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DOI 10.1007/s13300-017-0258-3
REVIEW
full-text papers of the studies were obtained for characteristics, study methods, interventions,
review. Corresponding authors of potentially outcomes, and adverse events. We used means
eligible studies were contacted if studies repor- and standard deviation (SD); where standard
ted data for which it was impossible to errors were provided, they were converted to
discriminate. SD. Corresponding authors were contacted for
Searches included terms such as ‘‘glycosy- detailed information where required. In terms
lated hemoglobin or HbA1c’’, ‘‘resistance train- of population characteristics, age, gender, BMI,
ing or strength training’’, and ‘‘type 2 diabetes’’. number, and duration of T2D of participants
Participants were at least 60 years old and had were recorded to compare the similarity of
T2D, which was defined by the World Health participants between trials.
Organization and the American Diabetes Asso- The primary outcome was HbA1c levels and
ciation’s criterion of fasting plasma glucose of at two secondary outcomes were muscular strength
least 7.0 mmol/l. Included RT was required to (% change in the one-repetition maximum
have a duration of at least 8 weeks because our (1-RM) or dynamometry) and muscle mass (LBM
main outcome of interest, HbA1c, reflects aver- or skeletal muscle mass). We selected only
age blood glucose concentration from the pre- whole-body lean mass or whole-body skeletal
vious 8–12 weeks. Trials including combined or muscle mass for LBM. If muscle strength was
mixed training and dietary supplements were reported as upper and lower body, we used the
excluded to focus on the effects of RT alone. We lower body because the lower body has a larger
included trials of RT that were structured and storage space for glucose disposal than the upper
supervised as described in terms of duration, body, which is more appropriate for T2D
frequency, intensity, and type to quantify the patients. In addition, development of lower body
training intervention and compliance except muscular strength is associated with advanced
for one trial [control (CON) group of [23]; daily physical activity of the elderly [24].
home-based RT]. Studies were excluded if the Regarding intervention, we recorded total
subjects were not human or patients had type 1 duration, frequency (times per week), intensity
diabetes or gestational diabetes. Duplicate (% of 1-RM), weekly volume (number of repeti-
studies or sub-studies of included trials were tions or sets 9 number of exercises 9 frequency),
also excluded from the analysis. session duration, target muscles of exercise,
Two reviewers (JHL and DHK) indepen- names of exercise machine or tool, and training
dently, in addition to another reviewer (CKK), place to compare the similarity of training
assessed the quality of the included studies methods between trials. The mean values were
using the PRISMA recommendations [22]. The used for calculation if the studies reported a
assessment of quality consisted of six items: range of data (e.g., 12.5, repetition 10–15).
appropriate generation of random allocation Detailed interventions about CON groups and
sequence, concealment of the allocation any additional supplements were also recorded.
sequence, blinding of the assessment and col-
lection outcomes, proportion of participants Data Analysis
lost to follow-up, complete outcome data, and
the intention-to-treat principle [22]. The Heterogeneity between studies was assessed
assessment was considered as a criterion to using the Cochran Q statistic [25]. In each
decide whether the selected studies were inclu- study, the effect size (ES) for the intervention
ded or not. was calculated as the difference between the
means of the post-measurement and pre-mea-
Data Extraction surement at the end of the intervention using
Hedges’ g. Separate meta-analyses of trials with
Data were extracted from all selected studies by HbA1c, muscle strength, and muscle mass were
two independent reviewers to record the performed to generate the mean ES and 95% CI.
detailed information regarding subject ESs were classified according to Cohen’s
Diabetes Ther
consisted of 2–3 sets (with the exception of [13] P\0.01) (Fig. 1). The absolute reduction of
where 3–5 sets were completed and home-based HbA1c was 0.50%. Univariate meta-regression
training of [23]), 8–15 repetitions, and 5–10 did not show heterogeneity between studies
exercises. The number of total sets per week (Q = 15.70, df = 9, P = 0.07), and thus, we did
ranged from 36 [29] to 81 [28], and the number not perform multivariate analysis with dura-
of total repetitions per week ranged from 320 tion, intensity, frequency, and weekly volume
[23] to 729 [28]. Intensities ranged from low variables. In other words, there were no corre-
(not specifically described in the CON groups of lations between RT’s duration, intensity, session
[23, 37]) to moderate/high (50–85% of the 1-RM times per week, and weekly volume (the total
in the experimental groups of number of sets and/or repetitions per week) and
[13, 15, 23, 28, 29, 42–44]). All training groups the changes in HbA1c levels.
progressively increased their resistance up to
80–85% of 1-RM over the duration of the
intervention on the basis of the progression of
1-RM tested at baseline and mid-study except
the CON groups of [23] and [42], but it is unsure
whether the training groups were asked to
exercise to the point of momentary muscular
failure. Of the remaining two low-intensity
groups, Mavros et al. [42] just reported that the
CON group’s resistance was set as low as possi-
ble and not progressed, but all the other things,
such as exercise type, frequency, volume, and
equipment, were the same as the experimental
group. In [23], the home-based training group
was supplied with one hand weight each and
completed a standard upper body RT program
in the home setting. We could not get further
information about that, although we contacted
two of the corresponding authors. In this cur-
rent study, the CON groups consisted of
non-exercise [15, 29, 43, 44] and aerobic train-
ing with static stretching exercises [28].
