Hipertrofia Muscular
Hipertrofia Muscular
Hipertrofia Muscular
https://doi.org/10.1007/s40279-018-1008-z
SYSTEMATIC REVIEW
Abstract
Background Currently, there are inconsistencies in the body of evidence for the effects of resistance and aerobic training
on skeletal muscle hypertrophy.
Objective We aimed to systematically review and meta-analyze current evidence on the differences in hypertrophic adapta-
tion to aerobic and resistance training, and to discuss potential reasons for the disparities noted in the literature.
Methods The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines were followed for
this review. The Downs and Black checklist was used for the assessment of methodological quality of the included studies.
A random-effects meta-analysis was employed. In total, three analyses were performed: (1) for whole-muscle knee extensor
data; (2) for type I fiber cross-sectional area; and (3) for type II fiber cross-sectional area.
Results The final number of included studies in the present review is 21. All studies were of good or moderate methodo-
logical quality. The meta-analysis for whole-muscle hypertrophy resulted in a significant pooled difference (p < 0.001) in
responses between the aerobic training and resistance training interventions. The pooled Hedge’s g, favoring resistance over
aerobic training, was 0.66 (95% confidence interval 0.41–90; I2 = 0%). The meta-analysis for type I fiber cross-sectional area
data resulted in a significant pooled difference (p < 0.001) between the aerobic training and resistance training groups. The
pooled Hedge’s g, favoring resistance training over aerobic training, was 0.99 (95% confidence interval 0.44–1.54; I2 = 24%).
The meta-analysis of type II fiber cross-sectional area data resulted in a significant pooled difference (p < 0.001) between
the aerobic training and resistance training groups. The pooled Hedge’s g, favoring resistance training over aerobic training,
was 1.44 (95% confidence interval 0.93–1.95; I2 = 8%).
Conclusions The results of this systematic review and meta-analysis suggest that single-mode aerobic training does not pro-
mote the same skeletal muscle hypertrophy as resistance training. This finding was consistent with measurements of muscle
hypertrophy both at the whole-muscle and myofiber levels. While these results are specific to the knee extensor musculature,
it can be hypothesized that similar results would be seen for other muscle groups as well.
4
* Jozo Grgic Fitness Academy, Zagreb, Croatia
[email protected] 5
Faculty of Kinesiology, University of Zagreb, Zagreb,
1 Croatia
Institute for Health and Sport (IHES), Victoria University,
6
Melbourne, VIC, Australia School of Medical and Health Sciences, Edith Cowan
2 University, Joondalup, WA, Australia
School of Exercise and Nutrition Sciences, Deakin
7
University, Burwood, Melbourne, VIC, Australia Department of Health Sciences, Lehman College, Bronx,
3 NY, USA
Centre for Sport Research, Deakin University, Burwood,
Melbourne, VIC, Australia
Vol.:(0123456789)
J. Grgic et al.
through Scopus, PubMed/MEDLINE, and SPORTDiscus. post-training muscle hypertrophy measurements. When
The following syntax was used for the search: (“resistance required, the Web Plot Digitizer software (Version 3.11;
training” OR “resistance exercise” OR “strength training” TX, USA: Ankit Rohatgi, 2017) was used for the extraction
OR “strength exercise” OR “weight training” OR “weight of data from figures. The coding was performed indepen-
exercise” OR “resistive exercise” OR “resistive training”) dently by two authors (JG and LM). Coding files were cross-
AND (“aerobic training” OR “aerobic exercise” OR “endur- checked between the authors, and any observed differences
ance training” OR “endurance exercise” OR running OR were resolved via discussion and agreement.
cycling) AND (hypertrophy OR “cross-sectional area” OR
“muscle size” OR growth OR “lean body mass” OR “muscle
2.4 Methodological Quality
fiber” OR biopsy OR “skeletal muscle” OR “muscle thick-
ness”). The search was conducted on 28 March, 2018. For
The Downs and Black checklist [28] was used for the assess-
the purpose of study selection, the search results were down-
ment of the methodological quality of the included studies.
loaded to the EndNote software (X8; Clarivate Analytics,
The standard checklist has 27 items, which refer to: report-
New York, NY, USA). The study selection was indepen-
ing (items 1–10); external validity (items 11–13); internal
dently performed by two authors (JG and LM) to prevent
validity (items 14–26); and statistical power (item 27). How-
selection bias. In the secondary search, the reference lists of
ever, given the specificity of included studies (i.e., exercise
all included publications were screened and the studies that
interventions), we added two items that refer to reporting of
cited the included studies were examined through the Scopus
compliance (item 28) and supervision of the exercise pro-
database. Furthermore, relevant review papers [12, 26] and
grams (item 29), as used in other studies [29–31]. With the
books [27] were searched for additional relevant studies.
adjusted checklist, the maximum score was 29 points. The
following classification was used for scoring the studies: (1)
2.2 Inclusion Criteria
good methodological quality (> 20 points); (2) moderate
methodological quality (11–20 points); and (3) poor meth-
Studies meeting the following criteria were included: (1)
odological quality (< 11 points) [29–31]. Two authors (JG
published in English and in a peer-reviewed journal; (2)
and FS) independently performed the quality assessment,
compared single-mode resistance training (an exercise type
and any observed differences were resolved via discussion
that requires exertion of force against a resistance performed
and agreement.
in a dynamic fashion [11]) and single-mode aerobic training
(any form of continuous or interval aerobic training was con-
sidered) provided both types of exercise were performed by 2.5 Statistical Analysis
similar muscle groups; (3) muscular hypertrophy was meas-
ured directly at the whole-muscle level (using ultrasound, Standardized mean differences (Hedge’s g) and 95% confi-
magnetic resonance imaging, and/or computed tomography) dence intervals (CIs) were calculated based on the following
or at the myofiber level using histological assessments of data: (1) pre- and post-intervention mean muscular hyper-
muscle biopsies; (4) the training program lasted a minimum trophy values; (2) pre- and post-intervention standard devia-
of 4 weeks; and (5) the participants were apparently healthy tions; (3) correlations between pre- and post-intervention
adults without any chronic disease or musculoskeletal injury. measurements; and (4) the number of participants in each
Studies that employed dietary interventions in which the par- group. If the studies presented standard errors (SEs), they
ticipants were in a diet-prescribed caloric deficit during the were √converted to standard deviations using the formula
training program were not considered for this review. By ( SE ⋅ n ). None of the included studies presented pre-to-
contrast, studies with dietary interventions such as protein post correlation values. Therefore, correlations were esti-
s2 +s2 −s2D
supplementation for both groups were considered eligible mated with the following formula: r = pre2⋅s post
�
, where spre
and were included in the review.
⋅s pre post
participants’ characteristics, including age, height, sex, and cedure for estimating correlation is explained in detail in the
training status (e.g., trained/untrained); (2) exercise prescrip- Cochrane Handbook for Systematic Reviews of Interventions
tion details for the resistance training and aerobic training [32]. In total, three analyses were performed: (1) for whole-
groups; (3) participants’ compliance with the training pro- muscle knee extensor data; (2) for type I fiber CSA; and (3)
grams; and (4) means and standard deviations for pre- and for type II fiber CSA. A meta-analysis for upper-body
J. Grgic et al.
musculature and other lower body muscle groups, such as publications, of which, two were included [6, 24]. Therefore,
posterior thigh muscles, could not be performed owing to the final number of included studies in this review is 21.
the small number of studies assessing these muscle groups.
