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Effect of Foot and Ankle Immobilization on Leg and Thigh Muscles' Volume and MorphologyA Case Study Using Magnetic Resonance Imaging.

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THE ANATOMICAL RECORD 291:1673–1683 (2008)
Effect of Foot and Ankle Immobilization
on Leg and Thigh Muscles’ Volume and
Morphology: A Case Study Using
Magnetic Resonance Imaging
JEAN-FRANÇOIS GROSSET* AND GLADYS ONAMBELE-PEARSON
Department of Exercise and Sport Sciences, Manchester Metropolitan University,
Alsager ST7 2HL, U.K
ABSTRACT
Our aim was to determine the time course of any changes in muscle
volume and shape in the lower limbs following immobilization. A healthy
young woman (29 years) had suffered a fracture of the fifth metatarsal of
the right foot. MRI scanning of her right thigh and calf muscles had been
performed 1 month before the injury (Pre) during a scan initially planned
as a teaching tool, 2 days following a 4-week immobilization period (Post),
and after a 2-month recovery period (Post12). The results show muscle
volume decrements in the triceps surae (TS), quadriceps (Quad), and
hamstring (Ham) of 21.9%, 24.1%, and 6.5%, respectively, between the
Pre and Post measurements. At Post12, the Quad and TS muscle volumes were still 5.2% and 9.5% lower, compared with the Pre data. The
Ham muscle volume, however, was 2.7% greater than at the Pre phase.
Following recovery, the increase in individual TS muscles volume was
limited to both proximal and medial (with respect to the knee joint) segments of the muscles. These results indicate very substantial and rapid
losses in muscle volumes, both proximally and distally to the immobilization site. The results also show that recovery is far from complete up to 2
months post cast removal. The results have implications for the requirements for rehabilitation for orthopedic patients. Anat Rec, 291:1673–
1683, 2008. Ó 2008 Wiley-Liss, Inc.
Key words: muscle volume; morphology; immobilization;
quadriceps; hamstring; triceps surae
INTRODUCTION
Total ankle immobilization with cast or composite
splint is a common practice after ankle sprain (Kerkhoffs et al., 2001) and metatarsal (Rammelt et al.,
2004) as well as ankle fracture (Vandenborne et al.,
1998a). The main inconveniences of such immobilization
are the subsequent muscle atrophy and reduction in
skeletal muscle functional capacity which may impair
functional abilities (Young and Skelton, 1994), postural
balance (Onambele and Degens, 2006; Onambele et al.,
2006), or maximal physical capacities recovery in athletes (Wilkerson, 1992). Strategies that may minimize
these effects are of considerable functional significance
to the individual.
One of the most predictable consequences of joint
immobilization is loss of lean muscle mass. The time
Ó 2008 WILEY-LISS, INC.
course of changes in muscle cross-sectional area (CSA) is
well documented showing a decrease following unilateral
lower limb suspension (ULLS—based on Berg et al.’s
model (Berg et al., 1991; Hather et al., 1992), immobilization (or a general decreased mobility) owing to a cast
(Vandenborne et al., 1998b), bed rest (Akima et al.,
2001), spaceflight (Narici et al., 2003), aging (Morse
et al., 2005), and prolonged diseases including cancer
*Correspondence to: Jean-François Grosset, Université Paris
13, UFR SMBH, Département STAPS, 74 rue Marcel Cachin,
93017 Bobigny Cedex, France. E-mail: jf_grosset@hotmail.com
Received 15 February 2008; Accepted 24 June 2008
DOI 10.1002/ar.20759
Published online 24 October 2008 in Wiley InterScience (www.
interscience.wiley.com).
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GROSSET AND ONAMBELE-PEARSON
(Evans, 2004). However, data on muscle volume modifications with cast or composite splint immobilization are
poorly documented, with the only information coming
from microgravity models: ULLS (Tesch et al., 2004),
bed rest (Alkner and Tesch, 2004a), or spaceflight
(LeBlanc et al., 2000). These authors reported a significant decrease in muscle volume following the hypoactivity period. To our knowledge, no data have been reported
on the immobilization-induced changes in muscle morphology. As eluded earlier, the literature on the relative
recovery of muscle volume/shape after immobilization is
scarce. Indeed, while Akima et al. (2000) reported an
estimated muscle volume recovery after short-term
spaceflight, to our knowledge, no data has in fact been
published on muscle shape modifications following a recovery period that precede an immobilization.