In the quality assessment, 88% reported
appropriate generation of a random allocation
sequence (7 of 8), 13% presented concealment
of the allocation sequence (1 of 8), 38% descri-
bed blinding of the assessment and collection
outcomes (3 of 8), 100% explained proportion
of participants lost to follow-up (8 of 8), 50%
exhibited complete outcome data (4 of 8), and
25% reported that the intention-to-treat prin-
ciple was used for statistical analyses (2 of 8).
Muscular Strength conducted over the long term [29] and/or much
RT significantly increased muscular strength in higher volume per week [13], indicating that
four trials (mean ES = 1.05, 95% CI = 0.26 to classifying into subgroups was impossible in the
1.84, P = 0.01) (Fig. 2). The relative increase of multivariate analysis.
strength was 38%, which included the results
from [28] presenting only percentage changes. Lean Body Mass
Univariate meta-regression showed hetero- RT in five trials did not result in a significant
geneity between studies (Q = 17.79, df = 3, effect on LBM (mean ES = 0.08, 95% CI = -0.15
P\0.01), and thus, we did further multivariate to 0.30, P = 0.50) (Fig. 3). The absolute increase
analysis with duration, intensity, frequency, of LBM was 0.78 kg. Univariate meta-regression
and weekly volume variables. However, there did not show heterogeneity between studies
were no correlations between RT session times (Q = 0.12, df = 4, P = 0.998), and thus, we did
per week (Q = 0.06, df = 1, P = 0.81) and weekly not perform multivariate analysis with dura-
total number of repetitions (Q = 0.06, df = 1, tion, intensity, frequency, and weekly volume
P = 0.81) and the changes in strength levels. We variables. In other words, there were no corre-
excluded RT’s duration, intensity, and weekly lations between RT’s duration, intensity, session
total number of sets for the multivariate analy- times per week, and weekly volume (the total
sis because all four trials performed at high
intensity [13, 15, 29, 43], only one trial was
number of sets and/or repetitions per week) and with other training components such as dura-
the changes in LBM. tion, frequency, weekly volume 1 (total number
of sets per week) and 2 (total number of repe-
Adverse Events titions per week) (P = 0.37, P = 0.82, P = 0.53,
P = 0.94, and P = 0.58, respectively). On the
The presence or absence of adverse events was basis of these findings, we might be able to
recorded in four of the ten trials. Two of these recommend that the elderly with T2D need to
reported that there were no adverse events concentrate more on intensity than duration,
[29, 44] and Ibañez et al. [13] stated that other frequency, and volume to improve both gly-
than transient musculoskeletal soreness, no cemic control and muscular strength all toge-
major complications or injuries were observed. ther. Gordon et al. [48] and Irvine et al. [49]
The fourth trial, Castaneda et al. [15], reported suggested in their meta-analysis reviews that
that there were three incidents of chest pain in higher RT intensity may be a paramount factor
subjects with coronary artery disease and five to benefit glucose control, and the meta-analy-
mild hypoglycemic events, but no exercise-re- sis review by Peterson et al. also showed that
lated injuries or adverse events in other high-intensity RT in healthy older adults
subjects. increases muscle strength more than low-in-
tensity RT (mean age 67 years) [50]. These
results of RT meta-analysis reviews are contrary
DISCUSSION to those of an AT meta-analysis review which
reported that the frequency of training may be
The primary results of this study are that RT more crucial for improving glycemic control
significantly reduced HbA1c by 0.50% and than intensity [20].
