Reviews / Commentaries / ADA Statements

METAANAlYSIS
EHectsof Card
Factors in Type 2 Di
A meta-analysis
A NNA CIIUDn:, MSCl.
l
ROB(RT J. PcnELu.. MD. Pli O I. ) ."
OBJECTIVE-ExerCISe IS:t comerslone of dl:tbctes management and tlK' prevenllon of m-
(Idem dl:lbetcs. Howe\er. the Impact of the mode of exercise on cardlo\'ascul:tr (CV) nsk factors
m type 1 diabetes IS unclear
RESEARCH DESIGN AND METHODS_We conducled a syslem:tllc review of the Ill
ermurc between 1970 :tnd Oclober 2009 III represcnt:t\l\'{' d:uab.1SCs for IhC' effC'Ct of :terobie or
rcsiSI:tncC' exercisc t"lInmg on dUlIcal markers of CV nsk, mdudmg control, d)'slipl-
deml:l, blood preSSUTl'" and body composl1lon III p:luenls Wllh Iype 2 diabetes,
RESULTS-Of 645 amdcs retrieved, 34 met our inclUSion mtena, most In\,estig.lted :teroblC
e:r,;erCISC alone. and \0 reponed eombmed C'xC'rClse lramlng AC'roble alone or combmed I\'lIh
resistance training (RT) slgmficantl), ImprovC'd HbA
l
< -0.6 and -0,67%. rrsJXCI1\'cly (95% C1
-0.98 10 -0 17 and -0,93 to -040, resprclI\rly). systolic blood preS5un: (SBP) -6.08 and
- 359 mmHg, rrsJXCllvcly (95% CI - 10,79 to - 1.36 and -6.93 to - 024. respcctl\'cly), and
tnglycendt-s -0.3 mmoVl. (95% CI -0.48 to -0 II and -0.57 to -002, rcspcCII\cly). W:lIst
Circumference \\';ts sigmficantly Improved -3.1 cm (95% CI -\0,310 - I 1) wllh combined
aC'robic and reSlstancr rxerclsc. 3hhough frwrr sludll.'S and more heterogcnell), of the responses
werr obser\'ed in Ihe lalter two markers. ReSistance exerC'lsc alone or combmed wllh an)' mher
form of exercise was not found to ha\'e any slgmficam effecl on CV markers
CONCLUSIONS_Aerobic exercISt' alone or eombmrd \\'lIh RT ImprOl'es glycemiC control.
SBP, tnglyccndrs. and \\';tlst Ci rcumference, Thc Imp;!ct of resistance exerCISC alone on OJ nsk
markers m Iype 2 diabetes remainS unclear
D
ia bctcs tS a chronic cond1lion
brought about b)' the body's Inabi'-
lIy 10 producc enough Insultn or 10
usc Ihe lIlsulln thm It produces. /\ s a result
of thiS IIlsulin Insufficiency. Ihere is an
Increase III the concentral ion of glucose
In the blood (known as hyperglycemia).
as well as Other rnelabolic abnomtahtlcs,
According 10 Ihe World Health Orgamza-
tlon, the number of Indl\'lduals wnh dI-
abetes worldwide has IIlcreascd from 30
millton In 1985 to 171 million In 2000(1);
DillllCfCS Clift 34: 1228- 1237, 2011
Ihese ralcs are expected 10 fun her Increase.
with the World Health Organization pre-
di cting thai the worldWide prevalence In
adulls will reach 6.4% by 20)0, corre-
sponding to a )9% Increase from 2000
to 2030 (2). Of Ihe diagnosed cases of
dlabctes, il IS cSllmatcd that approxI-
mately 90-95% of mdivlduals have type
2 diabetcs (3).
Type 2 diabetes IS an mdcpendent
nsk faclOr for both macro\'ascular disease
(e.g., myocardial tnfarct lon and stroke) and

from Ill( I Aging, Rch:lblluallon, and Care: Rnc:;arch (emno. Til( \..;I." >on lIuhh Rr.sc:arch Insutu!e.
P;l.rkwood Hosplla1.l.ondon, Omano. Carl;l.(!J, lhe" lfacuh)' of MedICine. or 8nllsh Columbll,
VJIlCOU\'er, Bnllsh Columbia, C:lrod.J, Ill( 'sc:hullCh Sc:hooI of Mcdle:lnt and OcnllSlry, Umwrsur of
Wtslcm DImino. London. OnlaTlO, CaOJda, and 'School of KmeSlOlogy. hcult), of Hulth 5c:Lc:ncc:s.
UI\L\'tl"Slt) OnClno, London. Ontaoo.
Correspondmg author RoIxnJ Ptudb. pctnolb@uwoCOl
Rrcell'td 6 2010 and XCfplc:d 19 FebroJ.!)' 2011
001 102JJ7/dc:101B81
ThIS antc1c contams Supplemenlary DJll onlme ;11 hllpJIc;trt.dlabetcsJoulTIJls orfl1ookuplsupp\!dol 10.