If the studies presented multiple data points, such as the 3.2 Study Characteristics
assessment of hypertrophy on both legs, and CSA values for
different subtypes of type II fibers (i.e., type IIa, type IIx), The pooled number of participants across studies was 509
the standardized mean differences and variances were cal- (median n = 22). The participants’ characteristics from the
culated separately and the average values were used for the included studies can be found in Table 1. The average dura-
analysis. tion of the training interventions amounted to 18 weeks
While we did not include studies in which the partici- (range 8–36 weeks). The most common training frequency
pants were in a diet-prescribed caloric deficit, two studies was three times per week (range 2–4). A summary of the
[7, 33] have reported significant weight loss in the group training programs and study details from individual studies
performing aerobic exercise, and one study reported signifi- can be found in Table 2. In two instances, the whole-muscle
cant weight loss in the group performing resistance training and fiber CSA values were reported in separate papers, even
[20]. To explore the extent to which these studies impacted though they were collected in the same sample of partici-
the pooled findings, we conducted two sensitivity analyses. pants [37, 38, 44, 45]. Fourteen studies used whole-muscle
One sensitivity analysis was performed by excluding the measures of hypertrophy, [6–9, 18–21, 33, 37, 39, 41, 43,
studies that reported significant weight loss in the group per- 44] while ten studies [6, 23, 24, 36, 38–40, 42, 43, 45] used
forming aerobic exercise, and the second sensitivity analysis histological assessments (five studies [6, 37–39, 43–45] used
excluded the study in which a significant weight loss was both). Five studies used computed tomography, [7, 9, 33,
observed in the resistance training group. These analyses 43, 44], five studies used magnetic resonance imaging, [18,
were carried out only for whole-muscle knee extensor data 21, 37, 39, 41] and four studies used ultrasound [6, 8, 19,
given that the studies reporting significant weight loss did 20]. All studies that measured muscle fiber CSA used sam-
not measure fiber CSA. ples from the vastus lateralis muscle and adenosine triphos-
The following effect size scale was used for the classifica- phatase histochemistry for the identification of muscle fiber
tion of magnitudes: small (≤ 0.2); medium (0.2–0.5); large types.
(0.5–0.8); and very large (> 0.8) effects [34]. The I2 statistic
was used to assess heterogeneity. We considered I2 values 3.3 Methodological Quality
of ≤ 50% to indicate low levels of heterogeneity; 50–75% to
indicate moderate levels of heterogeneity; and > 75% to indi- Based on the assessment of methodological quality, the
cate high levels of heterogeneity. SEs were plotted against included studies were classified as being of either good or
Hedge’s g to detect funnel plot asymmetry. The asymmetry moderate quality [Table S1 of the Electronic Supplementary
was tested using the trim and fill method [35]. The random- Material (ESM)]. Specifically, five studies [6, 23, 33, 44, 45]
effects model was used for all analyses. The statistical sig- were classified as being of good quality, while the remaining
nificance threshold was set at p < 0.05. All analyses were studies were classified as being of moderate quality [7–9,
performed using the Comprehensive Meta-Analysis soft- 18–21, 24, 36–43]. The median methodological quality score
ware, Version 2 (Biostat Inc., Englewood, NJ, USA). was 19 (range 15–24). Eight studies [6, 18, 21, 24, 36–39]
did not report participants’ compliance with the training
programs and, thus, did not receive a point on the item 28.
3 Results It was unclear in six studies [7, 36–38, 40, 41] whether the
training programs were supervised; therefore, these stud-
3.1 Search Results ies did not receive a point on item 29 of the checklist. The
methodological quality ratings for all studies can be found
The flow diagram of the literature search is presented in in Table S1 of the ESM.
Fig. 1. The initial search from the three databases resulted
in a total of 2809 search results. After the removal of dupli- 3.4 Meta‑Analysis Results
cates, the number of search results was reduced to 1953. Out
of the remaining search results, 1896 studies were excluded The meta-analyses were conducted only for the differences
based on title or abstract. Fifty-seven full-text papers were between the effects of resistance training and aerobic train-
read, and 19 studies were found that met the inclusion cri- ing on hypertrophy of knee extensors because no or limited
teria [7–9, 18–21, 23, 33, 36–45]. Forward citation track- data were available for other muscle groups.
ing and reference list screening included another 2859
Resistance vs. Aerobic Training for Hypertrophy
Identification
database searching
(n = 2,809)
• No resistance training or
aerobic training group
Records screened (n = 18)
(n = 1,953) • No hypertrophy
assessment (n = 12)
• Duplicate data (n = 4)
• Review paper (n = 2)
• Study conducted among
Full-text articles assessed adolescents (n = 1)
Eligibility
Ahtiainen et al. (2009) [6] Aerobic training: n = 9 9/0 58 ± 8 175 ± 6 75 ± 7 U
Resistance training: n = 10 10/0 61 ± 5 177 ± 3 80 ± 5 U
Bell et al. (2000) [36] Aerobic training: n = 11 7/4 22 ± 3 176 ± 9 73 ± 12 U
Resistance training: n = 11 7/4 22 ± 3 176 ± 9 73 ± 12 U
De Souza et al. (2013; 2014) [37, 38] Aerobic training: n = 8 8/0 24 ± 8 175 ± 8 72 ± 8 U
Resistance training: n = 11 11/0 26 ± 6 172 ± 4 74 ± 16 U
Farup et al. (2012) [39] Aerobic training: n = 7 7/0 23 ± 2 181 ± 5 78 ± 9 U
Resistance training: n = 7 7/0 23 ± 2 181 ± 5 78 ± 9 U
Ferrara et al. (2006) [7] Aerobic training: n = 9 9/0 50–79 NR 92 ± 4 U
Resistance training: n = 13 13/0 50–79 NR 92 ± 3 U
Hepple et al. (1997) [40] Aerobic training: n = 10 10/0 68 ± 1 NR 85 ± 4 U
Resistance training: n = 10 10/0 68 ± 1 NR 77 ± 3 U
Hudelmaier et al. (2010) [18] Aerobic training: n = 19 0/19 51 ± 3 166 ± 8 73 ± 16 U
Resistance training: n = 16 0/16 51 ± 3 166 ± 8 73 ± 16 U
Izquierdo et al. (2004) [20] Aerobic training: n = 11 11/0 68 ± 2 167 ± 3 77 ± 7 U
Resistance training: n = 10 10/0 65 ± 3 167 ± 4 81 ± 11 U
Izquierdo et al. (2005) [19] Aerobic training: n = 10 10/0 42 ± 3 177 ± 5 86 ± 14 U
Resistance training: n = 11 11/0 44 ± 3 175 ± 3 86 ± 12 U
Jubrias et al. (2001) [41]a Aerobic training: n = 14 NR 69 ± 1 NR NR U
Resistance training: n = 15 NR 69 ± 1 NR NR U
Karavirta et al. (2011) [42]b Aerobic training: n = 25 25/0 54 ± 8 176 ± 6 79 ± 10 U
Resistance training: n = 25 25/0 56 ± 6 178 ± 6 84 ± 10 U
Kraemer et al. (1995) [23] Aerobic training: n = 8 8/0 21 ± 4 178 ± 8 75 ± 7 T
