Muscle mass evaluation -
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Approaches to Assessment of Muscle Mass and Myosteatosis on Computed Tomography: A Systematic Review. Behrang Amini, MD, PhD , Behrang Amini, MD, PhD.
Department of Diagnostic Radiology, The University of Texas M. Anderson Cancer Center. Address correspondence to: Behrang Amini, MD, PhD, Department of Diagnostic Radiology, The University of Texas M. Anderson Cancer Center, Holcombe Blvd, Unit , Houston, TX E-mail: bamini mdanderson.
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Figure 1. Open in new tab Download slide. Figure 2. Table 1. Muscle Mass Assessment. Anatomic Landmarks.
Main Muscle Mass Measurement. Sarcopenia Cut Points Used. Male c. Muscle Thresholding Used. Threshold Range HU. Open in new tab. Table 2. Myosteatosis Assessment. Myosteatosis Cut Points b.
Main Myosteatosis Measurement. MyosteatosIs Cut Points Used. Used HU Threshold. Table 3. Image Analysis Details. Assessed Feature. Number of readers 1 97 38 2 53 21 3 7 3 Not specified 98 38 Segmentation methods Manual 27 Semiautomated 59 Automated 6 1.
Table 4. CT Acquisition Parameters. Google Scholar Crossref. Search ADS. The main objective of our study was evaluating muscle mass and quality through lower limb ultrasound in a cohort of COVID survivors.
As secondary objectives we performed i a correlation of the muscle ultrasound parameters with validated measures of muscle function, nutritional status and inflammatory indexes during hospital stay, ii an assessment of the association between muscle ultrasound parameters and probable sarcopenia and iii a definition of ultrasound parameters cut-off values associated with probable sarcopenia.
This was a cross sectional observational study. We evaluated patients attending a dedicated post-COVID outpatient clinic, who were previously hospitalized for SARS-CoV-2 pneumonia in the Internal Medicine Departments of the San Raffaele University Hospital, Milan, Italy The data presented in this study were collected in the visits that took place one month after hospital discharges, from the 15 th April till the 15 th July We are still collecting data on three- and six-months follow-ups.
The present study was part of the COVID-BioB study NCT , which aimed at characterizing hospitalized COVID patients, through the prospective collection of several demographic, anthropometric, clinical and laboratory variables, as previously described The COVID-BioB study protocol was approved by the San Raffaele University Hospital Ethics Committee protocol no.
A convenience sample size was used due to the setting of the COVID pandemic. During the follow-up visits, the patients underwent a multidimensional evaluation, consisting in: medical history, including self-reported weight loss during hospitalization, physical examination, anthropometric measurements to calculate the body mass index BMI , before hospital stay, and one month after hospital discharge, screening for sarcopenia through the Strength, Assistance with walking, Rising from a chair, Climbing stairs, and Falls SARC-F questionnaire 36 , assessment of muscle strength through the hand grip strength test 37 , evaluation of muscle performance with the Short Physical Performance Battery SPPB test 38 and screening for malnutrition with the Mini Nutritional Assessment Short Form MNA-SF questionnaire Patients suffering from dementia were generally helped by their care-givers in the compilation of the questionnaires.
Finally, all patients underwent muscle ultrasound of the dominant medial gastrocnemius, to assess muscle mass and quality. We chose to evaluate gastrocnemius muscle, because it has a pennate architecture, thus allowing the assessment of pennation angle.
Pennation angle is the angle formed at the fiber insertions into deep aponeurosis in pennate muscles and it is strongly correlated to muscle mass. Pennation angle was automatically calculated by the ultrasound software after the sonographer had manually identified the angle formed between muscle fiber insertions and deep aponeurosis.
By limb ultrasound, muscle quality can be assessed either with the determination of muscle echogenicity 40 , 41 , or with muscle stiffness However, there is no consensus on which of these parameters should be preferred, in the assessment of muscle quality by limb ultrasound.
