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Ultrasound assessment of muscle mass has potential to identify patients with low muscularity at intensive care unit admission: A retrospective study

Arai, Yuta Nakanishi, Nobuto Ono, Yuko Inoue, Shigeaki Kotani, Joji Harada, Masafumi Oto, Jun 神戸大学

2021.10

概要

Background & aims: Muscle mass is an important biomarker of survival from a critical illness; however, there is no widely accepted method for routine assessment of low muscularity at intensive care unit (ICU) admission. We hypothesize that ultrasound-based partial muscle mass assessments can reflect the trunk muscle mass. Therefore, we aimed to investigate whether ultrasound muscle mass measurements could reflect trunk muscle mass and identify patients with low muscularity. Methods: We performed a retrospective analysis of prospectively obtained ultrasound data at ICU admission. We included patients who underwent computed tomography (CT) imaging at the third lumbar vertebra (L3) within 2 days before and 2 days after ICU admission. Primary outcomes included the correlation between the femoral muscle mass measurements using ultrasound and the cross-sectional area (CSA) at L3 obtained by CT. Low muscularity was defined as a skeletal muscle index of 36.0 cm2/m2 for males and 29.0 cm2/m2 for females. Secondary outcomes included the correlation with the ultrasound measurements of the biceps brachii muscle mass and diaphragm thickness. Results: Among 133 patients, 89 underwent CT imaging, which included the L3. The patient mean age was 72 ± 13 years, and 60 patients (67%) were male. The correlation between the femoral muscle ultrasound and CT was ρ = 0.57 (p < 0.01, n = 89) and ρ = 0.48 (p < 0.01, n = 89) for quadriceps muscle layer thickness and rectus femoris muscle CSA, and these had the discriminative power to assess low muscularity, with the areas under the curve of 0.84 and 0.76, respectively. The ultrasound measurements of the biceps brachii muscle mass and diaphragm thickness were correlated with CT imaging [ρ = 0.57–0.60 (p < 0.01, n = 52) and ρ = 0.35 (p < 0.01, n = 79)]. Conclusions: Ultrasound measurements of muscle mass were correlated with CT measurements, and the measurements of femoral muscle mass were useful to assess low muscularity at ICU admission.

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参考文献

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Figure Legends

Figure 1. Flowchart of patients included in this study.

Among the 133 patients screened, 89 underwent computed tomography (CT) examinations at the

level of the third lumbar vertebra. Secondary outcomes included the ultrasound assessments of the

biceps brachii (n = 52) and diaphragm muscles (n = 79) (CT, computed tomography; L3, third

lumbar vertebra).

Figure 2. Relationships between the ultrasound measurements of the quadriceps muscle layer

thickness or rectus femoris muscle CSA and CT measurements of the cross-sectional area at the

third lumbar vertebra.

(A) Quadriceps muscle layer thickness and (B) Rectus femoris muscle CSA. The Spearman

correlation coefficient was used to investigate the relationships. CSA: cross-sectional area, CT:

computed tomography

Figure 3. Areas under the receiver operating characteristic curves (AUCs) were estimated to

determine the cutoff values of ultrasound assessments for low muscularity.

The Youden index was used to identify the optimal cutoff value. (A) Quadriceps muscle layer

thickness and (B) Rectus femoris muscle CSA. (A) cutoff value was 2.0 cm at the sensitivity of

83.3% and the specificity of 78.5% and (B) cutoff value was 4.66 cm2 at the sensitivity of 79.2%

and the specificity of 66.2%. AUC: areas under the receiver operating characteristic curves, CSA:

cross-sectional area, CI: confidence interval

Figure 4. Relationships with the ultrasound measurements of elbow flexor muscle thickness,

23

biceps brachii muscle CSA, sum of rectus femoris and biceps brachii muscle CSA, and diaphragm

thickness.

(A) elbow flexor muscle thickness, (B) biceps brachii muscle CSA, (C) sum of rectus femoris and

biceps brachii muscle CSA, (D) diaphragm thickness. CSA: cross-sectional area. Correlation

between ultrasound and computed tomography measurements were evaluated. The Spearman

correlation coefficient was used to investigate the relationships.

