Assessment of muscle mass using ultrasound with minimal versus maximal pressure compared with computed tomography in critically ill adult patients

doi:10.1016/j.aucc.2020.10.008

Australian Critical Care

Volume 34, Issue 4, July 2021, Pages 303-310

https://doi.org/10.1016/j.aucc.2020.10.008 Get rights and content

Abstract

Background

Preserved skeletal muscle mass identified using computed tomography (CT) predicts improved outcomes from critical illness; however, CT imaging have few limitations such that it involves a radiation dose and transferring patients out of the intensive care unit. This study aimed to assess in critically ill patients the relationship between muscle mass estimates obtained using minimally invasive ultrasound techniques with both minimal and maximal pressure compared with CT images at the third lumber vertebra level.

Methods

All patients were treated in a single Australian intensive care unit. Eligible patients had paired assessments, within a 72-h window, of muscle mass by ultrasound (quadriceps muscle layer thickness in centimetres, with maximal and minimal pressure) and CT axial cross-sectional area (cm²). Data are presented as mean (standard deviation), median (interquartile range), and frequencies [n (%)].

Results

Thirty-five patients [mean (standard deviation) age = 55 (16) years, median (interquartile range) body mass index = 27 (25–32) kg/m², and 26 (74%) men] contributed 41 paired measurements. Quadriceps muscle thickness measured using the maximal pressure technique was a strong independent predictor of lumbar muscle cross-sectional area. Within a multivariate mixed linear regression model and adjusting for sex, age, and body mass index, for every 1 cm increase in quadriceps muscle layer thickness, the lumbar muscle cross-sectional area increased by 35 cm² (95% confidence interval = 11–59 cm²). Similar univariate associations were observed using minimal pressure; however, as per multivariate analysis, there was no strength in this relationship [8 cm² (95% confidence interval = –5 to 22 cm²)].

Conclusion

Ultrasound assessment of the quadriceps muscle using maximal pressure reasonably predicts the skeletal muscle at the third lumbar vertebra level of critically ill patients. However, there is substantial uncertainty within these regression estimates, and this may reduce the current utility of this technique as a minimally invasive surrogate for CT assessment of skeletal muscle mass.

Introduction

Reduced skeletal muscle mass, determined by muscle cross-sectional area (CSA) at the lumbar vertebra (L3), using computed tomography (CT), has been shown to be an independent risk factor for increased mortality and morbidity in critically ill patients.[1], [2], [3], [4] Because of the radiation dose involved with CT imaging and the requirements for moving patients out of the intensive care unit (ICU), CT has limited utility as a widespread and repeatable method to quantify body composition.

Accordingly, minimally invasive techniques that can be performed at the bedside, such as ultrasound, may be useful to quantify muscle mass as part of usual care or within a clinical trial evaluating nutritional and/or physical therapy.[5], [6], [7], [8] Ultrasound is minimally invasive, and protocols using multiple anatomical sites for muscle thickness analysis have been validated against whole-body skeletal muscle mass using magnetic resonance imaging and dual-energy X-ray absorptiometry in healthy individuals.⁶^,⁹ However, in critically ill patients, the most appropriate ultrasound protocol to measure a muscle groups, such as quadriceps, remains uncertain.⁷^,¹⁰ There is further uncertainty as to whether the quadriceps muscle group is a robust estimate of the skeletal muscle CSA obtained by CT imaging, which remains the methodology that has proven associations between muscle mass and outcomes.⁷^,¹⁰ Therefore, it remains unclear whether ultrasound is a useful tool to assess low muscle muscularity or if it could be used to monitor the effect of interventions, such as nutrition therapy, in critically ill patients.⁷

The primary aim of this study was to explore the relationship between the skeletal muscle CSA assessed using CT imaging and quadriceps muscle layer thickness (QMLT) measurements using ultrasound with maximal and minimal pressure. These measurements were obtained from critically ill patients who had a CT scan and QMLT measurements within 72 h of each other. The secondary aims were to explore the relationship between low muscularity determined by CT analysis cut points and QMLT measurements, markers of nutritional status, and clinical outcomes. The tertiary aim was to compare two different software techniques to assess skeletal muscle CSA so as to validate a methodology that clinicians/researchers with limited access to radiologist expertise.

Section snippets

Study design and setting

This single-centre retrospective observational study was conducted at a tertiary referral Australian ICU from patients admitted between 2015 and 2019. A local database of patients who had QMLT measurements obtained using ultrasound during ICU admission for another research study was searched.¹¹ Data were included from patients if they also had an abdominal CT scan within 72 h of one of the QMLT measurements.¹⁰ All CT scans were performed for clinical purposes other than assessment of muscle

Results

Between August 2015 and July 2019, 96 patients had ultrasound images of the quadriceps muscle obtained during ICU admission (Fig. 1). After all exclusions and inspection of the CT images, data from 35 (64%) patients were included in the study, which provided 41 CT scans that were paired to an ultrasound measurement. CT scans were completed within 24 h of admission to the ICU for 33 (80%) episodes, and for eight (19%) episodes, CT scans were completed at a later time point.