Therefore, since our radiologists had more experience in the evaluation of muscle stiffness, we chose to investigate this aspect of muscle quality. During muscle ultrasound, the patients laid prone on the examination couch, with the foot positioned perpendicularly to the tibia outside the couch.
The ultrasound examinations were performed by two trained sonographers SD and MC. To improve acoustic coupling, abundant water-soluble transmission gel was used on the linear array probe MHz, General Electric model , using B-mode. The probe was set perpendicularly to the dermal surface, to get images, including both superficial and deep aponeurosis, and with an orientation coinciding with that of the muscle fascicles between the aponeuroses.
Images were obtained along the mid-sagittal line of the medial gastrocnemius at the mid-distance between its proximal and distal tendon insertions 43 , Depth was initially set at 30 mm, then it was modified during the examination range: mm to visualize the entire muscle thickness.
Resting Euclidean distance between the internal borders of the superficial and deep aponeuroses i. muscle thickness was assessed in three points of the muscle, equally spaced along the image, and a mean value was calculated. In addition, the angle between the fascicle and the deep aponeurosis i.
pennation angle was calculated. Images were stored as DICOM files, and transferred to a computer for processing. Muscle stiffness was measured by means of an AGFA Enterprise Imaging program.
The size of regions of interest ROI , to estimate the stiffness index SI , was set between 0. ROI were measured in three points of the medial gastrocnemius, equally spaced along the images.
Then a mean value of the three SI obtained, was calculated. The baseline characteristics of the study population, the main aspects of the COVID hospitalization, muscle and nutritional parameters one month after hospital discharge were described through descriptive statistics.
Continuous variables were presented as mean and standard deviation SD , when normally distributed, or with median and interquartile range IQR , when data had a skewed distribution. Comparisons were made with the chi-squared test for categorical variables, and with the Mann-Whitney U test, for continuous variables.
Cut-off values for muscle performance and strength were chosen, according to the European Working Group on Sarcopenia Guidelines 1 and to literature data We assessed the correlations between muscle ultrasound characteristics muscle thickness, pennation angle and muscle stiffness , measures of muscle function SPPB and Hand Grip Strength , nutritional status MNA-SF , age, SARC-F, inflammatory indexes [highest C Reactive Protein CRP and number of days with CRP above the upper normal limit, highest ferritin during hospital stay, highest white blood cells during hospital stay WBC ] and length of hospital stay through Spearman correlations.
Probable sarcopenia was defined as a reduced muscle strength at the hand grip test, accordingly to the European Working Group on Sarcopenia Guidelines 1. Binary logistic regression analyses were used, to assess the association between muscle ultrasound parameters, and probable sarcopenia.
Unadjusted and stepwise adjusted models were performed. Collinearity tests were run before performing the adjusted model; collinear variables were excluded from the multivariable model, and just one proxy of the severity of SARS-CoV-2 infection Non-Invasive Mechanical Ventilation and of clinical complexity before hospital admission number of chronic therapies were inserted in the model, in addition to the significant predictors at the univariable analyses.
Finally, we performed ROC analyses, to identify optimal cut-off values of muscle ultrasound characteristics thickness, stiffness and pennation angle associated with probable sarcopenia. The Area under the curve AUC was calculated as a summary of diagnostic accuracy. All statistical analyses were performed with SPSS version Two hundred and fifty-nine patients seen at a dedicated post-COVID outpatient clinic, were included in the study.
Table 1 shows the main baseline characteristics of the study population. Table 2 illustrates the main characteristics of their COVID hospitalization. Table 1 Baseline characteristics of the study population and their comparison among groups with pathologic and normal values of a sarcopenia screening tool,muscle strength and performance.
Table 2 Main characteristics of the COVID hospitalization of the study population and their comparison among groups with pathologic and normal values of a sarcopenia screening tool, muscle strength and performance.
Table 3 Muscle and nutritional characteristics one month after hospital discharge of the study population and their comparison among groups with pathologic and normal values of a sarcopenia screening tool, muscle strength and performance.