On the whole, despite a frequent practice of ankle
joint immobilization after injury, the impact of said
immobilization and the rate of recovery of both proximal
and distal (to the immobilized joint) muscle groups is
poorly characterized in terms of muscle morphology and
volume changes. The aim of our current investigation
was therefore to identify the changes associated with
total ankle immobilization with cast, using the quadriceps, hamstring, and triceps surae (TS) muscles as models of atrophy.
METHODS
Study Case
The current is the case of a moderately active, 29-year
old, Caucasian female, 171-cm tall, with a body mass of
58 kg. The subject was initially scanned by the authors
who used an MRI scanner as part of a teaching program, designed to instruct students on how to carry out
a full lower limb scan. The subject’s right leg (from calcuneus to iliac crest) was used. Unfortunately for the
subject, she broke the fifth metatarsal on her right foot
as a result of a bad fall, a month after the ‘‘teaching
scan’’ session. A cast was applied and remained in position for 28 days, during which time it served to minimize the movements of the right foot and ankle joint.
Two days following cast removal, a second scan, replicating the protocol used during the first scan, was performed by the authors. Finally a third scan, similar to
the previous two, was carried out after 2 months of recovery. Written informed consent was obtained for the
current study, which was approved by the ethics committee of the Manchester Metropolitan University.
Muscle Volume Measurement
Cod-liver oil tablets were first positioned along the tibial and femur bone using a surgical tape to identify positions of the scan. These markers were spaced at 7 cm
starting from the knee joint. The femur length, defined
as the distance from the most distal border of the lateral
femur condyle to the most proximal prominence of the
greater trochanter, was determined carefully using
ultrasonography (Mylab 25, Esaote Biomedica, Genova,
Italy). From the ultrasound images, accurate positioning
of the skin markers (cod-liver oil tablets) at 40% of the
femur length, proximal from the lateral femur condyle,
was feasible. The subject was then laid down in a 0.2 T
MRI scanner (G-Scan, Esaote Biomedica) in the supine
position, with the knee fully extended in a relaxed state.
Subsequently, seven sets of 52 axial slides (i.e., a total of
364 slides per session) were obtained along the leg and
the thigh using the appropriate coil for the anatomical
site and the size of the study case (i.e., coil no. 2). Scans
were run using T1-weighted three-dimensional isotrophic profiles (Turbo 3D T1 sequence) with the following
scanning parameters: echo time 5 16 ms; repetition
time 5 40 ms; field of view 5 180 mm 3 180 mm; matrix 5 256 3 256; slice thickness 5 2.8 mm; interslice
gap 5 0 mm.
All MRI images were then transferred to a Macintosh
labtop (iBook G4) for measurement of muscle anatomical
CSA (aCSA). The aCSA of every quadriceps and hamstring muscles were measured along the length of the femur up to the iliac crest. Muscle volumes were also
measured along the length of the tibia for the TS muscle
group. A segmental adipose volume index was evaluated
for the leg (AVILeg) and the thigh (AVIThigh) from the
most distal border of the lateral femur condyle, respectively, over 33.6 and 25.2 cm, and defined as the adipose
tissue volume between the skin and the muscles. A
DICOM file viewer and associated measurement software (OsiriX medical imaging software, OsiriX, Atlanta,
USA) was used to analyze one in five slides. The same
investigator completed the analysis in triplicate for all
muscles of interest and the average was recorded. For
lean skeletal muscle tissue measures, visible fat and
connective tissue were not included within the measurement region. Cod-liver oil tablets, bone and muscle
shape as well as veins locations were used to define the
common slides between two consecutive scans.
Assessment of Muscle Volume
The aCSA data gaps between the analyzed image
slides along each 7-cm segment were interpolated with
the trapezoidal numerical integration method using
Matlab (Matlab, The MathWorks, Natick, MA). Then,
the muscle volume and segmental fat volume index were
calculated as the sum of the measured and interpolated
aCSA of each muscle of interest with the length of the
segment.
The MRI scan (see Fig. 1) was taken at 40% of femur
length. The use of cod-liver oil tablets, together with
ultrasound imaging of the anatomical landmarks,
allowed this positioning to be accurately replicated at
the post and post12 phases. In addition, within our
sample MRI pictures shown in Fig. 1, as with all MRI
slices, bone and muscle contours, as well as blood vessels
locations, were also used to correctly match MRI slices
between phases.
No external markers were used to identify a specific
position along the leg. Instead, the position at 30% of
total tibial length was defined using data analysis and,
as with the thigh, this position was precisely characterized according to bone and muscle shape, as well as
blood vessels location.