Discussion

In this exploratory study, QMLT assessed by ultrasound using a maximal pressure method was a strong independent predictor of skeletal muscle CSA quantified using CT imaging. However, this signal was not present when QMLT was assessed using the minimal pressure method, and the automatic software program was used to assess the skeletal muscle CSA. Consistent with the skeletal muscle CSA technique, point estimates for the mean QMLT were lower in women and those with defined low muscularity.

The

Conclusions

Although ultrasound assessment of the quadriceps muscle reasonably predicts the mean axial skeletal muscle CSA of critically ill patients, substantial uncertainty within these regression estimates may reduce the utility of this technique as a noninvasive surrogate for CT assessment of skeletal muscle mass. The maximal pressure ultrasound technique appeared to perform better than the minimal pressure technique in predicting skeletal muscle CSA. Further research is warranted to determine if

Conflict of Interest

K.F. has received conference, travel grants, and/or honoraria from Baxter, Fresenius Kabi, Nutricia, Abbott, and Nestle Health Science (not related to this study). A.M.D. or his institution has received honoraria, travel grants, or project grant funding from Baxter, Cardinal Health, Fresenius Kabi, GSK, Medtronic, and Nutricia. A.M.D. has participated in advisory boards for Lyric Pharmaceuticals and Takeda. Y.A.A. has received honoraria from Baxter Healthcare Corporation.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

CRediT authorship contribution statement

Kate Fetterplace: Conceptualisation, Methodology, acquisition of the data, analysis and the interpretation of the data, Writing - original draft, Writing - review & editing. Lucy Corlette: acquisition of the data, Writing - review & editing. Yasmine Ali Abdelhamid: Methodology, acquisition of the data, Writing - review & editing. Jeffrey J. Presneill: analysis and the interpretation of the data, Writing - review & editing. Michael T. Paris: Methodology, Writing - review & editing. Damien Stella:

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Cited by (14)

