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Muscle Hypertrophy:

A Narrative Review on
Training Principles for
Increasing Muscle Mass
Louis P. Howe, MSc,1 Paul Read, CSCS,2 and Mark Waldron, PhD3
Medical and Sport Sciences, University of Cumbria, Lancaster, United Kingdom; 2Athlete Health and Performance
Research Centre, Aspetar Orthopaedic and Sports Medicine Hospital, Doha, Qatar; and 3School of Sport, Health and
Applied Science, St Mary’s University, Twickenham, United Kingdom and School of Science and Technology,
University of New England, Armidale, NSW, Australia

ABSTRACT it relates to the constraints of each spe- Therefore, recovery of lean muscle tis-
cific sport skill (85). Although neurolog- sue may be a significant objective that
ical factors primarily contribute to the should be achieved to restore the ath-
development of force, structural adapta- lete to full function after injury.
tions after long-term strength training
FORMANCE FOR MANY ATHLETES. Three proposed primary mechanisms
may also influence force generation
BECAUSE EMERGING EVIDENCE are responsible for training adaptations,
capacity (19), though the role of muscle including: mechanical tension, metabolic
hypertrophy is likely to be exaggerated stress, and muscle damage (65). Mechan-
for increasing maximal strength (49). ical tension refers to the loading of muscle
Nonetheless, increases in muscle mass and is proposed to disrupt skeletal muscle
are typically desirable in instances where structures, compromising the integrity of
athletes are required to produce large individual muscle fibers and leading to
OVERVIEW OF THE CURRENT LIT- forces against their external environment. cellular responses via stimulation of the
ERATURE RELATING, SPECIFI- Indeed, cross-sectional area of the limbs mTOR pathway (38). Local metabolic
CALLY, TO PROGRAMMING has been associated with both horizon- stress involves the accumulation of met-
VARIABLES. EVIDENCE-BASED tal and vertical power production in abolic by-products, such as blood lactate
RECOMMENDATIONS ARE PRO- elite athletes (93). This concept pro- (B[La]) and hydrogen ions ([H+]), caused
VIDED FOR THE DESIGN OF vides the rationale for developing the by a cumulative demand on fast glycoly-
EFFECTIVE RESISTANCE-TRAINING musculoskeletal system, before neural sis (32,89). It is thought that this meta-
PROGRAMS, WITH THE GOAL OF factors, as part of a “phase potentia- bolic perturbation has the potential to
INCREASING AN ATHLETE’S SKEL- tion periodization model” (85). There- stimulate anabolism through mecha-
ETAL MUSCLE MASS. fore, increases in muscle mass can, in nisms associated with increased local
many circumstances, support athletic release of myokines, greater reactive oxy-
INTRODUCTION development to a point. gen species production, cell swelling, and
ithin a strength and condi- acute hormonal responses (66). Lastly,

Alongside performance considerations,
tioning coach’s practice, the muscle damage is theorized to lead to
increasing muscle mass may also be
development of physical qual- hypertrophic responses (37), whereby
required after injury occurrence. During the inflammatory response and upregu-
ities that result in improvements in ath- the rehabilitation process, muscle atro-
letic performance are arguably at the lation of muscle protein synthesis to
phy is a key concern, secondary to un-
heart of the role. One such physical qual- loading (40). In cases where muscle
ity is maximal force development because atrophy is heightened because of immo-
muscle hypertrophy; resistance
Address correspondence to Dr. Louis P. Howe, bilization, the rehabilitation time has
louis.howe@cumbria.ac.uk. been suggested to be extended (8).

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exercise induced muscle damage results any given unit of time, is a key variable The mechanisms underlying the rela-
in greater muscle size. For the interested for consideration in the pursuit of mus- tionship between high training volume
reader seeking further understanding of cle hypertrophy. Much like increases and increased muscle mass are poten-
each mechanism and the underlying in maximal strength (44), muscle tially linked to the prolonged meta-
physiological adaptations, please refer hypertrophy is enhanced after high- bolic stress (34). A greater number of
to Schoenfeld (65). volume longitudinal programs, partic- total sets per body part increases the
Traditional beliefs of the most effective ularly when multiple sets are used, total duration placed on the relevant
strategies for the development of lean rather than single set routines (45). energy systems and variety of muscle
muscle tissue have recently been chal- This evidence has been used to support fibers during training. However, if pro-
lenged (17). This article reviews the cur- the current American College of Sports longed metabolic stress is responsible
rent body of literature related to training Medicine (ACSM) recommendations, for increases in muscle hypertrophy
considerations for increasing muscle which suggest prescribing multiple sets after high-volume routines, then
hypertrophy in young healthy adults. for advanced lifters to increase muscle coaches should carefully manage the
Where appropriate, this review will hypertrophy (4). Acutely, significant types of exercises that comprise their
indicate the training status of the sub- increases in muscle protein synthesis program, particularly if high-load exer-
jects used for each investigation. As have been observed after high- cises are included. For example, utiliza-
such, this will allow coaches to ade- volume training in comparison with tion of drop sets has the potential to
quately interpret the discussion in order low volume sessions (14), thus rein- heighten the accumulation of meta-
to suitably apply the findings in their forcing this recommendation. bolic by-products by placing greater
own strength and conditioning practice. Although acute responses are not lin- demand on the fast glycolytic energy
early accompanied by long-term in- systems (33). If a high number of sets of
In particular, this article discusses the this type of training were to be pre-
following foundational factors that creases in lean muscle mass (52),
numerous longitudinal studies have scribed across sessions in order to
should influence a coach’s decision- increase volume, then an athlete may
making when designing resistance train- demonstrated that high-volume train-
be taken beyond their recovery thresh-
ing programs for increasing muscle size: ing facilitates muscle hypertrophy
old, resulting in a blunting of the hyper-
 Training volume (20,59,60,63). Using ultrasound to mea-
trophy response (28).
 Load sure elbow flexor and extensor muscle
 Training frequency thickness, Radaelli et al. (60) showed It is important to emphasize that the
 Training to momentary muscular that 5 sets of exercises per training ses- relationship between volume and mus-
failure sion resulted in significantly greater cle growth is unlikely to be linear. That
 Exercise variation upper arm development when com- is; continual increases in training vol-
 Contraction type pared to one and 3 set routines, across ume would inevitably lead to a plateau
 Exercise order a 6-month training period. This in the development of muscle mass.
 Repetition tempo increase in muscle mass was accompa- This concept is supported by the
 Interset recovery nied by significantly superior gains in 5 recent findings of Amirthalingham
Evidence-based recommendations will repetition maximum (RM) loads for et al. (3). In their investigation, no sig-
be provided for the design of effective the bench press and lat pull-down after nificant difference in muscle hypertro-
resistance training programs, with the the high-volume intervention (60). phy was found between subjects who
goal of increasing an athlete’s skeletal Although findings of higher volumes performed either 5 sets of 10 repeti-
muscle mass. leading to superior gains in muscle tions or 10 sets of 10 repetitions over
This article does not describe, with any growth are not consistent throughout a 6-week period (3). Coaches should
detail, the physiological mechanisms the literature (11,50), a recent meta- appreciate each individual athlete’s
for increasing in muscle mass, nor does analysis identified a dose–response recovery capacity when prescribing
it examine the evidence relating to relationship between training volume training programs, with excessive vol-
specific training techniques aimed at and muscle hypertrophy (72). For umes leading to extended overreaching
increasing muscle hypertrophy. Like- example, high weekly volumes (.10 or, perhaps overtraining syndrome
wise, although a variety of nutritional total sets per body part, per week) (82). The net effect of this would be
and lifestyle factors can be manipu- were associated with greater increases a reduction in the capacity for anabolic
lated to augment the effects of hyper- in muscle mass than lower volumes processes because of a heightened cat-
trophy training (57), these will not be (,5 sets, per body part, per week), abolic status and increased protein
discussed herein. with an effect size of 0.241 (72). metabolism (46). In this sense, the rela-
Schoenfeld et al. (72) concluded that tionship between volume and hyper-
TRAINING VOLUME higher volume training produces trophy training is suggested to follow
Resistance training volume, described greater gains in muscle mass than an inverted U curve (70). As each indi-
as the amount of work completed for lower volume training. vidual possesses their own capacity to