Resistance training: n = 9 9/0 24 ± 5 175 ± 6 77 ± 14 T
McCarthy et al. (2002) [43] Aerobic training: n = 10 10/0 27 ± 2 179 ± 3 85 ± 6 U
Resistance training: n = 10 10/0 28 ± 1 180 ± 1 82 ± 4 U
Mikkola et al. (2012) [21] Aerobic training: n = 11 11/0 37 ± 7 181 ± 8 80 ± 13 U
Resistance training: n = 16 16/0 38 ± 6 178 ± 5 85 ± 16 U
Nelson et al. (1990) [24] Aerobic training: n = 4 4/0 30 ± 5 NR 82 ± 19 U
Resistance training: n = 5 5/0 27 ± 2 NR 70 ± 8 U
Poehlman et al. (2000) [9] Aerobic training: n = 14 0/14 29 ± 5 163 ± 5 59 ± 5 U
Resistance training: n = 17 0/17 28 ± 3 164 ± 7 58 ± 6 U
Sillanpää et al. (2008) [8] Aerobic training: n = 14 14/0 54 ± 8 179 ± 6 76 ± 9 U
Resistance training: n = 13 13/0 55 ± 6 177 ± 7 79 ± 5 U
Sipilä et al. (1995; 1997) [44, 45]c Aerobic training: n = 12 0/12 76–78 157 ± 2 67 ± 3 U
Resistance training: n = 12 0/12 76–78 160 ± 1 67 ± 3 U
Willis et al. (2012) [33] Aerobic training: n = 38 17/21 52 ± 9 88 ± 11 NR U
Resistance training: n = 44 18/26 50 ± 12 88 ± 16 NR U
Age, height, and mass data are reported as mean ± standard deviation or range
F female, M males, F females, NR not reported, T trained, U untrained, T trained
a
Magnetic resonance imaging scans were obtained from 25 participants
b
Muscle biopsies were obtained from 18 participants
c
Muscle biopsies were obtained from 16 participants
Age, height and mass data are reported as mean ± standard deviation or range
Table 2 Summary of studies included in the present meta-analysis that compared hypertrophic adaptations to resistance and aerobic training
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Ahtiainen et al. (2009) In wks 1–7, the Lower body: leg press, In wks 1–7, the par- Cycling 21 wks; 2 times Ultrasound (vastus Not reported Knee extensor muscle Knee extensor muscle
[6] participants per- knee extension, and ticipants trained for 30 per wk lateralis and vastus thickness: ↔ thickness: ↑
formed 3 sets per knee flexion min per session with intermedius); mus- Type I CSA: ↔ Type I CSA: ↔
exercise for 15–30 Upper body: bench the intensity set under cle biopsies (vastus Type II CSA: ↔ Type II CSA: ↑
repetitions with a press, triceps push- the aerobic threshold. lateralis)
load of 40–60% down, latissimus In wks 8–14, in one
1RM. In wks 8–14, pull-down, and of the two weekly ses-
the participants biceps curl sions, the participants
performed 3 sets per trained for 45 min per
exercise for 6–12 session with the inten-
repetitions with a sity set at 15 min under
load of 60–80% the aerobic threshold,
1RM. In wks 15–21, 10 min between the
Resistance vs. Aerobic Training for Hypertrophy
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Bell et al. (2000) [36] Progressive increase Lower body: leg press, Continuous aerobic Cycling 12 wks; 3 times Muscle biopsies Not reported Type I CSA: ↔ Type I CSA: ↑
in load by 4% every single leg knee training was performed per wk (vastus lateralis) Type II CSA: ↔ Type II CSA: ↑
3 wks from 72% flexion, single leg two times per wk. The
1RM to 84% 1RM, knee extension, and intensity was set as
performed for 2–6 calf raises power output recorded
sets per exercise and Upper body: bench at the ventilation
4–12 repetitions press, seated threshold. The training
pulldowns, shoulder duration was increased
press, and biceps from 30 to 42 min per
curl session (by 4 min every
4 wks)
Interval training was
done once per wk with
a work to rest ratio of
3:3 min. The intensity
was set as power
output recorded at 90%
VO2max. The interval
training started with 4
sets and was increased
by 1 set each 4 wk
De Souza et al. (2013; In wks 1 and 2, Lower body: leg press, In wks 1 and 2, the par- Running 8 wks; 2 times per wk MRI (knee extensors); Not reported Knee extensor CSA: Knee extensor CSA: ↑
2014) [37, 38]a the participants single leg knee flex- ticipants performed 20 muscle biopsies ↔ Type I CSA: ↑
performed 3 sets ion, and extension bouts at 80% vVO2max (vastus lateralis) Type I CSA: ↔ Type IIa CSA: ↑
per exercise for 12 Upper body: none with a work-to-rest Type IIa CSA: ↔ Type IIx CSA: ↔
repetitions. In wks ratio of 60:45 s. In wks Type IIx CSA: ↔
3 and 4, the partici- 3–4, the participants
pants performed 4 performed 20 bouts at
sets per exercise for 85–90% VO2max with
8–10 repetitions. a work-to-rest ratio
In wks 5 and 6, of 60:60 s. In wks
the participants 5–6, the participants
performed 5 sets performed 20 bouts
per exercise for 6–8 at 95% vVO2max with
repetitions. In wks a work-to-rest ratio
7 and 8, the partici- of 60:60 s. In wks
pants performed 3 7–8, the participants
sets per exercise for performed 15 bouts at
10–12 repetitions 80% vVO2max with a
work-to-rest ratio of
60:90 s
J. Grgic et al.
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Farup et al. (2012) In sessions 1–4, the Lower body: leg press, The first session of the Cycling 10 wks; 3 times MRI (knee extensors, Not reported Knee extensor CSA: Knee extensor CSA: ↑
[39] participants per- knee extension, and week was performed per wk knee flexors, and ↔ Type I CSA: ↔
formed 4–5 sets per knee flexion for 30–45 min at hip adductors, these Type I CSA: ↔ Type II CSA: ↑
exercise for 8–10 Upper body: none 60–75% of watt max. components were Type II CSA: ↔
repetitions. In ses- The second session summed for total
sions 5–10, the par- of the week was per- thigh CSA); muscle
ticipants performed formed for 2 × 20 min biopsies (vastus
4–5 sets per exercise at 60–85% of watt lateralis)
for 6–10 repetitions. max with a 5-min rest
In sessions 11–15, interval. The third
the participants session of the week
performed 5 sets per was performed for
Resistance vs. Aerobic Training for Hypertrophy
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Hudelmaier et al. In wk 1, the load was Lower body: back The training sessions Cycling 12 wks; 3 times MRI Not reported Knee extensor CSA: ↑ Knee extensor CSA: ↑
(2010) [18] set at 60% 1RM and squat, leg press, lasted for 60 min per wk (knee extensors, knee Knee flexor CSA: ↔ Knee flexor CSA: ↑
was increased by knee flexion, knee and consisted of a flexors, hip adduc- Adductor CSA: ↔ Adductor CSA: ↑
5–10% each week extension, hip 10-min warm-up, tors, and sartorius) Sartorius CSA: ↑ Sartorius CSA: ↑
to 80% 1RM in wks adduction, hip 40 min of continuous
5 and 6. In wk 7, abduction, and hip cycling, and a 10-min
the load was set at extension cooldown. In wks 1–3,
65–70% 1RM and Upper body: none the participants trained
was increased to with the intensity set at
70–75% 1RM for 55–85% of the VO2max
wks 8 and 9. In wks threshold. The intensity
10–12 the load was was increased by 5%
set at 75–80% 1RM. every 3 wks
The participants
performed either
3 sets per exercise
for 8–12 repetitions
done in 2–4 s total
repetition time or
1 set per exercise
for 6–12 repetitions
done in a 20-s total
repetition time.
