The critically ill may have significant functional impairment, with slow recovery and high mortality rates.1,2 Following prolonged mechanical ventilation, fewer than half survived beyond 1 year.3 Therefore, the early identification of patients at high risk of prolonged mechanical ventilation may significantly influence the manner of their care.
Sarcopenia is associated with extended mechanical ventilation, longer stays in hospital and the ICU, complications after emergency surgery, problems with disposal and mortality.4–6 It is also reported that sarcopenia, defined by skeletal muscle mass adjusted for BMI, is related to cardiometabolic risk factors.7 Various methods, including computed tomography (CT), MRI, dual-energy X-ray absorptiometry (DXA), bioimpedance analysis (BIA), muscle strength evaluation and ultrasound, have been used in determining the degree of sarcopenia.8 MRI and CT are considered to be best for assessing muscle quantity,9,10 but use of these methods may be hampered by clinical conditions, facility and personnel, lack of portability or their high costs.11 Ultrasound examination is noninvasive and can be performed at the bedside, and studies have shown that ultrasound measurement of muscle thickness correlates well with other methods.12–14 However, as yet, there is no standardised method of performing muscle ultrasound in clinical practice.14,15
This study aimed to investigate the association between BMI-rectus abdominis (BMI-RA) thickness ratio, defined as BMI divided by the thickness of the rectus abdominis measured by ultrasound, and the outcomes of the critically ill, to describe a standardised and reproducible method for measuring trunk muscle that is easy to use at the bedside, and to investigate the relationship between results from ultrasound examination and those from CT scan.
Materials and methods
Study design and setting
This retrospective study was carried out in two ICUs with 24 beds in total at Kaohsiung Veterans General Hospital (a tertiary referral teaching hospital) from October 2017 to June 2018. Ethical approval for this study (Ethical Committee Number VHGKS19-EM4-01) was provided by the institutional review board of Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan on 26 March 2019. Because all data including ultrasound measurements were already recorded in the medical records, a waiver was granted for individual written consent.
During the period of study, patients being transferred to ICU immediately after major abdominal procedures received a bedside ultrasound examination during the first week of ICU stay, or when clinically indicated (Fig. 1). Extended focused assessment sonography for trauma (eFAST) had been performed to evaluate patients by one of the investigators (Yang) since June 2015. The eFAST ultrasound examination assessed the abdomen, pelvis, pericardium and pleura.16 Since August 2017, the thickness of the rectus abdominis muscle over the upper abdomen had also been measured while performing eFAST. If the ICU stay was more than 1 week, the ultrasound examination was performed weekly.
Measurement of rectus abdominis
The thickness of rectus abdominis muscle over upper abdomen was measured by B mode ultrasonography while the patient was breathing quietly in the supine position (Fig. 2a). The measurement was performed using a Siemens ACUSON P300TM portable ultrasound system with LA523 linear transducer array (frequency bandwidth: 5.0 to 12.0 MHz) (Siemens Medical Solutions USA, Mountain View, California, USA). The distance between sheaths of rectus abdominis muscle was calculated on the screen by planimetric technique provided by the vendor of the ultrasound unit (Fig. 2b). Both sides of the upper abdomen were examined by ultrasound and the thickness of rectus abdominis was recorded in cm. Images were stored in the medical information system of the hospital and were retrospectively retrieved for analysis.
If an abdominal CT scan was performed within 3 days before or after the ultrasound examination, images of the CT scan were retrieved from the medical information system and viewed on the computer monitor. The thickness of rectus abdominis was measured by picture archiving and communications system viewer program (smartPACSTM, Taiwan Electronic Data Processing Co., Taipei, Taiwan). The boundaries of skeletal muscle of the cross-section at the level of the third lumbar vertebra were outlined on the monitor manually, and the enclosed area was calculated by the computer program to derive skeletal muscle area (SMA) (Supplement Fig. 1, https://links.lww.com/EJA/A445). Intra-observer and interobserver variations of ultrasound measurements were assessed 18 months after the end of the study period. The same analyst (Yang) read images of the first ultrasound examination of each patient without any markers on them, and a second analyst (Wang) blindly and independently analysed the same images. Intraclass correlation coefficients were calculated to test intra-observer and interobserver reliability.