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Muscle Hypertrophy

recover from a given amount of work, load training also recruits fast-twitch might be due to the low number of
strength and conditioning coaches muscle fibers, provided the working studies investigating the effects of train-
should use appropriate testing and set is continued close to volitional ing load on muscle hypertrophy. The
monitoring tools to identify thresholds fatigue (15). When high-load training use of low-load training strategies is
which maximize increases in muscle has been directly compared to low- supported by reports that training at
mass while maintaining the athlete’s load training, Mitchell et al. (51) found 30% 1RM resulted in greater acute
health. no significant difference in fiber-type- muscle protein synthesis relative to
specific hypertrophy. However, this high-load training (90% 1RM), provid-
LOAD study has been suggested to be under- ing low-load training is continued to
The manipulation of load during resis- powered (56), consequently lacking the failure (15). Additionally, Mitchell
tance training, which is typically pre- sensitivity required to establish a differ- et al. (51) showed that a low-load train-
sented as the percentage of maximal ence in fiber-type hypertrophy ing (30% 1RM) regime resulted in
load that can be used for any given between loading strategies. Because similar increases in whole muscle
movement, has been proposed as this investigation did establish a nonsig- cross-sectional area when compared
a vital factor in maximizing muscle nificant difference in type I hypertro- to high-load training (80% 1RM) over
hypertrophy (65). This is likely to phy between high-load and low-load a 10-week period. Furthermore, using
relate directly to the mechanism of training (17 versus 30%, respectively) a moderate loading scheme (8–12RM)
“mechanical tension,” as increased load (51), it may be that the lack of statistical or a variety of training loads (2–4RM,
results in an intensification of tension power prevented the identification of 8–12RM and 20–30RM) across a train-
on the musculotendinous unit. How- differences. Mitchell et al. (51) used ing week has been shown to result in
ever, loads exceeding 85% 1RM, while a sample size of 12 participants per similar increases in muscle mass after
maximizing mechanical tension, fail to group, which would achieve a poor sta- an 8-week intervention (71).
provide adequate stress to the fast gly- tistical power of 0.17, based on our own Therefore, when coaches are prescrib-
colytic system because of reduced time post hoc analysis, assuming an alpha ing a training stimulus for muscle
under tension (61). Therefore, as level of 0.05 and an effect size of 0.3 hypertrophy, high loads or low loads
a compromise in emphasizing both (d). It is important for coaches to note may be selected. Traditionally, loads
mechanical tension and metabolic that this investigation demonstrated .65% 1RM have been prescribed for
stress simultaneously, moderate loads very little difference between high- hypertrophy programs, which might
(70–85% 1RM) are traditionally recom- load and low-load training for type II not be necessary. This information
mended (4). fiber hypertrophy (16 versus 18%, might also be useful for injury rehabil-
It has been suggested that high-load respectively) (51). Further evidence is itation, where low-load training can be
training (.65% 1RM) leads to superior required to establish whether load de- an effective method to increase muscle
gains in muscle mass because of the termines fiber-type hypertrophy. Of mass without the augmented forces
recruitment and fatigue of higher course, coaches shouldn’t underesti- associated with high-load training,
threshold motor units (43,56). This mate the importance of recruiting leading to reduced joint loads.
outcome might be desirable among a wide range of motor units through
Although low-load training might be
athletes because hypertrophy of fast- the prescription of high and low loads.
equally as effective for muscle hyper-
twitch fibers is known to be much Indeed, in the development of muscle
trophy, coaches should not overlook
greater than slow-twitch muscle fibers cross-sectional area, which is deter-
the superior strength adaptations that
(1,88) and fast-twitch fibers demon- mined by the increase in myofibrillar
high-load training provides in compar-
strate higher velocity contractions proteins and thus muscle fiber diame-
ison with low-load training
(96). Fry (29) showed that programs ter, a reliance upon the hypertrophy of
(10,54,64,67). These differences are ex-
incorporating loads above 50% 1RM type I fibers also exists. Exercises that
plained by the principle of training
led to greater fast-twitch fiber hyper- activate a greater proportion of type I
specificity, whereby the all-out efforts
trophy compared with slow-twitch fibers would, therefore, be of equal use
required during high-load training pro-
fibers. Furthermore, during short- in maximizing hypertrophic adaptation.
duces maximal force, whereas low-load
duration isometric contractions with When considering whole muscle training requires only low-to-moderate
low load (30–45% 1RM), glycogen hypertrophy, a meta-analysis by forces in a fatigued state (18). As such,
depletion is nonexistent in type IIX Schoenfeld et al. (75) showed high- high-load training that results in the
fibers but rises significantly with load training (.65% 1RM) to be no accumulation of considerable training
increased resistance (90). more effective than low-load training volume may allow for increased muscle
Although these findings suggest that (,60% 1RM) for increasing skeletal strength alongside substantial increases
type II fibers are stimulated to a greater muscle mass. However, there was in muscle mass. Such adaptations have
degree when exposed to heavy load- a nonsignificant trend in favor of been defined as functional hypertro-
ing, it has been suggested that low- high-load training (p 5 0.076), which phy, where increases in muscle mass

