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106 M. Umbrello et al.
mass than other patients [2], and skeletal muscle mass loss amounts to nearly 2% per
day during the first week of ICU admission.
Observational studies have
shown that muscle wasting is associated with a longer
ICU stay and higher ICU and hospital mortality, as well as a higher incidence of
ICU-acquired weakness in survivors [3]. Indeed, muscle wasting is one of the
greatest problems in survivors of critical illness, which contributes to muscle
weakness and, ultimately, to a low perceived quality of life and to a significant
degree of functional disability [4].
The main reason for the assessment of lean body mass is thus twofold: first, to
assess the current lean body mass of the patient as part of the diagnosis of malnutrition and thereby of risk stratification; second, to monitor the progression of muscle
loss and/or recovery during the course of the acute illness, with the aim of tailoring
supportive or rehabilitation interventions. Indeed, the finding of a low muscle mass
is a key part to the diagnosis of mal nutrition, according to the most recent GLIM
criteria [5] and European guidelines on clinical nutrition [6]. Furthermore, assessment of muscle mass should be pivotal to guide interventions such as nutrition and
physical therapy, as it seems likely that patients at higher risk will benefit the most
from metabolic/nutritional support, provided that it is delivered in the right phase of
illness [7].
In the critical care setting, conventional tools to assess muscle size and function,
such as anthropometry or functional parameters as handgrip strength are unfeasible
due to the lack of cooperation and the significant shifts in body fluids, and there is a
clear need for standardized, easily performed, non-volitional measurement tools.
The objective assessment of both muscle quantity and quality may provide a more
feasible approach to the determination of muscle health in critically ill subjects.
While there are a number of such accurate methods to quantify muscle mass and
monitor the changes over time (as bioelectrical impendance analysis (BIA), computed tomography scan (CT), or ultrasound imaging (US)), these measurements are
still seldom performed in the routine clinical practice, and there is no consensus on
the best tool to use. A recent review systematically analyzed the methods used to
assess muscle wasting in critically ill patients and found that most studies (85%)
used US, nearly all the remaining studies used CT, and only a few investigations
used other methods such as BIA or biochemical parameters. The main muscles
assessed using US were rectus femoris and more in general the quadriceps muscle,
whereas studies using CT assessed the skeletal muscle cross-sectional area at the
third vertebrae (L3) level [3]
hile promising and emerging, these tools are
. W
increasingly used in the ICU and knowledge about their advantages and limitations
is essential.
The aim of the present chapter is to describe the emerging imaging techniques as
well as their limitations, to provide the diagnostic key points for metabolic and
nutritional support.
10 Monitoring of Muscle
Mass in Critically Ill Patients 107
Computed Tomography Scan
CT scan imaging is currently considered the gold standard for the quantification of
muscle mass [8]. The amount and quality of skeletal muscles can be assessed based
on the specific radiation attenuation, a parameter which is inversely related to muscle
fat content; pre-defined radiation attenuation ranges are used to demarcate
intermuscular adipose tissue (from -190 to -30 Hounsfield units—HU) and muscle
(-29 HU to +150 HU) [9]. The analysis is generally performed on a single-slice,
cross-sectional image at the level of the third lumbar vertebra (L3). The most used
metrics are the total skeletal muscle area (SMA, in cm
area to the total muscle mass, the skeletal area indexed to the square of body height
(SMI, cm
2 /m2
) (Fig. 10.1).
The determination of circumferential skeletal muscle area or psoas muscle area,
both typically obtained at the third lumbar (L3) vertebral level, is the most studied
approach. This region contains visceral, subcutaneous, and intermuscular adipose
tissue, psoas and paraspinal muscles, transversus abdominus, external and internal
oblique abdominals, and rectus abdominus. In healthy adults, the lower reference
range for psoas wall muscle area was shown to be <22.0 cm
females, and for SMA was <112.2 cm
2
in males and <75.6 cm2 in females, with a
graded decline observed among older compared to younger adults (especially
2
) or, to better relate the muscle
2
and <11.1 cm2 in
A cross sectional computed tomography (CT) image at the third lumbar vertebra (L3) showing skeletal muscle segments. The left
side of the figure shows the muscles used to measure the Skeletal Muscle Area: the Psoas Major (PM), Quadratus Lumborum
(QL), Erector Spinae group (ESp), Transversus Abdominis (TA), Internal Oblique (IO), External Oblique (EO), and Rectus Abdominis
Fig. 10.1 A cross-sectional computed tomography (CT) image at the third lumbar vertebra
(L3) showing skeletal muscle segments. The left side of the figure shows the muscles used to
measure the skeletal muscle area: the psoas major (PM), quadratus lumborum (QL), erector spinae
group (ESp), transversus abdominis (TA), internal oblique (IO), external oblique (EO), and rectus
abdominis (RA). The right side of the picture shows the segmentation of skeletal muscle area in
yellow
(RA). The right side of the picture shows the segmentation of Skeletal Muscle Area in yellow.
