Muscle wasting in intensive care patients: ultrasound observation of the M. quadriceps femoris muscle layer.

Abstract

Patients in intensive care exhibit a high degree of loss of muscle mass. Appropriate instruments are needed to document muscle wasting in these patients. The aim of this pilot study was to describe muscle wasting in patients in the intensive care unit.
Two-fold study setting: prospective longitudinal and cross-sectional single-blind.
A total of 118 patients in the intensive care unit (length of stay 1-98 days; male:female ratio 88:30; age 55 +/- 17 years) were included in a two-fold study setting.
Muscle layer thickness of the M. quadriceps femoris was documented using ultrasound measurement at well-defined points. Seventeen pilot-patients were measured twice; at baseline and after 28 days. In another group of 101 patients, muscle layer thickness was determined once after a random length of stay. The results of both groups were compared and correlated.
In both groups, M. quadriceps femoris thickness showed a significant negative correlation with length of stay in the intensive care unit (p < 0.01). Furthermore, muscle wasting in intensive care patients could be described using a logarithmic function.
Loss of muscle mass shows a negative correlation with length of stay, and seems to be higher during the first 2-3 weeks of immobilization/intensive care unit stay. Ultrasound is a valid and practical measurement tool for documenting muscle mass (e.g. muscle layer thickness) as part of the daily routine at an intensive care unit.

Full text

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ORIGINAL REPORT
J Rehabil Med 2008; 40: 185–189
J Rehabil Med 40
Journal Compilation © 2008 Foundation of Rehabilitation Information. ISSN 1650-1977
© 2008 The Authors. doi: 10.2340/16501977-0139
Objective: Patients in intensive care exhibit a high degree of
loss of muscle mass. Appropriate instruments are needed to
document muscle wasting in these patients. The aim of this
pilot study was to describe muscle wasting in patients in the
intensive care unit.
Design: Two-fold study setting: prospective longitudinal and
cross-sectional single-blind.
Patients: A total of 118 patients in the intensive care unit
(length of stay 1–98 days; male:female ratio 88:30; age 55 ±
17 years) were included in a two-fold study setting.
Methods: Muscle layer thickness of the M. quadriceps femoris
was documented using ultrasound measurement at well-de-
fined points. Seventeen pilot-patients were measured twice;
at baseline and after 28 days. In another group of 101 pa-
tients, muscle layer thickness was determined once after a
random length of stay. The results of both groups were com-
pared and correlated.
Results: In both groups, M. quadriceps femoris thickness
showed a significant negative correlation with length of stay
in the intensive care unit (p < 0.01). Furthermore, muscle
wasting in intensive care patients could be described using a
logarithmic function.
Conclusion: Loss of muscle mass shows a negative correla-
tion with length of stay, and seems to be higher during the
first 2–3 weeks of immobilization/intensive care unit stay.
Ultrasound is a valid and practical measurement tool for
documenting muscle mass (e.g. muscle layer thickness) as
part of the daily routine at an intensive care unit.
Key words: muscle wasting, intensive care, diagnostic ultra-
sound, muscle layer thickness.
J Rehabil Med 2008; 40: 185–189
Correspondence address: Richard Crevenna, University Depart-
ment of Physical Medicine and Rehabilitation, Medical Univer-
sity of Vienna/MUW, Währingergürtel 18-20, AT-1090, Vienna,
Austria. E-mail: richard.crevenna@meduniwien.ac.at
Submitted December 31, 2006; accepted September 20, 2007.
INTRoDuCTIoN
Critically ill patients exhibit a dramatic loss of lean body mass,
particularly skeletal muscle, irrespective of the adequacy of
nutritional support (1–4).
Muscle wasting is one of many common problems patients
in intensive care unit (ICu) have to deal with. These problems
have been specified in detail using the International Classifica-
tion of Functioning, Disability and Health (ICF) (5–9).