74 VOLUME 39 | NUMBER 5 | OCTOBER 2017

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and maximal strength occur simulta- training the same muscle group before findings infer an increase in the recruit-
neously (58). protein synthesis has returned to ment of high-threshold motor units (86).
homeostasis may impair the muscle In support of this, Burd et al. (14) re-
TRAINING FREQUENCY hypertrophy process (48); thus, 48–72 ported no differences in muscle adapta-
Training frequency is defined as the hours of rest between training sessions tion in low-load or high-load training
number of training sessions per unit for the same muscle group may be strategies, providing that each set was
of time. From the perspective of required to optimize the training completed to failure. However, it is dif-
increasing an athlete’s muscle mass, response (73). ficult to come to such conclusions where
training frequency relates directly to Although this general recommenda- training volume is not equated.
training volume. During a single train- tion is likely to be appropriate for Goto et al. (34) investigated the effects
ing session, the capacity to recover many athletes, it has been recently sug- of training to failure on muscle hyper-
from the work performed is limited. gested that higher training frequencies trophy in a 12-week study, where par-
Therefore, for high levels of training may be more beneficial for trained in- ticipants were volume-matched and
volume to be achieved, multiple ses- dividuals in stimulating greater muscle assigned to either a group that trained
sions are likely to be required. As train- hypertrophy (23). Because trained in- to failure or a group that incorporated
ing volume is a key factor in muscle dividuals adapt to resistance training in an intraset rest preventing failure from
growth (72), optimizing training fre- the long term by reducing the muscle occurring. With volume equated, the
quency will allow for volume to be protein synthesis response (22), distrib- “no-rest” group using repetition maxi-
maximized without excessive fatigue uting training volume across a higher mums achieved significantly greater
being incurred. frequency has the potential to increase muscle hypertrophy in the quadriceps,
In establishing the optimal training fre- the total time spent in a positive pro- along with higher levels of maximal
quency for muscle hypertrophy, Wern- tein balance by an athlete (23). Such an strength (34). This is similar to the find-
born et al. (94) showed that 2–3 approach would require a large reduc- ings of Schott (77), who also identified
training sessions per week was optimal. tion in training volume per session to training to failure induced superior
This is supported by a recent meta- avoid the accumulation of excessive hypertrophy adaptations compared to
analysis, identifying that 2 weekly fatigue. Dankel et al. (23) suggest strat- finishing a set before failure.
training sessions for the same muscle egies of high training frequency may be Although these findings indicate the
group led to significantly greater in- less than optimal for untrained individ- positive effects of training to failure,
creases in muscle mass compared to uals because the subsequent bouts of caution should be taken with routinely
one or 3 sessions per week (73). These resistance training would likely inter- prescribing this approach. Sundstrup
findings are in contrast to the tradi- fere with the increased protein synthe- et al. (86) reported that complete con-
tional practices of some bodybuilders, sis response for the preceding training centric failure was not required to
who are reported to train a single mus- session. Although this hypothesis is achieve full muscle activation using
cle group once per week (36). How- supported mechanistically, at present EMG analysis, with a plateau occur-
ever, it should be noted that both little evidence exists to confirm this ring during the final 3–5 repetitions
Schoenfeld et al. (73) and Wernborn theoretical model and future investiga- with a 15RM load. This is an important
et al. (94) included both untrained tions are required. consideration because routinely per-
and trained subjects in their analysis, forming resistance training to failure
potentially impacting the application MUSCULAR FAILURE may produce symptoms of overtrain-
for athletic populations. Training to momentary muscular fail- ing and subsequent threats to the ana-
For the majority of resistance-trained ure results in the inability to produce bolic status of athletes (39). Because
athletes, it is inevitable that the train- the necessary force to lift a load many of the studies evaluating the ben-
ing volume per session and training through the concentric phase (65). efits of training to failure are of relatively
frequency are inversely related, such When training to failure, it is hypoth- short duration, the long-term implica-
that an increase in training frequency esized that maximal motor unit recruit- tions are yet to be elucidated. Such find-
leads to a reduction in volume per ses- ment is achieved resulting in the fatigue ings have been identified in training
sion. In the case of a high-frequency of a greater number of muscle fibers programs for maximal strength (25).
training program, where a muscle (16,97), in turn leading to a greater Therefore, it is recommended that prac-
group is trained on multiple occasions, hypertrophic response. Performing titioners strategically expose their ath-
the training volume for each session repeated muscle contractions of a fixed letes to training that induces failure to
should be lower to prevent excessive load (i.e., a set) to failure is associated prevent the occurrence of overtraining.
weekly training volumes. High training with progressive increases in both the
frequency should be periodized strate- perception of effort (5) and muscle acti- EXERCISE VARIATION
gically, so that adequate recovery is vation levels (obtained from surface Traditionally, bodybuilders tend to
provided between sessions. Indeed, electromyography (EMG)) (86). These subscribe to the notion that broad