108 M. Umbrello et al.
≥60 years of age) [10]. Several studies in critically ill subjects have shown that
CT-scan defined sarcopenia is a risk factor for lower 30-day survival, higher hospital
mortality, and higher complications, and a low skeletal muscle quality at ICU
admission is independently associated with higher 6-month mortality in mechanically ventilated patients [
considering the SMI was found to range from 40.8 to 55.4 for male and from
34.9 to 38.9 cm
2 /m2
11]. In critically ill patients, the cutoff for a low LBM when
for females [12]. In the same meta-analysis, CT-defined low
muscle mass was confirmed to be associated to a lower 30-day and 1-year overall
mortality. The evalua tion of muscle quality as assessed by the radiation attenuation
seems at least as important as muscle mass: a lower muscle density upon ICU
admission, independent of muscle quantity, is associated with a lower 6-month
overall survival [
Severe
muscle
11].
depletion
or
sarcopenia is one of the most common complications
of acute and chronic illnesses. Sarcopenic obesity is also prevalent, albeit scarcely
investigated, in critically ill subjects. One of the potential advantages of CT scan as
compared to conventional tools for the assessment of LBM is that it is not biased by
the fluid overload that frequently presents in critically ill patients. Despite being a
relatively new measure tool in critical illnesses, the use of CT scan to analyze
sarcopenia has been well investigated for years, both in cancer and chronically ill,
COPD subjects, and has been associated with lower overall survival, worse physical
performance and higher systemic inflammatory burden [13, 14].
Although CT is considered the gold standard method to assess body composition
[15], its use in critical ill patients is limited by the amount of radiation exposure,
costs, time, and the risk associated with patient transport to the radiology facility, to
the extent that the use of CT scan solely for the assessment of LBM is generally not
considered feasible and the analyses have been conducted on CT exams performed
for other clinical indications; moreover, for all these reasons, this tool cannot be used
for follow-up measurements. Implementation of this technique could indeed offer
several advantages for the care of critically ill patients, although newer methods with
easier availability at the bedside are emerging, as explained below.
Bioelectrical Impedance Analysis
Bioelectrical impedance analysis (BIA) is a safe, quick, and inexpensive technique
for the assessment of body composition [16
insensible, alternating sinus oidal electric current through active electrodes and the
assessment of the total impedance to the flow of the current through recording
electrodes. This method allows for the estimation of body water, fat, and muscle
mass; based on the princ iple that body water is rich in electrolytes and is therefore an
accurate current conductor, whereas body cells act as a resistor to the current flow,
and on the fact that the vast majority of body water is stored in muscles, a person
with more muscle mass has higher probability of having more body water, which
leads to lower impedance. BIA technique requires the operator to place electrodes in
which is based on the injection of an
],
10 Monitoring of Muscle Mass in Critically Ill Patients 109
the right side on conventional metacarpal and metatarsal lines and record electrodes
in standard positions at wrist and ankle. The ratio of squared body height to the total
impedance results in total body water, which is the basis for all the other, so-called
classic BIA parameters, such as lean body mass, fat mass, and intracellular and
extracellular water. However, those parameters are calculated assuming static ratios
between compartments, and a fixed hydration of ti
tion specific; this
explains the lack of specificity in critically ill subjects, to the extent
that “classic” BIA is not recommended in these patients [
ssues, and equations are popula-
17].
The measure of the phase angle (PhA) has then emerged as an alternative
technique to overcome the BIA limitations, basing its main strength on the use of
raw impedance parameters while making no assumption on body composition. In
fact, the total opposition to the current through the body (i.e., impedance, Z ) can be
divided into two main components : resistance (R), i.e., the part of impedance caused
by the opposition to the flow of the current, which is inversely related to cell mass,
and can be further divided into intracellular and extracellular resistance, and reactance (Xc), i.e., the delay to a current change due to capacitance, which depends on
cell membrane integrity and is directly related cellular mass and structure. To
simplify, resistance can be considered a measure of total body water and resistance
a measure of cell mass. The total impedance Z is calculated as follows:
2
Z =
R
þ Xc
2
When an electric current passes a cell membrane, reactance causes a time delay,
creating a phase shift between voltage and current. The phase angle describes this
difference between the voltage and the current. The phase angle is, therefore,
considered an emergent surrogate marker of both quantity and quality of muscle
mass [17] (Fig. 10.2).
