster RC, Mano- 182. Manson JE, Rimm EB, Stampfer MJ, et al. control, risk factors and cardiovascular
har CU. The role of free-living daily Physical activity and incidence of non prognosis in patients with diabetes: 30
walking in human weight gain and obe- insulin-dependent diabetes mellitus in years of progress. J Hypertens Suppl
sity. Diabetes 2008;57(3):548 54 women. Lancet 1991;338(8770):774 8 2008;26(3):S7S13
170. Li G, Zhang P, Wang J, et al. The long- 183. Marcus RL, Smith S, Morrell G, et al. 196. Mourier A, Gautier JF, De Kerviler E, et
term effect of lifestyle interventions to Comparison of combined aerobic and al. Mobilization of visceral adipose tissue
prevent diabetes in the China Da Qing high-force eccentric resistance exercise related to the improvement in insulin
Diabetes Prevention Study: a 20-year with aerobic exercise only for people sensitivity in response to physical train-
follow-up study. Lancet 2008;371(9626): with type 2 diabetes mellitus. Phys Ther ing in NIDDM. Effects of branched-
17839 2008;88(11):134554 chain amino acid supplements. Diabetes
171. Liebreich T, Plotnikoff RC, Courneya 184. Marliss EB, Vranic M. Intense exercise Care 1997;20(3):38591
KS, Boule N. Diabetes NetPLAY: a phys- has unique effects on both insulin re- 197. Muller-Riemenschneider F, Reinhold T,
ical activity website and linked email lease and its roles in glucoregulation: im- Nocon M, Willich SN. Long-term effec-
counselling randomized intervention for plications for diabetes. Diabetes 2002; tiveness of interventions promoting
individuals with type 2 diabetes. Int J 51(Suppl. 1):S271S283 physical activity: a systematic review.
Behav Nutr Phys Act 2009;6:18 185. McAuley E, Blissmer B. Self-efficacy de- Prev Med 2008;47(4):354 68
172. Lind E, Ekkekakis P, Vazou S. The affec- terminants and con- sequences of phys- 198. Musi N, Fujii N, Hirshman MF, et al.
tive impact of exercise intensity that ical activity. Exerc Sport Sci Rev 2000; AMP-activated protein kinase (AMPK) is
slightly exceeds the preferred level: pain 28(2):85 8 activated in muscle of subjects with type
for no additional gain. J Health Psychol 186. McAuley PA, Myers JN, Abella JP, Tan 2 diabetes during exercise. Diabetes
2008;13(4):464 8 SY, Froelicher VF. Exercise capacity and 2001;50(5):9217
173. Lindstrom J, Ilanne-Parikka P, Peltonen body mass as predictors of mortality 199. Narayan KM, Boyle JP, Geiss LS, Saad-
M, et al. Sustained reduction in the inci- among male veterans with type 2 diabe- dine JB, Thompson TJ. Impact of recent
dence of type 2 diabetes by lifestyle in- tes. Diabetes Care 2007;30(6):1539 43 increase in incidence on future diabetes
tervention: follow-up of the Finnish 187. McDermott MM, Ades P, Guralnik JM, et burden: U.S., 20052050. Diabetes
Diabetes Prevention Study. Lancet al. Treadmill exercise and resistance train- Care 2006;29(9):2114 6
2006;368(9548):16739 ing in patients with peripheral arterial dis- 200. Narayan KM, Boyle JP, Thompson TJ,
174. Liu J, Laditka JN, Mayer-Davis EJ, Pate ease with and without intermittent Sorensen SW, Williamson DF. Lifetime
RR. Does physical activity during preg- claudication: a randomized controlled risk for diabetes mellitus in the United
nancy reduce the risk of gestational dia- trial. JAMA 2009;301(2):16574 States. JAMA 2003;290(14):1884 90
betes among previously inactive 188. McGavock J, Sellers E, Dean H. Physical 201. National High Blood Pressure Education
women? Birth 2008;35(3):188 95 activity for the prevention and manage- Program Working Group. National High
175. Loimaala A, Groundstroem K, Rinne M, ment of youth-onset type 2 diabetes Blood Pressure Education Program
et al. Effect of long-term endurance and mellitus: focus on cardiovascular com- Working Group report on hypertension
strength training on metabolic control plications. Diab Vasc Dis Res 2007;4(4): in diabetes. Hypertension 1994;23(2):
and arterial elasticity in patients with 30510 14558; discussion 59 60
type 2 diabetes mellitus. Am J Cardiol 189. McKay HG, King D, Eakin EG, Seeley JR, 202. Nelson ME, Rejeski WJ, Blair SN, et al.