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Muscle Hypertrophy

exercise variation is required to maxi- multijoint and single-joint exercises preferential hypertrophy of fast-twitch
mize muscle hypertrophy (36). A pro- have been shown to elicit regional dif- fibers with strategies such as eccentric-
posed rationale is that muscles such as ferences in muscle activation. For only training may also lead to nonuni-
the pectoralis major (47) and trapezius example, single-joint elbow extension form hypertrophy (discussed in the
(7) perform different movements of the exercise has been shown to increase following section). It is likely that each
same joint segment via the functional activation of the distal portion of the muscle contains multiple neuromuscu-
subdivisions of each muscle (6). As triceps brachii (91). Chronic adapta- lar compartments that can be selec-
such, manipulating exercises has the tions to these exercises led to greater tively overloaded through varying
potential to target large sections of increases in cross-sectional area in the exercise selection.
the muscle. For example, in the case distal region of the muscle after a 12-
of the pectoralis major, using a 158 week overloaded intervention program
decline during the bench press results CONTRACTION TYPE
(91). Similarly, Wakahara et al. (92)
in greater EMG activity of the sternal Eccentric muscle contractions increase
showed that a multijoint elbow exten-
fibers relative to the clavicular fibers the amount of mechanical stress on
sion exercise (dumbbell bench press)
(47). Therefore, to overload specific the musculotendinous units (7).
increased muscle activation levels of
portions of different muscles, a wider Although EMG amplitude is lower
the middle and proximal region of
variety of exercises is essential to during eccentric contractions, fast-
the triceps brachii, leading to greater
recruit and fatigue all muscle twitch fibers are preferentially recruited
growth in these areas. This suggests
subdivisions. over their slow-twitch counterparts,
that to maximize hypertrophic adapta-
leading to greater tension per muscle
The above concept may be extended tion, it is necessary to stress the muscle
fiber and a bias toward type II fiber
to muscles that possess numerous fi- across its different portions (proximal-
damage (78). The greater muscle dam-
bers orientated at a variety of angles distal) using a variety of exercises.
age incurred promotes an adaptive
between the origin and insertion. For Fonseca et al. (26) showed that chang- response in the fast-twitch fibers, which
example, both the long head and short ing exercises within a 12-week period possess greater potential for growth (1).
head of the biceps brachii musculature was more effective for increasing mus-
Traditional methods to determine
are architecturally classified as fusiform cle strength and hypertrophy com-
loads during a program typically use
(31); the biceps brachii is not function- pared to solely manipulations in
the concentric strength of the athlete
ally compartmentalized like the pector- training load. Within this investigation,
(i.e., percentage of 1RM). However,
alis major muscle. By manipulating hypertrophy of the vastus medialis and
because eccentric strength can be as
shoulder and elbow positioning, the rectus femoris was more for subjects
much as 45% greater than concentric
biceps brachii demonstrates a region- who varied exercises over 3-week
strength (41), it is likely that eccentric
specific muscle activation strategy cycles, compared to subjects who used
training is rarely exploited to its full
during supination (12). Furthermore, the same exercise throughout (26).
potential. Because submaximal eccen-
during elbow flexion, the biceps brachii This evidence supports the concept
tric training does not acutely raise mus-
does not uniformly shorten, suggesting of using numerous exercises to fully
cle protein synthesis when compared
that separate muscle fascicles contract exploit adaptations of muscle
to concentric training, the downstream
concentrically at varying rates thus hypertrophy.
effects on muscle hypertrophy are
manipulating the range in the work One potential mechanism for the likely to be limited if traditional ap-
produced for each muscle fiber (31). regional differences in hypertrophy proaches to quantify load are used
Nonuniform muscle fiber recruitment may be the compartmentalization of (21). However, when eccentric training
has also been shown to occur in the skeletal muscle (6). Within the neuro- is performed with maximal resistance,
hamstrings musculature, with EMG muscular system, sections of the mus- muscle protein synthesis is significantly
activity varying between the lower cle are innervated by specific motor greater than load-matched concentric
and upper fibers, depending on units that are responsible for orches- training (55). When eccentric training
whether the hamstrings were required trating the contraction of their respec- is applied over a number of weeks,
to flex the knee or extend the hip tive fibers (6). Indeed, even fusiform muscle hypertrophy adaptations are
against resistance (68). This finding muscle fibers terminate intrafascicu- shown to be superior to that of con-
was supported by the work of larly (31,95), meaning that there is centric training (62). Therefore, supra-
Mendez-Villanueva et al. (53), who potential for various neuromuscular maximal eccentric training is likely to
used functional magnetic resonance compartments to exist within a given induce greater hypertrophic adapta-
imaging to demonstrate regional differ- muscle. As fiber-type distribution tions, assuming that the necessary
ences in muscle activation of each head inside muscles is also region specific recovery is provided. However, this is
of the hamstrings during a variety of (47,83), intramuscular differences are not consistent within the literature,
posterior chain exercises. Likewise, likely to exist relative to function. with some studies identifying no differ-
during resisted elbow extensions, Therefore, resistance training targeting ence between modes of contraction

76 VOLUME 39 | NUMBER 5 | OCTOBER 2017

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(28). This is potentially because of dif- produced by large muscle groups, extremity (30), prefatiguing a muscle
ficulties in matching volume-load should be performed in the initial with a single-joint exercise has been
between conditions, with eccentric stages of a training session (2). As more shown to decrease the recruitment of
training requiring higher loads. repetitions can be completed with any the muscle during a multijoint exercise.
In a recent meta-analysis, Schoenfeld given load earlier in the training session This occurs alongside an increased
et al. (76) identified a nonsignificant (81), greater long-term accumulation of recruitment of the synergistic muscles
trend that eccentric-only training training volumes will occur in response during the compound movement (30).
induced greater hypertrophic adapta- to exercises that are performed during However, activating a muscle with
tions than concentric-only concentric these periods (80). Although this is a single-joint exercise but not to the
training for inducing hypertrophic dependent upon the design of the point of fatigue may increase its activa-
gains (P 5 0.076). Mean effect sizes training session, it is, therefore, possible tion in the subsequent multijoint exer-
for muscle growth after eccentric- that using multijoint exercises at the cise (42). Therefore, coaches may
only and concentric-only training were start of a training session will result in order exercises to strategically manip-
1.02 and 0.77 respectively, with an greater hypertrophic adaptations in ulate the recruitment patterns of prime
effect size difference of 0.27. The au- larger muscle groups. movers during exercises in order to
thors propose that because of many Although this provides one reason to alter muscle activation patterns.
of the studies included for analysis include multijoint exercises earlier in
matching the total repetitions per- the training session, little evidence ex- REPETITION TEMPO
formed and not total work, the higher ists to support this hypothesis. This is Explosive strength training demon-
amount of work completed was likely mostly due to the limited amount of strates a clear advantage over slow
to be a major influence on these find- studies investigating the relationship concentric training for strength devel-
ings (76). between chronic structural adaptations opment (13). This is likely to be due to
A further consideration with eccentric and exercise order (80). Of the research the higher forces that are required to
training is the identification of region- that does exist, Simão et al. (79) and increase acceleration during the con-
specific hypertrophy. Franchi et al. (27) Spineti et al. (84) both showed that centric phase of an appropriately
showed that although muscle hypertro- ordering training sessions such that loaded lift. However, when attempting
phy of the vastus lateralis was equal single-joint elbow extension and flex- to develop muscle mass, this relation-
between concentric and eccentric train- ion exercises were performed before ship is not evident (69). This poten-
ing, midportion hypertrophy was high- the bench press and lat pull-down, re- tially occurs because of the reduced
er in the concentric group, whereas the sulted in increased triceps muscle vol- lifting speed requiring less force, pro-
eccentric group experienced greater ume when compared to the reverse longing the duration of the set leading
growth in the distal division. This may order (effect size 5 2.07 and 1.08 versus to increased metabolic stress. When
be due to the change in muscle archi- 0.75 and 0.40). It should be noted that loads are lifted with the intention of
tecture, secondary to the activation of no difference was seen for the biceps achieving a high velocity, the forces
altered molecular responses, after a con- musculature between conditions in will be higher, increasing the tension
centric-only or eccentric-only training either investigation (79,84). However, of the muscle. In such instances where
intervention (27). Eccentric-only resis- neither study attempted to establish the repetition duration increases, load-
tance training leads to increases in fas- whether structural changes occurred ing must be reduced because of the
cicle length, whereas concentric-only in the pectoralis major and latissimus time component placing increased de-
training promotes greater pennation an- dorsi muscles, limiting the scope of mands on the involved energy systems
gles, indicating a higher number of sar- their conclusions. It is likely that (87). Therefore, manipulating repeti-
comeres in parallel (27). This has the muscles trained and fatigued in the tion tempo is just another example of
potential to alter the force–velocity early stages of a training session will the inverse-relationship between vol-
relationship of any given muscle, with accumulate higher training volumes ume and load.
an increased fascicle length (sarcomeres and therefore adapt to a greater extent.
The available evidence shows equivo-
in series) resulting in superior shorten- As such, practitioners should prioritize cal differences between short-
ing velocities (19). Conversely, a muscle exercises for completion in the initial repetition and long-repetition tempos
with a larger pennation angles has the stages of the training session based on for muscle hypertrophy development.
capacity to create higher levels of force the individual needs of the athlete (80). Tanimoto and Ishii (87) determined
because of an increased number of One issue with performing single-joint that as long as subjects trained to fail-
sarcomeres in parallel (19). exercises before multijoint exercises is ure, there was no significant difference
that the prefatigued muscle may alter in quadriceps hypertrophy after high-
EXERCISE ORDER the muscle activation patterns during load normal tempo training (1-second
It is generally recommended that mul- the multijoint exercise. In both the concentric: 1-second eccentric:
tijoint exercises, relying on work being lower extremity (9) and upper 1-second relaxation) when compared