A high
phase angle reflects higher cellularity and better cell membrane or
function, and is thus an indicator of cell health [18]. A recent meta-analysis has
confirmed that a low phase angle is associated with higher mortality and ICU length
of stay in critically ill patients [19]. Raw BIA parameters were shown to identify
critically ill patients with low skeletal muscle area on CT-scan, as defined by
previously found cut-offs, and BIA-derived low phase angle corresponded to low
CT-derived skeletal muscle area and density [
20].
Despite these several advantages,
some limitations can influence the accuracy, including instrument-related factors
(i.e., electrodes quality), technician-related factors (inter- and intra-operator variability) subject-related factors (i.e., supine position with each limb slightly away from
the body, after an overnight fast, and once the bladder is emptied), and environmentrelated factors (i.e., environmental temperature) [
21]. Indeed, the most common
limitation to the use of BIA in the critical care setting is the extent of fluid shift
and overhydration. Despite a correlation was consistently found between raw BIA
parameters and adverse outcome of critical illness, cut-off and reference values
remain elusive.
110 M.
Umbrello et al.
Fig. 10.2 Scheme of bioelectrical impedance analysis. Right panel: the body is composed of fat or
fat-free mass and water or water-free tissues. These different components result in different
impedances. To measure impedance, the circuit connects to two electrodes placed at the wrist and
two placed at the ankle. The human body is assumed as a conducting cylinder or, in newer devices,
as the sum of five separate cylinders. The picture shows BIA current injection and voltage
measurement.
direction of the phase angle to that of a reference population, enabling a visual interpretation of
the clinical relevance of the raw bioelectric impedance analysis values in the so-called BIVA
nomogram. The resistance R and reactance Xc are plotted as a bivariate vector. Reference values
are plotted as so-called tolerance ellipses in the coordinate system. Three tolerance ellipses are
distinguished, corresponding to the 50th, 75th, and 95th vector percentile of the reference population. Values located on the horizontal axis indicate an increase or a decrease in body cell mass,
while values located on the short axis indicate a loss of water or water retention. Lower left panel:
Body composition principles upon which the “classic,” BIA-derived estimations are based: fat-free
mass (FFM), total body water (TBW), intracellular water (ICW), extracellular water (ECW), and
body cell mass (BCM)
Upper left panel: Bioelectric impedance vector analysis relates the length and
10 Monitoring of Muscle Mass in Critically Ill Patients 111
Musculoskeletal Ultrasound
Ultrasound is increasingly being used to assess changes in muscle size and quality
over time. Advantages are the high spatial resolution, low procedural risks, absence
of ionizing radiation, and ease of use even early in the course of disease. Below we
provide an update on the most common techniques used to assess muscle mass and
quality in the critical care setting.
Respiratory Muscle Ultrasound
Respiratory muscles ultrasound includes the study of the diaphragm, accessory
inspiratory (parasternal, external intercostal, scalene, and sternocleidomastoid),
and expiratory muscles (transversus abdominis muscle, internal and external oblique
muscle) [22]. Diaphragm ultrasound is by far the more commonly used technique.
While the evaluation of diaphragm function is generally performed by the assessment of thickening and displacement, diaphragm expiratory thickness is considered
to be an indicator of central skeletal muscle mass [23]. The assessment of intercostal
muscles thickness has been recently proposed to complete the evaluation of respiratory muscles [
Diaphragm thickness represents a measure of diaphragm size obtained in the zone
of opposition. In practice, B-mode ultrasound is used with a 7.5–10 MHz linear
probe placed transversally on the late ral chest, between the eighth and tenth intercostal spaces in the mid-axillary line, in the zone of apposition of the diaphragm to
the ribcage. The image is acquired generally during tidal breathing in expiration, to
assess the relaxed expiratory thickness, which is supposed to represent the muscle
mass. The structures encountered by the ultrasound beam incl ude skin and soft
tissues, intercostal muscles (hypoechogenic), parietal and visceral pleurae
(hyperechogenic), diaphragm (hypoechogenic), and parietal and visceral peritoneum
(hyperechogenic) [
Reference v
1.1–1.4 mm in women and 1.3–1.9 mm in men [26, 27]. In general, a value of
1.73–2.19 mm at end-expiration is considered normal [28]. The position in which the
examination is performed should be kept constant, as the diaphragm appears thicker
in the upright compared to supine positions. A high reproducibility of right
hemidiaphragm measurements, and a good correlation with diaphragm electrical
activity have been found in invasively mechanically ventilated patients [29]
assessment of bilateral measures is difficult and poorly reproducible, and the right
diaphragm is easier to investigate.