BJ7/dcl(}'I88I/..fI)C1
() 2011 b) Ihr Amcncan Oiabeles Assoculion Readers may use thIS aTlicle as long as the work IS properly
rLled, the uSC: IS Wuc;lIional and nOi for profit, and I he work IS 1\01 Ste hupllcrutl\"C(:ommons.orgl
hctnsc:s1by-nc.ndlJ 01 for del ails
1218
microvascular disease (e.g .. rcunop.lthy
and ncphrop..lth)'), and IS often associated
wilh Olhcr cardiovascular (CV) disease
(CYO) nsk factors, Includtng high blood
pressurc (BP), d)'shpldcmia, obesi ty. lack
of phYSICal activit)', and smokmg (4.5).
Although glyccollc cont rol is a key thera-
peutic target for indiViduals wuh Iype 2
diabetes, the major cause of morbidity
and monalllY among this patient popula-
li on IS CVD. not melabolic d),sregulallon
(6). CVD IS the Icadlng cause of monaht)'
among indh'lduais wuh diabelcs (7,8),
accounting for 65% of all deaths among
thiS p..1(1ent group (9). Furthermorc, di-
abetcs IS twice as common among popu-
\at lons of patlcnts \V\lh hean failurc when
comparcd with mal ched control subJccts
(10), and patientS wLth dIabetes arc more
likely to devclop heart failurc after a myo
cardial infa rcl10n than nondiabetic tndi-
viduals(II).
Excrcise has long been recognizcd
as a cornerstone of diabetic managemcm
and Ihc prc\cntlon of mcident (habetes.
For example, the American College of
Spons Med!cllle curreml), recommends
Ihal mdlvtduals wllh type 2 diabetes
expend a nllnHllum cumulathe 100ai of
1,000 kc:tl pcr week of cnerg), from
ph }'sica I aCIl \' II ies (12). Met a -a nal yscs
havc shown thm aerobic or rcsistance
trainmg (RT) is related to stallsticall}, slg-
mficant Improvcments In glyccmlc con-
trol 0)-15). Support for thc cffect of
excrclse on olher CV nsk factors. how
ever, IS lackmg. Therefore, we conducled
Ihls revlcw to tnvCsllgalc the effects of aer-
obic excl"Clse, RT, and combmed aerobiC
and RT on CV nsk factors In type 2
diabctcs.
RESEARCH DESIGN AND
METHODS
Search strategy
The databases SPORTDlscus. SCOPUS.
PubMed, and C1NAHL were searched
usmg Simi lar search st rategies fOCUSing
on exercise interventions conductcd WIth
mdivlduals who we rc diagnosed wllh
type 2 (habetes. The searches were limIted
lO studies takmg place from 1970 to
care.diabetcsjoumals.org
Octobe r 2009 and studies published as
full reports m the English language.
References of relevant review artICles
and tnals were screened to ident ify arti-
cles thai were nOI found through the
dalab:lsc sc:l rches.
Inclusion alld exclusion criteria
The study populations consisted of indi-
VIduals aged ;2! 18 rears who have a diag-
nosis of type 2 diabetes and are engagmg
In a structured exercise program consist-
ing of aerobic exercise, progressive RT, or
combmed aerobic and progressive RT.
Because we were interested m exercIse
programs Ihal had the potential to meet
the American College of Spons Medi-
ci ne's recommendation that individuals
with type 2 diabetes expend a minimum
cumulative IOtal of I ,000 kcal per week of
energy from physical acthities. fomls of
exercise Ihal did not meellhis definttlon
(i.e., taH:hi) were not included. To be m-
cluded, the exercise mtervenllon had 10
be quantifiable m terms of frequency, In-
tenslly, time, and duralion. Only studies
whose treatment was allocated uSing a
randomized procedure and whose con-
trol group was nO! prescribed exercise as
part of the study were eligible for inclu-
sion. Because HbA
k
reOecls the :J.\"erage
blood glucose level during the precedmg
8--12 weeks, and gwen that we were in-
terested In the effects of sustained exercise
as opposed to aCUle bouts, we only in-
cluded trials In which the exercise mter-
vention had a minimum duration of 8
weeks. Finally, we only included studies
thaI measured at least one of the following
outcome measures.
Outcome measures
The chronic hyperglycemia that chamc-
tenzes type 2 diabetes is related to a
significant long-term sequelae, including
damage to and e\'entual failure of vanous
organs (macrovascular). and dIrectly re-
lated to the ltkelihood of developing
microvascuklr complications (8). There-
fore. our pnmary outcome measure was
HbA
le
, which nOI only provides an esti-
mate of overall control of blood glucose
levels within the preceding 8-- 12 weeks
but also is considered the gold standtud
for measunng long-term glycemIC control
(8. 16).
Our secondal)' outcomes mcluded
dyshpldem13 (HDl cholesterol]C]le\'els,
l Dl-C levels, triglyceride levels), systolic
BP (SBP). EMI. waist circumference, and
weight. Alt hough there is Strong evidence
to support the notion that improved
carc. diabelcsjournals.org
glycemic control reduces the risks of
mIcrovascular complicatIons. a relation-
ship between improved glycemIC control
and reduction in macrovascular complica-
\Ion has nOI been demonSiTated through
randomized controlled tnals (S.16).