2009;103(7):9727 Glasgow RE. The diabetes network In- Physical activity and public health in older
176. Loimaala A, Huikuri HV, Koobi T, Rinne ternet-based physical activity interven- adults: recommendation from the Ameri-
M, Nenonen A, VuoriI. Exercise training tion: a randomized pilot study. Diabetes can College of Sports Medicine and the
improves baroreflex sensitivity in type 2 Care 2001;24(8):1328 34 American Heart Association. Med Sci
diabetes. Diabetes 2003;52(7):1837 42 190. Mier N, Medina AA, Ory MG. Mexican Sports Exerc 2007;39(8):1435 45
177. Low PA, Walsh JC, Huang CY, McLeod Americans with type 2 diabetes: per- 203. Nichols GA, Koro CE. Does statin ther-
JG. The sympathetic nervous system in di- spectives on definitions, motivators, and apy initiation increase the risk for myop-
abetic neuropathy. A clinical and patho- programs of physical activity. Prev athy? An observational study of 32,225
logical study. Brain 1975;98(3):34156 Chronic Dis 2007;4(2):A24 diabetic and nondiabetic patients. Clin
178. Maiorana A, ODriscoll G, Goodman C, 191. Minuk HL, Vranic M, Hanna AK, Albi- Ther 2007;29(8):176170
Taylor R, Green D. Combined aerobic and sser AM, Zinman B. Glucoregulatory and 204. OGorman DJ, Karlsson HK, McQuaid S,
resistance exercise improves glycemic metabolic response to exercise in obese et al. Exercise training increases insulin-
control and fitness in type 2 diabetes. Di- non-insulin-dependent diabetes. Am J stimulated glucose disposal and GLUT4
abetes Res Clin Pract 2002;56(2):11523 Physiol 1981;240:E458 E464 (SLC2A4) protein content in patients
179. Malpass A, Andrews R, Turner KM. Pa- 192. Morrato EH, Hill JO, Wyatt HR, Ghush- with type 2 diabetes. Diabetologia 2006;
tients with type 2 diabetes experiences of chyan V, Sullivan PW. Are health care 49(12):298392
making multiple lifestyle changes: a professionals advising patients with dia- 205. Ogilvie D, Foster CE, Rothnie H, et al.
qualitative study. Patient Educ Couns betes or at risk for developing diabetes to Interventions to promote walking: sys-
2009;74(2):258 63 exercise more? Diabetes Care 2006; tematic review [see comment]. BMJ
180. Mamcarz A, Chmielewski M, Braksator 29(3):543 8 2007;334(7605):1204
W, et al. Factors influencing cardiac 193. Morrato EH, Hill JO, Wyatt HR, Ghush- 206. Oken E, Ning Y, Rifas-Shiman SL,

e164 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.org
Colberg and Associates

Radesky JS, Rich-Edwards JW, Gillman cular disease risk factors in individuals center study. Diabetes Care 2004;27(6):
MW. Associations of physical activity with type 2 diabetes: one-year results of 126570
and inactivity before and during preg- the look AHEAD trial. Diabetes Care 231. Ross R, Dagnone D, Jones PJ, et al. Re-
nancy with glucose tolerance. Obstet 2007;30(6):1374 83 duction in obesity and related comorbid
Gynecol 2006;108(5):1200 7 219. Plockinger U, Topuz M, Riese B, Reuter conditions after diet-induced weight
207. Paffenbarger RS Jr, Hyde RT, Wing AL, T. Risk of exercise-induced hypoglycae- loss or exercise-induced weight loss in
Lee IM, Jung DL, Kampert JB. The asso- mia in patients with type 2 diabetes on men. A randomized, controlled trial.