Skeletal muscle wasting in the critically ill is often masked
by fluid retention. In these circumstances the normal anthro-
pometric methods of assessing changes in body mass and
composition are not applicable, as the techniques all assume a
normal state of hydration (10). until recently, the only methods
that reliably measure wasting of lean tissue in critically ill
patients with presence of severe fluid retention have been in
vitro neutron activation analysis (IVNAA) (11) or assessing
changes in muscle fibre area using repeated muscle biopsies
(12–15). The former involves radiation and is not generally
available, and the latter is invasive and time-consuming. Both
methods can only really be used in research settings. Therefore,
a simple, non-invasive, clinically applicable method is needed
to assess rates of muscle wasting during critical illness in the
presence of severe oedema.
Strength measurement is not feasible at the intensive care
unit (ICu) for documenting muscle wasting, but there is a
proven relationship between strength and muscle thickness
of the human quadriceps femoris muscle (16, 17). To evalu-
ate the physiological muscle morphology of human thigh and
leg muscles, several similar imaging techniques, such as
computerized tomography (CT), magnetic resonance imag-
ing (MRI) or ultrasound, can be employed (18–21). Muscle
wasting has been observed by means of ultrasound after bed
rest, immobilization after operation, and in adults with severe
cerebral palsy (22–27).
Muscle wasting in patients in the ICU is a recent field of
research and, as yet, there is a lack of published data (28–30).
To our knowledge, there is no published clinical research docu-
menting changes in muscle mass and morphology in patients
in the ICu during immobilization over a median time-period
of 7 days.
The purpose of the present study was: (i) to measure muscle
wasting in patients in the ICu over a period of 28 days; (ii) to
determine whether a relationship could be identified between a
representative population of patients in the ICu and their length
of stay (LoS) at an ICu; and (iii) to verify whether ultrasound
measurements are a valid and practical measurement tool to
MuSCLE WASTING IN INTENSIVE CARE PATIENTS: uLTRASouND
oBSERVATIoN oF THE M. QuADRICEPS FEMoRIS MuSCLE LAYER
Wolfgang Gruther, MD1, Thomas Benesch, MS2, Carina Zorn, PhD1, Tatjana Paternostro-
Sluga, MD1, Michael Quittan, MD1, Veronika Fialka-Moser, MD1, Christian Spiss, MD3,
Franz Kainberger, MD4 and Richard Crevenna, MD1
From the 1Departments of Physical Medicine and Rehabilitation, 2Medical Statistics, 3Anaesthesia and Intensive Care
and 4Radiology and Osteology, Medical University of Vienna – MUW, Vienna, Austria

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W. Gruther et al.
document muscle mass (e.g. muscle layer thickness (MLT))
in daily routine in these patients.
METHoDS
All the procedures described in this study were approved by the local
ethics committee (number 037/2004) and informed consent was ob-
tained from all patients or proxy. The study was conducted at the ICu
– Department of Anesthesiology and Intensive Care, General Hospital
of Vienna, Medical university of Vienna, Austria.
Study design
It is difficult to establish a study in an ICU to observe patients over
several weeks due to the high turn-over and morbidity of these pa-
tients. Therefore, a “two-fold” study setting (group A, B) was chosen
to document muscle wasting (e.g. loss of MLT) over several weeks,
avoiding any selection bias.
In a prospective longitudinal setting (group A) muscle wasting of
pilot patients (n = 17) was documented: (i) at “baseline” (starting with
the next day after their referral to the ICu); and (ii) after 28 days.
In a cross-sectional setting (group B), muscle wasting of a larger
group of patients (n = 101) was determined only once, but after dif-
ferent time periods (after their referral to the ICu) to describe MLT
at variable lengths of stay.
To our knowledge there are no published data concerning the effect
size of muscle wasting in patients treated for a long time in the ICu,
which could be used for a sample size calculation.
Study population
In the year 2004, 968 patients transferred to the ICu of the general
hospital of Vienna had a LoS longer than 7 days and survived their
critical diseases (dismissed and deducted patients in 2004, annual
report entire General Hospital of Vienna).
A total of 125 patients (88 men and 30 women, aged 55 ± 17 years)
on a standard drug treatment were included in a two-fold study setting
during 2004. A total of 118 patients completed the study (Table I).
