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Inhomogeneous Muscle
Growth: A Systematic
Review
Aitor Zabaleta-Korta, MSc, Eneko Fernández-Peña, PhD, and Jordan Santos-Concejero, PhD, FECSS
Department of Physical Education and Sport, University of the Basque Country UPV/EHU, Vitoria-Gasteiz, Spain
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ABSTRACT increase in muscle anatomical cross- (13). This implies that if a muscle could
sectional area (ACSA). ACSA is consid- increase the ACSA of a certain region to
A literature search was performed in 2
ered a reliable measure to assess muscle a greater degree than other regions, it
databases (PubMed and Scopus) on
growth (16,46) and has been found to would alter its length-tension relation-
May 22, 2019. From the 14 studies ship and, consequently, also its angle-
be related to other indicators of muscle
included in the review, 13 found that force relationship.
hypertrophy, including muscle volume
the anatomical cross-sectional area of
and muscle thickness, which is the dis- The question arises whether such
some regions of a muscle increased to
tance between the deep and superficial regional muscle hypertrophy (RMH)
a greater degree than others. Some
aponeuroses (16). There are 2 methods within an individual muscle exists.
studies found increases in the distal mainly used to assess muscle ACSA: RMH (15,21,29) and other nonuniform
region, others reported increases in ultrasound and magnetic resonance intramuscular adaptations, such as
the middle region, and some found imaging (MRI). The gold standard changes in pennation angles (12), have
differences between regions but did when measuring muscle ACSA seems already been reported in previous
not report which increased the most. to be the latter because of the superior works, although some other articles
Hypertrophy between and within visualization it provides and less depen- show opposing results (5,11). It is
muscle heads is not homogeneous, dence on the operator as compared against this apparently contradictory
confirming that regional hypertrophy with the ultrasound (14,36). background that this review intends
actually happens in the quadriceps to examine whether there is evidence
The beneficial effect that muscle hyper-
femoris, triceps brachii, and biceps to support RMH in a given muscle
trophy has for both general sports-based
brachii muscles. when assessed with the gold standard
and resistance training–based sports
measurement technique.
performance has been reported else-
INTRODUCTION where (1,4,35); however, several aspects
MATERIALS AND METHODS
keletal muscle plays a key role in of muscle hypertrophy are yet to be
94 VOLUME 42 | NUMBER 5 | OCTOBER 2020 Copyright Ó National Strength and Conditioning Association
Copyright © National Strength and Conditioning Association. Unauthorized reproduction of this article is prohibited.
peer-reviewed articles in English were and adequacy of follow-up. Items 2–8 Three studies (12,22,31) analyzed the
selected. Citations from scientific con- can be rated with 0 or 1, so the highest effect of conventional resistance train-
ferences were excluded. To make the rate in the PEDro scale is 7, and the ing on the ACSA of different muscle
search more accurate, it was limited to lowest is 0. Zero points are awarded to heads. An exercise is performed in
the area of “medicine,” “biochemistry,” a study that fails to satisfy any of the a “conventional resistance training”
“genetics and molecular biology,” and included items, and 7 points to a study fashion when the subjects perform
“health professions” in Scopus data- that satisfies all of the included items. a lifting (concentric) and a lowering
base. In addition, “article” was used as (eccentric) phase, and they only rely
a keyword. RESULTS on their muscle strength to complete
STUDIES SELECTED the exercise. In all 3 studies, the sub-
LITERATURE SEARCH The search strategy yielded 1,069 stud- jects performed the leg extension exer-
In the database, the title and abstract ies as presented in the Figure. Another cise. The study by Ema et al. (12) found
search fields were searched. The fol- 21 studies were added from other sour- that the ACSA of the rectus femoris