ciation of changes in physical-activity intensive insulin therapy: comparison of Ann Intern Med 2000;133(2):92103
level and other lifestyle characteristics insulin glargine with NPH insulin as 232. Ross R, Janssen I, Dawson J, et al. Exer-
with mortality among men. N Engl basal insulin supplement. Diabetes Res cise-induced reduction in obesity and
J Med 1993;328(8):538 45 Clin Pract 2008;81(3):290 5 insulin resistance in women: a random-
208. Pagkalos M, Koutlianos N, Kouidi E, 220. Ploug T, Galbo H, Richter EA. Increased ized controlled trial. Obes Res
Pagkalos E, Mandroukas K, Deligiannis muscle glucose uptake during contrac- 2004;12(5):789 98
A. Heart rate variability modifications tions: no need for insulin. Am J Physiol 233. Sacco WP, Malone JI, Morrison AD,
following exercise training in type 2 di- 1984;247(6 Pt 1):E726 E731 Friedman A, Wells K. Effect of a brief,
abetic patients with definite cardiac au- 221. Poirier P, Mawhinney S, Grondin L, et al. regular telephone intervention by para-
tonomic neuropathy. Br J Sports Med Prior meal enhances the plasma glucose professionals for type 2 diabetes. J Behav
2008;42(1):4754 lowering effect of exercise in type 2 dia- Med 2009;32(4):349 59
209. Painter P, Carlson L, Carey S, Paul SM, betes. Med Sci Sports Exerc 2001;33(8): 234. Saris WH, Blair SN, van Baak MA, et al.
Myll J. Low-functioning hemodialysis 1259 64 How much physical activity is enough to
patients improve with exercise training. 222. Practice ACO. ACOG Committee opin- prevent unhealthy weight gain? Out-
Am J Kidney Dis 2000;36(3):600 8 ion. Number 267, January 2002: exer- come of the IASO 1st Stock Conference
210. Painter P, Carlson L, Carey S, Paul SM, cise during pregnancy and the and consensus statement. Obes Rev
Myll J. Physical functioning and health- postpartum period. Obstet Gynecol 2003;4(2):10114
related quality-of-life changes with exer- 2002;99(1):1713 235. Schoeller DA, Shay K, Kushner RF. How
cise training in hemodialysis patients. 223. Pruchnic R, Katsiaras A, He J, Kelley DE, much physical activity is needed to min-
Am J Kidney Dis 2000;35(3):48292 Winters C, Goodpaster BH. Exercise imize weight gain in previously obese
211. Pan XR, Li GW, Hu YH, et al. Effects of training increases intramyocellular lipid women? Am J Clin Nutr 1997;
diet and exercise in preventing NIDDM and oxidative capacity in older adults. 66(3):551 6
in people with impaired glucose toler- Am J Physiol Endocrinol Metab 2004; 236. Sharples L, Hughes V, Crean A, et al.
ance. The Da Qing IGT and Diabetes 287(5):E857E862 Cost-effectiveness of functional cardiac
Study. Diabetes Care 1997;20(4): 224. Ramachandran A, Snehalatha C, Mary S, testing in the diagnosis and management
537 44 et al. The Indian Diabetes Prevention of coronary artery disease: a randomised
212. Pavlou KN, Krey S, Steffee WP. Exercise Programme shows that lifestyle modifi- controlled trial. The CECaT trial. Health
as an adjunct to weight loss and mainte- cation and metformin prevent type 2 di- Technol Assess 2007;11(49):iiiiv,
nance in moderately obese subjects. abetes in Asian Indian subjects with ix115
Am J Clin Nutr 1989;49(Suppl. 5): impaired glucose tolerance (IDPP-1). 237. Shrier I. Stretching before exercise does
111523 Diabetologia 2006;49(2):289 97 not reduce the risk of local muscle in-
213. Peek ME, Tang H, Alexander GC, Chin 225. Rhodes RE, Warburton DE, Murray H. jury: a critical review of the clinical and
MH. National prevalence of lifestyle Characteristics of physical activity basic science literature. Clin J Sport Med
counseling or referral among African- guidelines and their effect on adherence: 1999;9(4):2217
Americans and whites with diabetes. a review of randomized trials. Sports 238. Sigal RJ, Kenny GP, Boule NG, et al.