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Muscle Hypertrophy

to a low-load, slow training group interset rest periods for increasing mus- Finally, exercise order, repetition
(3-seconds concentric: 3-seconds cle hypertrophy (35). tempo, and interset recovery periods
eccentric: 1-second relaxation). Fur- may all be manipulated at the program
thermore, a recent meta-analysis CONCLUSION level to present the athlete with a novel
showed no significant difference in Certain aspects of traditional hypertro- stimulus. These variables should be
muscle growth when comparing re- phy training have been recently chal- considered in relation to the individual
gimes consisting of 0.5–8 seconds for lenged. A more detailed understanding athlete goals and the desired outcome.
completion of the concentric phase of of key programming variables is there- Conflict of Interests and Source of Funding:
a lift (69). Thus, manipulating repeti- fore required to maximize training effec- The authors report no conflict of interests
tion tempo between blocks of training tiveness. Using the training principles and no source of funding.
provides coaches with another strategy outlined in this review, coaches can
that may provide a novel form of over- design and deliver evidence-based
load through increasing training vol- hypertrophy training that has the poten- Louis P. Howe
ume (via long-repetition duration) or tial to increase athletic performance or is a lecturer in
load (via short-repetition durations). expedite recovery from injury. Sports Rehabili-
tation at Univer-
The current body of evidence suggests
sity of Cumbria.
INTERSET RECOVERY that there is no ideal load prescription
Much like repetition duration, coaches to maximize muscle hypertrophy. In
may also change interset recovery pe- fact, from a loading perspective, there
riods to alter the balance of the train- appears to be very few constraints,
ing volume–load relationship. With providing that the intensity of effort
short-duration recovery periods is high. However, an important vari-
(,30-seconds), training volume may able that must be considered is training
be increased as training density rises. volume. High training volumes are Paul Read is
However, if insufficient recovery is pro- necessary for maximizing muscle a clinical
vided to fully replenish the anaerobic growth. This may be accomplished research scientist
energy stores (34), the load must be through a variety of approaches; one at Aspetar
reduced. Likewise, with higher interset being increased training frequency. Orthopaedic and
recovery periods, greater loads may be The current literature indicates that Sports Medicine
used for each set at the expense of between 2 and 3 training sessions per Hospital.
maintaining high training density, cou- muscle group per week are most effec-
pled with additional rest time (24). tive, although there may be potential
Research investigating interset recov- for superior gains in muscle hypertro-
ery periods suggests that short rest in- phy with the prescription of higher
tervals (#60-seconds) potentially frequencies (.3) in trained individuals.
compromise volume load because of Exercise variation is also important to Mark Waldron
drastic reductions in the load used, access all “functional compartments” of is a senior
when compared to longer recoveries individual muscles. This may be accom- lecturer in Exer-
(3-minutes) (74). This is supported by plished by including variations of basic cise Physiology at
Buresh et al. (17), who showed greater exercises that place stress on specific St Mary’s
increases in quadriceps cross-sectional muscle divisions. By incorporating a vari- University.
area when using longer (2.5 minutes), ety of exercises for a single muscle in the
compared to shorter (60 seconds) in- training program of an athlete, the
terset recoveries. However, caution hypertrophic response has the potential
should be applied when interpreting to be enhanced. Such adaptations may
these results, as in each of these studies also be obtained with varying the type of
volume was equated. Such control may contraction because concentric-only and
remove the benefits of using short re- eccentric-only loading strategies have
coveries because training density can- been shown to provide hypertrophic
not be increased. Whether shorter rest adaptations in different sections of a mus- 1. Adams G and Bamman MM. Characterization
periods permit tolerable increases in cle. Furthermore, it seems that eccentric- and regulation of mechanical loading-induced
training volume has not yet been stud- only training has the potential to increase compensatory muscle hypertrophy. Compr
ied. Therefore, further evidence is muscle mass beyond that of concentric- Physiol 2: 2829–2970, 2012.
required to make clearer recommenda- only training through the increase in 2. American College of Sports Medicine.
tions regarding the manipulation of total work performed. American College of Sports Medicine