Comparison between ultrasonography and computed tomography for measuring skeletal muscle mass in critically ill patients with different body mass index
2024, Clinical Nutrition ESPEN
Among critical patients, there is an early onset of changes in both the quantity and quality of muscle mass. It is essential to find tools that promptly identify this muscle mass loss. The aim of this study was to compare the ultrasonography of the quadriceps femoris to the gold standard, thigh computed tomography (CT) for assessing the musculature of critically ill patients with different body mass index who have suffered traumatic brain injury.
This is a prospective validation study in an Intensive Care Unit (ICU) specialized in trauma care, located at a tertiary teaching hospital. Our study involved a convenience sample of patients. Sequential ultrasound and CT scans were performed at three distinct time intervals: upon admission, between 24 and 96 h' post-admission, and finally, between 96 and 168 h' post-admission. For all ultrasound measurements, we conducted simultaneous quadriceps CT measurements. The correlation between measurements obtained by ultrasound and computed tomography at three different times and in three BMI ranges was analyzed, in individuals with normal weight, overweight and obese.
Results: We analyzed 252 images in 49 patients in time 1, 40 patients in time 2, and 37 in time 3 to compare the thickness quadriceps muscle using US and CT. Of these, 18 patients had a BMI ≤ 24.9 kg/m² (normal weight), 18 patients from 25 to 29.9 kg/m² (overweight), and 8 patients had a BMI ≥ 30 kg/m² (obese). The mean age was 37 years, the majority (94%) were male and the main comorbidities were: hypertension 12%, diabetes 4% and 14% smoking. The results revealed minor discrepancies between measurements obtained through the two methods, these changes were not influenced by the body mass index, with these variations being practically insignificant in the context of clinical application. Thus, the correlation and concordance between the values obtained found a strong positive correlation with good limits of agreement. The Spearman's correlation coefficients obtained were r = 0.89, 0.91 and 0.88, p < 0.01 at T1, T2 and T3 respectively for normal weight, r = 0.91, 0.80 and 0.81, p < 0.01 at T1, T2 and T3 respectively for overweight and r = 0.89, 0.94 and 0.84, p < 0.01 at T1, T2 and T3 respectively for obesity. In addition to a positive correlation, we observed a high agreement between the methods. The Bland & Altman analysis at time 1 showed, respectively, the bias of 1.46, 2.03 and 0.76. At time 2, the bias was 0.42, 3.11 and 2.12. At time 3, the bias was 2.26, 3.38 and 2.11 mm.
Our findings suggest that measure femoral quadriceps muscle thickness ultrasound-based exhibits a comparable performance to thigh CT. This conclusion stems from the excellent correlation and good agreement observed between ultrasound and CT, which is considered the gold standard for muscle assessment in critically ill patients.
This clinical trial is registered at REBEC https://ensaiosclinicos.gov.br/ identifier: RBR-2bzspnz. The protocol was approved, on July 30, 2019, by the Research Ethics Committee of the Hospital das Clínicas, Faculdade de Medicina de Ribeirão Preto – Trial Registration Number: 3,475,851.
Clinical practice guidelines for nutritional assessment and monitoring of adult ICU patients in China
2024, Journal of Intensive Medicine
The Chinese Society of Critical Care Medicine (CSCCM) has developed clinical practice guidelines for nutrition assessment and monitoring for patients in adult intensive care units (ICUs) in China. This guideline focuses on nutrition evaluation and metabolic monitoring to achieve optimal and personalized nutrition therapy for critically ill patients. This guideline was developed by experts in critical care medicine and evidence-based medicine methodology and was developed after a thorough review of the system and a summary of relevant trials or studies published from 2000 to July 2023. A total of 18 recommendations were formed and consensus was reached through discussions and reviews by expert groups in critical care medicine, parenteral and enteral nutrition, and surgery. The recommendations are based on currently available evidence and cover several key fields, including screening and assessment, evaluation and assessment of enteral feeding intolerance, metabolic and nutritional measurement and monitoring during nutrition therapy, and organ function evaluation related to nutrition supply. Each question was analyzed according to the Population, Intervention, Comparison, and Outcome (PICO) principle. In addition, interpretations were provided for four questions that did not reach a consensus but may have potential clinical and research value. The plan is to update this nutrition assessment and monitoring guideline using the international guideline update method within 3–5 years.
Ultrasound for measurement of skeletal muscle mass quantity and muscle composition/architecture in critically ill patients: A scoping review on studies' aims, methods, and findings
2024, Clinical Nutrition
This scoping review aimed to identify, explore, and map the objectives, methodological aspects, and results of studies that used ultrasound (US) to assess skeletal muscle (SM) in critically ill patients.
A scoping review was conducted according to the Joanna Briggs Institute's methodology. All studies that evaluated SM parameters from the US in patients admitted to the intensive care unit (ICU) were considered eligible. We categorized muscle thickness and cross-sectional area as parameters for assessing SM quantity, while echogenicity, fascicle length, and pennation angle analysis were used to evaluate muscle “quality” (composition/architecture). A literature search was conducted using four databases for articles published until December 2022. Independent reviewers selected the studies and extracted data. Descriptive statistics were calculated to present the results.
A total of 107 studies were included, the majority of which were prospective cohort studies (59.8 %) conducted in general ICUs (49.5 %). The most frequent objective of the studies was to evaluate SM quantity depletion during the ICU stay (25.2 %), followed by determining whether a specific intervention would modify SM (21.5 %). Most studies performed serial SM evaluations (76.1 %). The rectus femoris muscle thickness was evaluated in most studies (67.9 %), followed by the rectus femoris cross-sectional area (54.3 %) and the vastus intermedius muscle thickness (40.2 %). The studies demonstrated the feasibility and reproducibility of US for SM evaluation, especially related to quantitative parameters. Most studies (70.3 %) reported significant SM quantity depletion during hospitalization. However, the accuracy of the US in measuring SM varied across the studies.
The lack of detailed description and standardization in the protocols adopted by the studies included in this scoping review precludes the translation of the evidence related to US for SM assessment into clinical practice.
Reliability and feasibility of skeletal muscle ultrasound in the acute burn setting
2023, Burns
Citation Excerpt :
During compression, the position of the rectus femoris in relation to the femur may have been altered, introducing further variability. In the presence of oedema, the maximum-compression technique is nonetheless the more appropriate choice as it is thought to better reflect true muscle size [32,55]. Maximum-compression also offers a solution for exceptionally large thighs that exceed ultrasound penetration.
Despite the impact of muscle wasting after burn, tools to quantify muscle wasting are lacking. This multi-centre study examined the utility of ultrasound to measure muscle mass in acute burn patients comparing different methodologies.
B-mode ultrasound was used by two raters to determine feasibility and inter-rater reliability in twenty burned adults following admission. Quadriceps muscle layer thickness (QMLT) and rectus femoris cross-sectional area (RF-CSA) were measured, comparing the use of i) a single versus average measurements, ii) a proximal versus distal location for QMLT, and iii) a maximum- versus no-compression technique for QMLT.
Analysis of twenty burned adults (50 years [95%CI 42–57], 32%TBSA [95%CI 23–40]) yielded ICCs of> 0.97 for QMLT (for either location and compression technique) and> 0.95 for RF-CSA, using average measurements. Relative minimal detectable changes were smaller using no-compression than maximum-compression (6.5% vs. 15%). Using no-compression to measure QMLT was deemed feasible for both proximal and distal locations (94% and 96% of attempted measurements). In 9.5% of cases maximum-compression was not feasible. 95% of RF-CSA measurements were successfully completed.
Ultrasound provides feasible and reliable values of quadriceps muscle architecture that can be adapted to clinical scenarios commonly encountered in acute burn settings.
Research impact: Where does the rubber hit the road?
2022, Australian Critical Care
Validation of bedside ultrasound to predict lumbar muscle area in the computed tomography in 200 non-critically ill patients: The USVALID prospective study
2022, Clinical Nutrition
Citation Excerpt :
Ultrasound is a promising bedside method, involving no radiation and can be longitudinally performed to assess body composition [7,8]. Until now, five studies related ultrasound muscle thickness of the thigh or upper arm to SMA in the CT at the L3 level in non- or critically ill patients (Supporting Information, Table S1) [3,9–12]. The studies varied in ultrasound measuring points, degree of ultrasound compression and muscle thickness evaluation (Supporting Information, Table S1).
Skeletal muscle area (SMA) in the computed tomography (CT) at the third lumbar vertebra (L3) level is a proxy for whole-body muscle mass but is only performed for clinical reasons. Ultrasound is a promising tool to determine muscle mass at the bedside. It is still unclear how well ultrasound and which ultrasound measuring points can predict CT L3 SMA.
This prospective observational trial included 200 non-critically ill patients, who underwent an abdominal CT scan for any clinical reason within 48 h before the ultrasound examination. Ultrasound muscle thickness was evaluated at 3 measuring points on the thigh and 2 measuring points on the upper arm with minimal compression. On the CT scan, the entire L3 SMA was measured based on Hounsfield units. Using a model selection algorithm based on the Bayesian information criterion (BIC) and clinical considerations, a linear prediction model for CT L3 SMA based on the ultrasound muscle thickness and other independent variables was fitted and assessed with cross-validation.
67,5% and 32,5% of the patients were from surgical and medical wards, respectively. Mean ultrasound muscle thickness values were between 2,2 and 3,6 cm on the thigh and between 1,4 and 2,8 cm on the upper arm. All ultrasound muscle thickness values were higher in men than in women (P < 0,05). CT L3 SMA was 40 cm² higher in men than in women (P < 0,001). The final prediction model for CT L3 SMA included the following 4 independent variables: ultrasound muscle thickness at the ventral measuring point of the thigh in the short-axis plane, sex, weight, and height. It had a similar BIC (BIC of 1515) compared to larger models with 6–8 independent variables including multiple ultrasound measuring points (BIC of 1506–1519). Additional clinical considerations to choose the final model were less time consumption when measuring a single ultrasound measuring point and better anatomical overview at the short-axis plane. The final model predicted CT L3 SMA with a R² of 0,74 (P < 0,001) and a cross-validated R² of 0,65.
One single ultrasound measuring point at the thigh together with sex, height and weight very well predicts CT L3 SMA across different clinical populations. Ultrasound is a safe and bedside method to measure muscle thickness longitudinally to monitor the effects of nutrition and physical therapy.