J Gen Intern Med 2008;23(11): Med 2009;39(5):35575 Effects of aerobic training, resistance
1858 64 226. Richter EA, Garetto LP, Goodman MN, training, or both on glycemic control in
214. Pena KE, Stopka CB, Barak S, Gertner Ruderman NB. Muscle glucose metabo- type 2 diabetes: a randomized trial. Ann
HR Jr, Carmeli E. Effects of low-intensity lism following exercise in the rat: in- Intern Med 2007;147:357 69
exercise on patients with peripheral ar- creased sensitivity to insulin. J Clin 239. Sigal RJ, Kenny GP, Wasserman DH,
tery disease. Phys Sportsmed 2009; Invest 1982;69(4):78593 Castaneda-Sceppa C. Physical activity/
37(1):106 10 227. Richter EA, Ploug T, Galbo H. Increased exercise and type 2 diabetes. Diabetes
215. Penn L, Moffatt SM, White M. Partici- muscle glucose uptake after exercise. No Care 2004;27(10):2518 39
pants perspective on maintaining be- need for insulin during exercise. Diabe- 240. Sigal RJ, Kenny GP, Wasserman DH,
haviour change: a qualitative study tes 1985;34(10):1041 8 Castaneda-Sceppa C, White RD. Physi-
within the European Diabetes Preven- 228. Rimbert V, Boirie Y, Bedu M, Hocquette cal activity/exercise and type 2 diabetes:
tion Study. BMC Public Health 2008;8: JF, Ritz P, Morio B. Muscle fat oxidative a consensus statement from the Ameri-
235 capacity is not impaired by age but by can Diabetes Association. Diabetes Care
216. Pham H, Armstrong DG, Harvey C, Har- physical inactivity: association with in- 2006;29(6):1433 8
kless LB, Giurini JM, Veves A. Screening sulin sensitivity. FASEB J 2004;18(6): 241. Sigal RJ, Purdon C, Bilinski D, Vranic M,
techniques to identify people at high risk 7379 Halter JB, Marliss EB. Glucoregulation
for diabetic foot ulceration: a prospec- 229. Ronnemaa T, Marniemi J, Puukka P, during and after intense exercise: effects
tive multicenter trial. Diabetes Care Kuusi T. Effects of long-term physical of beta-blockade. J Clin Endocrinol
2000;23(5):606 11 exercise on serum lipids, lipoproteins Metab 1994;78(2):359 66
217. Physical Activity Guidelines Advisory and lipid metabolizing enzymes in 242. Singleton JR, Smith AG, Russell JW,
Committee. Physical Activity Guidelines type 2 (noninsulin-dependent) dia- Feldman EL. Microvascular complica-
Advisory Committee Report, 2008. Wash- betic patients. Diabetes Res 1988;7(2): tions of impaired glucose tolerance. Di-
ington (DC); U.S. Department of Health 79 84 abetes 2003;52(12):286773
and Human Services; 2008. p 683 230. Rosenstock J, Hassman DR, Madder RD, 243. Sjosten N, Kivela SL. The effects of phys-
218. Pi-Sunyer X, Blackburn G, Brancati FL, et al. Repaglinide versus nateglinide ical exercise on depressive symptoms
et al. Reduction in weight and cardiovas- monotherapy: a randomized, multi- among the aged: a systematic review. Int

care.diabetesjournals.org DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 e165
Exercise and type 2 diabetes

J Geriatr Psychiatry 2006;21(5):410 8 heterogeneous population recruited by 270. Wang Y, Simar D, Fiatarone Singh MA.
