Hindawi Publishing Corporation

Journal of Aging Research

Volume 2012, Article ID 284635, 12 pages
doi:10.1155/2012/284635

Review Article
Resistance Training and Older Adults with Type 2 Diabetes
Mellitus: Strength of the Evidence

Nina Hovanec,1 Anuradha Sawant,2 Tom J. Overend,2

Robert J. Petrella,3 and Anthony A. Vandervoort2
1 Healthand Rehabilitation Sciences Graduate Program, Western University, London, ON, Canada N6G 1H1
2 Schoolof Physical Therapy and Center for Physical Activity and Aging, Faculty of Health Sciences, Western University,
London, ON, Canada N6G 1H1
3 Department of Family Medicine, Western University, London, ON, Canada N6G 1H1

Correspondence should be addressed to Anthony A. Vandervoort, [email protected]

Received 30 April 2012; Revised 5 July 2012; Accepted 12 July 2012

Academic Editor: Bijan Najafi

Copyright © 2012 Nina Hovanec et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Objective. This paper analyzes the effects of resistance training (RT) on metabolic, neuromuscular, and cardiovascular functions
in older adults (mean age ≥ 65 years) with type 2 diabetes (T2DM). Research Design and Methods. A systematic review conducted
by two reviewers of the published literature produced 3 records based on 2 randomized controlled trials that assessed the effect
of RT on disease process measures and musculoskeletal/body composition measures. Statistical, Comprehensive Meta-Analysis
(version 2) software was used to compute Hedge’s g, and results were calculated using the random effects model to account
for methodological differences amongst studies. Results. Largest effect of RT was seen on muscle strength; especially lower body
strength, while the point estimate effect on body composition was small and not statistically significant. The cumulative point
estimate for the T2DM disease process measures was moderate and statistically significant. Conclusions. RT generally had a positive
effect on musculoskeletal, body composition, and T2DM disease processes measures, with tentative conclusions based on a low
number of completed RCTs. Thus, more research is needed on such programs for older adults (≥65 years) with T2DM.

1. Introduction improving physical fitness” [6, page 359]. Physical activity

and exercise will be used interchangeably in this paper.
Type 2 diabetes mellitus (T2DM) in older adults is an emerg- In terms of physical activity as a management method
ing epidemic [1]. (For the purpose of this paper, the term in populations living with T2DM, traditional focus has
“older adults” refers to individuals who are at least 65 years been given to aerobic training (AT) interventions [7, 8].
old.) It is an age-prevalent metabolic disorder, characterized Aerobic training activates large muscle groups to perform
by insulin resistance with relative insulin deficiency [2, 3], activities such as swimming and running, increasing the
with the highest prevalence found in individuals who are function of the heart, lungs, and muscle mitochondria to
80 years or older—an estimated number of 40 million is meet the heightened oxygen demands, ultimately resulting
expected in the United States by the year 2050 [1]. in cardiorespiratory fitness improvements [9]. Over the past
Physical activity is considered to be a cornerstone decade, interest has also emerged in conducting studies
of T2DM prevention and management [2, 4], and it is that assess the potential effect of resistance training (RT)
important to have accurate information for health care interventions in older individuals with T2DM [10–12].
organizations to integrate into their knowledge management Resistance training activates the muscular system to generate
strategies [5]. Physical activity refers to “the expenditure force against a resistive load [4]; it can be performed by
of energy above that of resting by contraction of skeletal utilizing various exercise machines, lifting free-weights (e.g.,
muscle to produce bodily movement,” while exercise is “a dumbbells), or doing calisthenics such as situps, pushups,
type of physical activity that involves planned, structured and crunches, and lunges. If RT is performed regularly, where
repetitive bodily movement performed for the purpose of the weight lifted is increased to moderate (50% of 1RM
2 Journal of Aging Research

(1RM represents 1 Repetition Maximum, which refers to the reported benefits of aerobic training, resistance training,
maximum weight that a person can lift once)) and high levels or a combination of the two on reducing HbA1c levels,
of intensity (>75% 1RM), it often leads to increased muscle which signifies improved glycemic control [25, 38, 44–47].
mass and improvements in muscular fitness [4, 13–15]. A recent meta-analysis demonstrated that supervised aerobic
Muscular fitness refers both to muscle strength, the amount or resistance training led to greater declines in HbA1c
of force produced by a muscle, and muscle endurance, levels than exercise advice only [44]. However, no previous
the ability of a muscle to “exert submaximal force for an meta-analysis has assessed the effects of RT in older adults
extended period of time” [16, page 27]. (≥65 years) with T2DM. At this time, the literature base
Resistance training may be more appealing and feasible may benefit from such a review, since older adults often
than AT for people with T2DM who are often overweight experience detrimental neuromuscular and sensorimotor
and sedentary [17], as well as for older adults, obese, and/or changes associated with aging (e.g., sarcopenia) placing them
frail individuals [4, 12, 18]. With advanced age, there is a at an increased risk for mobility problems, injury from
significant loss of muscle mass and strength, a phenomenon falls, and disability [21, 48]. Furthermore, T2DM is most
known as sarcopenia [19]. It has recently been indicated common in older adults, who as a result of this disease often
that older adults with T2DM tend to have greater muscle experience various comorbidities [49], further reducing their
mass loss, worse muscle quality (defined as the amount capacity to live independently (e.g., retinopathy, which may
of muscle strength per unit of regional muscle mass), lead to blindness; peripheral neuropathy, which may lead to
reduced upper and lower body strength, greater visceral foot ulcers and amputations; nephropathy, which over time
adipose content, as well as higher risk for functional decline could result in renal failure, etc.). Thus, the purpose of this
and disability than their healthy, age-matched counterparts paper is to conduct a systematic review of the best available
[20–24]. Resistance training might benefit older adults evidence, in order to assess the effect of RT on metabolic,
living with T2DM through muscle hypertrophy, enhanced neuromuscular, and cardiovascular functions in older adults
muscle quality, strength gains for greater power development with T2DM.
with more effective mobility function, and glycemic profile
improvements [25]. 2. Methods
Resistance training studies in populations with T2DM
were not readily available prior to 1997 [4]. The first This meta-analysis utilized the PRISMA as a framework
physical activity guidelines specifically designed for adults when selecting studies for inclusion in this paper [50]. This
with T2DM were developed by the American College of meta-analysis is not registered with any institution, such
Sports Medicine (ACSM) in the year 2000 [10]. As illustrated as the Cochrane Collaboration. The literature search was
in Figure 1, a modified timeline first introduced by Hills conducted until the end of August 2011, using electronic
and colleagues in 2010 [26], agencies such as the Canadian databases (Medline, EMBASE, AMED, PubMed, Scopus,
Diabetes Association (CDA), the American Diabetes Associ- CINAHL) that generated MESH terms based on the follow-
ation (ADA), the Canadian Society for Exercise Physiology ing keywords: resistance training, type 2 diabetes, and aged.
(CSEP), and ACSM now include RT recommendations The search terms were entered into the databases using the
within their physical activity guidelines [11, 27–37]. appropriate combinations of “OR” and “AND.” In order for
Due to the associated increases in blood pressure (BP) articles to be included in this paper, the following inclusion
that may be harmful, there could be unsubstantiated appre- and exclusion criteria needed to be satisfied.
hension in recommending RT, especially at higher intensities.
The main concern is that these BP increases could lead to
Inclusion Criteria
a stroke, myocardial ischemia, or retinal hemorrhage [4].
This may partially explain the historical dominance of AT (i) RCTs.
interventions in populations living with T2DM. However,
(ii) Published between the years 2000 and 2011.
there is a lack of scientific evidence that RT actually increases
any of the aforementioned risks, as no RT-related adverse (iii) RT interventions or a combination of RT and other
events have been reported in studies where individuals with forms of intervention (e.g., flexibility, weight loss,
T2DM were assessed [4, 38]. Additionally, past researchers standard care, etc.).
have suggested that RT may actually reduce BP levels [39– (iv) Participants with established T2DM.
41]. Finally, there are precautions that can be employed
to avoid potentially harmful side-effects of exercise, such (v) Participants’ mean age ≥65 years.
as avoiding physical activity under certain circumstances
(detailed by Gordon in 2002 [7]) and conducting appropriate
preexercise screens and assessments [7, 35, 42]. Exclusion Criteria
Skeletal muscles are the largest postprandial glucose (i) Participants with the presence of another chronic
uptake and glycogen storage sites in the human body and illness (e.g., cancer).
as such are integral in maintaining glucose homeostasis.
Resistance training may reverse or at least limit some of the (ii) Non-English publications.
aforementioned negative neuromuscular effects associated (iii) Studies reporting effect of RT in previously trained
with aging and/or T2DM [43]. Previous meta-analyses have participants.
Journal of Aging Research 3