Exclusion criteria were: a stay at the ICu shorter than 28 days for
group A and shorter than 7 days for group B; age less than 19 years;
neuromuscular disorders or critical illness neuropathy; and patients
with cancer treated with a palliative intention.
Outcome measurements
MLT of the M. vastus intermedius and M. rectus femoris were docu-
mented using high-resolution ultrasound. In group A, MLT of 17 pa-
tients was measured twice, at baseline (after a random LoS) and after
28 days. In group B, MLT of 101 patients was determined only once
(after a random LoS). The results of both groups were compared and
correlated with demographic and clinical data.
To detect muscle wasting, MLT of the quadriceps femoris muscle (M.
vastus intermedius and M. rectus femoris) was measured by high-reso-
lution real-time ultrasonography at well-defined points, as described in
other studies (22, 24, 25). MLT of the M. vastus intermedius and M. rectus
femoris was assessed bilaterally: (i) at the border between the lower and
upper two-thirds, and (ii) at the mid-point between the anterior superior
iliac spine and the upper pole of the patella, with the patient in a supine
position and the legs relaxed lying flat in extension. Mean MLT was
calculated by mean of the 2 measurements (measuring points (i) and (ii))
on each leg. The coefficient of variation for a single MLT measurement
is close to the 3% obtained in other studies (23, 30). MLT measurement
used in the present study improves the coefficient to 1.3% (23).
All ultrasound examinations were performed by the same operator,
who was blinded to the data analysis, with a portable ATL ultrasound
system (HDI-1000, ATL©, Bothell, uSA), using a L7-4 transducer
with a 5-cm linear array footprint.
For supplementation of the MLT measurements, the circumference
of the thigh was assessed with a tape measure bilaterally between the
2 previously-defined ultrasound measuring points.
Statistics
Data from all patients were analysed with the Statistical Package
for Social Sciences (SPSS 13 for Windows). Descriptive statistics
were calculated and presented as mean (± standard error of the mean
(SEM)) as appropriate. A correlation matrix was generated to assess
the degree of correlation among the variables (sex, age, height, weight,
body surface, thigh circumference, MLT, MLT difference after 28 days
at the ICU (MLTD), LOS). Pearson’s product-moment coefficient of
correlation was used for parametric data. Stepwise multiple regression
analysis was performed to identify dependent variables on MLT. Curve
estimation for best-fit was used to describe MLTD with respect to LOS
at the ICu. Null hypothesis was rejected when p < 0.05.
RESuLTS
Group A
In 17 patients, ultrasound representations of MLT in both legs
separately were characterized by a decrease in 27 thighs and
by an increase in 7 thighs (Fig. 1).
Correlation analysis showed a high significant negative cor-
relation between MLT of the right (p = 0.005) and left thigh
(p = 0.004), MLTD for the right (p = 0.006) and left thigh
(p = 0.003) and LoS at the ICu at baseline measurement. Height
Table I. Baseline characteristics of patients in intensive care units in
group A and B.
GroupAB
Sex (m/f)
Age (years), mean (SD)
Height (m), mean (SD)
Weight (kg), mean SD)
Body surface (m²), mean (SD)
Main diagnosis
Polytrauma
Cardiovascular
Transplantation
Pneumonia
Cancer
Abdominal disorders
Wound infection
other diseases
Incomplete (death/transfer)
SD: standard deviation.
14/3
55 (17)
1.74 (0.12)
84 (21)
2.02 (0.3)
74/27
55 (15)
1.76 (0.9)
81 (17)
2 (0.25)
5
4
2
3
2
1
–
–
5/2
29
23
8
12
14
9
4
2
–
Fig. 1. Muscle layer thickness changes in group A, from the first (after
a random length of stay) to the second measurement (after 28 days) in
both thighs.
0
1
2
3
4
5
6
0 10 2030 4050607080 90100
days
cm
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Muscle wasting in intensive care patients
revealed a high significant negative correlation (p = 0.003), and
age a significant positive correlation (p = 0.011) with LoS.
Thigh circumference, sex, weight and body surface did not cor-
relate with LoS at the ICu at baseline measurement.