Izquierdo et al. (2004) In wks 1–8, the par- Lower body: bilateral The training sessions Cycling 16 wks; 2 times Ultrasound (rectus Minimum of 90% Knee extensor CSA: Knee extensor CSA: ↑
[20] ticipants performed leg press, bilateral lasted for 30–40 min per wk femoris, vastus ↔
3–4 sets per exercise knee extension, per session. In wks lateralis, vastus
for 10–15 repeti- standing leg curl, 1–8, the participants medialis, and vastus
tions with a load of and/or hip adduc- trained with the intermedialis)
50–70% 1RM. In tion-abduction intensity that resulted
wks 9–16, the par- Upper body: bench in blood lactate levels
ticipants performed press, chest press, of 2–4 mmol·L−1. In
3–5 sets per exercise latissimus pull- wks 9–16, the partici-
for 5–6 repetitions down, and shoulder pants trained with the
with a load of press intensity that resulted
70–80% 1RM. Dur- in blood lactate levels
ing wks 9–16, one of 2–5 mmol·L−1. For
session per wk was blood lactate levels
performed using up to 4 mmol·L−1, the
a load of 30–50% training was performed
1RM for 3–4 sets continuously, whereas
and 6–8 repetitions the training for
(repetition cadence blood lactate levels
was as fast as pos- of 5 mmol·L−1 was
sible) performed for 30 s
interspersed with 30 s
of rest
J. Grgic et al.
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Izquierdo et al. (2005) In wks 1–8, the par- Lower body: bilateral The training sessions Cycling 16 wks; 2 times Ultrasound (rectus Minimum of 90% Knee extensor CSA: ↑ Knee extensor CSA: ↑
[19] ticipants performed leg press, bilateral lasted for 30–40 min per wk femoris, vastus
3–4 sets per exercise knee extension, per session. In wks lateralis, vastus
for 10–15 repeti- standing leg curl 1–8, the participants medialis, and vastus
tions with a load of and/or hip adduc- trained with the intermedialis)
50–70% 1RM. In tion-abduction intensity that resulted
wks 9–16, the par- Upper body: bench in blood lactate levels
ticipants performed press, chest press, of 2–4 mmol·L−1. In
3–5 sets per exercise latissimus pull- wks 9–16, the partici-
for 5–6 repetitions down, and shoulder pants trained with the
with a load of press intensity that resulted
70–80% 1RM. Dur- in blood lactate levels
Resistance vs. Aerobic Training for Hypertrophy
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Karavirta et al. (2011) In wks 1–7, the par- Lower body: leg press, In wks 1–7, the par- Cycling 21 wks; 2 times Muscle biopsies 99% in both groups Type I CSA: ↔ Type I CSA: ↔
[42] ticipants performed knee extension, ticipants trained for per wk (vastus lateralis) Type II CSA: ↔ Type II CSA: ↑
3 sets per exercise knee flexion, seated 30 min per session with
for 12–20 repeti- calf raise, hip the intensity set under
tions with a load of abduction, and hip the aerobic threshold.
40–60% 1RM. In adduction In wks 8–14, in one
wks 8–14, the par- Upper body: bench of the two weekly ses-
ticipants performed press, biceps curl, sions, the participants
2–4 sets per exercise triceps pushdown, trained for 45 min per
for 5–12 repetitions and latissimus pull- session with the inten-
with a load of down sity set at 15 min under
60–80% 1RM. In the aerobic threshold,
wks 15–21, the par- 10 min between the
ticipants performed aerobic-anaerobic
2–4 sets per exercise thresholds, 5 min
for 5–8 repetitions above the anaerobic
with a load of threshold, and 15 min
70–85% 1RM. under the aerobic
Twenty percent of threshold. In the sec-
the total work on the ond weekly session, the
leg press and knee participants trained for
extension exercises 60 min per session with
was performed with the intensity set under
40–50% 1RM for the aerobic threshold.
5–8 repetitions (rep- In wks 15–21, in one
etition cadence was of the two weekly ses-
as fast as possible) sions, the participants
trained 60 min per
session with the
intensity set at 30 min
under the aerobic
threshold, 2 × 10 min
between the aerobic-
anaerobic thresholds,
and 2 × 5 min above the
anaerobic threshold. In
the other weekly ses-
sion, the participants
trained for 90 min
per session with the
intensity set under the
aerobic threshold
J. Grgic et al.
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Kraemer et al. (1995) In 2 out of the 4 Lower body: squats, Continuous aerobic train- Running 12 wks; 4 times Muscle biopsies 100% in both groups Type I CSA: ↓ Type I CSA: ↑
[23] weekly training leg press, deadlift, ing was performed 2 per wk (vastus lateralis) Type IIa CSA: ↔ Type IIa CSA: ↑
sessions, the partici- knee extensions, times per wk with the Type IIc CSA: ↓ Type IIc CSA: ↑
pants performed 2–3 knee flexion, split intensity set at 80–85% Type IIx CSA: ↔ Type IIx CSA: ↔
sets per exercise for squats, and calf VO2max. The training
10–15 repetitions. raises duration was 40 min
In the remaining Upper body: bench per session
2 weekly training press, shoulder Interval training was
sessions, the partici- press, upright row, performed two times
pants performed 4–5 seated row, and per wk; the intervals
sets per exercise for biceps curl ranged from 200 to
5–6 repetitions 800 m with a work-to-
Resistance vs. Aerobic Training for Hypertrophy
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Mikkola et al. (2012) In wks 1–7, the par- Lower body: leg press, In wks 1–7, the par- Cycling and Nordic 21 wks; 2 times MRI (knee extensors) Minimum of 90% Knee extensor CSA: ↑ Knee extensor CSA: ↑
[21] ticipants performed knee extension and ticipants trained for walking (one per per wk
3–4 sets per exercise knee flexion, calf 30 min per session with session)
for 10–15 repeti- raises, and/or hip the intensity set under
tions with a load of adduction-abduction the aerobic threshold.