24

Figure 1

Ultrasound assessment

of femoral muscle

at the ICU admission

(n = 133)

No CT examination at L3 level

(n = 44)

Primary outcome

CT examination at L3 level

(n = 89)

Secondary outcome

Ultrasound assessment of

biceps brachii muscle

(n = 52)

Secondary outcome

Ultrasound assessment of

diaphragm muscle

(n = 79)

Figure 2

ρ = 0.57

p < 0.01

n = 89

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Table 1. Patient characteristics

All patients

Low muscularity*

Normal muscularity

Variables

(n = 89)

(n = 24)

(n = 65)

p-value

Age, mean ± SD, y

72 ± 13

76 ± 11

70 ± 13.6

0.07

60/29

16/8

44/21

0.93

Body mass index, mean ± SD, kg/m2

22.2 ± 4.4

18.6 ± 3.0

23.5 ± 4.0

< 0.01

APACHE II score

27 (24–30)

28 (25–32)

27 (23–30)

0.31

SOFA

8 (6–11)

8 (6–11)

10 (6–12)

0.66

Sepsis (Sepsis-3 criteria), n (%)

40 (49)

24 (56)

16 (41)

0.27

Postoperative admissions, n (%)

14 (16)

1 (4)

13 (20)

0.07

Mechanical ventilation, n (%)

78 (88)

19 (79.2)

59 (90.8)

0.16

Length of ICU stay, d

7 (5–14)

6 (4–11)

7 (5–17)

0.13

29 (18–51)

22 (15–44)

30 (21–51)

0.39

Mortality in the ICU, n (%)

16 (18.0)

4 (17)

12 (19)

0.85

Mortality in the hospital, n (%)

25 (28.1)

10 (41.7)

15 (23.1)

0.08

2.4 (1.8–3.1)

1.7 (1.4–2.0)

2.8 (2.1–3.2)

< 0.01

Rectus femoris muscle CSA (cm )

4.9 (3.9–6.5)

3.9 (2.9–4.6)

5.4 (4.1–7.1)

< 0.01

Elbow flexor muscle thickness (cm)†

2.8 (2.3–3.1)

2.3 (2.0–2.7)

3.2 (2.8–3.4)

< 0.01

Biceps brachii muscle CSA (cm2)†

6.1 (4.6–8.6)

5.1 (3.6–5.4)

6.8 (5.1–9.0)

< 0.01

Diaphragm thickness (mm)‡

1.8 (1.4–2.1)

1.7 (1.3–2.0)

1.8 (1.5–2.2)

0.28

102.8 (77.1–133.2)

69.2 (54.1–80.5)

118.9 (97.0–143.5)

< 0.01

Male/Female

Length of hospital stay, d

Ultrasound

Quadriceps muscle layer thickness (cm)

Computed tomography

CSA at 3rd lumbar vertebra (cm2)

APACHE: Acute Physiology and Chronic Health Evaluation; SOFA: Sequential Organ Failure Assessment; SD: standard deviation; ICU:

intensive care unit; IQR: interquartile range; CSA: Cross-sectional area

Data were presented as median (IQR) unless otherwise indicated.

* Low muscularity was defined as skeletal muscle index < 29.0 cm2/m2 for males and 36.0 cm2/m2 for female.

† Included number of patients was 52 with 13 of low muscularity and 39 of normal muscularity.

‡ Included number of patients was 79 with 22 of low muscularity and 57 of normal muscularity.