Timing of Measurements
As mentioned earlier, a first scan of the right thigh
and leg was done a month before complete immobilization of the right foot and ankle, a second scan 2 days
EFFECTS OF IMMOBILIZATION ON MUSCLE VOLUME
Fig. 1.
1675
Transverse MRI scans of the thigh at 40% femur length in (A) and at 30% tibia length in (B).
after the end of the 28-day immobilization period, and a
third scan after 2 months of recovery.
RESULTS
Figure 1 shows typical MRI scans with the individual
muscles identified in the thigh (Fig. 1A) and the leg
(Fig. 1B) at different measurement points (Pre, Post,
and Post12). These MRI scans demonstrate muscle volume changes following immobilization and recovery periods. Thus, atrophy is shown after the 28 days of immobilization (Post) relative to Pre measurement in both the
thigh and the leg muscles. In contrast, MRI scans of the
thigh and leg after the 2-month recovery period show a
degree of hypertrophy in comparison to immediately
postimmobilization.
The aCSA in the muscle groups of interest (quadriceps, hamstring, and TS) is illustrated at the Pre phase
in Fig. 2. As shown, all individual muscles constituting the quadriceps (see Fig. 2A), the hamstring (see
Fig. 2B), and the TS (see Fig. 2C) muscles differs in
length, origin, and insertion points, as well as shape and
volume.
Muscle Volume Changes
TS muscles. In the TS, the soleus muscle (Sol) is
the largest of the three individual muscles, with the second largest being the gastrocnemius medialis (GM) and
the smallest being the gastrocnemius lateralis (GL)
(Table 1). Neither the immobilization nor the recovery
periods modify that hierarchy. After 4 weeks of immobilization, gastrocnemii muscles volumes are the most
affected compared to Pre injury data. Between Post and
Post12 measurement points, the results indicates that
the gastrocnemii muscles, the most affected by immobilization, in fact showed the greatest volume improvement
(Table 1). Even so, after 2 months of recovery, the total
TS muscle volume was still 9.5% diminished, compared
to Pre immobilization data (Table 1).
Quadriceps muscles.
Among the quadriceps
muscles, vastus lateralis (VL) is the largest muscle, followed by the vastus intermedius (VI), the vastus medialis (VM), and finally the rectus femoris (RF; Table 1).
As with the TS, this order was not influenced by immobilization nor changed after recovery. The foot and ankle
immobilization leads to an important decrease in the
1676
GROSSET AND ONAMBELE-PEARSON
here were exhibited by those muscles that had the greatest decrease in muscle volume after immobilization (Table 1). Despite the volume increments at Post12 relative
to Post and between Pre and Post12, the whole quadriceps muscle volume was still 5.2% smaller.
Hamstring muscles. As for the hamstring muscle
group, the semitendinosus (ST) is the largest of the four
muscles constituting this muscle group, followed in size
by the biceps femoris long head (BFLH), the semimembranosus (SM), and the biceps femoris short head
(BFSH; Table 1). As with the two previous muscle
groups, this order is not affected by immobilization or
recovery period. Immobilization leads to a decrease in
the total hamstring muscle volume of 6.5%, with variations in individual muscle values. Interestingly, between
Pre and Post12 the total hamstring muscle volume in
fact shows a small increase (2.7%), though with a large
disparity between individual muscles (Table 1).
Muscle Morphology Changes
Owing to the fact that MRI scanners are not readily
available, coupled with the fact that analysis of a full
MRI data set is time consuming, in the view of facilitating future comparative work, we also determined the
precise location of aCSA modifications along the length
of individual muscles within the muscle groups of interest (Fig. 3). Thus, we describe here the changes seen at
discreet quartiles along the length of the limbs these
muscles are associated with.
TS muscles. Overall, the TS aCSA was decreased
along its length after immobilization (Fig. 3D). At the
Post12 phase, the TS aCSA was completely recovered
over the first 40% of its length, was increased (though not
back to baseline values) between 40% and 60% of its
length, and did not show any modifications relative to the
Postphase over the last 40% of its length. More details on
individual TS muscles are shown on Fig. 3A–C.