50–70% 1RM. In Upper body: bench In wks 8–14, in one
wks 8–14, the par- press, biceps curl, of the two weekly ses-
ticipants performed triceps pushdown, sions, the participants
2–5 sets per exercise and latissimus pull- trained for 45 min per
for 5–12 repetitions down session with the inten-
with a load of sity set at 15 min under
50–80% 1RM. In the aerobic threshold,
wks 15–21, the par- 10 min between the
ticipants performed aerobic-anaerobic
2–5 sets per exercise thresholds, 5 min
for 3–12 repetitions above the anaerobic
with a load of threshold, and 15 min
50–80% 1RM. under the aerobic
Twenty percent of threshold. In the sec-
the total work on the ond weekly session, the
leg press and knee participants trained for
extension exercises 60 min per session with
was performed with the intensity set under
40–50% 1RM for the aerobic threshold.
5–8 repetitions (rep- In wks 15–21, in one
etition cadence was of the two weekly ses-
as fast as possible) sions, the participants
trained 60 min per
session with the
intensity set at 30 min
under the aerobic
threshold, 2 × 10 min
between the aerobic-
anaerobic thresholds,
and 2 × 5 min above the
anaerobic threshold. In
the other weekly ses-
sion, the participants
trained for 60–90 min
per session with the
intensity set under the
aerobic threshold
J. Grgic et al.
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Nelson et al. (1990) The participants per- Lower body: knee In the first week, the Cycling 20 wks; 4 times Muscle biopsies Not reported Type I CSA: ↑ Type I CSA: ↔
[24] formed 3 sets for 6 extension and knee participants trained per wk (vastus lateralis) Type IIa CSA: ↑ Type IIa CSA: ↔
repetitions at 30°/s flexion for 30 min at 75% Type IIx CSA: ↑ Type IIx CSA: ↑
Upper body: none maximum heart rate.
In the second week,
the duration stayed the
same but the intensity
was increased to 80%
maximum heart rate.
The training duration
increased to 40, 50,
and 60 min for wks 3,
Resistance vs. Aerobic Training for Hypertrophy
4, and 5, respectively.
From wks 6 to 20, the
intensity increased to
85% maximum heart
rate and the training
duration was 60 min
Poehlman et al. The participants Lower body: leg press, In wks 1–4, the training Walking and running 28 wks; 3 times CT (knee extensors) A minimum of 90% Knee extensor CSA: Knee extensor CSA:
(2000) [9] performed 3 sets per knee extensions, and sessions lasted for per wk ↔ ↔
exercise with a load knee flexion 25 min. Every 4 wks
of 80% 1RM for 10 Upper body: bench (up to wk 16), the
repetitions press, shoulder training duration was
press, seated row, increased by 5 min.
triceps extensions, The training intensity
and biceps curls varied from 75 to 90%
of maximum heart
rate and consisted of
a continuous form of
training. In wks 16–28,
an interval training
session was added. In
wks 16–28, on the first
and third weekly ses-
sion, the participants
performed 45 min at
80% heart rate maxi-
mum. On the second
weekly session, the
participants performed
4 × 5 min at 95% heart
rate maximum with a
3-min rest
Table 2 (continued)
Study (year) Resistance training Resistance exercises Aerobic training Aerobic training Study duration; Method of hyper- Adherence Main findings
protocol employed in the protocol modality training frequency trophy assessment
program (site) Aerobic training Resistance training
Sillanpää et al. (2008) In wks 1–7, the Lower body: leg press, In wks 1–7, the par- Cycling 21 wks; 2 times Ultrasound (vastus 100% in both groups Knee extensor muscle Knee extensor muscle
[8] participants per- knee extension, and ticipants trained for per wk lateralis and vastus thickness: ↑ thickness: ↑
formed 3 sets per knee flexion 30 min per session with intermedius)
exercise for 15–30 Upper body: bench the intensity set under
repetitions with a press, triceps the aerobic threshold.
load of 40–60% pushdown, and latis- In wks 8–14, in one
1RM. In wks 8–14, simus pull-down of the two weekly ses-
the participants sions, the participants
performed 3 sets per trained for 45 min per
exercise for 6–12 session with the inten-
repetitions with a sity set at 15 min under
load of 60–80% the aerobic threshold,
1RM. In wks 15–21, 10 min between the
the participants aerobic-anaerobic
performed 3 sets per thresholds, 5 min
exercise for 5–8 rep- above the anaerobic
etitions with a load threshold, and 15 min
of 70–90% 1RM under the aerobic
threshold. In the sec-
ond weekly session, the
participants trained for
60 min per session with
the intensity set under
the aerobic threshold.
In wks 15–21, in one
of the two weekly ses-
sions, the participants
trained 60 min per
session with the
intensity set at 30 min
under the aerobic
threshold, 2 × 10 min
between the aerobic-
anaerobic thresholds,
and 2 × 5 min above the
anaerobic threshold. In
the other weekly ses-
sion, the participants
trained for 90 min
per session with the
intensity set under the
aerobic threshold
Sipilä et al. (1995; In wk 1, the load was Lower body: leg press, Progressive increase in Walking (twice per 18 wks; 3 times CT (knee extensors, Aerobic training Knee extensor CSA: Knee extensor CSA: ↑
1997) [44, 45]a set at 60% 1RM. In knee extension, walking duration from wk) and step aero- per wk knee flexors, and group: 87% ↔ Knee flexor CSA: ↔
wks 2–11, the load knee flexion, and 1500 m to 2700 m per bics (once per wk) calves); muscle Resistance training Knee flexor CSA: ↔ Calves CSA: ↑
was increased to calf raises session. Step aerobics biopsies (vastus group: 83% Calves CSA: ↑ Type I CSA: ↑
70% 1RM. In wks Upper body: none sessions lasted for lateralis) Type I CSA: ↔ Type IIa CSA: ↔
12–16, the load was 40 min. Training Type IIa CSA: ↔ Type IIx CSA: ↔
increased to 75% intensity progressively Type IIx CSA: ↔
1RM. The partici- increased from 50%,
pants performed 3–4 60–70%, to 80% of
sets per exercise and heart rate reserve
8–10 repetitions
J. Grgic et al.
Resistance vs. Aerobic Training for Hypertrophy
cross-sectional area VO2peak peak oxygen consumption MRI magnetic resonance imaging CT computed tomography VO2max velocity at maximal oxygen uptake, ↑ indicates significant increase
1RM one-repetition maximum, CSA cross-sectional area, CT computed tomography, MRI magnetic resonance imaging, VO2 oxygen consumption, VO2max maximal oxygen consumption, CSA
Knee extensor CSA: ↑
type I fiber CSA. Therefore, the analysis of type II CSA
Resistance training
included nine studies [6, 23, 24, 36, 38, 39, 42, 43, 45].