Table 1: Outcome measures.

Body composition measures Musculoskeletal measures Type 2 diabetes process measures
Fasting glucose (mmol/L)
Muscle strength
(i) Upper body strength Glycosylated hemoglobin (HbA1c) (%)
(ii) Lower body strength
Whole body lean tissue mass (kg) Muscle quality (defined as 1RM strength Blood pressure
kg/unit lean body mass kg) Serum/fasting insulin (pmol/L)
Whole body fat mass (kg)
Muscle fiber size Lipids
(i) Type I cross sectional area (CSA) (µm2 ) (i) Total cholesterol (mmol/L)
(ii) Type II CSA (µm2 ) (ii) HDL cholesterol (mmol)
(iii) Triglycerides
(iv) Free fatty acids (FFAs) (µmol/L)
groups; 2–4 sets, 10–15 reps [32]
Health Canada: light (60 min/d)

ADA : AT 150 min/w moderate;

w/t major muscle groups, start

CDA: AT 150 min/w, moderate

(50–70% HRmax) to vigorous
w/t 1 set, 10–15 reps, progress
able/willing): RT 3 d/w, ∼8ex.

RT 3 d/w, 3 sets, 8–10 reps for

moderate-intensity PA, 5 d/w;

CSEP: for adults >65 years of

moderate weight, progress to
2 sets of 10–15 reps, progress
all major muscle groups [36]
RT details not specified [31]

intense, 150 min/w (more if

to moderate (30 min/d) AT;

150 min/w; RT using major

age AT moderate-vigorous,
(>70% HRmax); RT 3 d/w,
CDA: AT 3 d/w, moderate-
204 d/w; all major muscle

muscle groups, 2 d/w [30]

to 3 sets, 8 reps at heavier
to 3 sets, 8–12 reps [35]

start 1 set 10–15 reps at

ACSM-CDC: 30 min/d

1995 1998 2000 2002 2003 2006 2007 weight [28]2008 2010 2011
ACSM/ADA position stand: AT
ACSM/AHA: for adults <50−60
3d/w; 8–10 ex. all major muscle

150 h/w, moderate to vigorous,

ACSM position stand: RT 1 set;

5 d/w, 55–79% HRmax, or 40–

8–12 reps for 8−10 ex; 10–15

ACSM position stand: 10−30

RT 2-3 nonconsecutive d/w,

muscle groups (UE, LE, and

RT 1–3 d/w, 1 set, 8–12 reps,

optimal insulin action, 5-10

groups, 1set, 10–15 reps [10]

vigorous (75–80%1RM) for

74% HRmax reserve, 20–60
min/d 40-70 % Vo2max AT,

min; RT ligth, weights, high

patients, high RT for young

progress to 8–10 reps with

ADA position stand: AT 3–

for adults >50–60 2-3 d/w

core), 10–15 reps per set,

exercises involving major
reps for older adults [33]

moderate (50%1RM) or
reps, in nealry all T2DM

3 d/w no more than 2

heavier weights [28]

1 set, 10–15 reps [37]

consecutive days
only [11]

Figure 1: Chronological Timeline of PA Recommendations for T2DM from Various Professional Organizations [modified from [26]].
PHAC [Public Health Agency of Canada]; CSEP [Canadian Society for Exercise Physiology]; CDA [Canadian Diabetes Association]; ACSM
[American College of Sports Medicine]; ADA [American Diabetes Association]; CDC [Centers for Disease Control and Prevention]; AHA
[American Heart Association]. PA [Physical Activity]; RT [resistance training]; AT [aerobic training]; UE [upper extremity]; LE [lower
extremity]; HRmax [maximum heart rate]; VO2 max [maximal oxygen uptake/consumption]; d [days]; w [week]; w/t [with]; reps [repetitions];
ex [exercises]; h [hour]; min. [minute].

(iv) Studies reporting effect of RT on outcome measures or by comparison to the ratings provided on the PEDro
not relevant to this paper (see Table 1 for all relevant website. To limit redundancy, Cohen’s Kappa values were not
outcome measures). calculated since there were no major disagreements between
the authors (i.e., >95% agreement).
The aforementioned inclusion and exclusion criteria
were developed in order to obtain the most recent (2000– Outcome Measures. The primary outcome measures were
2011), scientifically rigorous (RCTs) evidence on the specific grouped into three major areas including body composition,
effect of resistance training in older adults with type 2 musculoskeletal, and type 2 diabetes disease process mea-
diabetes. Various studies, review articles, and commentaries sures. Table 1 summarizes the major outcome headings and
that did not satisfy the inclusion criteria were used to inform their respective measures.
the introduction and the discussion sections of this paper.
Furthermore, NH and AS independently reviewed and rated Methodological Quality of the Studies. Internal validity of
the articles and any differences were resolved by discussion studies included in this paper was assessed using the PEDro
4 Journal of Aging Research

Table 2: Participant characteristics.

Fasting Fasting
Gender Whole body BMI Diabetes HbA1c
Source Group (n) Age (years) glucose insulin
(M/F) fat mass (kg) (kg/m2 ) duration (years) (%)
(mmol/L) (pmol/L)
∗
Brooks et al.
[17] Exercise 31 66 ± 11.1 10/21 35 ± 5.6 30.9 ± 6.1 8 ± 5.6 8.7 ± 5.6 8.79 ± 2.7 116 ± 167.4
Castaneda et al. Control 31 66 ± 5.6 19/12 33.7 ± 13.4 31.2 ± 5.6 11 ± 5.6 8.4 ± 1.7 9.85 ± 3.8 115 ± 176.9
[13]
Dunstan et al. Exercise 16 67.6 ± 5.2 10/6 33.1 ± 7.4 31.5 ± 3.7 7.6 ± 5.4 8.1 ± 1 9.5 ± 2.3 132.9 ± 63
[53] Control 13 66.5 ± 5.3 6/7 35.6 ± 6.8 32.5 ± 3.8 8.8 ± 7.9 7.5 ± 1.1 9.4 ± 2.1 101.9 ± 25.8
All measures are provided as means ± SD.
∗ Brooks et al. [17] and Castaneda et al. [13] included the same cohort of participants.