Stepwise multiple regression analysis showed that LoS at
the ICu at baseline measurement was the only variable with
an influence on MLTD on the right (p = 0.006) and left thigh
(p = 0.003).
Group B
In 101 patients the correlation analysis showed a high signifi-
cant negative correlation between MLT of the right (p < 0.0001)
and left thigh (p < 0.0001) and LoS at the ICu at baseline
measurement. Thigh circumference of both legs revealed a
high significant negative correlation (p = 0.003) with LoS.
Age showed a high significant positive correlation (p = 0.001)
with LOS. Height revealed a significant negative correlation
(p = 0.031) with LoS. Sex, weight and body surface did not
correlate with LoS at the ICu at baseline measurement.
Stepwise multiple regression analysis showed that LoS at
the ICu at baseline measurement (p < 0.0001) and thigh cir-
cumference (p = 0.006) were the only variables that influenced
MLT on the right thigh.
Influences on MLT on the left thigh were LOS at the ICU
at baseline measurement (p < 0.0001), thigh circumference
(p < 0.0001) and height (p = 0.016).
Additional calculations (multiple regression analyses) to
study the effects of height on LoS while controlling the age
effect were performed. No effects were found.
Curve estimation for best fit revealed that the logarithmic
function fits best to MLT of both thighs with respect to LOS
at the ICu (Fig. 2).
DISCuSSIoN
To summarize, muscle mass losses of the M. vastus intermedius
and M. rectus femoris show a correlation with LoS at the ICu.
Muscle mass losses during the first 2–3 weeks of stay in the
ICu are considerably higher than in all other patient collectives
examined. There are differences concerning speed of muscle
wasting in the patients during their stay. Muscle wasting can be
described best by using a logarithmic function. MLT measuring
is more suitable for muscle atrophy documentation than size
quantification with a measuring tape.
This study aimed to determine whether real-time ultrasound
could provide quantitative data that: (i) elucidates muscle wast-
ing in MLT of the M. vastus intermedius and M. rectus femoris
of the patients over a period of 28 days; and (ii) determines
whether a relationship can be identified between a representa-
tive population of patients and their LoS at an ICu.
Establishing a study setting on an ICu observing patients
over several weeks is difficult because of the high turn-over and
morbidity of these patients. To solve this problem, a two-fold
study setting was chosen to limit drop-out rates, to be able to
document muscle wasting over several weeks and to calculate
a realistic model of a whole ICu population.
As outlined in the introduction, muscle wasting in patients
in ICU is a recent field of research. To our knowledge there
is only one study, which documented muscle wasting using
an imaging technique in an usual ICu setting. Reid et al. (30)
demonstrated an ultrasound technique for documenting muscle
wasting at 3 different muscle groups.
Imaging techniques for studying and measuring muscle
mass in vivo have included MRI and ultrasound (25, 31–33).
Recent studies compared these imaging techniques and found
no significant differences between them in measurements of
muscle mass (18–20).
Examination of muscle wasting in patients in ICu with ultra-
sound was chosen because it is more practicable and feasible
than using CT or MRI on an ICu and overcomes many of the
problems associated with anthropometric and body composi-
tion measurements (10). Several measuring parameters have
been described for documenting muscle mass with ultrasound
(16, 25, 26). In the present study MLT of the M. quadriceps
femoris was used for documenting muscle wasting because:
(i) it is well described (22–27) and easy to determine even in
highly reduced muscle architecture; (ii) M. quadriceps femoris
is important in the remobilization process because it flexes the
hip and extends the knee simultaneously (34) while standing
up; and (iii) there is a proven relationship between strength
and muscle thickness of the human quadriceps femoris muscle
(16, 17).
The present study shows that real-time ultrasound was
indeed useful in quantifying configurational changes of the
M. quadriceps femoris architecture. Muscle wasting in MLT
of the M. vastus intermedius and M. rectus femoris showed a
high significant correlation with the LOS at the ICU in both
groups A and B. Stepwise multiple regression analysis showed
that LOS at the ICU was the only variable with an influence
on MLTD in both groups.