The meta-analysis of type II fiber CSA data resulted in a
significant pooled difference (p < 0.001) between the aerobic
training and resistance training groups (Fig. 4). The pooled
Hedge’s g, favoring resistance training over aerobic training,
Knee extensor CSA:
a large effect size. The funnel plots and trim and fill method
did not suggest any funnel plot asymmetry in either of the
↔
4 Discussion
group: 89%
group: 84%
Adherence
exercises on Cybex
Resistance exercises
Lower body: 4
Upper body: 4
fied which)
fied which)
Study Hedges' g Lower limit Upper limit p-value Hedges' g and 95% CI Statistical weight (%)
Ahtiainen et al. (2009) [6] 0.69 -0.21 1.59 0.132 7.12
De Souza et al. (2013) [37] 0.15 -0.73 1.03 0.737 7.46
Farup et al. (2012) [39] 0.86 -0.18 1.90 0.104 5.39
Ferrara et al. (2006) [7] 1.07 0.19 1.95 0.017 7.46
Izquierdo et al. (2004) [20] 0.53 -0.30 1.36 0.212 8.26
Jubrias et al. (2001) [41] 0.62 -0.16 1.40 0.121 9.24
McCarthy et al. (2002) [43] 1.18 0.26 2.10 0.012 6.81
Poehlman et al. (2000) [9] 0.00 -0.68 0.68 1.000 12.14
Sipilä and Suominen (1995) [44] 0.37 -0.41 1.15 0.355 9.24
Willis et al. (2012) [33] 0.95 0.51 1.39 < 0.001 26.86
Pooled effect 0.66 0.41 0.90 < 0.001
-3 -2 -1 0 1 2 3
Favors aerobic Favors resistance
Fig. 2 Forest plot of the differences between the effects of aerobic and resistance training on whole-muscle measures of muscle size. The x-axis
denotes Hedge’s g (standardized mean differences). The whiskers denote the 95% confidence intervals (CIs)
Study Hedges' g Lower limit Upper limit p-value Hedges' g and 95% CI Statistical weight (%)
Ahtiainen et al. (2009) [6] 0.60 -0.28 1.48 0.180 11.06
Bell et al. (2000) [36] 0.88 0.03 1.72 0.042 11.37
De Souza et al. (2014) [38] 2.70 1.48 3.93 < 0.001 8.72
Farup et al. (2012) [39] 0.67 -0.34 1.69 0.192 9.98
Hepple et al. (1997) [40] 1.36 0.42 2.30 0.004 10.65
Karavirta et al. (2011) [42] 0.54 -0.38 1.45 0.254 10.76
Kraemer et al. (1995) [23] 2.07 0.93 3.22 < 0.001 9.19
McCarthy et al. (2002) [43] 1.33 0.39 2.26 0.005 10.69
Nelson et al. (1990) [24] -1.43 -2.77 -0.09 0.037 7.44
Sipilä et al. (1997) [45] 1.02 0.02 2.01 0.046 10.15
Pooled effect 0.99 0.44 1.54 < 0.001
-4 -3 -2 -1 0 1 2 3 4
Favors aerobic Favors resistance
Fig. 3 Forest plot of the differences between the effects of aerobic and resistance training on type I muscle fiber cross-sectional area. The x-axis
denotes Hedge’s g (standardized mean differences). The whiskers denote the 95% confidence intervals (CIs)
With aerobic cycling training, a large number of muscular exercise modes are different. As little as 2 weeks of resist-
contractions (from 118,000 to 145,000 contractions per leg) ance training has been shown to result in significant hyper-
has been suggested as a requirement to impart a sufficient trophy of the knee extensor muscle group [49]. However, it
stimulus for muscle hypertrophy [12]. Such training sessions is possible that the hypertrophy rate is slower in response to
usually last from 30 to 45 min. In comparison, with resist- aerobic training [26]. Therefore, Konopka and Harber sug-
ance training, protocols involving three sets performed at gested that to achieve similar muscular growth, aerobic train-
80% of one repetition maximum and lasting approximately ing frequency should be higher than the resistance training
5–10 min per session have been shown to result in a robust frequency [12]. These authors suggested that four to five
growth of the knee extensor musculature [46]. Therefore, sessions of aerobic training per week might be needed to
regardless of the potential for aerobic training to induce achieve comparable muscle growth to ‘traditional’ resist-
some degree of muscle hypertrophy, resistance training is ance exercise programs [12]. Nineteen out of the 21 stud-
likely a more time-efficient mode of exercise for achieving ies included in the present meta-analysis employed aerobic
this outcome. This may be important given that the lack of training frequencies of two and three times per week. There-
time for exercise is commonly proposed as an important fore, it is possible that greater increases in muscle size with
perceived barrier to exercise participation [47, 48]. aerobic training would be observed if the included studies
While resistance training likely provides a greater (and had employed higher training frequencies.
more time-efficient) stimulus for inducing muscle hypertro- The differential effects of aerobic and resistance exercise
phy compared with aerobic training modalities, it is possible stimuli for inducing muscle hypertrophy might be explained
the time courses of muscular growth induced by these two
Resistance vs. Aerobic Training for Hypertrophy
Study Hedges' g Lower limit Upper limit p-value Hedges' g and 95% CI Statistical weight (%)
Ahtiainen et al. (2009) [6] 1.95 0.89 3.01 < 0.001 11.20
Bell et al. (2000) [36] 0.88 0.03 1.73 0.044 13.39
De Souza et al. (2014) [38] 3.08 1.77 4.39 < 0.001 8.87
Farup et al. (2012) [39] 1.07 0.01 2.13 0.047 11.20
Karavirta et al. (2011) [42] 1.62 0.56 2.68 0.003 11.20
Kraemer et al. (1995) [23] 2.09 0.95 3.23 < 0.001 10.35
McCarthy et al. (2002) [43] 1.74 0.74 2.74 0.001 11.78
Nelson et al. (1990) [24] 0.21 -0.97 1.39 0.726 10.04
Sipilä et al. (1997) [45] 0.73 -0.25 1.71 0.144 11.98
Pooled effect 1.44 0.93 1.95 < 0.001
-5 -4 -3 -2 -1 0 1 2 3 4 5
Favors aerobic Favors resistance
Fig. 4 Forest plot of the differences between the effects of aerobic and resistance training on type II muscle fiber cross-sectional area. The x-axis
denotes Hedge’s g (standardized mean differences). The whiskers denote the 95% confidence intervals (CIs)
by differences in their capacity to activate post-exercise ana- The meta-analysis results for type I and type II fiber CSA
bolic signaling responses in skeletal muscle. For example, support those seen for whole-muscle measures of hyper-
the degree of post-exercise p70S6 K (p70 kDa ribosomal trophy. Given that the present meta-analysis favored resist-
protein subunit kinase 1) phosphorylation in skeletal mus- ance training for increasing both type I and type II fiber
cle is in some studies highly correlated (r = 0.82–0.99) with CSA, there appears to be no fiber-type specific hypertrophy
muscular hypertrophy consequent to long-term resistance response to aerobic vs. resistance training. Some of the dif-
training [50–52]. It has been reported that the phospho- ferences in results between the studies for muscle fiber CSA
rylation of p70S6 K is increased immediately following could be the result of the modality of aerobic training. For
both aerobic and resistance exercise [53]. However, when instance, Kraemer et al. [23] reported that aerobic training,
assessed 4 h after training, the phosphorylation of p70S6 K in the form of running, induced a decrease in type I and type
remained increased only with resistance exercise, and simi- II fiber CSA.