Therefore, our secondary outcomes in-
cluded dyslipidemia, a condition that is
commonly charactetized In patients with
Iype 2 diabetes by the Matlierogenic lipid
t n a d ~ of h}'pcrtriglyceridemla. low levels
of HDl-C, and a predominance of small.
dense, lDl -C particles (17) and that has
an established relationshIp with risk of
macrovascular comphcal1ons (S). SSP
is a marker of hypertension that has a
st ronger association with risk of CVO
and renal disease than diastolic DP
(DBP) {IS}. ObesllY is a prominent risk
factor of type 2 diabetes, With an esti-
mated S6% of individuals with Iype 2
diabetes bemg o\'erwelght or obese. of
whom 52% are obese and 8.1 % are
morbIdly obese (19). Moreover, obesity
is an mdependent risk factor for CVO
(20), and weight loss among patients
wllh diabetes is often associated with
reduced clinical symptoms and mortal-
ity nsk {2 1}. Therefore, our secondary
outcomes included BMI and weight
as measures of changes m body compo-
sition.
Statistical analysis
Statistical analysis was performed uSing
Review Manager 5 soft ware (RevMan
5.0.17, Cochrane CollabomlLon, Oxford,
U.K.). For continuous outCOlnes pre-
sented on the same scale, we used a
weighted mean diffcrence (WtvID) calcu-
lated using the final follow-up P values pro-
vided for the interven\lon and control
groups to anal}rze the SiZe of the intervention
effecLS. \Vhen continUOUS outcomes were
not presented on the same scale, Sland'ud-
!Zed mean differences (SMDs) were used 10
anal}'%e the size of the mten'enlion effecLS
for the inten'ention and control groups al
Ihe studies' last reponed end pomts. In the
evem that stud}' outcomes were presented
as change scores, the first author of the
study was contacted with a request for pre-
post data. Studies whose authors did not
respond \\ithin I month's lime or whose
prepost data could not be obtamed from
the Cochrane Collabomtion's library of re-
views (13) were excluded (22,23). All data
were initially analyzed wuh a fixed effecLS
model. A standard -i test was used to as-
sess the presence of helerogeneity bet ween
studies. \\ilh an 0: significance level of 0.05
used as an indicator of the presence of
Chlldy k and PI,.clfa
significant heterogeneuy. The degree of in-
consIstent)' among stud}' results was
estimated usmg the 11 parameter, where
an 12 parameter >50% was considered
indicative of substantial heterogeneity.
Where heterogeneity was found, the anal-
ysis was redone using a random effects
model.
RESULTS- In Ihe mitial search of the
databascs. 645 amcles were initially iden-
tified. The most common reasons for
excluding articles were lack of a no-
exercise or standard care control group:
exercise mten'enl1on could not be quan-
tified in terms of frequency, intensity,
dumtion, and \lme; study im-estigating
the effects of aCllle exercise; wrong study
design: and irrelevant study population.
A total of 34 amcles were mcluded In the
review, wuh two studies (24,25) includ-
ing three treatment anns (a combmed aero-
bic and RT arm, an aerobiC exercIse arm,
and an RT arm) and one study (26) tn-
eludmg twO treatment arms (a combmed
ae robic and RT arm and an aerobic exer-
cise arm). Therefore, 21 studies (24-26,
Supplementary Refs. 51-518) reported
outcomes on the effects of aerobic exer-
cise. eight studies looked at the effects of
RT (24,25, Supplementary Refs. 519-
524), and 10 studies reported on the
effects of combmed ae robic and RT m
type 2 diabetes (24-26, Supplementary
Refs. 525-531). Four studies reported
results through separate pubhcal10ns
(Supplementary Refs. 51-53,512, and
S 13).
Characteristics of included studies
Aerobi c exercise. The majority of studies
(21 studies) mc1uded tnvestigated the
effects of aerobic exercise among patients
wlIh type 2 dmbetes (Table l). The fre-
quency of prescribed exercise ranged
from a minImum of one to a maxImum
of sewn sessions per week, with 13 of the
studies prescribing exercise 3 days per
week. Exercise mtensity was reported m
terms of percentage of VOz max, V0
2
peak, or maximum heart rate (HR): one
stud}' reponed exercise intensity in terms
of kilocalones expended per week. The
intensllY of exercise mnged between 50
and S5% V0
2
max or V0
2
peak and 55
and 85% maximum HR. length of exer-
cise sessions ranged between 40 and
75 mm, and dur.mon of exercise mler-
\'ention ranged between 2 months and
I rear.
RT. All eight studies looking at the effects
of RT (Table 2) invoked three supervised
DIAIIETE5 WR(, VOlIJME 34. MAl 2011 1229
Exerci se tIIlll C(lrdiowl SCII ltlr risll
Table 1---Cll(lr(lCICri Slks of (llI'obic exercise /rials
Studr
Kaplan et aI. , 1985
(Supplemental), Ref. 57)
Ronnemaa et aI., 1986 and
1988 (lipid results for 1986
stud}') (Supplementary
Refs. 512 and 513)
Wmg et a1.. 1988
(Supplementary Ref. 515)
Razetal.,1994
(Supplemental)' Ref. 511)
Ugtenbcrg et al., 1997
(Supplementary Ref. 58)
t-,-Iouricr et aI., 1997
(Supplememal)' Ref. 510)
Boudou et al" 2001 (lipid
results) and 2003
(Supplementary Refs.