lowing MeSH terms and key words, ces. After removing 249 duplicates, 38 increased significantly more (p ,
combined with the Boolean operators studies were determined to be poten- 0.01) than the rest of the heads of the
(AND, OR), were used: hypertrophy, tially relevant to the topic based on the quadriceps femoris. Hisaeda et al. (22)
csa, cross-sectional area, MRI, muscle information in the abstract, from which found that when the leg extension was
architecture, nonuniform muscle 14 met the inclusion criteria. Excluded performed with high absolute intensity
growth. The search was performed in studies had at least one of the following (4–5 repetition maximum [RM]), the
PubMed and Scopus databases. characteristics: (a) injured or ill sub- rectus femoris was the only head of
Twenty-one more studies were identi- jects, (b) intervention shorter than 4 the quadriceps femoris that increased
fied using the snowball technique. weeks, (c) did not measure, or did its ACSA significantly from baseline
not report ACSA, or (d) ACSA of just after the intervention. When the exer-
INCLUSION CRITERIA 1 region measured. The overall sample cise was performed with low absolute
Studies were eligible for further analysis for the present systematic review re- intensity (15–20 RM), the only signifi-
if the following inclusion criteria were sulted in 254 healthy subjects (159 cant increase in ACSA at the end of the
met; (a) studies were written in English; men and 95 women) with an age range intervention was seen in the vastus lat-
(b) studies measured the ACSA of 1 of 20–29 years (Table 1). eralis. Narici et al. (31) found significant
muscle in at least 2 separate areas; (c) increases in the growth of the quadri-
studies had to be made in healthy LEVEL OF EVIDENCE AND
ceps femoris heads after training leg
human beings, with no age limit; (d) QUALITY OF STUDIES
extensions for 6 months: rectus femoris
studies had to include a resistance train- According to the Oxford’s level of evi-
(27.9%) . vastus lateralis (19.5%) .
ing intervention of at least 4 weeks; (e) dence, 4 of the included 14 studies had
vastus medialis (18.7%) . vastus inter-
ACSA had to be measured in any mus- an evidence level 1b (high-quality
medius (17.4%). The authors stated that
cle using the MRI technique because it RCTs) and 6 of the 14 studies had an
the seat of the leg extension machine
provides a superior visualization and is evidence level of 2b (individual cohort
was in a “slight negative slope”; hence,
less dependent on the operator as com- study or low-quality RCTs). The re-
it is difficult to determine whether par-
pared with ultrasound (14,36). maining 4 studies had an evidence level
of 3b (individual case-control study) ticipants were seated with a hip flexion
angle of 908, greater than 908, or less
QUALITY ASSESSMENT due to the following reasons: noncon-
secutive study and not correctly than 908. This may have influenced the
Oxford’s level of evidence (33) and the
applied reference standards. Scores findings because the rectus femoris is
Modified Physiotherapy Evidence
from PEDro scale were on average a hip flexor and a knee extensor. Per-
Database (PEDro) scale (30) were used
4.035 6 1.3 and ranged from 3 to 6 forming knee extensions while the hip
by 2 independent observers to assess
(Table 2). is in greater hip flexion places the rec-
the methodological quality of the ar-
tus femoris in a position of active insuf-
ticles included in the review. Oxford’s
level of evidence ranges from 1a to 5, EVIDENCE OF REGIONAL ficiency at the top of the movement
HYPERTROPHY and may have changed the force dis-
with 1a being systematic reviews of
high-quality, randomized, controlled tribution among the 4 heads of quad-
Differences in the growth of
trials (RCTs) and 5 being expert opin- muscle heads after training. On- riceps femoris.
ions. The modified PEDro scale con- ly 6 of the 14 included studies reported Two studies (23,32) analyzed the effect
sists of 8 different items related to comparisons of the ACSAs of the heads of isokinetic leg flexion/extensions on
scientific rigor. The items include ran- of the analyzed muscles after the inter- the ACSAs of the different heads of the
dom allocation, concealment of alloca- vention. All of them found preferential quadriceps femoris. Both Housh et al.