Fig. 2. Anatomic cross-sectional area (aCSA) of the quadriceps
muscles in (A), hamstring muscles in (B), and triceps muscles in (C)
for Pre immobilization measurement. (A) VL, vastus lateralis; VI, vastus
intermedius; RF, rectus femoris; VM, vastus medialis; Quad, quadriceps. (B) BFSH, biceps femoris short head; BFLH, biceps femoris
long head; ST, semitendinosus; SM, semimembranosus; Ham, hamstring. (C) Sol, soleus; GL, gastrocnemius lateralis; GM, gastrocnemius
medialis; TS, triceps surae.
muscle volume of all the individual muscles constituting
the quadriceps, and importantly, even though this muscle group is not directly immobilized. Between Pre and
Post measurement points, muscle volumes are
decreased, and after 2 months of recovery, a significant
increase in all the individual quadriceps muscle volumes
is evident. It is notable that the greatest increments
Quadriceps muscles. By and large, the quadriceps muscle group showed a reduction in aCSA along its
length after 1 month of immobilization (Fig. 4E). After
2 months of recovery, the quadriceps aCSA had recovered its baseline values in the first two quartiles but
was still slightly reduced in the last two quartiles,
though values came close to Pre data. More details on
individual quadriceps muscles are shown on Fig. 4A–D.
Hamstring muscles. All in all, hamstring aCSA
was slightly decreased after immobilization in the first
quartile, was unchanged in the middle two quartiles,
and decreased in the last quartile (Fig. 5E). After
2 months of recovery, whilst in the first quartile hamstring aCSA is still the same as Post values, it is increased over and above Pre values in the second and
third quartiles, and in the last quartile, hamstring
aCSA has recovered to Pre values. More details on individual hamstring muscles are shown in Fig. 5A–D.
Subcutaneous Adipose Tissue Content Changes
The subcutaneous adipose tissue volume in both the
thigh and the leg shows conspicuous decreases of 9.0%
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EFFECTS OF IMMOBILIZATION ON MUSCLE VOLUME
TABLE 1. Quadriceps, hamstring, and triceps surae muscle volume as well as subcutaneous thigh and leg
adipose tissue volume index before and after immobilization and after 2 months of recovery
Muscle volume
3
3
Pre (cm )
Post (cm )
Sol
GL
GM
TS
VL
VI
RF
VM
Quad
BFSH
BFLH
ST
SM
Ham
409
95
194
701
461
396
199
365
1,421
83
170
232
164
651
339
70
139
548
345
279
187
268
1,079
74
162
215
156
608
Thigh
Leg
1,259
782
1,145
702
3
Post12 (cm )
D Pre/Post (%)
D Pre/Post12 (%)
380
217.1
87
226.7
171
228.3
635
221.9
412
225.3
384
229.5
204
26.2
346
226.4
1,346
224.1
76
210.8
189
24.7
236
27.4
166
24.8
668
26.5
Subcutaneous adipose volume index
1,172
29.0
710
210.2
D Post/Post12 (%)
27.2
29.0
211.8
29.5
210.7
22.9
2.6
25.1
25.2
28.4
11.1
1.7
1.1
2.7
12.0
24.1
23.1
15.9
19.6
37.7
9.4
29.0
24.8
2.7
16.6
9.8
6.2
9.8
26.9
29.2
2.3
1.2
Quadriceps: VL, vastus lateralis; VI, vastus intermedius; RF, rectus femoris; VM, vastus medialis. Hamstring: BFSH,
biceps femoris short head; BFLH, biceps femoris long head; ST, semitendinosus; SM, semimembranosus. Triceps surae: Sol,
soleus; GL, gastrocnemius lateralis; GM, gastrocnemius medialis.
and 10.2%, respectively, between Pre and Post measurements (Table 1). After 2 months of recovery, both values
slightly increased by 2.3% and 1.2%, respectively, for the
thigh and the leg. At the Post12 relative to the Pre
phase, the subcutaneous adipose tissue volumes were
still smaller by 6.9% and 9.2% for the thigh and the leg,
respectively (Table 1). As shown in Fig. 6, the decrease
in the subcutaneous adipose tissue volume after immobilization does not show any localization as it is evenly
distributed along the two limbs of interest. The recovery
period did not modify to any noticeable degree, the distribution of subcutaneous fat either in the thigh or in
the leg when comparing the Post12 with the Post
phase.
Anthropometric Data
The subject’s right femur and tibia lengths were,
respectively, 41.0 and 40.3 cm. The quadriceps length
was 42.8 cm with individual muscles measuring 32.2 cm
(RF), 33.9 cm (VI), 35.3 cm (VL) and 36.7 cm (VM). The
total hamstring length was 41.4 cm with individual muscle lengths of 23.2, 28.8, 34.4 and 26.0 cm, respectively,
for BFSH, BFLH, ST, and SM. Finally, the TS muscle
length was 39.5 cm, made up of one long [the Sol muscle
(35.3 cm)], and two shorter [the GL and GM muscles
(23.8 and 24.6 cm, respectively)] components.