Diaphragm thickening represents the contraction of the muscle during breathing
and is used to quantify the magnitude of the inspiratory effort. Diaphragm excursion
is usually assessed both via B- and M-mode ultrasonography. M-mode has the
advantage to visualize the movem ent of the diaphragm over the respiratory cycle
24].
25] (Fig. 10.3).
alues f
or end-expiratory thickness in healthy volunteers are about
. T
he
112 M. Umbrello et al.
Fig. 10.3 Ultrasonographic assessment of diaphragm thickness and thickening. Left panel: ultrasonographic assessment of the diaphragm in the zone of opposition using a 7.5–10 MHz linear
probe. Right panel: view in B-mode (upper) and M-mode (lower) of the diaphragm thickness. In
both modalities, the probe is placed in plane with an intercostal space between the eighth and the
tenth rib. Diaphragm thickness is measured at end inspiration and end expiration and the thickening
fraction is calculated according to the formula: TF = (T
EI-TEE
)/T
EI
× 100
[25]. The thickening fraction is calculated as the difference between thickne ss at end
inspiration and end expiration divided by the end-expiratory thickness ×100. Abnormal thickening has been defined as a fraction of less than 20%. The percentage of
thickening during normal breathing is around 30% and 35% on both sides in healthy
men and women [27] while around 11% in mechanically ventilated subjects [29].
Limb Muscles
The most common site for muscle ultrasound is the rectus femoris: this muscle is
easy to identify and to analyze with a single image, and is considered a functionally
important muscle for the performance of daily living while at the same time is
subject to significant wasting during bed rest and illness, more than muscles of the
upper limbs [30]. This technique allows for the assessment of both muscle mass
(thickness or cross-sectional area (CSA)) and quality (echodensity), as well as an
estimate of the muscle force-generating capacity (the pennation angle).
Rectus femoris ultrasound is generally performed using a high-frequency, linear
transducer array probe (8–12 MHz), using the B-mode setting. Briefly, patients are
studied in the semirecumbent position with extended knees; the probe is placed on
the anterior part of the thigh, at 1/2 or 2/3 of an imaginary line connecting the
anterior superior iliac spine and the midpoint of the proximal border of the patella. A
10 Monitoring of Muscle Mass in Critically Ill Patients 113
mark can be drawn on the skin to increase reproducibility of subseq uent measurements. The transducer is oriented transverse to the longitudinal axis of the thigh at a
90° angle; the probe is coated with water-soluble transmission gel to increase the
acoustic contact and care is taken to reduce as much as possible the pressure on the
tissues and the consequent distortion of the image. Typical values of quadriceps
thickness and rectus femoris CSA in healthy volunteers have
2.6 cm and between 4.53 and 8.68 cm
2
[31, 32], respectively. On the other side, in
critically ill patients, average values at ICU admission have ranged between 0.98 and
2.23 cm for quadriceps thickness and from 2.26 to 4.42 cm
been reported to be
2
for rectus femoris CSA
[33, 34]. Such widely scattered values depend on the lack of a universally standardized technique for muscle ultrasound.
Information about muscle compo
sition can be gathered by quantification of
muscle echodensity, which is calculated by performing grey-scale analysis of
image pixels using standard softwares for image editing. This process has been
shown to correlate with bioptic findings, as it reflects the muscle composition: an
increased echogenicity represents a more homogenous muscle [35]. Quantification
of muscle echodensity requires exporting the muscle ultrasound scan as a digital
image file for subsequent, offline computer analysis, and the absolute value of
density of the image critically depends on the settings which the image was acquired
with. Changes in quadriceps muscle echodensity have been associated with negative
outcomes [34].
Eventually, muscle architecture can be described by the pennation angle, i.e., the
angle of insertion of muscle fibers into their aponeurosis, which provides information about muscle strength: the larger the pennation angle, the more contractile
material is present, and thus the higher is the capacity to produce force [36]. The
rectus femoris pennation angle is measured with the same method and in the same
position of muscle area and thickness; a longitudinal view is obtained by rotating the
probe parallel to either the lateral or medial head of the muscle. Few studies
investigated the pennation angle in critically ill subjects; in healthy subjects, the
average pennation angle of the rectus femoris has been reported to range from
8.76 ± 1.78 to 17.5 ± 3.9° [32]. In critically ill patients at ICU admission, the
pennation angle was 10.8 ± 2.6° [37], and an angle <4.4° was found to be associated
with a worse outcome [38] (Fig. 10.4).