scale—a valid [51] and reliable [52] tool to evaluate study findings was established based on the assessment of the effect
quality. Article ratings are included as PEDro scores listed in size and its associated confidence intervals, rather than other
Table 3, while rating criteria are detailed in Table 5. methods, such as the calculation of Fail Safe N, which can
lead to widely varied estimates [58]. The results reported
Statistical Analyses. Statistical software (Comprehensive were calculated using the random effects model, in order to
Meta-Analysis—version 2) for meta-analysis of binary, con- account for methodological differences amongst studies. The
tinuous, and diagnostic data was used for computation statistical significance for the effect sizes’ statistical tests (i.e.,
of Hedge’s g (a measure of effect size). Hedge’s g values Hedge’s g) was set at P < 0.05.
were used to assess the influence of strengthening exercises
on body composition, musculoskeletal measures, and type
2 diabetes disease outcomes (previously summarized in 3. Results
Table 1). The effect sizes were interpreted as small, medium Three [13, 17, 53] of the 446 citations were included in
and large if they were 0.2, 0.5, and 0.8, respectively [54]. the final analysis (Figure 2). However, 2 of the citations
A 95% confidence interval was constructed around the [13, 17] are technically considered one study, since their
point estimate of the effect size. Any standard errors that findings are based on the same pool of participants, but they
were reported by study authors were √
converted to standard are both included in the meta-analysis since each of them
deviations using the √ formula SD = n ∗ SE, where SD is the provides relevant but different outcome measures. A total
standard deviation, is the square root symbol, n refers to of 32 effect sizes, evaluating the effect of strength training
the sample size, ∗ represents the multiplication function, and on the disease process (20 effect sizes) and muscle quality
SE is the standard error [55]. (12 effect sizes), were extracted from the included studies.
The statistical significance of the differences in the effects Participant and study characteristics are described in Tables
of RT on body composition, muscle quality, and strength 2 and 3 respectively.
along with moderator variables included for the effect on
disease processes was computed by Page’s L statistic with
the use of PASW 18 statistical software to calculate the 3.1. Effect of RT on T2DM Disease Process Measures. Serum
sum of squares (SS) between groups, as well as total SS. insulin [17, 53], HbA1c [17, 53], HDL [13, 53], LDL and
Page’s L statistic was then calculated using the formula total cholesterol [13, 53], fasting glucose [17, 53], and BP
L = [N − 1]r 2 , where N is the total number of effect [13, 53] were analysed to evaluate the effect of RT on the
sizes and r 2 is the product of SSbetween /SStotal . (Further disease process. The overall cumulative point estimate of this
details regarding Page’s L statistic can be found in [56]) effect size was statistically significant (Hedge’s g = −0.246;
When performing meta-analysis, the overall effect of an P = 0.023; 95% CI: −0.458, −0.034).
For individual variables, the effect of RT on BP (Hedge’s
intervention can be influenced by use of particular outcome
g = −0.540; P < 0.001; CI: −0.832, −0.248), insulin (Hedge’s
measures or intervention strategies. Page’s L statistics was
g = 0.505; P = 0.016; CI: 0.094, 0.916), total cholesterol,
utilized to elucidate such differences in the current study.
and LDL cholesterol (Hedge’s g = 22120.464, P = 0.002; CI:
The presence of heterogeneity among the moderator −0.760, −0.169) was statistically significant. However, the
variables was evaluated by the Q statistic using a random effect of RT on fasting glucose (Hedge’s g = −0.121; P =
effects model. The studies were considered heterogeneous 0.559; CI: −0.526, 0.284), HbA1c (Hedge’s g = −0.463; P =
if the P value of the Q statistic was <0.1, which has been 0.145; CI: −1.084, 0.159), and HDL cholesterol (Hedge’s g =
proposed as the appropriate alternative to the conventional 0.134; P = 0.517; CI: −0.271, 0.539) was not as consistent
P < 0.05, when there is a low number of articles included between studies in terms of magnitude of improvement and
in a review [57]. Publication bias was not assessed, since fluctuations in control group. Also, the differences in effects
there were only three articles included, and any conclusions of RT on fasting glucose, insulin, HBA1c, cholesterol, HDL,
that are drawn from the results that emerge from this meta- FFA, and BP were not statistically significant (L(19) = 14.109;
analysis cannot be taken as definitive. The robustness of the P > 0.05).
Journal of Aging Research 5

Identification
446 records identified through Hand-searching of included articles
database searching was done, but no additional records
were identified

Screening
154 duplicates removed

250 records
292 records screened excluded; 6
records included

• Low mean
Eligibility

36 full-text articles assessed for age [31]

eligibility • AT focus [1]
• Not a complete
study (e.g. summary;
7 records included in qualitative only methods
synthesis (6 from screen + 1 from and design
full article assessment) reported) [2]
• Duplicate [1]

3 records included in
Included

quantitative synthesis
(meta-analysis)

Figure 2: Study selection diagram [50] AT-aerobic training.

3.2. Effect of RT on Body Composition Measures. Lean body effect sizes and statistical significance needs to be considered
mass [17, 53] and fat body mass [53, 59] were analysed with caution.
to evaluate the effect of RT on body composition. The The heterogeneity (Q-values with their respective df
cumulative point estimate effect of RT on body composition and P values) for all moderator variables is summarized in
was small but not statistically significant (Hedge’s g = 0.199; Table 4. However, the number of studies included in the
P = 0.197; CI: −0.103, 0.500). The effect of RT on lean body analysis is too small to infer definitive conclusions regarding
mass (Hedge’s g = 0.395; P = 0.220; CI: −0.237, 1.028) was heterogeneity.
larger than on fat body mass (Hedge’s g = 0.066; P = 0.749;
CI: −0.339, 0.471), but neither was statistically significant. 4. Discussion

3.3. Effect of RT on Musculoskeletal Measures. Whole body, The purpose of this paper was to conduct a systematic
lower and upper body muscles strength [13, 53], and muscle review and meta-analysis of the currently available evidence,
quality were analysed to evaluate the effect of RT on overall in order to assess the effect of resistance training in older
adults with T2DM. The findings generally show that RT
muscle strength and quality. The cumulative point estimate
has an effect on the musculoskeletal system, disease process,
effect of RT on muscle strength (Hedge’s g = 1.05; P <
and body composition to varying degrees (see Table 6 for
0.001; 95% CI: 0.699, 1.404) and overall quality (Hedge’s g = a summary of the outcome measures, their respective effect
0.816 P = 0.008; 95% CI: 0.216, 1.415) were large and sizes, and statistical significances). Overall, RT had the largest
statistically significant. The largest effect of RT was on lower effect on the musculoskeletal measures, followed by disease
body strength (Hedge’s g = 1.415; P < 0.001; CI: 0.864, process measures, while the smallest effect was seen on the
1.967), followed by upper body strength (Hedge’s g = 0.974; body composition measures.
P < 0.001; CI: 0.453, 1.494), and both were statistically It is not surprising that RT had the largest effect on
significant. The effect of RT on whole body strength was musculoskeletal measures, as it is a well-established mode of
also large and statistically significant (Hedge’s g = 0.802; exercise to induce neuromuscular changes, such as increased
P = 0.002; CI: 0.291, 1.313). muscle size and strength [15]. Specifically, findings from
The effect of RT on muscle quality (Hedge’s g = 1.460; this analysis indicate that RT increases muscle strength and
P < 0.001; CI: 0.906, 2.015) was large and statistically signif- quality. These effects could be quite consequential for the
icant. The differences in effect of RT on body composition, investigated population, as aging and T2DM are linked with
muscle quality, and strength were not statistically significant reduced muscle mass and strength, increased adiposity, and
(L(11) = 13.762; P > 0.05). However, the CI ranges were wide a sedentary lifestyle [12].
for all measures (musculoskeletal, disease process, and body Although the underlying molecular causes of T2DM
composition); as such any conclusion drawn based on the are unknown, it has been associated with obesity, visceral
6 Journal of Aging Research

Table 3: Study characteristics.