244. Smith AG, Singleton JR. Impaired glu- acute exercise. Biochem Biophys Res Adaptations to exercise training within
cose tolerance and neuropathy. Neurol- Commun 2001;284(2):490 5 skeletal muscle in adults with type 2 di-
ogist 2008;14(1):239 257. Tsang T, Orr R, Lam P, Comino E, Singh abetes or impaired glucose tolerance: a
245. Smith SC Jr, Allen J, Blair SN, et al. AHA/ MF. Effects of tai chi on glucose ho- systematic review. Diabetes Metab Res
ACC guidelines for secondary preven- meostasis and insulin sensitivity in older Rev 2009;25(1):13 40
tion for patients with coronary and other adults with type 2 diabetes: a random- 271. Watt MJ, Heigenhauser GJ, Dyck DJ,
atherosclerotic vascular disease: 2006 ised double-blind sham-exercise- con- Spriet LL. Intramuscular triacylglycerol,
update: endorsed by the National Heart, trolled trial. Age Ageing 2008;37(1): glycogen and acetyl group metabolism
Lung, and Blood Institute. Circulation 64 71 during 4 h of moderate exercise in man.
2006;113(19):236372 258. Tudor-Locke C, Bell RC, Myers AM, et J Physiol 2002;541(Pt 3):969 78
246. Snowling NJ, Hopkins WG. Effects of al. Controlled outcome evaluation of the 272. Wei M, Gibbons LW, Kampert JB,
different modes of exercise training on First Step Program: a daily physical ac- Nichaman MZ, Blair SN. Low cardiore-
glucose control and risk factors for com- tivity intervention for individuals with spiratory fitness and physical inactivity
plications in type 2 diabetic patients: a type II diabetes. Int J Obes Relat Metab as predictors of mortality in men with
meta-analysis. Diabetes Care 2006; Disord 2004;28(1):1139 type 2 diabetes. Ann Intern Med 2000;
29(11):2518 27 259. Tufescu A, Kanazawa M, Ishida A, et al. 132(8):60511
247. Stellingwerff T, Boon H, Gijsen AP, Ste- Combination of exercise and losartan 273. Wei M, Gibbons LW, Mitchell TL, Ka-
gen JH, Kuipers H, van Loon LJ. Carbo- enhances renoprotective and peripheral mpert JB, Lee CD, Blair SN. The associ-
hydrate supplementation during pro- effects in spontaneously type 2 diabetes ation between cardiorespiratory fitness
longed cycling exercise spares muscle mellitus rats with nephropathy. J Hyper- and impaired fasting glucose and type 2
glycogen but does not affect intramyo- tens 2008;26(2):31221 diabetes mellitus in men. Ann Intern
cellular lipid use. Pflugers Arch 2007; 260. Tuomilehto J, Lindstrom J, Eriksson JG, Med 1999;130(2):89 96
454(4):635 47 et al. Prevention of type 2 diabetes mel- 274. Weinsier RL, Hunter GR, Desmond RA,
248. Stevens RJ, Kothari V, Adler AI, Stratton litus by changes in lifestyle among sub- Byrne NM, Zuckerman PA, Darnell BE.