DISCUSSION
To our knowledge, the current case study is the first
systematic documentation of muscle volume and shape
changes following a complete ankle immobilization and
recovery period for all the individual muscles that constitute the ankle flexors, the knee extensors, and the
knee flexors.
Immobilization
In the present case study based on a cast-induced
ankle immobilization, we have found a disparity
between the individual muscle volume changes within
the TS as well as within the muscles indirectly affected,
including the quadriceps and hamstrings. The rate of
muscle loss was in fact 20.78%/day for the TS. Within
the quadriceps and hamstring muscle groups, the rate of
muscle loss were 20.86%/day and 20.23%/day, respectively. Tesch et al. (2004), using ULLS for 5 weeks,
found an 8.8% and a 10.5% decrease in quadriceps and
TS muscles volumes, respectively, corresponding to rates
of muscle losses of 20.25 and 20.30%/day, respectively.
Similarly, Alkner and Tesch (2004a) reported decreases
in both quadriceps and TS volumes of 10% and 16%,
respectively, after 29 days of bed rest. They report also
that the vasti muscles decreased by 10%, whilst the RF
did not change. This was unlike the events that Vanderborne et al. (1998b) report for the maximal CSA of the
TS, with a recorded 220% to 232% decrease after
8 weeks of cast immobilization (i.e., 20.36 to 20.57%/
day). Similarly, following a 17 days spaceflight, Le Blanc
et al. (2000) found a decrease in muscle volume of 10%
in the TS (20.58%/day), 6% in the quadriceps (20.35%/
day), and 3% in the hamstrings (20.17%/day). The data
in the current case study would suggest that complete
ankle immobilization may lead to a greater lost of muscle volume than the other hypoactivity models, where
whilst movements are still allowed, degree of loading is
substantially decreased.
Furthermore, compared to the previously cited studies
we have shown that the antigravity knee and ankle extensor muscles are the most affected by immobilization.
Surprisingly, we have found that ankle immobilization
leads to a relatively greater atrophy in the quadriceps
than in the TS, the latter being directly immobilized
with the ankle cast. More specifically, the present case
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GROSSET AND ONAMBELE-PEARSON
study showed that, in the TS, a greater influence of
immobilization can be seen on the gastrocnemii muscles
compared to the soleus muscle. These results would tend
to contrast with previous studies reporting that muscles
with predominantly slow muscle fibers (such as the soleus with 75% slow oxidative fibers) are more affected
than those with relatively fewer slow fibers (e.g., the
gastrocnemii, where only 55% of fibers are slow oxidative), in response to unloading (Fitts et al., 2000). For
the quadriceps muscle, as in previous studies (Akima
et al., 2001; Alkner and Tesch, 2004b; Tesch et al.,
2004), we have found that the three vastii muscles are
more affected by immobilization than the RF. The RF,
being a multijoint muscle, was less susceptible to immobilization-induced changes compared with the three
vasti muscles that only act as knee extensors. In the
current case study, similar to the events in the quadriceps muscle, in the hamstring muscle, atrophy following
immobilization is mainly confined to the only monoarticular muscle (BFSH) while the three biarticular muscles
(BFLH, ST, and SM) are less affected by unloading.
To our knowledge, the current case study is the first
systematic description of all individual muscle shape
changes for the three muscle groups involved in the
ankle immobilization (TS, quadriceps, and hamstring
muscles). As illustrated in Figs. 3–5, the regional modifications due to unloading are muscle dependent. However, the main loss of muscle volume occurs in the greatest extent around the region of peak CSA (the muscle
‘‘belly’’). Nonetheless, for a number of individual muscles
(including soleus, GL, GM, VL, VM, and BFLH) hypoactivity seems to also lead to marked changes in proximal
or distal muscle shape. The mechanisms for this lack of
uniformity in CSA losses remain to be investigated.