As outlined before, a two-fold study setting is needed to
detect muscle wasting in these patients over a period of at
least 28 days, and to calculate a realistic model of a whole
ICu population. using only one group of patients, with a fixed
Fig. 2. Example of curve estimation: muscle layer thickness of the right
thigh in group B with respect to the length of stay at the intensive care
unit at baseline measurement.
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W. Gruther et al.
time period of 28 days between the MLT measurements, would
have led to an election bias including only patients with an
expected stay of several weeks.
The exact underlying mechanisms of muscle mass losses
are still unknown (2–4, 30). Studies that examined changes in
body mass and composition in these patients observed a loss
of lean tissue (MLT) or protein loss from skeletal muscles
(2–4, 30).
In the present study, the observed muscle mass losses dur-
ing the first 2–3 weeks in ICU were similar to those described
by Reid et al. (30), but considerably higher than in all other
patient collectives or healthy subjects in bed rest experiments
(22–27, 35) examined using ultrasound. Reid et al. (30) showed
that energy balance probably made no apparent difference to
the rate of lean tissue loss, and implies that energy balance
makes no difference to the rate of muscle wasting. Related
to the presented data, the enormous rates of muscle wasting
in these patients cannot be explained by bed rest at the ICu
alone, and appear to be a main consequence of the disease
and its treatment.
In contrast to the findings of Reid et al. (30), differences in
the speed of muscle wasting in patients during their stay at an
ICu were found in the presented study. Muscle mass losses in
MLT of the M. vastus intermedius and M. rectus femoris can
be described best by a logarithmic function. Reid et al. docu-
mented muscle wasting in patients in an ICu over a time period
of between 5 and 39 (median 7) days. The observation period
was much smaller than in the present study (group A: 1–60
days, mean 15 days; group B: 1–98 days, mean 24 days) and
long-term effects could not be observed by Reid et al. (30).
In the present study, no correlation could be found in group
A between thigh circumference measurement and LoS. In
group B, thigh circumference showed a correlation with LoS
at the ICu. We found 3 possible explanations: (i) muscle mass
in group A was documented after a shorter LoS because of the
study setting (2 measurements, at baseline and after 28 days).
The patients show oedemas more often at the beginning of
their stay at an ICu because of their positive water balance.
(ii) Group B was a larger group of patients. (iii) Patients in
group A suffered from more severe diseases then the patients
in group B because of different exclusion criteria (group A:
LoS ≤ 28 days; group B: LoS ≤ 7 days).
Surprisingly, height showed a significant negative correlation
and age a significant positive correlation with LOS in group
A and B in the present study. Furthermore, additional calcu-
lations (multiple regression analyses) to study the effects of
height on LoS while-controlling the age effect did not reveal
any effects of height on LoS. A possible explanation could be
that younger patients are on average taller than older patients,
recover faster and are earlier transferred.
Limitations of the present study include: (i) the patients
received a lot of different pharmaceuticals during their stay,
some of which may have effects on muscle wasting (29). Be-
cause of the mixed population of acute and chronic patients
in the present study it was not possible to make a correlation
between drug intake and muscle mass loss. (ii) The purpose of
the present study was to describe a reliable model of muscle
wasting in acute and chronic ICu patients during their stay at
the ICu. It was not possible to say which patients with less
MLT had less MLT before the onset of their illness and which
had less MLT because they had already lost it as a result of
their illness and before admission to the study. (iii) Strength
measurements are not feasible at the ICu for documenting
muscle wasting. The present study cannot draw any conclusions
about muscle strength in the patients in ICu, although there is
a proven relationship between strength and muscle thickness
of the human quadriceps femoris muscle (16, 17).
In conclusion, ultrasound seems to be a valid and practi-
cal measurement tool for use in daily routine at the ICu for
documenting muscle mass (e.g. MLT). Further studies are
required to identify the main factors involved in muscle wast-
ing, particularly since muscle mass loss is more distinctive in
ICu patients than in other patient populations. Further research
is also needed to establish rehabilitation options for patients
in intensive care in order to minimize muscle wasting during
their stay at the ICu.
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