Data collection and outcomes
Characteristics of patients, including age, sex, height, weight, diagnosis at admission, reason for transfer to ICU, duration of mechanical ventilation, ICU stay, hospital stay, follow-up period and final condition, were retrospectively retrieved from medical records. The Charlson comorbidity index17,18 and Acute Physiology Chronic Health Evaluation II (APACHE II) score19 were calculated based on the information and data collected on the day of transfer to ICU. Serum albumin levels and vital signs on the days of ICU admission and ultrasound examination were also collected retrospectively from medical records. Sequential Organ Failure Assessment (SOFA) score20 and BMI were calculated based on the data on the day of each ultrasound measurement of the rectus abdominis. Images were retrieved from the medical information system and skeletal muscle index (SMI) was derived from SMA adjusted by the square of body height.10,21 Sarcopenia was defined by the cut-off value reported by the Korea National Health and Nutrition Examination Survey.22 BMI-RA thickness ratio was defined as BMI divided by the averaged thickness of rectus abdominis on both sides of the upper abdomen.
The primary outcome measure was in-hospital mortality. Secondary outcomes were duration of mechanical ventilation, ICU stay and hospital stay. Prolonged mechanical ventilation was defined as failed weaning from mechanical ventilation within 14 days after the first ultrasound examination. Only the first BMI-RA thickness ratio measured after admission to ICU was used in the analyses of primary and secondary outcomes. Results of ultrasound measurements after the first week were analysed for correlation with CT scan results if available. The follow-up period was defined as days between the first ultrasound examination and discharge from the hospital or the last follow-up at the outpatient department of the hospital.
Continuous variables in normal distribution were compared using Student's t-test and expressed as mean ± SD. For continuous variables not normally distributed, the data were compared using Mann--Whitney U test and expressed as median [IQR]. For multiple comparisons, P values were corrected for false discovery rate by the Benjamini--Hochberg method. Categorical variables were presented as a number or as a percentage and compared using χ2 test or Fisher's exact test. Correlation analysis was performed to assess the correlation between ultrasound measurement and CT scan findings, and the correlation between BMI-RA thickness ratio and other variables. A receiver operating characteristic (ROC) curve was used to assess in-hospital mortality predictions. The cut-off value on the ROC curve was calculated by obtaining the best Youden index ((sensitivity + specificity) -1). Survival curves as a function of days were generated using Kaplan--Meier analysis and compared using Mantel--Cox test. Linear regression was used to analyse the association between continuous variables and lengths of stay in ICU, in hospital and duration of mechanical ventilation. Multivariable logistic regression analysis was applied to identify risk factors for in-hospital mortality and prolonged mechanical ventilation. The results were reported as Wald χ2P value and adjusted odds ratio (OR) with 95% confidence interval (95% CI).
Statistical analyses were performed using GraphPad Prism version 6.07 for Windows (GraphPad Software, San Diego, California, USA), PASW Statistics version 18.0 for Windows (SPSS Inc., Chicago, Illinois, USA), R version 3.4.4 (R Foundation for Statistical Computing, Vienna, Austria) and G∗Power version 18.104.22.168.23 All statistical tests were two-tailed, with the level of significance set to P value less than 0.05.
There were 27 patients transferred to the ICU after major abdominal surgery and all received eFAST ultrasound examination within the first week of admission (Fig. 1). The median duration between the day of admission to ICU and the day of the first ultrasound examination was 2.2 ± 2.2 days (range: 0 to 6 days). The mean age of the patients was 67.9 ± 11.3 years, and 18 (66.7%) underwent emergency surgery. Patient characteristics and diagnoses are summarised in Table 1. The median follow-up time was 63 days (range: 13 to 312 days). Thirteen patients required mechanical ventilation for more than 14 days after the first ultrasound examination. The in-hospital mortality was 25.9% (7 of 27). No local infection or poor healing of abdominal wounds was observed. The intraclass correlation coefficients of the same observer and different observers were 0.93 (95% CI: 0.86 to 0.97) and 0.87 (95% CI: 0.75 to 0.94), respectively.