78 VOLUME 39 | NUMBER 5 | OCTOBER 2017

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position stand. Progression models in signalling molecule phosphorylation in young 24. de Salles BF, Simão R, Miranda F, Novaes
resistance training for healthy adults. Med men. J Physiol 588: 3119–3130, 2010. Jda S, Lemos A, and Willardson JM. Rest
Sci Sports Exerc 41: 687–708, 2009. 15. Burd NA, West DW, Staples AW, interval between sets in strength training.
3. Amirthalingam T, Mavros Y, Wilson GC, Atherton PJ, Baker JM, Moore DR, Sports Med 39: 765–777, 2009.
Clarke JL, Mitchell L, and Hackett DA. Holwerda AM, Parise G, Rennie MJ, 25. Folland JP, Irish CS, Roberts JC, Tarr JE,
Effects of a modified German volume Baker SK, and Phillips SM. Low-load and Jones DA. Fatigue is not a necessary
training program on muscular hypertrophy high volume resistance exercise stimulates stimulus for strength gains during
and strength. J Strength Cond Res 2016 muscle protein synthesis more than resistance training. Br J Sports Med 36:
[Epub ahead of print]. high-load low volume resistance 370–373, 2002.
4. An HJ, Choi WS, Choi JH. Kim JN and Min exercise in young men. PLoS One 5:
26. Fonseca RM, Roschel H, Tricoli V, de
KO. Effects of muscle activity and number e12033, 2010.
Souza EO, Wilson JM, Laurentino GC,
of resistance exercise repetitions on 16. Burd NA, Mitchell CJ, Churchward-Venne Aihara AY, de Souza Leão AR, and
perceived exertion in tonic and phasic TA, and Phillips SM. Bigger weights may Ugrinowitsch C. Changes in exercises are
muscle of young Korean adults. J Phys Ther not beget bigger muscles: Evidence from more effective than in loading schemes to
Sci 27: 3455–3459, 2015. acute muscle protein synthetic responses improve muscle strength. J Strength Cond
5. Antonio J. Nonuniform response of skeletal after resistance exercise. Appl Physiol Nutr Res 28: 3085–3092, 2014.
muscle to heavy resistance training: Can Metab 37: 551–554, 2012.
27. Franchi MV, Atherton PJ, Reeves ND, Flück
bodybuilders induce regional muscle 17. Buresh R, Berg K, and French J. The effect M, Williams J, Mitchell WK, Selby A,
hypertrophy? J Strength Cond Res 14: of resistive exercise rest interval on Beltran Valls RM, and Narici MV.
102–113, 2000. hormonal response, strength, and Architectural, functional and molecular
6. Armstrong RB, Warren GL, and Warren JA. hypertrophy with training. J Strength Cond responses to concentric and eccentric
Mechanisms of exercise-induced Res 23: 62–71, 2009. loading in human skeletal muscle. Acta
muscle fibre injury. Sports Med 12: 18. Campos GE, Luecke TJ, Wendeln HK, Physiol 210: 642–654, 2014.
184–207, 1991. Toma K, Hagerman FC, Murray TF, Ragg 28. Fry AC and Kraemer WJ. Resistance
7. Arlotta M, Lovasco G, and McLean L. KE, Ratamess NA, Kraemer WJ, and exercise overtraining and overreaching:
Selective recruitment of the lower fibers of Staron RS. Muscular adaptations in Neuroendocrine responses. Sports Med
the trapezius muscle. J Electromyogr response to three different resistance- 23: 106–129, 1997.
Kinesiol 21: 403–410, 2011. training regimens: Specificity of repetition
29. Fry AC. The role of resistance exercise
maximum training zones. Eur J Appl Physiol
8. Arthur RC, Liotta FJ, Klootwyk TE, Porter intensity on muscle fibre adaptations.
88: 50–60, 2002.
DA, and Mieling P. Potential risk of Sports Med 34: 663–679, 2004.
rerupture in primary achilles tendon repair 19. Cormie P, McGuigan MR, and Newton RU.
30. Gentil P, Oliveira E, de Araújo Rocha Júnior V,
in athletes younger than 30 years of age. Developing maximal neuromuscular power:
do Carmo J, and Bottaro M. Effects of
Am J Sports Med 33: 119–123, 2005. Part 1—Biological basis of maximal power
exercise order on upper-body muscle
production. Sports Med 41: 17–38, 2011.
9. Augustsson J, Thomeé R, Hörnstedt P, activation and exercise performance.
Lindblom J, Karlsson J, and Grimby G. 20. Correa CS, Teixeira BC, Cobos RC, J Strength Cond Res 21: 1082–1086, 2007.
Effect of pre-exhaustion exercise on lower- Macedo RC, Kruger RL, Carteri RB,
31. George PP, Asakawa DS, Delp SL, Zajac FE,
extremity muscle activation during a leg Radaelli R, Gross JS, Pinto RS, and
and Drace JE. Nonuniform shortening in the
press exercise. J Strength Cond Res 17: Reischak-Oliveira Á. High-volume
biceps brachii during elbow flexion. J Appl
411–416, 2003. resistance training reduces postprandial
Physiol 92: 2381–2389, 2002.
lipaemia in postmenopausal women.
10. Berger RA. Effect of varied weight J Sports Sci 33: 1890–1901, 2015. 32. Godfrey RJ, Madgwick Z, and Whyte GP.
training programs on strength. Res Q The exercise-induced growth hormone
33: 169–181, 1962. 21. Cuthbertson DJ, Babraj J, Smith K, Wilkes
response in athletes. Sports Med 33: 599–
E, Fedele MJ, Esser K, and Rennie M.
11. Bottaro M, Veloso J, Wagner D, and Gentil 613, 2003.
Anabolic signalling and protein synthesis in
P. Resistance training for strength and human skeletal muscle after dynamic 33. Goto K, Sato K, and Takamatsu K. A single
muscle thickness: Effect of number of sets shortening and lengthening exercise. Am J set of low intensity resistance exercise
and muscle group trained. Sci Sports 26: Physiol Endocrinol Metab 290: 731–738, immediately following high intensity
259–264, 2011. 2006. resistance exercise stimulates growth
12. Brown JM, Solomon C, and Paton M. hormone secretion in men. J Sports Med
22. Damas F, Phillips S, Vechin FC, and
Further evidence of functional Phys Fitness 43: 243–249, 2003.
Ugrinowitsch C. A review of resistance
differentiation within biceps brachii. training-induced changes in skeletal 34. Goto K, Ishii N, Kizuka T, and Takamatsu K.
Electromyogr Clin Neurophysiol muscle protein synthesis and their The impact of metabolic stress on
33: 301–309, 1993. contribution to hypertrophy. Sports Med hormonal responses and muscular
13. Bruce-Low S and Smith D. Explosive 45: 801–807, 2015. adaptations. Med Sci Sports Exerc 37:
exercise in sports training: A critical review. 955–963, 2005.
23. Dankel SJ, Mattocks KT, Jessee MB,
J Exerc Physiol 10: 21–33, 2007. Buckner SL, Mouser JG, Counts BR, 35. Grgic J, Lazinica B, Mikulic P, Krieger JW,
14. Burd NA, Holwerda AM, Selby KC, West DW, Laurentino GC, and Loenneke JP. and Schoenfeld BJ. The effects of short
Staples AW, Cain NE, Cashaback JGA, Frequency: The overlooked resistance versus long inter-set rest intervals in
Potvin JR, Baker SK, and Phillips SM. training variable for inducing muscle resistance training on measures of muscle
Resistance exercise volume affects hypertrophy? Sports Med 47: 799–805, hypertrophy: A systematic review. Eur J
myofibrillar protein synthesis and anabolic 2017. Sport Sci 22: 1–11, 2017.