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Research paperAssessment of muscle mass using ultrasound with minimal versus maximal pressure compared with computed tomography in critically ill adult patients

Abstract

Background

Methods

Results

Conclusion

Introduction

Section snippets

Study design and setting

Results

Discussion

Conclusions

Conflict of Interest

Funding

CRediT authorship contribution statement

J Crit Care

Chest

Int J Surg

Crit Care Resuscit

Clin Nutr

Aust Crit Care

Clin Nutr

Low skeletal muscle area is a risk factor for mortality in mechanically ventilated critically ill patients

Crit Care

Skeletal muscle predicts ventilator-free days, ICU-free days, and mortality in elderly ICU patients

Crit Care

Association of energy and protein delivery on skeletal muscle mass changes in critically ill adults: a systematic review

JPEN - J Parenter Enter Nutr

Update on body composition tools in clinical settings: computed tomography, ultrasound, and bioimpedance applications for assessment and monitoring

Eur J Clin Nutr

Ultrasonography to measure quadriceps muscle in critically ill patients: a literature review of reported methodologies

Anaesth Intensive Care

Outcome measures in critical care nutrition interventional trials: a systematic review

Nutr Clin Pract

Prediction and validation of total and regional skeletal muscle mass by ultrasound in Japanese adults

Eur J Appl Physiol

Research paper
Assessment of muscle mass using ultrasound with minimal versus maximal pressure compared with computed tomography in critically ill adult patients