Table 1 -
n = 27
||16 (59%)/11 (41%)
||67.9 ± 11.3 (63.5 to 72.4)
|ICU stay (days)
||16 [2 to 58]
|APACHE II score
||26.1 ± 7.3 (23.2 to 29.0)
||6.3 ± 3.1 (5.0 to 7.5)
|RA thickness (cm)
||0.74 ± 0.17 (0.68 to 0.81)
|BMI (kg m−2)
||25.9 [17.5 to 51.1]
|Charlson comorbidity index
||4.2 ± 1.9 (3.5 to 5.0)
|Hospital stay (days)
||31.6 ± 19.3 (23.9 to 39.2)
|MV duration (days)
||12 (1 to 81)
|Successful weaning in 14 days/prolonged MV
||14 (52%) / 13 (48%)
|Successful weaning/failure at discharge
||20 (74%) / 7 (26%)
|Alive/death at discharge
||20 (74%) / 7 (26%)
|Admission after elective surgery
| Upper gastrointestinal tract cancer
| Colorectal cancer
| Other tumours or disease
|Admission after emergency surgery
| Upper gastrointestinal tract perforation
| Small bowel obstruction, ischaemia, or perforation
| Colon perforation, diverticulitis, or cancer
| Other peritonitis
Data are expressed as mean ± standard deviation (95% CI), median [range] or n (%).APACHE II, Acute Physiology and Chronic Health Evaluation II; MV, mechanical ventilation; RA, rectus abdominis; SOFA, Sequential Organ Failure Assessment.
In total, 51 ultrasound measurements of the rectus abdominis were made for the 27 patients. There were 20 CT scans performed within 3 days before or after the 51 ultrasound examinations, including 16 performed close to the first ultrasound examination of each patient (Fig. 1). No association was found between sarcopenia defined by SMI and outcomes of the 16 patients (Supplement Table 1, https://links.lww.com/EJA/A445). Among all 20 CT scans, the thickness of rectus abdominis measured by ultrasound correlated significantly with the thickness measured by CT scan (P = 0.0211) and SMA at the third lumbar spine level (P = 0.0027). No significant association was found between the BMI-RA thickness ratio and results from the 20 CT scans (Supplement Table 2, https://links.lww.com/EJA/A445).
BMI-RA thickness ratio is associated with in-hospital mortality
In nonsurvivors, the disease severity and the first BMI-RA thickness ratio measured after admission to ICU were significantly higher than survivors (BMI-RA thickness ratio: 47.9 [34.9 to 58.6] and 37.5 [25.1 to 42.5], respectively, P = 0.013; APACHE II score: 34 [29 to 39] and 25 [19 to 28.7], respectively, P = 0.013; SOFA score: 8 [6 to 10] and 5 [4 to 7], respectively, P = 0.018) (Table 2). In multivariable logistic regression analysis, the BMI-RA thickness ratio was found to be associated with in-hospital mortality (OR: 1.22, 95% CI: 1.01 to 1.48, P = 0.041; Table 3).
Table 2 -
Characteristics of patients according to clinical outcomes
||Condition at discharge
||Prolonged mechanical ventilation
||≤ 14 days
||64 [63 to 77]
||69.5 [56.0 to 79.5]
||−11 to 12
||70.7 ± 10.1
||65.4 ± 12.1
||−3.5 to 14.2
||34 [29 to 39]
||25.0 [19.0 to 28.7]
||−15 to −2
||28.9 ± 7.4
||23.5 ± 6.3
||−0.03 to 10.9
||8 [6 to 10]
||5 [4 to 7]
||−6 to −1
||7.9 ± 3.4
||4.7 ± 1.8
||1.1 to 5.4
||5 [4 to 6]
||4 [2 to 6]
||−3 to 1
||4.6 ± 1.7
||3.9 ± 2.0
||−0.7 to 2.2
|Albumin (g dl−1)
||2.3 [1.6 to 2.7]
||2.5 [2.3 to 2.9]
||−0.1 to 1
||2.4 ± 0.5
||2.7 ± 0.5
||−0.7 to 0.06
||27.5 [24.0 to 34.7]
||25.8 [22.9 to 29.4]
||−9.2 to 2.0
||27.4 [24.2 to 33.6]
||25.6 [22.2 to 28.8]
||−1.2 to 7.7
||0.67 [0.53 to 0.77]
||0.76 [0.65 to 0.84]
||−0.03 to 0.26
||0.69 ± 0.11
||0.79 ± 0.2
||−0.24 to 0.026
||47.9 [34.9 to 58.6]
||37.5 [25.1 to 42.5]
||−23.6 to −2.0
||43.4 [35.0 to 52.5]
||36.2 [23.7 to 41.8]
||1.2 to 18.6
Data are presented as median [IQR] or mean ± SD.APACHE II, Acute Physiology Chronic Health Evaluation II score; CCI, Charlson comorbidity index; CI, confidence interval; RA, rectus abdominis; Ratio, BMI-RA thickness ratio; SOFA, Sequential Organ Failure Assessment score.
aStatistically significant with Benjamini–Hochberg correction.
