Clinical review: peripheral muscular ultrasound in the ICU

Abstract

Muscular weakness developing from critical illness neuropathy, myopathy and muscle atrophy has been characterized as intensive care unit-acquired weakness (ICUAW). This entity occurs commonly during and after critical care stay. Various causal factors for functional incapacity have been proposed. Among these, individual patient characteristics (such as age, comorbidities and nutritional status), acting in association with sustained bed rest and pharmacological interventions (included the metabolic support approach), seem influential in reducing muscular mass. Long-term outcomes in heterogeneous ICUAW populations include transient disability in 30% of patients and persistent disabilities that may occur even in patients with nearly complete functional recovery. Currently available tools for the assessment of skeletal muscle mass are imprecise and difficult to perform in the ICU setting. A valid alternative to these imaging modalities is muscular ultrasonography, which allows visualization and classification of muscle characteristics by cross-sectional area, muscle layer thickness, echointensity by grayscale and the pennation angle). The aim of this narrative review is to describe the current literature addressing muscular ultrasound for the detection of muscle weakness and its potential impact on treatment and prognosis of critically ill patients when combined with biomarkers of muscle catabolism/anabolism and bioenergetic state. In addition, we suggest a practical flowchart for establishing an early diagnosis.

Keywords: ICU-acquired weakness; Muscle cross-sectional area; Muscle echointensity; Muscle layer thickness; Pennation angle; Peripheral muscular ultrasound; Skeletal muscle.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1

Ultrasound distinctive appearance of muscle tissue. The figure shows a transverse (a) and longitudinal (b) ultrasound scan of elbow flexor (bicep brachialis) in healthy (1) and long-term ICU (2) subjects. In the axial image, muscle consists of primarily hyper-echogenic areas scattered with small bright curved echoes of superficially random orientations. In the sagittal plane, these bright echoes are seen to be the fibrous tissue that surrounds muscle fibers and fascicles and which organize into recognizable striations. In bipennate or multi-pennate muscles, a central aponeurosis can be identified as an area of thickened fibrous tissue that when followed distally becomes the tendon. Bone is highly echogenic with a deep shadow beneath the bright hard edge. Subcutaneous fat is typically of similar echogenicity to muscle and is interposed with brighter, poorly organized strips of connective tissue. Near the myotendinous junction, the myofascial fibrils merge, resulting in increased echogenicity and higher anisotropy. In the healthy tissue, the hyper-echogenic muscle is interspersed with bright fibro adipose tissue and the bone reflection is bright and sharply defined; in the long-term ICU patient, the muscle tissue appears as non-homogenous and reduced in its mass

Fig. 2

Muscle cross-sectional area. This figure depicts the cross-sectional area of the rectus femoris perpendicular to its longitudinal axis. The quadriceps femoris is a group of muscles composed by three vastus muscles (medialis, intermedius, and lateralis) and the rectus femoris which presents a proximal insertion in the anterior inferior iliac spine and other insertion in the supra-acetabular sulcus. Left side: standardized level of ultrasound scan of the lower limb; in the supine position, the probe should be placed at 2/5 of an imaginary line between the anterior parts of the thigh from the anterior inferior iliac spine to the midpoint of the proximal border of the patella. Right side: the figure depicts the cross-sectional area (red circle) of the rectus femoris (RF) perpendicular to its longitudinal axis. VI vastus intermedius, VM vastus medialis, VL vastus lateralis

Fig. 3

The muscle layer thickness detected by ultrasound. Quadriceps femoris detected by ultrasound in a transverse scan. The rectus femoris (RF) layer thickness and vastus intermedius (VI) are represented (red lines). VM vastus medialis, VL vastus lateralis

Fig. 4

The muscle ultrasound echointensity. An example of the grayscale histogram in the transverse (right) and longitudinal (left) axis of the rectus femoris

Fig. 5

The muscle ultrasound pennation angle. The figure represents a longitudinal view of quadriceps rectus femoris muscle. The pennation angle is calculated between the intercept of fascicular path to the lower aponeurosis. Additionally, the muscle length can be measured. These two variables may be used to determine the strength of the muscle, as the lower is the angle, the lower is the length, and the lower is the strength. The right panel represents a representative reduction in pennation angle after 1 week of ICU stay

Fig. 6

The muscle ultrasound flowchart for the assessment and minimization of ICUAW. This flowchart suggests a protocol for logical and early identification of ICUAW. Ideally, within the first 48 h, a first muscle ultrasound assessment should be performed for a baseline picture of patient muscle characteristics (the evaluation should at least regard the quadriceps rectus femoris, and it may be “omni-comprehensive” of muscle thickness (TH), cross-sectional area (CSA), echointensity (if the operator is familiar with any image editing software), pennation angle. At the same time, the cognitive impairment should be evaluated using standard reproducible scales (such as the Richmond agitation sedation scale and the confusion assessment method for the ICU). If these scores are in the normal range, the application of manual muscle testing such as the medical research council scale is possible. These first evaluations might be reconsidered within the first 7–10 days after the admission in the ICU, and their modifications over time, integrated with each other as well as with the reevaluation of MRC scale, allow an accurate diagnosis of ICUAW and should be used to modify the different patient-dependent factors, such as pharmacological strategies, muscular overloading or inactivity, and metabolic derangements. RASS Richmond agitation sedation scale, CAM-ICU confusion assessment method for the ICU, ICU intensive care unit, MRC Medical Research Council scale, TH muscle thickness, CSA cross-sectional area, ICUAW ICU-acquired weakness