lar results were seen for muscle protein synthesis [53]. These The majority of remaining studies included in this meta-
acute differences in signaling responses between aerobic and analysis employed cycling as opposed to running. Cycling
resistance exercise might also reflect potential differences in may have a more localized stress on the knee extensor mus-
the time course of muscular growth induced by both exercise culature than running, and, thus, might have a more pro-
modes. Future long-term studies might consider exploring nounced effect on the hypertrophic response of this muscle
this topic further by incorporating measurements of mus- group. That said, Coggan and colleagues measured fiber
cle hypertrophy at multiple time points during aerobic and CSA of the gastrocnemius muscle and reported that walking/
resistance training interventions. running was sufficient for increasing muscle fiber CSA, [56]
One additional matter worthy of discussion when com- albeit in untrained older adults. Running involves concen-
paring these two modes of exercise is motor unit recruit- tric actions coupled with eccentric actions and, thus, it may
ment. Henneman’s size principle suggests that motor units result in higher levels of muscle damage than cycling (likely
are recruited in an orderly fashion [54]. During exercise, owing to the shock waves associated with the loading pattern
smaller motor units are recruited first and, as force produc- of running), which is a concentric-only mode of exercise
tion requirements increase, larger units are sequentially [57]. In that regard, some studies show that, during the initial
recruited as well [55]. Therefore, resistance exercise per- phases of training, in the presence of damage, muscle protein
formed to momentary muscular failure ultimately elicits synthesis may be directed more towards restoring this dam-
activation of the entire motor unit pool, which, in turn, age than to building the contractile protein pool [58].
should stimulate increases in muscle size. However, dur- The study by Nelson et al. [24] is the only study to show
ing long-lasting submaximal exercise, such as continuous an advantage for aerobic training over resistance training
cycling (the most common form of aerobic exercise across for type I fiber CSA hypertrophy. However, it needs to be
the included studies), the highest threshold motor units are acknowledged that in this study there were considerable
not necessarily activated [55]. Therefore, it is possible that differences between the groups at baseline. For instance,
the greater muscular hypertrophy observed with resistance the group performing resistance training had on aver-
training is, at least partially, explained by these differences age 8% body fat, while the aerobic training group had on
in recruitment. average 20% body fat. Furthermore, the group performing
J. Grgic et al.
(e.g., cycling vs. running) and including trained individuals, strengthening exercise programme. J Back Musculoskelet Rehabil.
which likely show divergent adaptive responses to exercise 2018;31(2):355–62.
15. Short KR, Vittone JL, Bigelow ML, et al. Age and aerobic exer-
compared with untrained individuals. cise training effects on whole body and muscle protein metabo-
lism. Am J Physiol Endocrinol Metab. 2004;286(1):E92–101.
Compliance with Ethical Standards 16. Harber MP, Konopka AR, Douglass MD, et al. Aerobic exer-
cise training improves whole muscle and single myofiber size
Funding No external sources of funding were used to assist in the and function in older women. Am J Physiol Regul Integr Comp
preparation of this article. Physiol. 2009;297(5):R1452–9.
17. Harber MP, Konopka AR, Undem MK, et al. Aerobic exercise
training induces skeletal muscle hypertrophy and age-dependent
Conflict of interest Jozo Grgic, Luke C. Mcllvenna, Jackson J. Fyfe, adaptations in myofiber function in young and older men. J Appl
Filip Sabol, David J. Bishop, Brad J. Schoenfeld, and Zeljko Pedisic Physiol. 2012;113(9):1495–504.
have no conflicts of interest that are directly relevant to the contents of 18. Hudelmaier M, Wirth W, Himmer M, et al. Effect of exercise
this review. intervention on thigh muscle volume and anatomical cross-sec-
tional areas: quantitative assessment using MRI. Magn Reson
Med. 2010;64(6):1713–20.
19. Izquierdo M, Hakkinen K, Ibanez J, et al. Effects of combined
References resistance and cardiovascular training on strength, power, muscle
cross-sectional area, and endurance markers in middle-aged men.
1. Fyfe JJ, Loenneke JP. Interpreting adaptation to concurrent com- Eur J Appl Physiol. 2005;94(1–2):70–5.
pared with single-mode exercise training: some methodological 20. Izquierdo M, Ibanez J, Häkkinen K, et al. Once weekly combined
considerations. Sports Med. 2018;48(2):289–97. resistance and cardiovascular training in healthy older men. Med
2. Garber CE, Blissmer B, Deschenes MR, et al. American Col- Sci Sports Exerc. 2004;36(3):435–43.
lege of Sports Medicine position stand: quantity and quality 21. Mikkola J, Rusko H, Izquierdo M, et al. Neuromuscular and car-
of exercise for developing and maintaining cardiorespiratory, diovascular adaptations during concurrent strength and endurance
musculoskeletal, and neuromotor fitness in apparently healthy training in untrained men. Int J Sports Med. 2012;33(9):702–10.
adults: guidance for prescribing exercise. Med Sci Sports Exerc. 22. Folland JP, Williams AG. The adaptations to strength train-
2011;43(7):1334–59. ing: morphological and neurological contributions to increased
3. American College of Sports Medicine. American College strength. Sports Med. 2007;37(2):145–68.
of Sports Medicine position stand: progression models in 23. Kraemer WJ, Patton JF, Gordon SE, et al. Compatibility of high-
resistance training for healthy adults. Med Sci Sports Exerc. intensity strength and endurance training on hormonal and skeletal
2009;41(3):687–708. muscle adaptations. J Appl Physiol. 1995;78(3):976–89.
4. Fyfe JJ, Bishop DJ, Stepto NK. Interference between concurrent 24. Nelson AG, Arnall DA, Loy SF, et al. Consequences of com-
resistance and endurance exercise: molecular bases and the role bining strength and endurance training regimens. Phys Ther.
of individual training variables. Sports Med. 2014;44(6):743–62. 1990;70(5):287–94.
5. Ozaki H, Loenneke JP, Thiebaud RS, et al. Resistance training 25. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items
induced increase in VO 2 max in young and older subjects. Eur for systematic reviews and meta-analyses: the PRISMA statement.
Rev Aging Phys Act. 2013;10(2):107. Ann Intern Med. 2009;151(4):264–9.
6. Ahtiainen JP, Hulmi JJ, Kraemer WJ, et al. Strength, endurance 26. Ozaki H, Loenneke JP, Thiebaud RS, et al. Cycle training induces
or combined training elicit diverse skeletal muscle myosin heavy muscle hypertrophy and strength gain: strategies and mechanisms.
chain isoform proportion but unaltered androgen receptor concen- Acta Physiol Hung. 2015;102(1):1–22.
tration in older men. Int J Sports Med. 2009;30(12):879–87. 27. Schoenfeld B. Science and development of muscle hypertrophy.
7. Ferrara CM, Goldberg AP, Ortmeyer HK, et al. Effects of aerobic Champaign, IL: Human Kinetics Inc. 2016.
and resistive exercise training on glucose disposal and skeletal 28. Downs SH, Black N. The feasibility of creating a checklist for the
muscle metabolism in older men. J Gerontol A Biol Sci Med Sci. assessment of the methodological quality both of randomised and
2006;61(5):480–7. non-randomised studies of health care interventions. J Epidemiol
8. Sillanpaa E, Hakkinen A, Nyman K, et al. Body composition and Community Health. 1998;52(6):377–84.
fitness during strength and/or endurance training in older men. 29. Davies TB, Kuang K, Orr R, et al. Effect of movement velocity
Med Sci Sports Exerc. 2008;40(5):950–8. during resistance training on dynamic muscular strength: a system-
9. Poehlman ET, Dvorak RV, DeNino WF, et al. Effects of resistance atic review and meta-analysis. Sports Med. 2017;47(8):1603–17.
training and endurance training on insulin sensitivity in nonobese, 30. Grgic J, Schoenfeld BJ, Skrepnik M, et al. Effects of rest interval
young women: a controlled randomized trial. J Clin Endocrinol duration in resistance training on measures of muscular strength:
Metab. 2000;85(7):2463–8. a systematic review. Sports Med. 2018;48(1):137–51.