Study ID Sample
Intervention (duration, frequency,
(reference Size (n),
intensity, session duration, sets of reps, Outcome measure ( P value) Authors conclusion
number), intervention
equipment: exercises)
PEDro score design
(i)16 weeks
Whole-body lean tissue mass (0.04)
(ii) 3 d/week
Lower body muscle strength (<0.001) 16 weeks of RT
(iii) weeks 1–8: 60–80% of baseline
Exercise: Upper body muscle strength (<0.001) resulted in
1RM; weeks 10–14: 70–80% of
∗ n = 31 Muscle quality (<0.001) musculoskeletal and
Brooks et al. mid-study 1RM
RT + SC Type I fiber CSA (0.04) metabolic
[17] (iv) 45 min/session (5 min warmup;
Control: Type II fiber CSA (0.04) improvements, and it
PEDro: 7 5 min cooldown)
n = 31 HbA1c (<0.001) is a mode of exercise
(v) 3 sets of 8 reps
SC Fasting insulin (0.27) worth considering as
(vi) 5 pneumatic machines: upper
Fasting glucose (0.92) an adjunct to SC
back, chest press, leg press, knee
Whole body strength (0.0001)
extension, and flexion
(i) 16 weeks
(ii) 3 d/week
(iii) weeks 1–8: 60–80% of baseline
Exercise: Whole body fat mass (0.26) RT was feasible
1RM; weeks 10–14: 70–80% of
∗ n = 31 Total cholesterol (0.59) among older adults
Castaneda mid-study 1RM
RT + SC LDL cholesterol (0.13) with type 2 diabetes,
et al. [13] (iv) 45 min/session (5 min warmup;
Control: HDL cholesterol (0.46) and it resulted in
PEDro: 6 5 min cooldown)
n = 31 Systolic BP (0.05) improved metabolic
(v) 3 sets of 8 reps
SC Diastolic BP (0.52) control
(vi) 5 pneumatic machines: upper
back, chest press, leg press, knee
extension, and flexion
(i) 24 weeks
(ii)3 d/week
(iii) weeks 1-2: 50–60% 1RM; progress
to: 75–85% 1RM
A 16-week
(iv) 45 min/session (5 min warmup; Total cholesterol (N/A)
progressive,
Exercise: 5 min cooldown) LDL cholesterol (N/A)
high-intensity RT
n = 16 (v) 3 sets of 8–10 reps (minus HDL cholesterol (N/A)
Dunstan et al. program was effective
RT + WL abdominal curls) HbA1c (<0.01)
[53] in improving
Control: (vi) Free weights and multiple station Fasting insulin (N/A)
PEDro: 4 glycemic control and
n = 13 weight machine; 9 exercises: bench Fasting glucose (0.06)
muscle strength in
WL press, leg extension, upright row, Systolic BP (<0.05)
older adults with
lateral pull down, standing leg curl Diastolic BP (<0.05)
T2DM
with ankle weights, dumbbell seated
shoulder press, dumbbell seated biceps
curl, dumbbell biceps kickback,
abdominal curls
RT: resistance training; SC: standard care; d: days; min: minutes; sec: seconds; b/w: between; reps: repetitions; UE: upper extremity;
LE: lower extremity; CSA: cross sectional area; HbA1c: glycosylated hemoglobin; WL: weight loss).
∗ Brooks et al. [17] and Castaneda et al. [13] include the same intervention and participants but different outcome measures.
 P value reported by the authors.

adiposity, and physical inactivity, which all contribute to an counterparts [20, 22]. Reductions in muscle strength and
increased risk of developing cardiovascular disease and vari- quality have been linked to an increased risk of physical
ous disabilities [2, 23, 24]. As such, older adults with T2DM disability, such as mobility problems and falls [48]. Findings
are placed at “double jeopardy” with regards to their health from the current meta-analysis suggest that muscle strength
status, which greatly increases their dependence on health and quality improvements in older adults with T2DM could
care services [1]. A large US-based, cross-sectional study induce greater functional capacity and reduce the risk of
illustrated this point when older adults (70–79 years) with disabilities. Furthermore, muscle quality and strength gains
and without T2DM were compared [1]. Various publications may result in greater physical activity participation in various
from this study showed that those with T2DM had lower populations [60–62], including older adults with T2DM
muscle strength and quality [21], accelerated muscle loss [13], which could in turn improve this populations’ overall
(i.e., loss of knee extensor strength at a more rapid rate), and health status by reducing negative disease outcomes.
excessive muscle mass loss (i.e., greater loss in the amount In addition to improvements in muscle quality (the
of leg lean mass) when compared with healthy, age-matched measure of strength per unit of muscle mass), one study
Journal of Aging Research 7