SI and 52)
Cuff el aI., 2003 (22)
Imervemion
Diet \'S, exercise
(wal king) \'5. diet +
exercise I'S. control
Exercise (wal kmg, Jogging,
or skiing) \'S, control
(no mstruCllons re: exercise)
Diet + exercise
(walkmg) 1'5. diet
ExeTCIse (bicycle,
treadmill, rowmg
machine) \'5. control
Aerobic exercise (e.g ..
bICycle ergometer,
SI\1mmmg, rowing) I'S,
no exercise control
Training + BCAA supplement
1'$, naming + placebo 1'5,
sedentary + BCAA supplemelll
\'s. sedemal)' + placebo
Continuous + imermillent
exercise 1"$. control (exercised
on ergomet("T at a constant mte
of 60 r,p,m, for 20 mm at low
intensitr [30 WI)
Aerobic (treadmill, bicycle,
recumbem slepper, ellipl1ca1
trainer, rOl11ng machme)
\'5. combmed aerobiC + PRT
I"S. control (usual care)
1230 DIABETES CARE, VOWM{ 34, Moll' 2011
Frequency. Imensay. I1mc. dural10n
ExerCise group: 8/10
sessions: 1 sessions
unknown
F: I day/week
I: 60-70% max
T: iO-6O mm
D: 10 weeks
F: 5-7 S("sslons/weck
I: 70% Val max
T: 45 mm
D: 4 months
F: 4 days/week
I: -1.561 kcallweek
T: 3 mllcslsesslOn
D: 10 weeks
F: 3 days/week
I : 65% of max
T' 60 mm
D: 12 weeks
F: J days/week
I: 60-80% Val max
T: 50 mm
D: 26 weeks
Pretr;unmg period. then:
F: 1 dayslwrek
I : 75% of peak supcr.'ised
45,mm qehng class
plus
F: I day/week
I : 5 exercises at 85% of V0
2
(on an ergoq-cle)
scparated by 3 mill of
exercise at 50% VOl peak.
Both for :
D: 2 months
F: 1 days/week
I: 75% of V0
2
peak super.'lscd
45,mlll cycling class
plus
F: 1 day/week
I: 5 exercises at 85% of V0
2
peak
sepamted by 3 nun of exercise
at 50% Val peak.
Both for:
D: 2 months
F: 3 days/week
I: 60-75% IiRR
T: 75 mill
D; 16 weeks
Adherence
Directly super"scd:
log book
Exercise dianes
314 dars superVised
for first 10 weeks
213 directly supervised
sessions/week
Supcr.'ised group exerclSC
first 6 weeks, then
tmmmg:ll home:
log book
super.'lscd
Directly supervised
Directly supel"o1sed
carc. diaocl C5journals.org
Table I-COIuiulied
Study
Van Rooijen et aI., 2()(H
(Supplemental)' Ref. 514)
MiddlebrookI' et aI., 2006
(Supplemental)' Ref. 59)
Brassard et a\., 2007
(subjects ha\'e LV
diastolic dysfunwon)
(Supplementary Ref. 53)
Kadoglou et aI., 2007
(Supplemental)' Ref. 55)
Kadoglou et al.. 2007
(Supplementary Ref. 56)
SIgal Ct aI., 2007 (24)
Brun et al.. 2008
(Supplementary Ref. S4)
care.diabetesjournals.org
Intervention
Home exercise (walkmg) +
hospital-based aerobics VS.
control (relaxation exercises)
ExerClse \"s. no exercise control
Exercise (bicycle ergometer) \'s.
control (no aerobic
exercise or RT)
Exercise (mamly cyclmg.
treadmill walking/running.
calisthenics) \s. control
(mamtain habuual actl\lties)
Exercise (treadmill, cycling.
calisthentcs) \'s. control
(mmntain habitual aCtl\l!les)
Aerobic (treadmIll , bicycle
ergometer) \'5. RT vs.
comhmcd \'5. control
Exercise (walkmg,joggmg.
or gymnastics) \'5. control
(rout ine care)
Frequency, intensity, ume, duration
Home exercise:
F: 2X/day
I: moderate RPE of 12-14
(-somewhat hard" on
Borg scale)
T: stan at 10 and work up to
45 min/session
D: 12 weeks
Hospital aerobics:
F: 6 sessions
I: 55-69% max HR
(RPE 12-1 4)
T: 45 mm
D: 6 sessions
F: 3 days/week
I: 70-80% max HR
T: 30 mm
D: 6 months
F: 3 days/week
I: 60-70% VOz max
T: 30 mm
D: 12 months
F: 4 days/week
I: 50--85% VOl max
T: 45-60 mm
D: 16 weeks
F: 4 days/week
I: 50-75% VOl peak
T: 45-60 mm
D: 6 months
F: 3 days/week
I: start at 60%, work up to
75% max HR
T: start at 15 min, work
up to 45 min
D: 22 weeks
I-month educational penod
(8 2-h sessions OVCT
4 weeks): I h of exercise
education + I h of learning
to cycle at ventilator threshold
for 20-45 min.