Supplemental File

Ultrasound assessment of muscle mass has potential to identify patients with low muscularity at

intensive care unit admission: A retrospective study

Table S1. Equipment used in this study

Tokushima University Hospital

Tokushima Prefectural Central Hospital

Ultrasounds

HI VISION Preirus, Hitachi

Medical Corporation, Tokyo, Japan

LOGIQ P9, GE healthcare, WI, USA

Transducers

EUP-L73S liner transducer (4–9

MHz), Hitachi Medical

Corporation, Tokyo, Japan

12L-RS liner transducer (5–13 MHz),

GE healthcare, WI, USA

Computed Tomography

Aquilion 16, Canon Medical

Systems, Tochigi, Japan

Philips Brilliance iCT, Philips

Healthcare, OH, USA

Figure S1 Ultrasound measurement images of limb thickness

A. Elbow flexor muscle thickness was measured from the superficial fascia of the biceps brachii

muscle to the uppermost part of the humerus. B. Quadriceps muscle layer thickness was measured

from the superficial fascia of the rectus femoris to the uppermost part of the femur.

Figure S2 Ultrasound measurement images of limb cross-sectional area

A. Biceps brachii muscle cross-sectional area was measured by tracking the muscle area shown in

the transverse plane. B. Rectus femoris muscle ross-sectional area was measured by tracking the

muscle area shown in the transverse plane.

Figure S3 Image of diaphragm thickness measurement

Diaphragm is observed as hypoechogenic muscular layer bordered by the echogenic layer of

peritoneum and diaphragmatic pleurae.

Figure S4 Image of a computed tomography measurement

The white line tracing includes the total muscle area in the third lumbar vertebra, which includes

the psoas, quadratus lumborum, transversus abdominis, external and internal obliques, and rectus

abdominis muscles.

Table S2 Reproducibility of measurements

Correlation coefficient

Variables

Bland-Altman 95% CI

Bias

95% CI

Quadriceps muscle layer thickness

0.99

< 0.01

Rectus femoris muscle CSA

0.99

< 0.01

Elbow flexor muscle thickness

0.99

< 0.01

−0.230 ± 0.126 −0.514 to 0.054

Biceps brachii muscle CSA

0.96

< 0.01

0.028 ± 0.094

−0.184 to 0.240

Diaphragm thickness

0.98

< 0.01

0.045 ± 0.036

−0.030 to 0.120

Quadriceps muscle layer thickness

0.99

< 0.01

−0.290 ± 0.307 −0.985 to 0.405

Rectus femoris muscle CSA

0.99

< 0.01

0.059 ± 0.076

−0.113 to 0.231

Elbow flexor muscle thickness

0.99

< 0.01

0.020 ± 0.251

−0.548 to 0.588

Biceps brachii muscle CSA

0.99

< 0.01

0.004 ± 0.075

−0.165 to 0.173

Diaphragm thickness

0.97

< 0.01

0.040 ± 0.027

−0.016 to 0.096

Intra-observer reproducibility

−0.190 ± 0.091 −0.396 to 0.016

0.113 ± 0.067

−0.039 to 0.265

Inter-observer reproducibility

CI: confidence interval, CSA: cross-sectional area

Reproducibility was assessed for 10 patients in limb and for 20 patients in diaphragm. The Pearson

correlation coefficient and Bland-Altman plot were determined by using JMP statistical software

version 13.1.0 (SAS Institute Inc., Cary, NC, USA).

Table S3 The values of quadriceps muscle layer thickness and rectus femoris muscle crosssectional area in various populations

Variables

median (IQR)

All

133

2.4 (1.9–3.2)

Male

85

2.6 (2.0–3.3)

Female

48

2.1 (1.8–2.9)

Young (< 70 years)

59

2.9 (2.1–3.5)

Older (≥ 70 years)

74

2.1 (1.7–2.7)

All

133

5.0 (3.9–7.0)

Male

85

5.8 (4.1–7.9)

Female

48

4.5 (3.7–5.7)

Young (< 70 years)

59

6.5 (4.3–8.8)

Older (≥ 70 years)

74

4.5 (3.5–5.6)

Quadriceps muscle layer thickness (cm)

Rectus femoris muscle cross-sectional area (cm2)

IQR: interquartile range

We presented the data of quadriceps muscle layer thickness and rectus femoris muscle crosssectional area in all 133 patients who had the ultrasound assessment at the ICU admission. The data

was also shown in sex and age (young or older).

...

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