Table 4: Heterogeneity for moderator variables. skeletal muscle approximately two to four times, leading to
improvements in glucose intolerance and insulin action [65–
Variable Q-value df (Q) P-value
67]. This underlying mechanism may partially explain some
All disease process measures 42.387 19 0.002 of the effects of RT on the disease process outcomes in this
BP 2.171 3 0.538 meta-analysis.
Fasting glucose 0.364 1 0.546 Resistance training also had some effects on various
Fasting insulin 0.181 2 0.913 markers of the disease process associated with T2DM,
HbA1c 3.099 2 0.212 including HbA1c, BP, fasting insulin, fasting glucose, HDL,
HDL 0.055 1 0.814 total and LDL cholesterol. For example, findings from
Total cholesterol and LDL 3.079 3 0.380 this meta-analysis indicated a nonsignificant, medium-sized
All musculoskeletal measures 31.313 11 0.001
effect of RT on reducing HbA1c, with a wide CI range. This
could be the result of low sample size and a few studies;
Muscle quality 8.184 4 0.085
all of the results of this meta-analysis should be considered
Muscle strength 2.675 2 0.262
with caution. Nevertheless, reduction of HbA1c is considered
Body composition 3.256 3 0.354 one of the most important markers for glucose control,
and a small change or improvement in this marker may
result in a significantly reduced risk of developing diabetic
that was included in this meta-analysis reported outcomes comorbidities. Findings from a prospective study might help
specifically regarding the cross-sectional area (CSA) of mus- illustrate this point further, as decreasing HbA1c by 1% could
cle fibers [17]. Although these outcome values could not be reduce the risk of any diabetes-related complication by 21%
meta-analyzed since only one study included these measures, [68]. Although this paper cannot confidently conclude that
the fact that fiber hypertrophy resulted warrants further RT can effectively reduce HbA1c levels in older adults with
discussion. Brooks and colleagues showed that following a T2DM, a previous meta-analysis by Boulé and colleagues
16-week RT intervention the training group increased the was able to illustrate that RT was equally effective as AT at
CSA of type I and type II fibers, while the control group improving glycemic control in middle-aged adults [25]. On
participants showed the opposite trend—a reduction in the the other hand, recently Jorge and colleagues compared RT,
CSA of both fiber types [17]. As well as strength gains leading AT, combined AT and RT, and a control group that received
to more effective force production, the increase in the CSA standard care [39]. They did not find significant reductions
of muscle fibers, especially type I muscle fibers, might lead in HbA1c within any of the exercise groups when compared
to a better delivery of oxygen through the greater capillary with the control group [39]. However, all groups had small
density and number of oxidative mitochondria [16]. In sample sizes and the control group might have improved
addition, these changes may improve the delivery of glucose their diet during the time of the intervention while their
from the blood to the muscle, while fiber hypertrophy standard care medication also could have contributed to the
may provide greater glycogen storage capacity within the small difference between groups. Previous researchers have
muscles of individuals affected by T2DM and thus potentially demonstrated that, in addition to RT effectively reducing
improve insulin resistance [16, 17]. The hypothesis that HbA1c levels, it can also increase glucose disposal and storage
muscle hypertrophy or larger muscle mass is associated capacity, improve lipid, as well as cardiovascular disease risk
with improved insulin sensitivity and glucose tolerance has profiles in adults with T2DM [69–71].
previously been recognized [63]. This meta-analysis also showed a moderate effect of RT
A further elaboration may help to explain how RT on BP, and a small effect on total and LDL cholesterol.
might influence the interaction between the neuromuscular However, the effect of RT on body composition measures,
system and the underlying disease process of T2DM. Skeletal including lean body mass and fat mass, was small and non-
muscles represent the largest glucose deposition sites in significant. The positive effect of RT on BP and cholesterol
the human body, which is negatively affected by insulin may be promising, since achieving lower BP with exercise
resistance—a defining feature of T2DM [64]. It has been is indicative of improved cardiovascular function, while a
suggested that people with T2DM have a defective insulin- reduction in cholesterol levels, especially LDL, may help
dependent pathway, which is responsible for activating reduce the risk of micro- and macrovascular complications,
glucose transporters of the muscles to help move the glucose such as atherosclerosis, stroke, and myocardial infarction [2].
from the blood into the cells [65]. However, individuals Past researchers have also found positive changes of BP that
with T2DM do not appear to have a flawed contraction- might have been induced by RT [39, 40]. These findings may
stimulated pathway for glucose transport [65]. For example, be of considerable value for those with T2DM who have a
RT would induce a muscular contraction, in turn stimulating two- to fourfold greater risk of developing cardiovascular
the translocation of the GLUT-4 (glucose transporter) to disease [72]; improvements in LDL cholesterol as well as BP
the tissue’s cell membrane to dock and activate in order could improve health outcomes for this group. Improved
to accept the glucose molecules from the blood into the physical function could lead to a greater ability to participate
cell. Thus, glucose could enter the cell via this contraction- in various physical activities safely and enjoyably and in turn
stimulated pathway even in individuals with T2DM whose reduce the sedentary behavior often found in individuals
insulin-dependent pathway is defective [65]. Furthermore, with T2DM. However, some researchers did not find that
exercise has shown to increase GLUT4 expression in human RT led to a reduction in BP [53], nor improvements in
8 Journal of Aging Research

Table 5: PEDro rating details.

Intention- Between-
Study ID Random Concealed Baseline Blind Blind Blind Adequate Point estimates
to-treat group
(PEDro score) allocation allocation comparability subjects therapists assessors followup and variability
analysis comparisons
Brooks et al.
Yes No Yes No No Yes Yes Yes Yes Yes
(7) [17]
Castaneda
Yes No No No No Yes Yes Yes Yes Yes
et al. (6) [13]
Dunstan et al.
Yes No Yes No No No No No Yes Yes
(4) [53]

Table 6: Summary of resistance training effect on outcome measures.

Outcome Hedge’s g P value Effect description (statistical significance)

Disease processes −0.271 0.008 Medium (significant)
BP (systolic/diastolic mmHg) − 0.540 <0.001 Large (significant)
HbA1c (%) −0.463 0.145 Medium (not significant)
Total and LDL cholesterol −0.464 0.002 medium (significant)
Fasting glucose −0.121 0.559 Small (not significant)
Fasting insulin 0.505 0.016 Medium (significant)
HDL cholesterol 0.134 0.517 Small (not significant)
Body composition 0.199 0.197 Small (not significant)
Lean body mass 0.395 0.220 Small (not significant)
Fat body mass 0.066 0.749 Small (not significant)
Muscle strength 1.05 <0.001 Large (significant)
Lower body muscle strength 1.415 <0.001 Large (significant)
Upper body muscle strength 0.974 <0.001 Large (significant)
Whole body muscle strength 0.802 0.002 Large (significant)
∗
Further muscle measures Exercise Control P value
Baseline 61 ± 27.8 51 ± 22.3
Quality <0.001
Final 100 ± 33.4 48 ± 22.3
Baseline 4068 ± 1425.3 4546 ± 1503.3
Type I CSA (µm2 ) 0.04
Final 4928 ± 2071.2 4381 ± 1692.6
Baseline 3885 ± 1547.8 4330 ± 1926.4
Type II CSA (µm2 ) 0.04
Final 4605 ± 1575.7 4201 ± 1870.8
BP-blood pressure; HbA1c: glycosylated hemoglobin; LDL: low density lipoprotein cholesterol; HDL: high-density lipoprotein cholesterol; CSA: cross sectional
area.
 Negative values denote a decrease in the outcome measure (i.e., this is a positive effect, since a reduction in disease processes, such as lowered BP, LDL, and

HBA1c, indicates an improvement in disease management).

∗ Further muscle measures were not entered into CMA; all values are means ± SE, taken from [17].

the LDL cholesterol levels following AT, RT, or combined when the weight and/or body composition is unaltered [25].
training [25]. Further studies are needed in order to better Future studies are needed to confirm this claim for older
understand the potential effect of RT on BP and cholesterol adults with T2DM.
in people with T2DM [53]. Although previous reviews indicate that RT can positively
The fact that body composition was not altered may impact functional and metabolic changes in people with
be due to the short intervention durations, or it could be T2DM, this is the first meta-analysis that suggests that RT
attributed to the low number of studies included in this may benefit older adults (≥65 years) in the management of
meta-analysis. However, despite RT apparently not having their disease. It is important to have accurate information
an effect on the body composition of older adults with for health care organizations to be able to integrate physical
T2DM, their metabolic control could still be impacted by activity recommendations into their knowledge management
exercise alone, since Boulé et al. indicated that RT and/or strategies [5]. However, there are insufficient high quality
AT can enhance insulin sensitivity and glycemic control even studies (only 2 original RCTs, providing 3 records) that
Journal of Aging Research 9