The causes of muscle atrophy resulting from extended
and rigid immobilization are likely to stem from a fall in
muscle protein synthesis associated with an increase in
muscle protein breakdown as previously evidenced
through (i) decreased muscle fiber CSA (Edgerton et al.,
1995), (ii) reduced fiber diameter (Widrick et al., 1999),
(iii) sarcomere dissolution and endothelial degradation
(Oki et al., 1995), (iv) reduced overall number of muscle
fibers (Kasper et al., 2002), and (v) decreased proportion
Fig. 3. Anatomical cross-sectional area (aCSA) of the three triceps
surae muscles according to the total triceps surae muscle length
before (Pre) and after immobilization (Post), and after 2 months of recovery (Post12). (A) Soleus (Sol), (B) gastrocnemius lateralis (GL), (C)
gastrocnemius medialis (GM), (D) triceps surae (TS). Q1, Q2, Q3, and
Q4 represent the four quartiles (every 25% of total muscle length). In
the soleus muscle at Post, the aCSA is not modified along the first
quartile of its length. However, the three following quartiles show
marked reductions in aCSA values compared with Pre data. At
Post12, the increase in the aCSA values seems to be located in the
second quartile with a complete recovery of the soleus aCSA. However, the first, third, and fourth quartiles are not yet back to baseline
values at that stage. In both the GL and GM muscles, immobilization
led to a decrease in aCSA throughout the length of each of the two
muscles. After 2 months of recovery, GL and GM aCSA completely
recovered, and even slightly increased over the first two quartiles. In
addition, aCSA is greatly increased in the third quartile (though still
lower than Pre data), whereas it is still at Post data values at the
Post12 phase in the last (fourth) quartile.
EFFECTS OF IMMOBILIZATION ON MUSCLE VOLUME
1679
of slow-twitch fibers (Edgerton et al., 1975). However,
the inconveniences of such immobilization treatment
may not only be focused on the decrease in the contractile element but may also result in (vi) an increase in the
intramuscular connective tissue (Oki et al., 1995), (vii) a
reduction in the number of mitochondrias (Rifenberick
et al., 1973), and (viii) a decrease in capillary density
within the muscle tissue (Jozsa et al., 1990). Hence, a
combination of some or all of the earlier changes would
lead to a loss of muscle extensibility, strength, and endurance (Kannus et al., 1992a,b) thus contributing to a
characteristically slow recovery of the skeletal muscle
fibers (Booth and Seider, 1979; Fitts and Brimmer, 1985;
Kannus et al., 1992b, 1998a,b; Kvist et al., 1995).
Recovery of Skeletal Muscle Volume and Shape
The current case study has shown substantial though
localized muscle volume recovery in the three muscle
groups of interest, following 2 months of recovery. The
most affected muscle groups by the immobilization were
both the TS and the quadriceps, as they both still
showed a degree of muscle volume deficit after the 2month recovery period. The rate of muscle growth over
the recovery period was 0.26%/day for the TS and
0.41%/day for the quadriceps surae. Different from the
aforementioned muscle groups, the hamstring muscle
group was much less affected by immobilization, was
seen to fully recover, and in fact surpassed preinjury
muscle volume at the postrecovery phase. The rate of
muscle growth was 0.16%/day for the hamstring. To our
knowledge, Akima et al. (2000) are the only authors
reporting data on muscle volume recovery using a 9- to
16-day spaceflight model. On the one hand, these
authors observed a complete recovery in knee extensor
and flexor muscles volumes after 1 month in two astronauts, and after 4 months in a third. On the other hand,
in the TS, one astronaut recovered after 1 month and
the other 2 after 4 months. Unfortunately, these authors
do report numerical data associated with the recovery.
This, however, is unsurprising as few studies to date in
fact report rates of change in CSA over a reloading
period in human models. A rare comparable example to
Fig. 4. Anatomical cross-sectional area (aCSA) of the four quadriceps muscles according to the total quadriceps muscle length before
(Pre) and after immobilization (Post), and after 2 months of recovery
(Post12). (A) Vastus lateralis (VL), (B) vastus intermedius (VI), (C) rectus femoris (RF), (D) vastus medialis (VM,) (E) quadriceps (Quad). Q1,
Q2, Q3, and Q4 represent the four quartiles (every 25% of total muscle length). After immobilization, the reduction in the VL, VI, and VM
aCSAs were localized along the entire length of each respective muscle. After the recovery period, VL aCSA was fully recovered over the
first two quartiles, was increased in the third quartile (though not back
to baseline values), and was not changed relative to Post data in the
last quartile. A similar pattern was observed in the VI aCSA within the
first three quartiles. In contrast to the VL, a slight increase in the VI
aCSA was found in the last quartile. In the VM, Post12 aCSA measurement data show a complete recovery for the first three quartiles
and no modification in the last quartile (relative to Post data). The RF
seems to be the least affected of the four quadriceps muscles, as the
only changes were observed in the third quartile with a reduction of
the aCSA between Pre and Post immobilization. A complete recovery
and even a slight increase in the RF aCSA was found after 2 months
of recovery.