Then:
F: 2 days/week
I: at the level ofthe ventilalOl)'
threshold
T: 45 min/session
D: 11 months
Clllldylt mill PelrellCl
Adherence
Physical activity log:
atlendance log
2 days/week of supervised
group exercise: fiued with HR
monitors 10 ensure correct
intenslt), and duration
Directly supervised
Di rectly superVised
Directly supervised
SupervIsed weekly for fi rst
4 weeks. bIweekly thereafter:
logs: ldenufication scanning
at gym: HR mont tors
Actint}' log: HR mOntlOr
10 ensure correct trainmg
intenSIty
DIASHES CARE. VOLUME 34, (1, 1..1, 2011 1231
Exucise alld cardio\'Uscular risk
Table l-Conl inued
Inlerventlon FrequenC)'. InlenSLI)'. ume. durmion Adherence
lambt'rs el aI, 2008 (26) F 3 da)'s/week DIrect I)' supervised Combmed endurnnce ..
strength tr:l1nlOg (CIrcuIt)
\'5. endumnce (simIlar to
ci rcull-same mtenSlty
but no strength tmmmg
exerclSCs) \'5 control
160-85% max HR; RT: Slaned al
60%, mcreased 10 85% I RM.
NOJlma et al. 2008
(Supplememal)' Ref. S17)
AerobIc tr:l1nlOg (suggested
walkmg. JOggmg, c}"chng,
5 .... 1mmlOg) \'5 comrol
(routme care)
AerobIc Imlnlng (walking!
3 selS or 10-15 reps
T 60 mm/sesslon
o 3 months
F al least 3 days/week
I nOI staled
T al least 30 mm/seSSlon
D.12momhs
F 4-5 days/week
Not assessed
HR monuors; at least
W}"cherle)' el aI., 2008
(Supplementary Ref. S18) Joggmg) .. cal onc
resl riCllon \s. caloric
reStrlCIIOn
I 60-65% HR max Increased
to 75-80% HR max by
week 12
I dIrectly supenised
session/week
T 25-30 mIn/sessIon mcreased
10 55-60 mm/sesslon br
wtek 12
o 12 wttks
SCM. br.mchcd-chaln amino acid, D, duranon, F. frcqutnc)': H RR. hc-an nlf restlVC. I. InICOSU)'. l \'. Jefl \cmncular. PRT. pmgrCl$lvc lT$IStancc lnlning. rcps.
rcpcll1l0ns. RM. rcpClIlIon maximum. RPE. nllng of PCTCCI\'Cd cxcnlon. T. lime
exercise sessIOns per week. wIth the study
by Sigal et al. (24) switching to biweekly
supervised sessions after I month of su-
pervised traimng sessions. Exercise dura-
tion varied between each interventIon and
ranged belween 8 weeks and 6 months.
Exercise Intenslt)' ranged between 50 and
80% one repetition maximum among the
studies.
Combined aerobic and RT. Ten studies
were seleCled for inclusion wuhm thiS
exercise category (Table 3). The majorny
of the studies directly monitored the com-
pliance of the subjects with the exercise
protocol for al least one session per week.
with one stud)' switching to btweekly suo
pervised exercise sessions after 1 month
of traming and one stud)' rel)'mg on ac-
lIVII)' logs to momtor patient adherence to
the exercise protocol. Six of Ihe studies
mvolved an exercise program carried
out three times per week, two studies in-
volved tWO weekI)' sessions, one study in-
\'oked four weekly sessions, and one
study involved a goal of partiCipants en-
gaging In exercise 5 da),s per week. Inten-
Sity of the prescribed aerobIc exercise
\'aried between an initial exercise inten-
Sll)' of 35% HR maximum 10 an upward
maximum of 85% HR max. The reSIS-
tance component of the interventions
varied in terms of prescnbed load, repe-
tition, and number of sets. Duration of
the imer.'emions ranged belween 8 weeks
and 24 months. with nine of the ten
1132 DV,8f.TES CARE. VOLUME 34, MAY 201 1
slUdles havlIlg a duration of al least 3
months.
Out comes
HbA
lc
' AerobiC exerCIse reduced HbA
lc
by 0.6% (-0.62 HbA
tc
WMD, 95% CI -
0.98 to -0.27). RT al one was not found
to ha\'e a stausl1call), stgmficant effect
on HbA
lc
(-0.33 HbA
lc
WMD, 95% CI
-0.72 to 0.05). Combined aerobiC and RT
reduced HbA
lc
by 0.67% (-0.67 HbA
lc
WMD. 95% CI -0.93 to -0.40). which
IS conSidered both stallsllcally and chni-
call)' significant.
D),slipidemia. Aerobic exercise was not
found to ha\'e a significant effect on HDL-
e (-0 HDL w ~ m , 95% C1 -0.05 10
0.05) and LDL-C (-0. 10 WMD, 95% C1
-0.44 to 0.24). Howe\'er. aerobiC exer-
cise was related to a 0.3 mmoVL decrease
(-0.29 WMD, 95% CI -0.48 to -0.11)
In tnglycerides. Estimates of the effects of
RT on HDL-C and LDL-C WeTe nOl made
because on I}' twO slUdies in\,esugaled
Ihesc outcomes. Because only Sigal et al.
(24) im'estigated the effects of RT on tri-
glycende levels, a summaI)' of effect was
not calculated for thiS outcome. Com-
billed aerobIC and RT was nOI found to
ha\'e a sigmficant effect on HDL-C (0.05
HDLC WMD. 95% C1 -0.05 to 0.15)
and LDL-C (-0.07 LDL-C WMD, 95%
CI -0.25 to 0.1l), but lowered triglycer-
Ides by 0.3 mmoVL (-0.30 triglycerides
WMD. 95% C1 -0.57 to -0.02). The
numbe r of t nals in this anal)'sis was
small.