increased muscular strength by 38% in elderly There are several other important reasons
patients with T2D, although there was no why high-intensity RT might be necessary for
change in LBM. the elderly with T2D. Two primary risk factors
In terms of HbA1c, we cannot explain the for development of T2D in the elderly are cen-
training effects by finding principal variables tral obesity and physical inactivity [2]. Lack of
because there is homogeneity between studies. physical activity is closely associated with the
One possible interpretation is that different reduction of muscular strength and muscle
baseline HbA1c levels might affect the training mass, which may aggravate diabetes through
effects as subgroups with high baseline HbA1c decreased vascular supply and peripheral neu-
levels showed a slight tendency to decrease ropathy [51]. In addition to that, decreased
more than subgroups with low baseline HbA1c muscle mass compromises glycemic control as
levels after training (P = 0.30). This result was skeletal muscle plays an important role in glu-
supported by previous studies [20, 45–47]. In a cose clearance from blood vessels and storage
previous review with a meta-analysis (mean age [52]. Moreover, muscular strength and muscle
58 years), no RT components were associated mass decrease with aging [53], so that it is
with changes in HbA1c, like this current review important for diabetic patients, especially dia-
[20]. In contrast, Mavros et al. reported in their betic elders, to increase both their muscular
randomized study that only the high-intensity strength and muscle mass through RT, in par-
training group showed improvement of HbA1c ticular high-intensity training. High-intensity
levels, i.e., this improvement was not shown in RT (70–90% 1-RM) more effectively improved
the low-intensity RT group [42]. Therefore, it is both muscular strength and muscle mass in the
unclear to date whether intensity, as well as elderly as well as young people [54]. The greater
other training components, is a paramount increase of muscular strength through high-in-
factor of RT for effectively improving HbA1c. tensity RT possibly helps the elderly more
However, the current review shows that the effectively to improve their low physical activ-
effect of RT on HbA1c levels is more closely ity, which is one of the risk factors for T2D.
influenced by exercise intensity in comparison Central obesity in the elderly, another risk
Diabetes Ther
factor for T2D, may be alleviated more by homeostasis [28]. There are several possible
high-intensity RT than by low-intensity RT [42]. reasons for our result. First, detailed informa-
This is probably attributed to high-intensity RT tion cannot be obtained regarding morpholog-
increasing fatty acid oxidation by promoting ical changes, such as muscle volume, single
the oxidative function of mitochondria [55]. fiber cross-sectional area, satellite cell concen-
Furthermore, in a previous study, only tration/differentiation, or architectural modifi-
high-intensity RT was shown to decrease HbA1c cations through the measurement of LBM, so
levels in the elderly whereas the low-intensity that it is not possible to determine the degree of
training did not in spite of both groups’ hypertrophic/atrophic changes of muscle mass
increased muscle mass [42]. Castaneda et al. also [59]. Second, given that carbohydrate, fat, and
reported that high-intensity training decreases protein metabolism are interrupted in diabetes
HbA1c twice as much as moderate-intensity [60] and declined vascular supply and periph-
training because glucose uptake in skeletal eral neuropathy may be the reasons why muscle
muscle could be increased more at high inten- mass loss is related to impaired glycemic control
sity than at low or moderate intensity [15]. The [51], T2D may have negative effects on the
majority of the trials in this current study con- alterations of muscle mass. Lastly, no trials
ducted at high intensity reported no adverse involved additional dietary supplements, such
effects other than transient musculoskeletal as protein, to promote muscle protein synthesis.
soreness and mild hypoglycemic events even Such a result agrees with that of Irvine et al.
though all subjects were untrained and had not in a previous meta-analysis review showing the
previously participated in exercise training. reduction of HbA1c without increased LBM
Therefore, we should be able to recommend [49]. This is probably due to enhanced glucose
that elderly patients with T2D perform RT with clearance from the circulation through the
high intensity rather than low or moderate increased number of glucose transporter-4
intensity. However, high-intensity RT should be (GLUT4) and insulin receptors in skeletal mus-
supervised by experienced instructors or exer- cle cells without an increase in muscle mass
cise physiologists to ensure the safety of the [44]. GLUT4 plays a crucial role in transporting
elderly, and further studies are needed to glucose into tissues, and it is stimulated by
determine whether high intensity is a primary muscle contraction and/or insulin in skeletal
training factor compared to other training muscle tissues [61]. Other possible reasons for
components and whether the intensity is improved glycemic control without elevation of
defined by high percentage of 1-RM or high LBM are the improvement of intracellular
degree of effort, such as training at low or insulin signaling [62] and the activation of
moderate percentage of 1-RM until failure. glycogen synthase and protein kinase B by RT
The decrease of muscle mass with aging is [43]. Moreover, RT is reported to reduce the
closely related to a decline in metabolic func- concentration of plasma free fatty acid (FFA),
tion [56] and glycemic control [13]. An increase which improves insulin sensitivity [43], as the
in muscle mass can be equivalent to augmen- decrease of plasma FFA levels leads to reduce
tation of the glucose reservoir [13] because the intramyocellular triglyceride levels, which is
majority of insulin-stimulated glucose uptake correlated with improved insulin sensitivity
occurs in skeletal muscle [57] and increased [63].