IM. The UKPDS risk engine: a model for jects with impaired glucose tolerance. Free-living activity energy expenditure
the risk of coronary heart disease in Type N Engl J Med 2001;344(18):134350 in women successful and unsuccessful at
II diabetes (UKPDS 56). Clin Sci (Lond) 261. U.S. Department of Health and Human maintaining a normal body weight. Am J
2001;101(6):6719 Services Centers for Disease Control and Clin Nutr 2002;75(3):499 504
249. Stewart KJ. Role of exercise training on Prevention. National Diabetes Fact Sheet: 275. Wenger NK, Froelicher ES, Smith LK, et
cardiovascular disease in persons who General Information and National Esti- al. Cardiac rehabilitation as secondary
have type 2 diabetes and hypertension. mates on Diabetes in the United States, prevention. Agency for Health Care Pol-
Cardiol Clin 2004;22(4):569 86 2007. Atlanta (GA): U.S. Department of icy and Research and National Heart,
250. Suh SH, Paik IY, Jacobs K. Regulation of Health and Human Services Centers for Lung, and Blood Institute. Clin Pract
blood glucose homeostasis during pro- Disease Control and Prevention; 2008 Guidel Quick Ref Guide Clin 1995;17:
longed exercise. Mol Cells 2007;23(3): 262. U.S. Preventive Services Task Force. 123
2729 Screening for coronary heart disease: 276. Willey KA, Singh MA. Battling insulin
251. Sui X, Hooker SP, Lee IM, et al. A prospec- recommendation statement. Ann Intern resistance in elderly obese people with
tive study of cardiorespiratory fitness and Med 2004;140(7):569 72 type 2 diabetes: bring on the heavy
risk of type 2 diabetes in women. Diabetes 263. Vincent KR, Braith RW, Feldman RA, et weights. Diabetes Care 2003;26(5):
Care 2008;31(3):550 5 al. Resistance exercise and physical per- 1580 8
252. Szewieczek J, Dulawa J, Strzalkowska D, formance in adults aged 60 to 83. J Am 277. Williams DM. Exercise, affect, and ad-
Batko-Szwaczka A, Hornik B. Normal Geriatr Soc 2002;50(6):1100 7 herence: an integrated model and a case
insulin response to short-term intense 264. Vinik AI. Neuropathy. In The Health Pro- for self-paced exercise. J Sport Exerc
exercise is abolished in type 2 diabetic fessionals Guide to Diabetes and Exercise. Psychol 2008;30(5):47196
patients treated with gliclazide. J Diabe- Alexandria (VA): American Diabetes As- 278. Williams DM, Dunsiger S, Ciccolo JT,
tes Complications 2009;23(6):380 6 sociation 1995. p. 18397 Lewis BA, Albrecht AE, Marcus BH.
253. Szewieczek J, Dulawa J, Strzalkowska D, 265. Vinik AI, Ziegler D. Diabetic cardiovas- Acute affective response to a moderate-
Hornik B, Kawecki G. Impact of the cular autonomic neuropathy. Circula- intensity exercise stimulus predicts
short-term, intense exercise on post- tion 2007;115(3):38797 physical activity participation 6 and 12
prandial glycemia in type 2 diabetic pa- 266. Wadden TA, West DS, Delahanty L, et months later. Psychol Sport Exerc 2008;
tients treated with gliclazide. J Diabetes al. The Look AHEAD study: a descrip- 9(3):231 45
Complications 2007;21(2):1017 tion of the lifestyle intervention and the 279. Williams K, Prevost AT, Griffin S, et al.
254. The Today Study Group, Zeitler P, Ep- evidence supporting it. Obesity 2006; The ProActive trial protocola random-
stein L, et al. Treatment options for type 14(5):73752 ised controlled trial of the efficacy of a
2 diabetes in adolescents and youth: a 267. Wagner H, Degerblad M, Thorell A, et al. family-based, domiciliary intervention
study of the comparative efficacy of met- Combined treatment with exercise train- programme to increase physical activity
formin alone or in combination with ros- ing and acarbose improves metabolic among individuals at high risk of diabe-
iglitazone or lifestyle intervention in control and cardiovascular risk factor tes [ISRCTN61323766]. BMC Public
adolescents with type 2 diabetes. Pediatr profile in subjects with mild type 2 dia- Health 2004;4:48
Diabetes 2007;8(2):74 87 betes. Diabetes Care 2006;29(7): 280. Williamson DA, Rejeski J, Lang W, et
255. Thomas DE, Elliott EJ, Naughton GA. 14717 al. Impact of a weight management
Exercise for type 2 diabetes mellitus. Co- 268. Wahren J, Ekberg K. Splanchnic regula- program on health-related quality of
chrane Database Syst Rev 2006;3: tion of glucose production. Annu Rev life in overweight adults with type 2
CD002968 Nutr 2007;27:329 45 diabetes. Arch Intern Med 2009;
256. Tomas E, Sevilla L, Palacin M, Zorzano 269. Wang JH. Effects of tai chi exercise on 169(2):16371
A. The insulin-sensitive GLUT4 storage patients with type 2 diabetes. Med Sport 281. Wing RR. Exercise and weight control.