10. DeLorme TL. Technics of progressive resistance exercise. Arch 31. Grgic J, Schoenfeld BJ, Davies TB, et al. Effect of resistance train-
Phys Med Rehabil. 1948;29(5):263–73. ing frequency on gains in muscular strength: a systematic review
11. Kraemer WJ, Ratamess NA, Flanagan SD, et al. Understanding and meta-analysis. Sports Med. 2018;48(5):1207–20.
the science of resistance training: an evolutionary perspective. 32. Higgins JPT, Deeks JJ, Altman DG, on behalf of the Cochrane
Sports Med. 2017;47(12):2415–35. Statistical Methods Group, editors. Chapter 16.1.3.2. Imputing
12. Konopka AR, Harber MP. Skeletal muscle hypertrophy after aero- standard deviations for changes from baseline. In: Higgins JP,
bic exercise training. Exerc Sport Sci Rev. 2014;42(2):53–61. Green S, editors. Cochrane handbook for systematic reviews of
13. Ceccarelli G, Benedetti L, Arcari ML, et al. Muscle stem cell and interventions. Version 5.1.0 (updated March 2011). Cochrane Col-
physical activity: what point is the debate at? Open Med (Wars). laboration, Chichester, UK; 2011.
2017;12:144–56. 33. Willis LH, Slentz CA, Bateman LA, et al. Effects of aerobic and/
14. Rutkowska-Kucharska A, Szpala A. The use of electromyo- or resistance training on body mass and fat mass in overweight or
graphy and magnetic resonance imaging to evaluate a core obese adults. J Appl Physiol. 2012;113(12):1831–7.
J. Grgic et al.
34. Cohen J. Statistical power analysis for the behavioral sciences. 48. Siddiqi Z, Tiro JA, Shuval K. Understanding impediments and
Hilsdale: Lawrence Earlbaum Associates; 1988. enablers to physical activity among African American adults:
35. Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based a systematic review of qualitative studies. Health Educ Res.
method of testing and adjusting for publication bias in meta-anal- 2011;26(6):1010–24.
ysis. Biometrics. 2000;56(2):455–63. 49. Counts BR, Buckner SL, Mouser JG, et al. Muscle growth: to
36. Bell GJ, Syrotuik D, Martin TP, et al. Effect of concurrent infinity and beyond? Muscle Nerve. 2017;56(6):1022–30.
strength and endurance training on skeletal muscle properties 50. Terzis G, Georgiadis G, Stratakos G, et al. Resistance exer-
and hormone concentrations in humans. Eur J Appl Physiol. cise induced increase in muscle mass correlates with p70S6
2000;81(5):418–27. kinase phosphorylation in human subjects. Eur J Appl Physiol.
37. de Souza EO, Tricoli V, Roschel H, et al. Molecular adaptations 2008;102(2):145–52.
to concurrent training. Int J Sports Med. 2013;34(3):207–13. 51. Baar K, Esser K. Phosphorylation of p70(S6 k) correlates with
38. de Souza EO, Tricoli V, Aoki MS, et al. Effects of concurrent increased skeletal muscle mass following resistance exercise. Am
strength and endurance training on genes related to myostatin J Physiol. 1999;276(1 Pt 1):C120–7.
signaling pathway and muscle fiber responses. J Strength Cond 52. Mayhew DL, Hornberger TA, Lincoln HC, et al. Eukaryotic ini-
Res. 2014;28(11):3215–23. tiation factor 2B epsilon induces cap-dependent translation and
39. Farup J, Kjolhede T, Sorensen H, et al. Muscle morphological skeletal muscle hypertrophy. J Physiol. 2011;589(Pt 12):3023–37.
and strength adaptations to endurance vs. resistance training. J 53. Wilkinson SB, Phillips SM, Atherton PJ, et al. Differential effects
Strength Cond Res. 2012;26(2):398–407. of resistance and endurance exercise in the fed state on signalling
40. Hepple RT, Mackinnon SL, Goodman JM, et al. Resist- molecule phosphorylation and protein synthesis in human muscle.
ance and aerobic training in older men: effects on VO2peak J Physiol. 2008;586(Pt 15):3701–17.
and the capillary supply to skeletal muscle. J Appl Physiol. 54. Duchateau J, Enoka RM. Human motor unit recordings: ori-
1997;82(4):1305–10. gins and insight into the integrated motor system. Brain Res.
41. Jubrias SA, Esselman PC, Price LB, et al. Large energetic adap- 2011;1409:42–61.
tations of elderly muscle to resistance and endurance training. J 55. Edström L, Grimby L. Effect of exercise on the motor unit. Muscle
Appl Physiol. 2001;90(5):1663–70. Nerve. 1986;9(2):104–26.
42. Karavirta L, Hakkinen A, Sillanpaa E, et al. Effects of combined 56. Coggan AR, Spina RJ, King DS, et al. Skeletal muscle adaptations
endurance and strength training on muscle strength, power and to endurance training in 60- to 70-yr-old men and women. J Appl
hypertrophy in 40-67-year-old men. Scand J Med Sci Sports. Physiol. 1992;72(5):1780–6.
2011;21(3):402–11. 57. Millet GY, Lepers R. Alterations of neuromuscular function after
43. McCarthy JP, Pozniak MA, Agre JC. Neuromuscular adaptations prolonged running, cycling and skiing exercises. Sports Med.
to concurrent strength and endurance training. Med Sci Sports 2004;34(2):105–16.
Exerc. 2002;34(3):511–9. 58. Damas F, Phillips SM, Libardi CA, et al. Resistance training-
44. Sipila S, Suominen H. Effects of strength and endurance training induced changes in integrated myofibrillar protein synthesis are
on thigh and leg muscle mass and composition in elderly women. related to hypertrophy only after attenuation of muscle damage. J
J Appl Physiol. 1995;78(1):334–40. Physiol. 2016;594(18):5209–22.
45. Sipila S, Elorinne M, Alen M, et al. Effects of strength and endur- 59. Steele J, Butler A, Comerford Z, et al. Similar acute physiological
ance training on muscle fibre characteristics in elderly women. responses from effort and duration matched leg press and recum-
Clin Physiol. 1997;17(5):459–74. bent cycling tasks. PeerJ. 2018;6:e4403.
46. Mitchell CJ, Churchward-Venne TA, West DW, et al. Resistance 60. Mazzetti SA, Kraemer WJ, Volek JS, et al. The influence of direct
exercise load does not determine training-mediated hypertrophic supervision of resistance training on strength performance. Med
gains in young men. J Appl Physiol. 2012;113(1):71–7. Sci Sports Exerc. 2000;32(6):1175–84.
47. Gibala MJ. High-intensity interval training: a time-efficient strat-
egy for health promotion? Curr Sports Med Rep. 2007;6(4):211–3.