Table 3 -
Multivariable logistic regression model predicting in-hospital mortality and prolonged mechanical ventilation
||APACHE II score
||0.88 to 1.43
||0.82 to 2.47
||BMI-RA thickness ratio
||1.01 to 1.48
|Prolonged mechanical ventilation
||APACHE II score
||0.81 to 1.18
||1.06 to 3.75
||BMI-RA thickness ratio
||0.99 to 1.36
APACHE II, Acute Physiology and Chronic Health Evaluation II; CI, confidence interval; SOFA, Sequential Organ Failure Assessment.
Using the ROC curve to assess BMI-RA thickness ratio in predicting in-hospital mortality, the cut-off value was selected as 44.2 (area under curve: 0.81) (Supplement Fig. 2, https://links.lww.com/EJA/A445). In patients with a BMI-RA thickness ratio greater than 44.2, survival was worse, and the probability of remaining on mechanical ventilation for more than 14 days was higher (Supplement Table 3, https://links.lww.com/EJA/A445).
Factors associated with mechanical ventilation, ICU stay and hospital stay
The BMI-RA thickness ratio calculated from the first ultrasound examination following transfer to ICU significantly correlated with ICU stay, hospital stay, and duration of mechanical ventilation (Table 4). Linear regression analysis demonstrated a significant relationship between the BMI-RA thickness ratio and hospital stay, but not ICU stay and duration of mechanical ventilation (Supplement Fig. 3, https://links.lww.com/EJA/A445). In multivariable logistic regression analysis including APACHE II score, SOFA score and the BMI-RA thickness ratio, the SOFA score was associated with prolonged mechanical ventilation (OR: 1.99, 95% CI: 1.06 to 3.75, P = 0.033; Table 3).
Table 4 -
Correlation between BMI-RA thickness ratio and other variables
||0.01 to 0.67
||−0.23 to 0.51
||−0.05 to 0.63
||−0.48 to 0.27
||0.42 to 0.85
||−0.81 to −0.33
||0.15 to 0.74
||0.11 to 0.73
||0.22 to 0.78
APACHE II, Acute Physiology Chronic Health Evaluation II score; CCI, Charlson comorbidity index; CI, confidence interval; ICU, intensive care unit; MV, mechanical ventilation; RA, rectus abdominis; SOFA, Sequential Organ Failure Assessment score.
We have shown that the BMI-RA thickness ratio was significantly associated with in-hospital mortality, a relationship that persisted even after adjustment for APACHE II and SOFA scores. We also found that the thickness of rectus abdominis measured by ultrasound correlated well with CT measurements. However, there was no relationship between CT measurements and the BMI-RA thickness ratio, suggesting that the BMI-RA thickness ratio contributed more information than a simple linear measurement alone. Also, ultrasound measurements demonstrated good intra-observer and interobserver reproducibility, leading us to believe that our method may be used as a standardised method of measuring the thickness of the rectus abdominis.
Skeletal muscle mass is highly important in immune function, glucose disposal, protein synthesis and mobility,24–26 but quantity and quality of muscle may be affected by disease and activity,9,27 and muscle wasting occurs rapidly in ICU.28 Sarcopenia is associated with mechanical ventilation, postoperative status, surgical complications, hospital and ICU stay, problems with disposal and mortality.4–6,29–31 A previous study reported that sarcopenia was present in 43.1% of surgical ICU patients,32 and in our study, sarcopenia was present in 56.25% of the 16 patients having CT scans within the first week of admission to ICU. However, no association was found between sarcopenia and outcomes, possibly due to the low number of patients in our study.