compartment is a postendocytic and Sci 2008;52:230 8 In Ruderman N, Devlin JT, Schneider

e166 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.org
Colberg and Associates

SH, Kriska A, Eds. Handbook of Exercise 286. Yeh SH, Chuang H, Lin LW, Hsiao CY, quan exercise on metabolic control in
in Diabetes. Alexandria (VA): American Wang PW, Yang KD. Tai chi chuan ex- women with type 2 diabetes. Am J Chin
Diabetes Association; 2002. p. 355 64 ercise decreases A1C levels along with Med 2008;36(4):64754
282. Winnick JJ, Sherman WM, Habash DL, increase of regulatory T-cells and de- 292. Ziegler D, Gries FA, Spuler M, Lessmann
et al. Short-term aerobic exercise training crease of cytotoxic T-cell population in F. The epidemiology of diabetic neurop-
in obese humans with type 2 diabetes mel- type 2 diabetic patients. Diabetes Care athy. Diabetic Cardiovascular Auto-
litus improves whole-body insulin sensi- 2007;30(3):716 8 nomic Neuropathy Multicenter Study
tivity through gains in peripheral, not 287. Yeung EW, Yeung SS. Interventions for Group. J Diabetes Complications 1992;
hepatic insulin sensitivity. J Clin Endocri- preventing lower limb soft-tissue inju- 6(1):49 57
nol Metab 2008;93(3):771 8 ries in runners. Cochrane Database Syst 293. Zierath JR, He L, Guma A, Odegoard
283. Wycherley TP, Brinkworth GD, Noakes Rev 2001;3:CD001256 Wahlstrom E, Klip A, Wallberg-Hen-
M, Buckley JD, Clifton PM. Effect of ca- 288. Young LH, Wackers FJ, Chyun DA, et al. riksson H. Insulin action on glucose
loric restriction with and without exer- Cardiac outcomes after screening for transport and plasma membrane GLUT4
cise training on oxidative stress and asymptomatic coronary artery disease in content in skeletal muscle from patients
endothelial function in obese subjects patients with type 2 diabetes: the DIAD withNIDDM.Diabetologia1996;39(10):
with type 2 diabetes. Diabetes Obes study: a randomized controlled trial. 1180 9
Metab 2008;10(11):106273 JAMA 2009;301(15):154755 294. Zoppini G, Targher G, Zamboni C, et al.
284. Yates T, Davies M, Gorely T, Bull F, 289. Zee RY, Romero JR, Gould JL, Ricupero Effects of moderate-intensity exercise
Khunti K. Rationale, design and baseline DA, Ridker PM. Polymorphisms in the training on plasma biomarkers of in-
data from the Pre-diabetes Risk Educa- advanced glycosylation end product- flammation and endothelial dysfunction
tion and Physical Activity Recommenda- specific receptor gene and risk of inci- in older patients with type 2 diabetes.
tion and Encouragement (PRE-PARE) dent myocardial infarction or ischemic Nutr Metab Cardiovasc Dis 2006;16(8):
programme study: a randomized con- stroke. Stroke 2006;37(7):1686 90 5439
trolled trial. Patient Educ Couns 2008; 290. Zhang C, Solomon CG, Manson JE, Hu 295. Zwierska I, Walker RD, Choksy SA,
73(2):264 71 FB. A prospective study of pregravid Male JS, Pockley AG, Saxton JM. Upper-
285. Yates T, Khunti K, Bull F, Gorely T, Da- physical activity and sedentary behav- vs lower-limb aerobic exercise rehabili-
vies MJ. The role of physical activity in iors in relation to the risk for gestational tation in patients with symptomatic pe-
the management of impaired glucose diabetes mellitus. Arch Intern Med ripheral arterial disease: a randomized
tolerance: a systematic review. Diabeto- 2006;166(5):543 8 controlled trial. J Vasc Surg 2005;42(6):
logia 2007;50(6):1116 26 291. Zhang Y, Fu FH. Effects of 14-week tai ji 112230

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