tion, comparability of groups at hypertrophy of some heads inside (23) and Narici et al. (32) found that
baseline, analysis by intention to treat, a given muscle (12,22,23,31,40,44). some heads grew significantly more
95
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Regional Hypertrophy
than others after training. The study by Finally, one study used the YoYo tech- regions of a muscle or muscle head
Housh et al. (23) studied whether a pref- nology in their training intervention. increased to a greater degree than others
erential growth of the heads of the The YoYo technology allows the ath- (12,15,21–23,26,29,31,32,40,43,44,46).
quadriceps femoris could happen in lete to train the eccentric part of an Seven studies (12,22,26,29,31,44,46) ana-
response to leg extension training. The exercise. The force generated in the lyzed the differences in the growth of
authors reported that the growth that concentric phase is returned in the regions of the biceps brachii, triceps bra-
rectus femoris underwent was signifi- eccentric phase, forcing the athlete to chii, and quadriceps femoris muscles
cantly larger to that experienced by overcome the force eccentrically. after conventional resistance training.
vastus medial and vastus lateralis. In Seynnes et al. (40) reported an increase Many of them found increases in the
contrast to the studies performed with of 11.4% in the ACSA of rectus femoris, distal region (12,22,46), others reported
conventional training, Narici et al. (32) 8.6% in the ACSA of vastus medialis, increases in the middle region (22,44,46),
reported a preferential hypertrophy of and 6.3% in the ACSA of vastus later- and some found differences between re-
vastus medialis and vastus intermedius alis after training leg extension (and gions but did not report which increased
over vastus lateralis and rectus femoris resisted leg flexions, because of the the most (26,29,31). However, it cannot
in their study. However, similar to the YoYo technology) for 35 days, 3 times be stated that a specific region increases
study by Narici et al. (31), the authors per week. The increase in vastus inter- its ACSA in response to conventional
did not report if the participants were medius ACSA was not significant. training because there is not a clear pat-
seated with a hip flexion angle of 908, tern in the results.
greater than 908, or less than 908; hence, Differences in the growth of dif- Six studies (15,21,23,32,43,46) used
it is unclear whether this may have ferent regions of a muscle. From eccentric only or isokinetic resistance
influenced the force distribution among the 14 studies included in the systematic training in their interventions. In con-
the 4 heads of quadriceps femoris. review, 13 found that the ACSA of some trast to the findings of the studies that
97
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Regional Hypertrophy
Table 2
Included studies and main outcomes
measured at the proximal and distal mentioned lengthening phase, this Franchi et al. (17) found that pY397-
tendons in rats was not the same when region had the shortest sarcomere FAK levels were 4-fold in the distal site
the muscle was contracted by exciting length (7). This would mean that the after eccentric training in the vastus
it externally (24). The authors sug- overlap between filaments inside this lateralis, compared with concentric
gested that a probable reason for this region of the muscle would be higher, training. Similarly, Franchi et al. (15)
is an intramuscular force transmission explaining the higher strain found. found significant differences in muscle
pathway that would evoke different architecture: the participants who per-
strain in the different regions of the The molecular events that regulate the formed eccentric leg extensions expe-
muscles. Another study saw that the physiological response to mechanical rienced greater increases in fascicle
distal region of a muscle in birds was stress may also explain the regional length, whereas those who performed
suffering the highest strain while response to exercise. A recent study concentric leg extensions underwent
lengthening during a run. Higher strain found that the focal adhesion kinase greater increases in pennation angle.
would theoretically lead to a larger (FAK) phosphorylation differs region- One possible explanation is that eccen-
hypertrophy of the region (38). In addi- ally between eccentric and concentric tric training may promote the hyper-
tion, it was also found that during the training. In particular, this study by trophy of the distal part of the
99
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Regional Hypertrophy
understood, RMH seem to happen in 10. Damas F, Barcelos C, Nobrega SR, et al.
Jordan Santos- Individual muscle hypertrophy and strength
the quadriceps femoris, biceps brachii,
Concejero is responses to high vs. low resistance
and triceps brachii muscles. This is
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