Site-specific sarcopenia may be present before whole-body sarcopenia.15,33 Ishida et al.34 reported that the thickness of the rectus abdominis correlated better with expiratory pressure production than with thickness of other abdominal muscles.33 The thickness of the rectus abdominis among different groups has been evaluated with various methods (Supplement Table 4, https://links.lww.com/EJA/A445).8,12,33–36 In our study, neither the thickness of the rectus abdominis nor the BMI alone was associated with outcomes. Tandon et al.37 reported that combining BMI and thigh muscle thickness measured by ultrasound can identify patients with sarcopenia. Similarly, in this study, we have found that the BMI-RA thickness ratio, derived from dividing BMI by the average thickness of the rectus abdominis on both sides of the upper abdomen, is associated with in-hospital mortality, duration of mechanical ventilation and hospital stay. However, in a multivariable analysis adjusting for APACHE and SOFA scores, the BMI-RA thickness ratio is only significantly associated with in-hospital mortality but not prolonged mechanical ventilation.
An ideal method for assessing muscle composition of patients in ICU should be easy to perform at bedside with reasonable reproducibility and minimal impact on organ function. CT is one of the gold standards for assessing muscle quantity.9,10 However, critically ill patients are often too unstable to be transferred to another facility, hence the use of CT, MRI and DXA to detect sarcopenia is not easy.38,39 Traditional markers, such as serum albumin and BMI, are neither good markers for malnutrition and lean body mass nor good predictors of mortality.30,40–44 In critically ill patients, testing muscle strength may be difficult to perform in patients under sedation, and BIA often may be affected by hydration status and presence of oedema.38 Ultrasound is noninvasive and can evaluate muscle strength and quality. It is reported that muscle thickness measured by ultrasound correlated with measurements from MRI and CT.12–14,45–49 We also found that the thickness of the rectus abdominis measured by ultrasound correlated with the thickness measured by CT and SMA at the third lumbar spine level. This implies that ultrasound may be an ideal alternative for evaluating trunk muscle, such as the rectus abdominis in critically ill patients.
There is no standardised method of performing muscle ultrasound in clinical practice.15 Ultrasound examination may be affected by image acquisition, image processing and analysis, skills of examiners and differing technological capabilities of machines.50 Nevertheless, studies have reported that great interobserver reliability of ultrasound examination can be achieved.32,51 In our retrospective study, all ultrasound measurements were performed by a single investigator using only one ultrasound machine before the outcomes of patients were known. Intra-observer and interobserver variations were independently assessed, and with a substantial temporal separation between analyses to mitigate recall bias. The high intraclass correlation coefficients indicate good reliability of the current method. However, a prospective study involving different examiners independently examining the same patient on the same day and reviewing images blindly sometime later, should be carried out to consolidate the reproducibility and interobserver reliability of current method. We did not observe any adverse events such as wound contamination, wound infections and delayed healing in this series.
There are several limitations of our study. The high disease severity and recent surgical condition of patients enrolled in our retrospective study mean that a larger prospective study enrolling more patients with different conditions is warranted to further study the role of BMI-RA thickness ratio in the care of critically ill patients. We did not assess the quality, function and serial changes of rectus abdominis measurements. The relationship between the BMI-RA thickness ratio and sex, age and sarcopenia defined by other methods, and serial change in the BMI-RA thickness ratio during the course of illness, remain to be investigated. Hence, larger prospective studies comparing ultrasound examination with other methods of sarcopenia evaluation, and taking muscle quality, strength evaluation and frailty assessment into consideration, are needed to elucidate the role of ultrasound examination of the rectus abdominis and BMI-RA thickness ratio in the care of critically ill patients.
This study demonstrates that using ultrasound to measure the thickness of the rectus abdominis muscle is safe and easy to perform in the surgical ICU. The BMI-RA thickness ratio is related to ICU stay, hospital stay, duration of mechanical ventilation and in-hospital mortality of patients transferred to ICU after major abdominal surgery. Larger prospective studies are required to confirm the reliability of measuring thickness of the rectus abdominis by ultrasound and the relationship between the BMI-RA thickness ratio and outcomes in critically ill patients.
Acknowledgements relating to this article
Assistance with the study: we would like to thank Ms. Ho-shan Hsiao for her assistance in patient registry of the study.
Financial support and sponsorship: none.
Conflicts of interest: none.
Presentation: part of patients was enrolled in a poster presented at SG-ANZICS 2018, 17–21 May, Singapore.
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