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GROSSET AND ONAMBELE-PEARSON
the current case study is a case report of a cast immobilization (4 weeks nonweight bearing; 4 weeks weight
bearing) after bimalleolar fracture. The authors showed
that, after 1 month of recovery, the lateral gastrocnemius exhibited 5% greater CSA, whereas the medial
gastrocnemius and soleus muscles still showed 10%
CSA deficit, compared to preimmobilization (Vandenborne et al., 1998a). Other comparable studies have
been based on 7 weeks of cast immobilization after unilateral ankle malleolar fractures. These studies have
reported an incomplete recovery after 10 weeks of
reloading, in the CSA of the TS muscle (Stevens et al.,
2004, 2006). Lastly, Kawashima et al (2004) reported a
complete recovery of knee extensors and flexors CSA
after a 1-month reloading period, following a 20-day bed
rest period. The earlier studies are thus evidence that
data on volume changes, during a recovery period, after
cast immobilization, is in short supply.
The present case study is, to our knowledge, also the
first to report data on muscle shape changes during the
ambulatory period following a 4-week ankle immobilization. Similar to events during the immobilization period,
the recovery period led to a great variability in the muscle shape changes. Indeed, although all individual
muscles showed a trend toward returning to baseline
values after 2 months of recovery, it is notable that recovery was not uniform along the length of individual
muscles. We have found that for all individual muscles,
either the distal or the proximal region depending on
the muscle under consideration, did not in fact recover
by the end of the recovery period. The few studies concerned with muscle shape changes were conducted
alongside resistance training effects and have in fact led
to contradictory results. Indeed, whilst a greater
increase at the distal end of the VL has been reported
by Housh et al. (1992), other authors have noted greater
changes in the proximal region of this muscle (Narici
et al., 1989, 1996). Changes in muscle shape along the
Fig. 5. Anatomical cross-sectional area (aCSA) of the four hamstring muscles according to the total hamstring muscle length before
(Pre) and after immobilization (Post), and after 2 months of recovery
(Post12). (A) Biceps femoris short head (BFSH), (B) biceps femoris
long head (BFLH), (C) semitendinosus (ST), (D) semimembranosus
(SM), (E) hamstring (Ham). Q1, Q2, Q3, and Q4 represent the four
quartiles (every 25% of total muscle length). We observed no modification in BF SH aCSA data in the first quartile when comparing both
Post and Post12 to Pre values. In the other three quartiles, values
changed with immobilization but remained constant between the Post
and Post12 measurement points. In other words, the recovery period
did not affect the shape of the BF SH. The aCSA of the BF LH
decreased in the first quartile of its length after immobilization, and
retained the same degree of atrophy after the recovery period. Conversely, the next two quartiles of the BF LH aCSA increased after
immobilization and even exhibited greater levels than baseline after
the 2-month recovery period. The aCSA of the BF LH in the last quartile of the total length of the thigh was decreased after immobilization,
but recovered Pre values at the Post12 phase. Compared to all other
individual muscles, interestingly, the ST muscle showed an alteration
in the location of its maximal CSA, with the said site changing from
the third quartile to exactly the middle of the ST muscle. Finally, the
SM aCSA only slightly decreased after immobilization in the first and
last quartiles. Conversely, aCSA was increased to some degree in the
middle two quartiles. After recovery, the SM aCSA was slightly
increased compared to Post data.
EFFECTS OF IMMOBILIZATION ON MUSCLE VOLUME
1681
that the aforementioned microdamage is responsible of
the soreness express by subjects within the first few
reloading days. Dix and Eisenberg (1990) reported that
stretching muscle to a new rest length leads to the accumulation of polysomes end mitochondria at the myotendinous junctions, the appearance of nascent sarcomeres,
and elevated concentration of mRNA for myosin heavy
chain at the myotendinous junctions. These effects
would tend to explain the rapid recovery of the CSA and
muscle mass after immobilization or unloaded situation
(Bajotto and Shimomura, 2006).
Changes in Subcutaneous Adipose
Tissue Levels
Fig. 6. Anatomical cross-sectional area (aCSA) of the subcutaneous adipose tissue (SAT) measured along the length of the femur for
the thigh (in A) and along the tibia for the leg (in B), before (Pre) and
after immobilization (Post), and after 2 months of recovery (Post12).
length of the VI with training (Housh et al., 1992) are
reported as being minimal.