address the full impact of RT in older populations with 6. Conclusion

T2DM. As such, confidence in conclusions based on the
presented findings is limited. Furthermore, no study has Although strong conclusions cannot be drawn from this
included RT interventions with adults who were 80 years or meta-analysis, the potential role of RT to help older adults
older, despite this age group having the highest prevalence in the management of T2DM should be considered given
of T2DM [1]. Given the high prevalence and incidence of the current trends in aging, obesity, and diabetes. In 2005,
T2DM in geriatric populations [73], more research is needed managing diabetes and its complications cost the Canadian
to assess the potential benefits of RT for this age cohort. acute healthcare system $5.6 billion [76], while in the
Also, some studies have suggested that there is an additive US the current approximated annual cost is surpassing
benefit from combining AT and RT exercises for adults with $134 billion dollars [1]. Also, these figures are excluding
T2DM [9, 74, 75]. Future research should explore the effect the personal costs endured by those with the disease and
of combined exercise training in populations who are at least their families, associated with morbidity induced by various
65 years old. diabetic complications [1]. More recent statistics suggest
Finally, the importance of conducting appropriate preex- that, factoring the cost of undiagnosed diabetes, prediabetes,
ercise screens prior to implementing an RT or any exercise and gestational diabetes, the total cost of diabetes in the
intervention cannot be overlooked [7]. This is of particular US in 2007 totaled to $218 billion [77]. Considering that
interest when working with older/clinical populations who 26.9% of older adults in the US (approximately 10.9 million
may have various complications and comorbidities, resulting individuals) have diabetes [77], there ought to be specific
in absolute or relative contraindications to physical activity and appropriately designed interventions for this cohort.
detailed in [7, page 276] and elaborated further by other Inclusion of RT in the management of T2DM has been
researchers [18, 49]. recognized and supported by previous reviews [4, 12, 25,
Measures that could provide additional insight into the 47, 78, 79] and physical activity guidelines [27, 29, 34].
benefits/risks of RT, such as muscle quality, fiber CSAs, Future studies will help to confirm whether the metabolic
changes in free fatty acid [17], and/or triglyceride concen- benefits obtained with RT in younger populations could also
trations [53], and medication reduction [13] were reported positively impact older adults with T2DM, including the
only in some papers and thus could not be meta-analyzed. As rapidly expanding population aged 80 years or more.
a result, a better understanding of the impact of RT in older
adults with T2DM requires additional study.
References
5. Limitations [1] S. R. Gambert and S. Pinkstaff, “Emerging epidemic: diabetes
in older adults: demography, economic impact, and patho-
There are several limitations in this meta-analysis that are physiology,” Diabetes Spectrum, vol. 19, no. 4, pp. 221–228,
worth noting. Firstly, 68% of total participants from all three 2006.
records are Hispanic. As such, the generalizability of the [2] R. I. G. Holt, C. S. Cockram, A. Flyvbjerg, and B. J. Goldstein,
findings to different ethnic origins may be limited, due to the Textbook of Diabetes, Wiley-Blackwell, London, UK, 4th
diversity of psychosocial and potentially genetic factors. edition, 2010.
Secondly, using the terms physical activity and exercise [3] “American Diabetes Association,” Diabetes basics: Type 2.,
interchangeably may have varying outcome implications. For 2010, http://www.diabetes.org/diabetes-basics/type-2/?utm
instance, studies that focus on physical activity may report source=WWW&utm medium=DropDownDB&utm content=
different outcomes and result in alternate findings when Type2&utm campaign=CON.
[4] R. J. Sigal, G. P. Kenny, D. H. Wasserman, and C. Castaneda-
compared to studies using a targeted training approach with
Sceppa, “Physical activity/exercise and type 2 diabetes,” Dia-
predefined aims. betes Care, vol. 27, no. 10, pp. 2518–2539, 2004.
Thirdly, the inclusion and exclusion criteria were devel- [5] A. Kothari, N. Hovanec, R. Hastie, and S. Sibbald, “Lessons
oped to obtain the most relevant evidence for the population from the business sector for successful knowledge manage-
of older adults with type 2 diabetes, but with this strict ment in health care: a systematic review,” BMC Health Services
criteria there is a risk that perhaps relevant studies that did Research, vol. 11, article 173, 2011.
not meet the specified inclusion requirements could have [6] J. E. Yardley, A. Alberga, G. P. Kenny, and R. J. Sigal, “Lifestyle
provided some additional insight for this paper. issues: exercise,” in Textbook of Diabetes, R. I. G. Holt, C. S.
Fourthly, there is a risk of having a confounding variable Cockram, A. Flyvbjerg, and B. J. Goldstein, Eds., pp. 358–379,
effect by including Dunstan et al. [53], since their RT Wiley-Blackwell, London, UK, 4th edition, 2010.
intervention was combined with a weight loss component. [7] N. F. Gordon, “The exercise prescription,” in Handbook
Thus, it is not possible to have a definitive conclusion about of Exercise in Diabetes, pp. 269–288, American Diabetes
Association, New York, NY, USA, 2nd edition, 2002.
the independent effect the RT intervention might have had if
[8] H. Wallberg-Henriksson, J. Rincon, and J. R. Zierath, “Exercise
it was not combined with the weight loss component. in the management of non-insulin-dependent diabetes melli-
Despite these limitations, a rigorous approach has been tus,” Sports Medicine, vol. 25, no. 1, pp. 25–35, 1998.
undertaken to provide the first precise meta-analysis that [9] A. Maiorana, G. O’Driscoll, C. Goodman, R. Taylor, and D.
assessed the currently available RCTs for RT effects on Green, “Combined aerobic and resistance exercise improves
metabolic, musculoskeletal, and cardiovascular factors in glycemic control and fitness in type 2 diabetes,” Diabetes
adults 65 years or older with type 2 diabetes. Research and Clinical Practice, vol. 56, no. 2, pp. 115–123, 2002.
10 Journal of Aging Research