Body composition. No statistically signif-
icant relauonships were found between
an}' of the exercise categories and changes
in B ~ I I or bod)' mass; because only one
RT slUdy reponed BMI as an outcome,
estImates of effecl were not calculated for
BMI wilhm this exercise category. Aero-
bic exercise was not related \0 changes
in B ~ I I (-0.33 BMI WMD, 95% CI
-1.26 to 0.61) or bod)' mass (0.16
bod)' mass WMD. 95% CI - 3.43 to
3.76). RT was not related to changes In
body mass (-0. 48 body mass WMD.
95% CI -4.98 \0 4.02). Combmed aer-
obic and RT was not related \0 changes
In BMI (-0.78 BMI WMD. 95% CI - 1.89
to 0.33) or body mass (- 1.02 bod)' mass
WMD, 95% CI - 2.85 to 0.82). However.
waist CIrcumference did show improve-
ment (- 3. 1 cm) after combined aerobic
and RT (-3. 1 WMD, 95% CI - 10.3 to
-1.2). This difference was significant .
SBP. Aerobic exercise was related to a
dec rease to SBP of 6 mmHg (- 6.08
WMD, 95% CI -10.79 to -l.36). This
decrease was found to be statisllcally
sigmficant, but there was sigmficant
heterogeneu)' prescnt. RT was not re-
lated to a statisticall)' Significant change
In SBP among patients with type 2 dia-
beles (-4.36 WMD, 95% CI -12.14 to
3.42). Combined aerobic and RT is re-
lated to a decrease in SBP or 3.59 mmHg
carc.diabetesjournals.org
Table 2-Chararlerislics of RT Irials
Study
Dunstan et al. 1998
(Supplementary Ref. S22)
Castaneda et a1.. 2002
(Supplementary Ref S2l)
Dunstan et aI., 2002
(Supplementary Ref. 523)
BaldI et 31 , 2003
(Supplementary Ref. 519)
Brooks et aI, 2007
(Supplementary Ref S20)
Sigal et al . 2007 ( 24)
Cheunget a],. 2009
(Supplementary Ref. 524)
Interyentton
RT vs. no exercIse
control
RT vs, nontrammg
control
Moderate weIght loss +
supervised high-mtenstt),
RT \'5, moderate weight
loss + control
Moderate mtenSll)' RT
\"S, nontrammg control
RT \"S, nontrammgcontrol
RT vs, control
RT \'5. rouune care
Frequency. mtenslty, time, duratlon
F 3 da)'s/ ..... eek
I: 50-55% of I RM
T' 3 setS of 10-15 reps
(2 setS only for first 2 weeks)
D: 8 ..... eeks
F 3 dars/week
I 60-80% of 1 RM progressmg
1070-80%
of mldslud), I
T 3 sets of S-IO reps
D: 16 weeks
F: 3 days/week
I: 50-60% of 1 RM progreSSing
10 75-85% of 1 RM
T J sets of 8-10 reps
0 : 6 months
F' 3 days/week
1 max wetght at whtch
subject could complete
10 upper and 15 lower
body selS; increased by
5% when subject
completed prescnbed
CIrcuits and reps
T: 2 setS of 12 reps
(I set onl)' for first week)
D 10 weeks
F: 3 day"Sl\\letk
L 60-80% of I RM for
8 weeks. then 70-80%
of mldstudy I RM
T' 3 setS of 8 reps
0 : 16 weeks
F: J days/week
I max weight at which
"r can be done
T 2-3 setS of 7-9 reps
0: 22 weeks
F 5 day"Slweek + 2 supeT\'l.sed
sessions lsI month then 1
supervised session each month
I: Increased lension of band
when 12 reps performed wnh
good form
T' 2selsof 12 reps
o 16 weeks
D, duration, F, frtqucncy. I. tnlensnr. reps. repcllllons. RM, rt:pcllllon Ilwumum, RPE. ra1lng of pcrctl\td tumon, T. umt
Chutlyh and Pelreila
Adherence
DIrectly supervised
Directly superVISed
DIrectly supervised
Duecdy supen'lSed
DIrectly supemsed
SupeT\llsed weekly for fiT5t 4
weeks, biweekly thereafter;
logs; Identificatlon scannmg
al gym, HR monitors
DIary
(- 3.59 WMD, 95% C1 -6.93 to -0.24).
This dcrrease was statistically significant .
of CV
risk factors is a priority among individuals
with type 2 diabetes, because CVD is the
leading cause of death among individuals
\vith diabetes (8). Funhcnnore, IndIviduals
with type 2 diabetes are at an Increascd nsk
of microvascular complications. According
to the 2008 Canadian Diabetes Associa-
tion guidelines, the main interventions
for reducing risk of CVD include control-
ling blood glucose and blood lipid levels,
as well as controlling BP (8). Therefore.
care.diabeltSjoumals.org
1233
Excrcisc and can/jowlsc lliar risll
Tabl e 3-Characlcr;Slics of mid RT Irill'S
Study
Tesslerct al.. 2000
(Supple me mary Ref. S30)
MaJomna el aI. , 2002
(Supplementary Ref. S29)
Cuff el al. . 2003 (22)
LOl!llaala et aI., 2003
(Supplement:u)' Ref. 527)
Balducci et aI. , 2004
(Supplememary Ref 525)
L01!llaala el aI., 2007
(Supplementary Ref. 528)
Sigal et al.. 2007 (24)
ImeryemlOn
Mixed acroblc (rapid walkmg) ..