muscle mass can contribute to decreasing the Whether or not RT improves glycemic con-
secretion of insulin, which is necessary to trol more than AT is still controversial. In the
maintain a normal glucose tolerance [52]. current review, the absolute reduction of HbA1c
However, in our review, there is no change in is 0.50% in the RT groups. A meta-analysis
LBM even though previous studies reported that review by Yang et al. reported that RT and AT
increase in LBM is positively associated with the decrease HbA1c by 0.32% and 0.46%, respec-
improvement of insulin sensitivity and gly- tively [21]. A meta-analysis review by Umpierre
cemic control [30, 58] and that increased LBM et al. also showed that AT reduces HbA1c a little
may be a primary mediator of glucose more than RT does (AT, 0.73%; RT, 0.57%) [47].
Diabetes Ther
However, other previous studies reported that study that investigated the effects of RT on
the effects of RT on glycemic control may be glycemic control as well as strength and muscle
similar to those of AT [49, 64, 65]. The com- mass in older T2D. Second, we included almost
bined training effect (RT ? AT) may also be all previous RT studies that measured HbA1c as
controversial because Snowling and Hopkins an index of glycemic control in elderly diabetic
did not find more benefits from combined patients over the age of 60. Lastly, we identified
training regarding glycemic control [66], the importance of intensity of exercise training
whereas Sigal et al. reported that combined rather than duration, frequency, and volume
training significantly reduces HbA1c more than for improving glycemic control and muscle
AT or RT alone [46]. We can probably explain strength and mass by separately analyzing the
the controversy in terms of the training meth- training variables. Thus, this study extends our
ods variables, such as intensity, frequency, and knowledge to provide an effective therapeutic
duration, and the characteristics of participants, strategy to optimize both glycemic control and
such as age, BMI, and levels of baseline HbA1c. muscle strength and mass in the elderly with
These variables make it difficult to compare RT, T2D.
AT, and combined training in terms of effec- However, there are some limitations in our
tiveness for glycemic control. study. First, the number of articles might not be
RT may improve glycemic control through a adequate because we retrieved articles only
different physiological mechanism from AT published in English, which also has a potential
[67]. RT plays an important role in increasing publication bias. Only five of the ten trials
strength and mass of muscles, whereas AT is measured muscle strength; among them one is
effective for reducing body fat by enhancing not included because the study presented the
oxygen utilization [68]. Thus, elderly patients results with only graphs, so that we did not get
with T2D need to choose the type of training precise data; and four trials measured muscle
depending on their physical condition, pur- mass by DEXA. Although we contacted several
pose, and preference to improve their glycemic authors to obtain additional data or clarify
control. However, elderly patients with T2D issues about study design, we could not acquire
may not have enough physical function to do the additional data regarding the secondary
AT with sufficient intensity and volume to outcomes. Accordingly, there is a heterogeneity
improve glycemic control because they most between studies regarding muscle strength;
likely are obese or have cardiovascular disease although homogeneity was presented between
[28, 69]. The American Diabetes Association trials regarding HbA1c and muscle mass, no
recommended AT with moderate intensity for training variables explicitly explain the differ-
at least 150 min per week for diabetics [70]. ences between subgroups. As all five trials con-
Moreover, muscle weakness starts after the age ducted RT with similar intensity, we could not
of 50 [71] and the phenomenon worsens after divide them into subgroups, such as low and
the age of 65 [72], which aggravates impaired high intensity regarding muscle strength. Sec-
glycemic control in the elderly with T2D [51]. ond, we extracted the data of muscle strength
Therefore, for elderly patients, it would be from different parts, such as whole body [15],
helpful to know the importance of RT as a lower body [28, 43], and quadriceps muscles
treatment method. However, on the basis of the [29]; besides, four trials measured muscle
finding in the current review, the extent of strength by 1-RM [13, 15, 28, 43] and one trial
decreased absolute levels of HbA1c after RT is presented it as the number of repetitions mul-
relatively small in the diabetic elderly. Thus, it tiplied by the load in kilograms [29]. Third, one
could be recommended for diabetic patients to study did not involve a CON group [13] and two
combine RT with other managements such as studies had a low-intensity training group and
medical and/or dietary treatment for better home-based RT group as CON groups [23, 42];
results. we included these last two trials in the RT
The strength of the study lies in its study group, which may increase the risk of bias.
design. First, this was the first meta-analysis However, several reviews reported that no
Diabetes Ther
differences exist in effect sizes between ran- and does not involve any new studies of human
domized and nonrandomized trials [73, 74]. or animal subjects performed by any of the
authors.
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