[10] A. Albright, M. Franz, G. Hornsby et al., “ACSM position [27] American College of Sports Medicine and American College
stand on exercise and type 2 diabetes,” Medicine and Science of Sports Medicine position stand, “Progression models in
in Sports and Exercise, vol. 32, no. 7, pp. 1345–1360, 2000. resistance training for healthy adults,” Medicine and Science in
[11] W. G. Hornsby and R. D. Chetlin, “Resistance training,” in Sports and Exercise, vol. 41, no. 3, pp. 687–708, 2009.
Handbook of Exercise in Diabetes, N. Ruderman, J. T. Devlin, [28] S. R. Colberg, A. L. Albright, B. J. Blissmer et al., “Exercise
S. H. Schneider, and A. Kriska, Eds., pp. 311–319, American and type 2 diabetes: American College of Sports Medicine and
Diabetes Association, New York, NY, USA, 2nd edition, 2002. the American Diabetes Association: joint position statement,”
[12] K. A. Willey and M. A. Fiatarone Singh, “Battling insulin Diabetes Care, vol. 42, no. 12, pp. 2282–2303, 2010.
resistance in elderly obese people with type 2 diabetes: bring [29] Canadian Diabetes Assocation Clinicl Practice Guidelines
on the heavy weights,” Diabetes Care, vol. 26, no. 5, pp. 1580– Expert Committee, “Physical activity and diabetes,” Canadian
1588, 2003. Diabetes Journal, vol. 32, supplement 1, pp. S37–S39, 2008.
[13] C. Castaneda, J. E. Layne, L. Munoz-Orians et al., “A [30] Canadian Society for Exercise Physiology, “Canadian physical
randomized controlled trial of resistance exercise training to activity guidelines for older adults-65 years & older,” 2011,
improve glycemic control in older adults with type 2 diabetes,” http://www.csep.ca/CMFiles/Guidelines/CSEP-InfoSheets-
Diabetes Care, vol. 25, no. 12, pp. 2335–2341, 2002. adults-ENG.pdf.
[14] D. W. Dunstan, R. M. Daly, N. Owen et al., “Home-based resis- [31] R. R. Pate, M. Pratt, S. N. Blair et al., “Physical activity and
tance training is not sufficient to maintain improved glycemic public health: a recommendation from the Centers for Disease
control following supervised training in older individuals with Control and Prevention and the American College of Sports
type 2 diabetes,” Diabetes Care, vol. 28, no. 1, pp. 3–9, 2005. Medicine,” Journal of the American Medical Association, vol.
[15] A. M. Swank and P. Hagerman, “Resistance-training strategies 273, no. 5, pp. 402–407, 1995.
for individuals with type 2 diabetes,” in Resistance Training for [32] Health Canada, Canada’s Physical Activity Guide to Healthy
Special Populations, pp. 244–260, Delmar, Albany, NY, USA, Active Living, 1998.
2010. [33] American College of Sports Medicine and American College
[16] J. L. Ivy, “Exercise physiology and adaptations to training,” of Sports Medicine Position Stand, “Exercise and physical
in Handbook of Exercise in Diabetes, J. T. Ruderman, S. H. activity for older adults,” Medicine and Science in Sports and
Schneider, and A. Kriska, Eds., pp. 23–62, American Diabetes Exercise, vol. 30, no. 6, pp. 992–1008, 1998.
Association, New York, NY, USA, 2nd edition, 2002. [34] American Diabetes Association, “Diabetes mellitus and exer-
[17] N. Brooks, J. E. Layne, P. L. Gordon, R. Roubenoff, M. cise,” Diabetes Care, vol. 25, supplement1, pp. S64–S68, 2002.
E. Nelson, and C. Castaneda-Sceppa, “Strength training [35] Canadian Diabetes Association Clinical Practice Guidelines
improves muscle quality and insulin sensitivity in Hispanic Expert Committee, “Physical activity and diabetes,” Canadian
older adults with type 2 diabetes,” International Journal of Journal of Diabetes, vol. 27, pp. S24–S26, 2003.
Medical Sciences, vol. 4, no. 1, pp. 19–27, 2007. [36] R. J. Sigal, G. P. Kenny, D. H. Wasserman, C. Castaneda-
[18] O. Theou, L. Stathokostas, K. P. Roland et al., “The effective- Sceppa, and R. D. White, “Physical activity/exercise and type 2
ness of exercise interventions for the management of frailty: a diabetes: a consensus statement from the American Diabetes
systematic review,” Journal of Aging Research, vol. 2011, Article Association,” Diabetes Care, vol. 29, no. 6, pp. 1433–1438,
ID 569194, 2011. 2006.
[19] A. A. Vandervoort, “Aging of the human neuromuscular [37] W. L. Haskell, I. M. Lee, R. R. Pate et al., “Physical activity and
system,” Muscle and Nerve, vol. 25, no. 1, pp. 17–25, 2002. public health: updated recommendation for adults from the
[20] W. P. Seok, B. H. Goodpaster, S. L. Jung et al., “Excessive loss American College of Sports Medicine and the American Heart
of skeletal muscle mass in older adults with type 2 diabetes,” Association,” Medicine and Science in Sports and Exercise, vol.
Diabetes Care, vol. 32, no. 11, pp. 1993–1997, 2009. 39, no. 8, pp. 1423–1434, 2007.
[21] S. W. Park, B. H. Goodpaster, E. S. Strotmeyer et al., [38] N. J. Snowling and W. G. Hopkins, “Effects of different modes
“Decreased muscle strength and quality in older adults with of exercise training on glucose control and risk factors for
type 2 diabetes: the health, aging, and body composition complications in type 2 diabetic patients: a meta-analysis,”
study,” Diabetes, vol. 55, no. 6, pp. 1813–1818, 2006. Diabetes Care, vol. 29, no. 11, pp. 2518–2527, 2006.
[22] W. P. Seok, B. H. Goodpaster, E. S. Strotmeyer et al., [39] M. L. M. P. Jorge, V. N. de Oliveira, N. M. Resende et al.,
“Accelerated loss of skeletal muscle strength in older adults “The effects of aerobic, resistance, and combined exercise
with type 2 diabetes: the health, aging, and body composition on metabolic control, inflammatory markers, adipocytokines,
study,” Diabetes Care, vol. 30, no. 6, pp. 1507–1512, 2007. and muscle insulin signaling in patients with type 2 diabetes
[23] E. W. Gregg, C. M. Mangione, J. A. Cauley et al., “Diabetes and mellitus,” Metabolism, vol. 60, no. 9, pp. 1244–1252, 2011.
incidence of functional disability in older women,” Diabetes [40] L. A. Gordon, E. Y. Morrison, D. A. McGrowder et al.,
Care, vol. 25, no. 1, pp. 61–67, 2002. “Effect of exercise therapy on lipid profile and oxidative
[24] E. W. Gregg, G. L. A. Beckles, D. F. Williamson et al., “Diabetes stress indicators in patients with type 2 diabetes,” BMC
and physical disability among older U.S. Adults,” Diabetes Complementary and Alternative Medicine, vol. 8, article 21,
Care, vol. 23, no. 9, pp. 1272–1277, 2000. 2008.
[25] N. G. Boulé, E. Haddad, G. P. Kenny, G. A. Wells, and R. J. [41] P. L. Gordon, E. Vannier, K. Hamada et al., “Resistance
Sigal, “Effects of exercise on glycemic control and body mass in training alters cytokine gene expression in skeletal muscle
type 2 diabetes mellitus: a meta-analysis of controlled clinical of adults with type 2 diabetes,” International Journal of
trials,” Journal of the American Medical Association, vol. 286, Immunopathology and Pharmacology, vol. 19, no. 4, pp. 739–
no. 10, pp. 1218–1227, 2001. 749, 2006.
[26] A. P. Hills, S. P. Shultz, M. J. Soares et al., “Resistance training [42] T. J. Overend, T. H. Versteegh, E. Thompson, T. B. Birming-
for obese, type 2 diabetic adults: a review of the evidence,” ham, and A. A. Vandervoort, “Cardiovascular stress associated
Obesity Reviews, vol. 11, no. 10, pp. 740–749, 2010. with concentric and eccentric isokinetic exercise in young and
Journal of Aging Research 11