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Muscle Hypertrophy

36. Hackett DA, Johnson NA, and Chow CM. 48. MacDougall JD, Gibala MJ, Tarnopolsky MA, 58. Poliquin C. The Poliquin International
Training practices and ergogenic aids used MacDonald JR, Interisano SA, and Certification Program: Theory Manual 1.
by male bodybuilders. J Strength Cond Yarasheski KE. The time course for East Greenwhich, RI: Poliquin
Res 27: 1609–1617, 2013. elevated muscle protein synthesis Performance Center, 2009.
37. Hill M and Goldspink G. Expression and following heavy resistance exercise. Can J
59. Radaelli R, Botton CE, Wilhelm EN,
Appl Physiol 20: 480–486,
splicing of the insulin- like growth factor Bottaro M, Lacerda F, Gaya A, Moraes K,
gene in rodent muscle is associated with Peruzzolo A, Brown LE, and Pinto RS. Low-
muscle satellite (stem) cell activation 49. Mattocks KT, Buckner SL, Jessee MB, and high-volume strength training induces
following local tissue damage. J Physiol Dankel SJ, Mouser JG, and Loenneke JP. similar neuromuscular improvements in
549: 409–418, 2003. Practicing the test produces strength muscle quality in elderly women. Exp
equivalent to higher volume training. Med Gerontol 48: 710–716, 2013.
38. Hornberger TA, Chu WK, Mak YW,
Sci Sports Exerc 2017 [Epud ahead of
Hsiung JW, Huang SA, and Chien S. The 60. Radaelli R, Fleck SJ, Leite T, Leite RD,
role of phospholipase D and phosphatidic Pinto RS, Fernandes L, and Simao R. Dose
acid in the mechanical activation of mTOR 50. McBride JM, Blaak JB, and Triplett- response of 1, 3 and 5 sets of resistance
signalling in skeletal muscle. Proc Natl McBride T. Effect of resistance exercise exercise on strength, local muscular
Acad Sci USA 103: 4741–4746, 2006. volume and complexity on EMG, strength, endurance and hypertrophy. J Strength
and regional body composition. Eur J Appl Cond Res 29: 1349–1358, 2015.
39. Izquierdo M, Ibañez J, González-Badillo JJ,
Physiol 90: 626–632, 2003.
Häkkinen K, Ratamess NA, Kraemer WJ, 61. Robbins DW, Goodale TL, Docherty D,
French DN, Eslava J, Altadill A, Asiain X, 51. Mitchell CJ, Churchward-Venne TA, Behm DG, and Tran QT. The effects of load
and Gorostiaga EM. Differential effects of West DW, Burd NA, Breen L, Baker SK, and training pattern on acute
strength training leading to failure versus and Phillips SM. Resistance exercise load neuromuscular responses in the upper
not to failure on hormonal responses, does not determine training-mediated body. J Strength Cond Res 24: 23–29,
strength, and muscle power gains. J Appl hypertrophic gains in young men. J Appl 2009.
Physiol 100: 1647–1656, 2006. Physiol 113: 71–77, 2012.
62. Roig M, O’Brien K, Kirk G, Murray R,
40. Järvinen TA, Järvinen TL, Kääriäinen M, 52. Mitchell CJ, Churchward-Venne TA, McKinnon P, Shadgan B, and Reid WD.
Aärimaa V, Vaittinen S, Kalimo H, and Parise G, Bellamy L, Baker SK, Smith K, The effects of eccentric versus concentric
Järvinen M. Muscle injuries: Optimising Atherton PJ, and Phillips SM. Acute resistance training on muscle strength and
recovery. Best Pract Res Clin Rheumatol post-exercise myofibrillar protein mass in healthy adults: A systematic review
21: 317–331, 2007. synthesis is not correlated with with meta-analysis. Br J Sports Med 43:
resistance training-induced muscle 556–568, 2009.
41. Jones DA and Rutherford OM. Human
hypertrophy in young men. PLoS One
muscle strength training: The effects of 63. Rønnestad BR, Egeland W, Kvamme NH,
24: e89431, 2014.
three different regimens and the nature of Refsnes PE, Kadi F, and Raastad T.
the resultant changes. J Physiol 391: 53. Mendez-Villanueva A, Suarez-Arrones L, Dissimilar effects of one- and three-set
1–11, 1987. Rodas G, Fernandez-Gonzalo R, Tesch P, strength training on strength and muscle
Linnehan R, Kreider R, and Di Salvo V. MRI-
42. Júnior VAR, Bottaro M, Pereira MCC, mass gains in upper and lower body in
based regional muscle use during
Andrade MM, Júnior PRWP, and Carmo untrained subjects. J Strength Cond Res
hamstring strengthening exercises in elite
JC. Electromyography analyses of muscle 21: 157–163, 2007.
soccer players. PLoS One 11: e0161356,
pre-activation induced by single joint 64. Schmidtbleicher D and Haralambie G.
exercise. Rev Bras Fisioter 14: 158–165, Changes in contractile properties of
2010. 54. Moss BM, Refsnes PE, Abildgaard A,
muscle after strength training in man. Eur J
Nicolaysen K, and Jensen J. The effects of
43. Kraemer WJ and Ratamess NA. Appl Physiol 46: 221–228, 1981.
maximal effort strength training with
Fundamentals of resistance training: 65. Schoenfeld BJ. The mechanisms of muscle
different loads on dynamic strength, cross-
Progression and exercise prescription. hypertrophy and their application to
sectional area, load-power and load–
Med Sci Sports Exerc 36: 674–688, 2004. resistance training. J Strength Cond Res
velocity relationships. Eur J Appl Physiol
44. Krieger JW. Single versus multiple sets of 75: 193–199, 1997. 24: 2857–2872, 2010.
resistance exercise: A meta-regression. 66. Schoenfeld BJ. Potential mechanisms for
55. Moore DR, Phillips SM, Babraj JA, Smith K,
J Strength Condit Res 23: 1890–1901, a role of metabolic stress in hypertrophic
and Rennie MJ. Myofibrillar and collagen
2009. adaptations to resistance training. Sports
protein synthesis in human skeletal muscle
45. Krieger JW. Single vs. multiple sets of in young men after maximal shortening and Med 43: 179–94, 2013.
resistance exercise for muscle lengthening contractions. Am J Physiol 67. Schoenfeld BJ, Ratamess NA, Peterson
hypertrophy: A meta-analysis. J Strength Endocrinol Metab 288: 1153–1159, MD, Contreras B, Sonmez GT, and Alvar
Cond Res 24: 1150–1159, 2010. 2005. BA. Effects of different volume-equated
46. Kreher JB and Schwartz JB. Overtraining 56. Ogborn D and Schoenfeld BJ. The role of resistance training loading strategies on
syndrome: A practical guide. Sports Health fiber types in muscle hypertrophy: muscular adaptations in well-trained men.
4: 128–138, 2012. Implications for loading strategies. J Strength Cond Res 28: 2909–2918,
47. Lauver JD, Cayot TE, and Scheuermann Strength Cond J 35: 20–25, 2014. 2014.
BW. Influence of bench angle on upper 57. Phillips SM. A brief review of critical 68. Schoenfeld BJ, Contreas B, Tiryaki-
extremity muscular activation during bench processes in exercise-induced muscular Sonmez G, Wilson JM, Kolber MJ, and
press exercise. Eur J Sport Sci 16: 309– hypertrophy. Sports Med 44: 71–77, Peterson MD. Regional differences in
316, 2016. 2014. muscle activation during hamstrings