RT (2 sets of 20 reps of
major muscle groups)
(trcull tr:unmg (7 RT +
8 aerobic exercises)
VS, cont rol
Combmed aerobiC (treadmill ,
bicycle. recumbem stepper.
clltpttcaltmmer, rowing
machme) .. PRT (5
exercises of major muscle
groups) \'5, control
(usual C:lre)
Ci rCUli tralnmg (8 exercises
for upper and lower
extremlll es) vs. no exercise
comrol
Aerobic cxerclse (ircadmlll,
bicycle, or elhpllcal) ... RT
(6 exercises for major muscle
groups) \'s standard
care control
ExerCIse (Joggmg or walkmg ..
RT) \'S, control
AerobIC exercise (t readtntll,
bicycle ergomeler) +
RT \s. comrol
1234 DIARETES \'01 mil: 34, MAY 2011
Frequency. intensity. lime, dur:l1Ion
F 3x /week
I. 35- 59% HR max progressmg
to 60-79% HR max at week 4
unul the end of the stud)':
2 sets of 20 reps
T 60 mm (20 aerobic. 20 RT)
D: 16 weeks
F' 3 days/week
[. 55% pretrammg MVC to 65%
b)' week 4 (RT): 70% peak
baselme HR - 85% b}' week
6 {aerobic}
T60mm
D: 8 weeks
Work:rest 45: 15 s
F: 3 da)'s/week
I. 60-75% HRR: 2 sets of 12 reps
T' 75 min
0: 16 weeks
F: 2 days/week
[: 70-80% max \'olulltary
COntraction for 10-12 reps:
65-75% Val max
T: minimum 30 olIO altarge( HR
D: 12 months
F: 3 days/week
I 40-80% HR reser\'e (aerobic);
J sets of 12 reps (RT) al
40-60% 1 RM (n.'tesled
every 3 weeks)
T 30 mm aerobiC" 30 mtn RT
D. 12 months
F 2
1: 65-75% VOl max
T mUltnlUm 30 mill at target
HR or
D: 12 months
RT:
F: 2 da)'s/week
1: 70-80% 1 R1'> l
T: Three selS of 10-12 reps
D: 12 months
F: 3 da)'s/week
1. start al 60, work up to
75% max HR
T start at 15 mtn. work
up to 45 min
D: 22 weeks
RT;
Adherence
Directl}, super .... lsed
Directly supemsed
One super.lsed
seSSion/week
Two (of four) supervised
sessions/week: exercise
dillry: exemse HR and
mtenSII}' cont rolled
Supervised weekly for first 'I
weeks, biweekly thereafter:
logs, identifi callon scanning
at gym: HR monnors
care.diabetcsjournal s.org
CllUdyll (luci
Table 3-COIrtinued
Study lnteryentlon
Frequency. rntensHy. lime. durallon Adherence
F: 3 days/week
l ' max weight at whrch
"1" can be done
T: 2-3 sets of 7-9 reps
D: 22 weeks
Krousel-Wood et aI. , 2008
(Supplementary Rd. S26)
Exercise tapes (combined
aerobic + PRT) vs. no
exercise cont rol
F: goal of 5 days/week
I: 3-6 t.IETs while using tape
T: 10-. 20-. and JO-mrn tapes
D: 3 months
Activit} logs
umbers et a1. . 2008 (28) Circuli training (combined
endurance + RT)
F: 3 days/week Directly supen'ised
I: 60-85% max HR;
\'5. control RT: started at 60%. Increased
!O 85% 1 Rt.'l, 3 setS of
IO-IS reps
T: 60 min
D: 3 months
D. duranon. F. frequency, HRR. hean rale reserve, 1, intensity: max. ma!l:rmum, METs, m(13bohc eqUIvalents: MVC. "oluntar}' COntrnClion. PRT.
progreSSive reSISlance tr:umng: reps, repeUlions: RM, repelilion maximum: T. lllne
we selected our outcome measures in this
re\' iew on the basis of these modifiable
risk factors for CYO.
For each 1 % increase in the level of
HbA
te
, the relative risk of CVO increases
by 1.18% (27), whereas each 1 % decrease
in HbA
1c
levels is associated with a 37%
reduction in microvascular complications
and a 14% reduction in myocardial in-
farctions (28). Further, lowering HbA
1e
in patients with t)'pe 2 diabetes decreases
the absolute risk of de\'c\oping coronary
heart disease by 5-17% and all cause
monality by 6-15% (29). Because the re-
lationship between the risk of CVD and
death from CY causes is Hnear (28), we
can extend our findings of the effects of
exercise on HbAlc levels to the associated
reductions in CVO risk. The 0.67% re-
duction in HbA
lc
levels associated with
combined aerobic and RT is related to a
26% decrease in risk of microvascular
complications and a 10% decrease in
rate of myocardial infarctions. Similarl)"
the 0.6% decrease In HbA] c levels related
to invoh"ement in aerobic exercise is as-
sociated with a 22% decrease in microvas-
cular complications risk and an 8%
reduclion in myocardial infarction rate.