It i
ell known how limb muscle size, structure, and function deteriorate during
s w
the course of ICU stay, by approximately 3% per day in the first week of ICU stay
[2]; US findings of reduced rectus femoris CSA were found to be associated with
poor clinical outcomes [39]. Using CT-scan as the reference method to define low
muscle mass, a cut off value of <2 cm for quadriceps muscle layer thickness and a
rectus femoris CSA of <4.7 cm
2
were found [40]. However, several limitations have
to be taken into careful account when using specific cutoffs for muscle US, specifically the lack of external validation in the majority of the studies, and the lack of
standardization as for the site of measurements.
The use
of US to measure muscle mass has consistently been found to be reliable
and associated with excellent inter- and intra-rater coefficients; feasibility, defined as
the percentage of measurements that are obtainable, ranges from 75% to 100%
114 M. Umbrello et al.
Fig. 10.4 Ultrasonographic assessment of the quadriceps muscle. Left panel: the image shows the
standardized level of the ultrasound scan of the lower limb; in the supine position, the linear probe is
placed on the anterior part of the thigh, at 2/3 of an imaginary line connecting the anterior superior
iliac spine (ASIS) and the midpoint of the proximal border of the patella, with the probe perpendicular to the muscle. Upper right panel: the picture shows a longitudinal scan of the quadriceps
muscle; the pennation angle is measured at the intercept of the fascicular path (dashed line) to the
lower aponeurosis (solid) line. Lower middle panel: the figure shows a transverse scan of the
quadriceps muscle, which is composed by three vastus muscles (medialis, intermedius, and
lateralis) and the rectus femoris; the red dashed line represents the rectus femoris cross sectional
area, the double-arrow line depicts the quadriceps muscle layer thickness. Lower right panel: the
diagram shows the grayscale histogram in a transverse axis of the rectus femoris. VI vastus
intermedius, VM vastus medialis, VL vastus lateralis
[2, 41]. A longitudinal validation study assessed the intra- and inter-observer
reliability of muscle ultrasound at two measurements sites: on the midpoint or on
the two-thirds of the length between the anterior superior iliac spine and the upper
border of the patella. Intra- and inter-observer reliability coefficients were 0.74 and
0.76 at the “midpoint” and 0.83 and 0.81 at the “two-thirds” site, respectively,
showing how the method is reproducible, with a higher reliabil
33]
site [
.
A wide range of
studies showed a negative correlation between US-assessed
ity at the two-third
muscle size and quality and ICU length of stay or mortality. A significantly higher
reduction of muscle mass was shown in critically ill non-survivors, together with a
significant increase in muscle echo-density over the first week of stay, again of a
higher extent in non-survivors. Interestingly, the change in rectus femoris area was
related to the cumulative protein deficit over the first week of ICU stay, suggesting
how changes in muscle size and quality seem related to the outcome of critically ill
patients, and to be influenced by nutritional management strategies [
42].
Muscle
ultrasound has also shown to be an early predictor of physical disability, as the
change in rectus femoris CSA over the first week of ICU stay is a strong predictor of
muscle weakness at hospital discharge [34] and the loss of pennation angle during
10 Monitoring of Muscle Mass in Critically Ill Patients 115
the first week of ICU stay predicts the subsequent development of ICU acquired
weakness [37].
A potent ial advantage of muscle ultrasound, as compared with other
methods for
the assessment of lean body mass, such as bioelectrical impedance, is that it can be
less dependent on body hydration state [43]. The literature seems consistent in the
utility of rectus femoris ultrasound (especially the cross-sectional area at the lower
third of the thigh) to track the loss of muscle mass and possibly muscle function and
as a mark er of severity of illness and possible negative outcome. However, so far, no
unanimous cutoffs to define sarcopenia or an increased risk of mortality have
convincingly been reported, and the relationship of muscle ultrasound with nutritional or physical intervention, despite promising, is yet to be demonstrated. Part of
this uncertainty strictly depends on the variability in probe settings, and position, and
a shared, standardized protocol is needed.
Conclusions
Prolonged bed rest diminished nutritional intake, and the catabolic response associated with critical illnesses contributes to a decline in muscle size and function.
Research has demonstrated that a low muscle mass and quality upon ICU admission
can prolong the duration of ICU stays and lead to complications. Despite the
availability of various tools to assess lean body mass, their utilization in critical
illness remains limited. Future research is needed to evaluate the utility of these tools
more effectively in critical care and explore their potential as targets for specific
interventions.
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