older adults,” Journals of Gerontology A, vol. 55, no. 4, pp. [58] J. A. C. Sterne, M. Egger, and D. Moher, “Addressing reporting
B177–B182, 2000. biases,” in Cochrane Handbook for Systematic Reviews of
[43] N. K. LeBrasseur, K. Walsh, and Z. Arany, “Metabolic benefits Interventions. Version 5.0.1, J. P. T. Higgins and S. Green, Eds.,
of resistance training and fast glycolytic skeletal muscle,” chapter 10, 2008, 2008, http://www.cochrane-handbook.org/.
American Journal of Physiology, vol. 300, no. 1, pp. E3–E10, [59] F. Castaneda, J. E. Layne, and C. Castaneda, “Skeletal muscle
2011. sodium glucose co-transporters in older adults with type 2
[44] D. Umpierre, P. A. B. Ribeiro, C. K. Kramer et al., “Physical diabetes undergoing resistance training,” International Journal
activity advice only or structured exercise training and of Medical Sciences, vol. 3, no. 3, pp. 84–91, 2006.
association with HbA1c levels in type 2 diabetes: a systematic [60] M. E. Nelson, M. A. Fiatarone, C. M. Morganti, I. Trice, R. A.
review and meta-analysis,” Journal of the American Medical Greenberg, and W. J. Evans, “Effects of high-intensity strength
Association, vol. 305, no. 17, pp. 1790–1799, 2011. training on multiple risk factors for osteoporotic fractures: a
[45] B. Strasser, U. Siebert, and W. Schobersberger, “Resistance randomized controlled trial,” Journal of the American Medical
training in the treatment of the metabolic syndrome: a Association, vol. 272, no. 24, pp. 1909–1914, 1994.
systematic review and meta-analysis of the effect of resistance [61] M. A. Fiatarone, E. F. O’Neill, N. D. Ryan et al., “Exercise
training on metabolic clustering in patients with abnormal training and nutritional supplementation for physical frailty
glucose metabolism,” Sports Medicine, vol. 40, no. 5, pp. 397– in very elderly people,” The New England Journal of Medicine,
415, 2010. vol. 330, no. 25, pp. 1769–1775, 1994.
[46] N. G. Boulé, G. P. Kenny, E. Haddad, G. A. Wells, and R. [62] L. C. Rall and R. Roubenoff, “Body composition, metabolism,
J. Sigal, “Meta-analysis of the effect of structured exercise and resistance exercise in patients with rheumatoid arthritis,”
training on cardiorespiratory fitness in Type 2 diabetes Arthritis Care and Research, vol. 9, no. 2, pp. 151–156, 1996.
mellitus,” Diabetologia, vol. 46, no. 8, pp. 1071–1081, 2003. [63] W. J. Miller, W. M. Sherman, and J. L. Ivy, “Effect of
[47] D. E. Thomas, E. J. Elliott, and G. A. Naughton, “Exercise strength training on glucose tolerance and post-glucose
for type 2 diabetes mellitus,” Cochrane Database of Systematic insulin response,” Medicine and Science in Sports and Exercise,
Reviews, vol. 3, Article ID CD002968, 2006. vol. 16, no. 6, pp. 539–543, 1984.
[48] N. De Rekeneire, H. E. Resnick, A. V. Schwartz et al., [64] R. A. DeFronzo, E. Jacot, E. Jequier, E. Maeder, J. Wahren, and
“Diabetes is associated with subclinical functional limitation J. P. Felber, “The effect of insulin on the disposal of intravenous
in nondisabled older individuals: the health, aging, and body glucose. Results from indirect calorimetry and hepatic and
composition study,” Diabetes Care, vol. 26, no. 12, pp. 3257– femoral venous catheterization,” Diabetes, vol. 30, no. 12, pp.
3263, 2003. 1000–1007, 1981.
[49] R. J. Petrella, K. Aizawa, K. Shoemaker et al., “Efficacy
[65] J. R. Zierath, A. Krook, and H. Wallberg-Henriksson, “Insulin
of a family practice-based lifestyle intervention program to
action and insulin resistance in human skeletal muscle,”
increase physical activity and reduce clinical and physiological
Diabetologia, vol. 43, no. 7, pp. 821–835, 2000.
markers of vascular health in patients with high normal blood
pressure and/or high normal blood glucose (SNAC): study [66] V. A. Hughes, M. A. Fiatarone, R. A. Fielding et al., “Exercise
protocol for a randomized controlled trial,” Trials, vol. 12, increases muscle GLUT-4 levels and insulin action in subjects
article 45, 2011. with impaired glucose tolerance,” American Journal of Physiol-
[50] D. Moher, A. Liberati, J. Tetzlaff, and D. G. Altman, “PRISMA ogy, vol. 264, no. 6, part 1, pp. E855–E862, 1993.
Group. Preferred reporting items for systematic reviews and [67] F. Dela, K. J. Mikines, M. von Linstow, N. H. Secher, and H.
meta-analyses: the PRISMA statement,” PLoS Medicine, vol. 6, Galbo, “Effect of training on insulin-mediated glucose uptake
no. 7, Article ID e1000097, 2009. in human muscle,” American Journal of Physiology, vol. 263,
[51] N. A. de Morton, “The PEDro scale is a valid measure of the no. 6, pp. E1134–E1143, 1992.
methodological quality of clinical trials: a demographic study,” [68] I. M. Stratton, A. I. Adler, H. A. W. Neil et al., “Associ-
Australian Journal of Physiotherapy, vol. 55, no. 2, pp. 129–133, ation of glycaemia with macrovascular and microvascular
2009. complications of type 2 diabetes (UKPDS 35): prospective
[52] C. G. Maher, C. Sherrington, R. D. Herbert, A. M. Moseley, observational study,” British Medical Journal, vol. 321, no.
and M. Elkins, “Reliability of the PEDro scale for rating quality 7258, pp. 405–412, 2000.
of randomized controlled trials,” Physical Therapy, vol. 83, no. [69] M. K. Holten, M. Zacho, M. Gaster, C. Juel, J. F. P. Woj-
8, pp. 713–721, 2003. taszewski, and F. Dela, “Strength training increases insulin-
[53] D. W. Dunstan, R. M. Daly, N. Owen et al., “High-intensity mediated glucose uptake, GLUT4 content, and insulin sig-
resistance training improves glycemic control in older patients naling in skeletal muscle in patients with type 2 diabetes,”
with type 2 diabetes,” Diabetes Care, vol. 25, no. 10, pp. 1729– Diabetes, vol. 53, no. 2, pp. 294–305, 2004.
1736, 2002. [70] A. Honkola, T. Forsén, and J. Eriksson, “Resistance training
[54] J. Cohen, Statistical Power Analysis for the Behavioral Sciences, improves the metabolic profile in individuals with type 2
Academic Press, New York, NY, USA, 1969. diabetes,” Acta Diabetologica, vol. 34, no. 4, pp. 245–248, 1997.
[55] J. P. T. Higgins and S. Green, “Cochrane Handbook for [71] T. P. Wycherley, M. Noakes, P. M. Clifton, X. Cleanthous, J.
Systematic Reviews of Interventions,” 2011, http://www B. Keogh, and G. D. Brinkworth, “A high-protein diet with
.cochrane-handbook.org/. resistance exercise training improves weight loss and body
[56] L. Li and W. R. Schucany, “Some properties of a test for composition in overweight and obese patients with type 2
concordance of two groups of rankings,” Biometrika, vol. 62, diabetes,” Diabetes Care, vol. 33, no. 5, pp. 969–976, 2010.
no. 2, pp. 417–423, 1975. [72] J. A. Beckman, M. A. Creager, and P. Libby, “Diabetes and
[57] The Cochrane Collaboration, “Diversity and heterogene- atherosclerosis epidemiology, pathophysiology, and manage-
ity,” 2002, http://www.cochrane-net.org/openlearning/html/ ment,” Journal of the American Medical Association, vol. 287,
mod13-3.htm. no. 19, pp. 2570–2581, 2002.
12 Journal of Aging Research

[73] M. Warren, “Physical activity: exercise prescription for the

older adult with type 2 diabetes,” Topics in Geriatric Rehabili-
tation, vol. 26, no. 3, pp. 221–232, 2010.
[74] T. S. Church, S. N. Blair, S. Cocreham et al., “Effects of aerobic
and resistance training on hemoglobin A1c levels in patients
with type 2 diabetes: a randomized controlled trial,” Journal of
the American Medical Association, vol. 304, no. 20, pp. 2253–
2262, 2010.
[75] D. J. Cuff, G. S. Meneilly, A. Martin, A. Ignaszewski, H. D.
Tildesley, and J. J. Frohlich, “Effective Exercise Modality to
Reduce Insulin Resistance in Women With Type 2 Diabetes,”
Diabetes Care, vol. 26, no. 11, pp. 2977–2982, 2003.
[76] A. Ohinmaa, P. Jacobs, S. Simpson, and J. A. Johnson, “The
projection of prevalence and cost of diabetes in Canada: 2000
to 2016,” Canadian Journal of Diabetes, vol. 28, no. 2, pp. 1–8,
2004.
[77] American Diabetes Association, Diabetes basics: Diabetes
Statistics, 2012, http://www.diabetes.org/diabetes-basics/dia-
betes-statistics/.
[78] S. F. E. Praet, R. A. M. Jonkers, G. Schep et al., “Long-standing,
insulin-treated type 2 diabetes patients with complications
respond well to short-term resistance and interval exercise
training,” European Journal of Endocrinology, vol. 158, no. 2,
pp. 163–172, 2008.
[79] S. F. E. Praet and L. J. C. van Loon, “Exercise therapy in Type 2
diabetes,” Acta Diabetologica, vol. 46, no. 4, pp. 263–278, 2009.