These effects are comparable to that of
drug monotherapy, which is related to a
0.5-1.5% decrease in HbA\c, depending
on the pharmaceutical agent used and the
baseline HbA
lc
level of the individual
(30). Because the extent of HbA
lc
reduc-
tion is positively related to the baseline
value of HbA
1e
, combined aerobic and
care.diaoclcsjournals.org
strength training, as well as aerobic train-
ing. may be the preferred first-line treat-
ment option for individuals with lower
baseline HbA
1c
values who want to delay
the onset of pharmaceutical treatment.
Future studies should also consider the
impact of concomitant use of nonphar-
macologic and drug Iherap)'on CV causes
of type 2 diabetes.
According to the Canadian Diabetes
Association, BP treatment targets for in-
dividuals with type 2 diabetes include
maintenance of SBP < 130 mmHg (8).
Both aerobic and combined aerobic and
RT exercise were related to statisti cally
significant declines in SBP (6 mmHg and
3,59 mmHg, respewvely) . Moreover. the
mean SBP of the aerobic exercise trials
ranged between 126 and \33 mmHg at
last follow-up (mean SSP eo 130 mmHg).
whereas the mean SBP of the combmed
aerobic and RT ranged between 129 and
138 mmHg (mean SBP eo 134 mmHg) at
last follow-up. Therefore, aerobic and
combined aerobic and RT exercise have
the potential to have a clinically signifi-
cant impact on the presence of hyperten-
sion among individuals with type 2
diabetes. Both combined aerobic and
RT, as well as aerobic exercise, were found
to decrease triglyceride levels by 0.3
mmoVL Howeve r, we did not find stat is-
uca! support for the existence of a rela-
tionship bet ween aerobic or RT and
improved HDL-C and LDL-C among in-
dIviduals with type 2 diabetes. In a ran-
domized controlled trial of the effeCls
of aerobic exercise on lipid levels in
overweight individuals with mild-to-
moderate dyslipidemia. it was found
that improvements in lipid levels were
more closely associated with exercise
quantity than exercise intenSi t y or im-
provements in fitness (3 1). Therefore,
perhaps exercise imerventions preSCrib-
ing higher levels of exerc ise quantity
need to be carried out to positively affect
lipid le\'e\s in individuals with type 2
diabetes.
Our meta-anal ysis found lillIe sup-
pan for the benefi ts of RT on 01 risk
factors in type 2 diabetes. The energy
expenditure of RT is affected by the
number of setS and repetitions. reSI in-
terval, number of repeti tions. velOCity of
movement, and load involved in the
workout (32). Moreover, the energy ex-
penditure of RT exercises al so depends on
the combinations of muscle groups
worked (e.g., exercises im'olving greater
muscle mass are associated with signifi-
cantly larger energy expenditure) (33).
Therefore, perhaps the RT intervemions
included in this analysis were not con-
ducted at an intensity high enough to elicit
meaningful increases in energy expendi-
ture. Bloomer (34) carried OUt a random-
ized cross-over toal invohing 10 healthy
men to compare the energy expenditure
and physiologic responses to moderate-
duration resistance versus aerobi c ex-
erci se. They found that despi te being
matched for total time and relative inten-
sity. the energy cost of continuous aerobic
D I,\BETE!i CARE, VOLUM[ 34. MAY 2011 1235
Exercise amI cardiOWlSclllar risll
exercise was greater than thm of intem,it-
tent resistance exercise (34). Therefore, fu-
ture studies on the effect of RT in type 2
diabetes should investigate the effects of
high- repet it ion, high-set weight lifting,
which is carried out at higher aerobic lev-
els than the more tradi tional power-lifting
approach. When designi ng future aerobic
exercise inte rventions, endurance exer-
cises should be presc ribed in te rms of
VOl rese rve, not VOl max, because VOl
reserve has been established as being
directly rel ated to other relative (HR
reserve, HR max, the Borg rat ing of Per-
ceived Exertion 6-20 scale) and absolute
(metabolic equivalents) classifications of
exe rcise intensity (35). Further. future
studies could identify individual meta-
bolic targets, such as the maximal level
of lipid oxidation during exercise. This
in tum would allow future meta-analysts
to more accurately compare the effects of
different intensity le\'els of exercise on
outcomes of interest.
Combined aerobic exercise and RT, as
well as aerobic exercise carried Out on its
own, laking place al least two times per
week m an intenSity of 60-85% of an in-
dividual's HR maximum, is related to sta-
tistically Significant declines in HbA
Ic
,
triglyce ride levels, waist Circumfe rence,
and SSP among individuals with type 2
diabetes: however . these exe rcise ap-
proaches are not related to signirlcant
changes in weight or BMI. or to statisti-
cally Significant changes in HDL-C and
LDL-C levels. When RT is not combined
with other forms of exercise, it is not sig-
nificantly related to changes in HbA\c lev-
els or to changes in SSP. More research
needs to be conducted before the effects
of RT on HDL-C. LDL-c' and t riglyceride
le\'els can be discerned.
Addi tional reference sources can be
found in the Supplementary Data.
Acknowledgments-No potent ial conflicts of
interest relevant to this article were reported.
t\.e. was im'oked 10 the construction and
search stmtegy and contnbuted 10 \1'TLling Ihe
manuscnJX. RJ .P. was Im'olved in the concep-
tion and construction of the search strategy,
adjudIcation of articles mcluded in the analysis.
and writing and editing the manuscript.
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