80 VOLUME 39 | NUMBER 5 | OCTOBER 2017

Copyright ª National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
exercise. J Strength Cond Res 29: 159– 78. Shepstone TN, Tang JE, Dallaire S, muscular function in young men. J Appl
164, 2015. Schuenke MD, Staron RS, and Philips SM. Physiol 100: 1150–1157, 2006.
69. Schoenfeld BJ, Ogborn DI, and Krieger Short-term high- vs. low-velocity isokinetic 88. Tesch PA and Karlsson J. Muscle fiber
JW. Effect of repetition duration during lengthening training results in greater types and size in trained and untrained
resistance training on muscle hypertrophy of the elbow flexors in young muscles of elite athletes. J Appl Physiol 59:
hypertrophy: A systematic review and men. J Appl Physiol 98: 1768–1776, 1716–1720, 1985.
meta-analysis. Sports Med 45: 577–585, 2005.
89. Tesch PA, Colliander EB, and Kaiser P.
2015. 79. Simão R, Spineti J, de Salles BF, Oliveira Muscle metabolism during intense, heavy-
70. Schoenfeld BJ. Science and Development LF, Matta T, Miranda F, Miranda H, and resistance exercise. Eur J Appl Physiol
of Muscle Hypertrophy. Champaign, IL: Costa PB. Influence of exercise order on Occup Physiol 55: 362–366, 1986.
Human Kinetics, 2016. pp. 51–56. maximum strength and muscle thickness in
90. Tesch PA, Ploutz-Snyder LL, Yström L,
untrained men. J Sports Sci Med 9: 1–7,
71. Schoenfeld BJ, Contreras B, Ogborn D, Castro MJ, and Dudley GA. Skeletal
Galpin A, Krieger J, and Sonmez GT. muscle glycogen loss evoked by resistance
Effects of varied versus constant 80. Simão R, de Salles BF, Figueiredo T, Dias I, exercise. J Strength Cond Res 12: 67–73,
loading zones on muscular adaptations and Willardson JM. Exercise order in 1998.
in trained men. Int J Sports Med resistance training. Sports Med 42: 251–
91. Wakahara T, Miyamoto N, Sugisaki N,
37: 442–447, 2016. 265, 2012.
Murata K, Kanehisa H, Kawakami Y,
72. Schoenfeld BJ, Ogborn D, and Krieger JW. 81. Simão R, Figueiredo T, Leite RD, Jansen A, Fukunaga T, and Yanai T. Association
Dose-response relationship between and Willardson JM. Influence of exercise between regional differences in muscle
weekly resistance training volume and order on repetition performance during activation in one session of resistance
increases in muscle mass: A systematic low-intensity resistance exercise. Res exercise and in muscle hypertrophy after
review and meta-analysis. J Sports Sci 19: Sports Med 20: 263–273, 2012. resistance training. Eur J Appl Physiol 112:
1–10, 2016. 82. Smith LL. Overtraining, excessive exercise, 1569–1576, 2012.

73. Schoenfeld BJ, Ogborn D, and Krieger JW. and altered immunity: Is this a T Helper-1 92. Wakahara T, Fukutani A, Kawakami Y, and
Effects of resistance training frequency on versus T Helper-2 lymphocyte response? Yanai T. Nonuniform muscle hypertrophy:
measures of muscle hypertrophy: A Sports Med 33: 347–364, 2003. Its relation to muscle activation in training
systematic review and meta-analysis. 83. Sola OM, Herring S, Zhang G, Huang X, session. Med Sci Sports Exerc 45: 2158–
Sports Med 46: 1689–1697, 2016. Hayashida N, Haines LC, Thomas R, 2165, 2013.

74. Schoenfeld BJ, Pope ZK, Benik FM, Hester Kakulas BA, and Sauvage LR. Significance 93. Waldron M, Worsfold PR, Twist C, and
GM, Sellers J, Nooner JL, Schnaiter JA, of the biopsy site of the latissimus dorsi Lamb KL. Changes in anthropometry and
Bond-Williams KE, Carter AS, Ross CL, muscle for fiber typing. J Heart Lung performance, and their inter-relationships,
Just BL, Henselmans M, and Krieger JW. Transplant 11: 315–319, 1992. across three seasons in elite youth rugby
Longer interset rest periods enhance 84. Spineti J, de Salles BF, Rhea MR, Lavigne league players. J Strength Cond Res 28:
muscle strength and hypertrophy in D, Matta T, Miranda F, Fernandes L, and 3128–3136, 2014.
resistance-trained men. J Strength Cond Simão R. Influence of exercise order on 94. Wernbom M, Augustsson J, and Thomee R.
Res 30: 1805–1812, 2016. maximum strength and muscle volume in The influence of frequency, intensity,
75. Schoenfeld BJ, Wilson JM, Lowery RP, and nonlinear periodized resistance training. volume and mode of strength training on
Krieger JW. Muscular adaptations in low- J Strength Cond Res 24: 2962–2969, whole muscle cross-sectional area in
versus high-load resistance training: A 2010. humans. Sports Med 37: 225–264, 2007.
meta-analysis. Eur J Sport Sci 16: 1–10, 85. Stone MH, Stone ME, and Sands WA. 95. Wickiewicz TL, Roy RR, Powell PL, and
2016. Principles and Practice of Resistance Edgerton VR. Muscle architecture of the
76. Schoenfeld BJ, Ogborn D, Vigotsky AD, Training. Champaign, IL: Human Kinetics, human lower limb. Clin Orthop Relat Res
Franchi M, and Krieger JW. Hypertrophic 2007. 179: 275–283, 1983.
effects of concentric versus eccentric 86. Sundstrup E, Jakobsen MD, Andersen CH, 96. Widrick JJ, Stelzer JE, Shoepe TC, and
muscle actions: A systematic review and Zebis MK, Mortensen OS, and Andersen Garner DP. Functional properties of human
meta-analysis. J Strength Cond Res 2017 LL. Muscle activation strategies during muscle fibers after short-term resistance
[Epub ahead of print]. strength training with heavy loading vs. exercise training. Am J Physiol Regul Integr
77. Schott J, McCully K, and Rutherford OM. repetitions to failure. J Strength Cond Res Comp Physiol 283: 408–416, 2002.
The role of metabolites in strength training. 26: 1897–1904, 2012. 97. Willardson JM, Norton L, and Wilson G.
II. Short versus long isometric contractions. 87. Tanimoto M and Ishii N. Effects of low- Training to failure and beyond in
Eur J App Physiol Occup Physiol 71: 337– intensity resistance exercise with slow mainstream resistance exercise programs.
341, 1995. movement tonic force generation on Strength Cond J 32: 21–29, 2010.

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