The origin of the skeletal muscle hypertrophy exhibited during the recovery period is likely to come from
the opposite effects to those associated with immobilization. Indeed, the main factor regulating the synthesis/
degradation of proteins in skeletal muscles has been
shown to be the increase/decrease in the mechanical
load applied to the muscular system (for a review, see
Boonyarom and Inui, 2006). Thus, the increase in load
on skeletal muscle during the recovery period after longterm complete immobilization can be assimilated to
either/both exercise training and/or mechanical stretching activities, which are known to lead to an upregulation of protein synthesis (Hornberger and Esser, 2004)
and thus to result in muscle fiber hypertrophy (Widrick
et al., 2002). However, few studies have focused on the
effects of reloading on skeletal muscles. Animal studies
have shown that muscle reloading after spaceflight (12.5
days) or hind limb suspension (2 weeks) leads to myofiber lesions (Krippendorf and Riley, 1993, 1994) and,
particularly, sarcomere damage (Krippendorf and Riley,
1994; Vijayan et al., 1998, 2001). The reloading period
has also been shown to result in an increase in hydroperoxide levels in rat soleus muscle, indicating an oxidative stress elevation (Lawler et al., 2006) as well as
inflammation, and muscle membrane damage (Nguyen
and Tidball, 2003a,b). In human subjects, it is inferred
We report here a decrease in the segmental AVILeg as
well as AVIThigh after 1-month total ankle immobilization. The opposite effect was found after the 2-month recovery period, though values still differed from preimmobilization data. The loss of adipose volume was evenly
distributed along the leg and the thigh. These results
are in contrast with the only study to our knowledge
concerned with changes in fat content in the thigh following plaster immobilization. Indeed, Ingemann-Hansen and Halkjaer-Kristensen (1977) reported unchanged
calculated fat thigh volume after 4–5 weeks of one-leg
immobilization in soccer players. However, these authors
were focusing on thigh fat and not on subcutaneous adiposity. This would explain the difference with the results
in the current study. Further investigations are therefore needed to better understand the changes in leg and
thigh adiposity after ankle immobilization.
Recommendations for Future Work
With such striking atrophy in the limbs directly in series with the cast, we would propose that, to limit immobilization effects, the recovery of the subject needs to not
only follow the standard rehabilitation protocol, but also,
immobilization protocols ought to be adapted so as to
enable a degree of exercise training. For instance, if
practitioners were encouraged to use a removable splint,
this would enable the patient to detach the contraption
for a short period every day, thus allowing them to exercise, and thus limit the process of atrophy. Indeed, it has
been shown that application of moderate stretching (30
min/day) helps prevent fiber shortening during disuse
(Williams, 1990). Furthermore, studies show that adding
small amounts of stretching/mobilization during detraining, arrests muscle atrophy in the soleus (YamashitaGoto et al., 2001; Gomes et al., 2007). In a recommendable intervention programme, exercise would initially
entail slowly and carefully moving the ankle joint in
order to provide a contractile/stretching stimulus to the
muscles. Another solution might be to use electrostimulation, during the recovery period, directly onto the
muscles of interest, with the cast/splint in situ. In either
case, exercise intensity would then be gradually
increased as recovery progresses, hence preventing/limiting atrophy.
CONCLUSION
We have systematically investigated the manner in
which both the volume and the shape of the quadriceps,
hamstring, and TS muscles change following a month-
1682
GROSSET AND ONAMBELE-PEARSON
long ankle immobilization and a 2-month recovery period. Muscle volumes changes varied extensively within
and between muscle groups. Interestingly, even though
the knee was not immobilized, the quadriceps muscle
volume was more affected by ankle immobilization than
the TS. The results of the current case study need to be
confirmed on a larger population; yet they do suggest
that knee exercises during ankle immobilization could
be used to prevent the likely marked quadriceps atrophy. Moreover, the present study suggests the importance of awareness of the localized aspect of the degree
of CSA changes. Indeed, based on our current data, we
propose that a conclusion that hyper/hypoactivity has
resulted in a seemingly nonexistent modification in CSA,
may in fact only be owing to where, along the length of
the muscle, the CSA snapshot has been taken and is
therefore not necessarily representative of what the
muscle as a whole will have experienced.
ACKNOWLEDGMENTS
The authors are indebted to Albane, without whom
this study would not have been possible.
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