The comparisons between patients with pathological versus normal values of muscle function and of SARC-F are shown in Tables 1 — 3. Many patients presented an overlap of pathological tests as illustrated by the Venn Diagram in Figure 1. Figure 1 Number of people with a pathologic value of a sarcopenia screening tool, hand grip strength and muscle performance test.
SARC-F, Screening tool for sarcopenia; SPPB, Short Physical Performance Battery. The patients with an impaired muscle function or with a pathological SARC-F score were older and more often females, compared to individuals with a normal muscle function. They had a lower weight and a higher burden of chronic therapies, both before hospital admission and one month after hospital discharge.
Furthermore, their muscle stiffness was higher. Pennation angle and weight loss during hospital stay did not differ. Muscle thickness was significantly lower in patients with reduced versus those with normal muscle strength 1. This finding was confirmed in patients with reduced versus those with normal muscle performance 1.
Muscle stiffness was higher in patients with reduced muscle strength compared to patients with normal muscle strength 87 versus Also in patients with reduced muscle performance muscle stiffness was higher compared to patients with normal muscle performance Figure 2 illustrates the muscle US images of a patient with reduced muscle strength i.
probable sarcopenia and of a patient with normal muscle strength. Figure 2 Comparison of the limb ultrasound images of a patient with A and without probable sarcopenia B. A Muscle thickness: 1. RED DOTTED ARROW: muscle thickness; ORANGE ARROW: muscle deep aponeurosis; BLU CIRCLE LINE: pennation angle; GREEN line: muscle fascicle length.
The patients with a pathological muscle performance were more comorbid than patients with normal muscle performance. Table 4 shows the results of the Spearman correlations among muscle ultrasound characteristics, and the measures of muscle function and nutritional status, age, inflammatory indexes, and length of hospital stay.
Table 4 Spearman correlations among muscle ultrasound characteristics, measures of muscle function and nutritional status, age, inflammatory indexes and length of hospital stay.
We detected significant direct correlations, between muscle thickness and pennation angle p 0. Pennation angle had a direct correlation with nutritional status p 0. Instead, muscle stiffness showed a direct correlation with age p 0. Muscle stiffness had an inverse correlation with grip strength p At the univariable binary logistic regression model age OR 1.
Muscle stiffness adjusted OR 1. Cut-offs for probable sarcopenia identified by the ROC analyses were as follows: 1. The results for pennation angle were not statistically significant AUC 0. ROC curves are illustrated in Figures 1S—3S. In this observational study, we found that one month after hospital discharge, COVID survivors with reduced muscle function displayed low muscle mass and increased muscle stiffness at the ultrasound evaluation of the dominant medial gastrocnemius as compared with those with normal muscle function.
The finding of increased muscle stiffness was confirmed in patients with a pathological SARC-F score too. Moreover, we detected a significant correlation between muscle ultrasound parameters and age, nutritional status and muscle performance. Finally, we detected an association between muscle stiffness and probable sarcopenia and with the ROC analyses we identified the cut-offs of the muscle ultrasound parameters, associated with probable sarcopenia.
Our findings refer to preliminary data, collected one month after hospital discharge. The 3 and 6 months follow ups of the patients of this study are ongoing. Indeed, it is of paramount importance to continue follow up visits over time, because it has been reported that musculoskeletal symptoms can persist 3 and 6 months after hospitalization in COVID survivors Assessing whether these symptoms are underpinned by alteration of muscle function, mass and quality will allow the characterization of the COVID disease on muscles, and the long-term effects of acute sarcopenia, that are presently unknown Our results on the negative correlation between both muscle thickness and age, and pennation angle and age are in line with the typical architectural remodelling of ageing 47 characterized by decreased muscle size, and reduced pennation angles Indeed, muscle thickness and pennation angle are characteristics of the muscle architecture, that are strongly related one to the other, as previously demonstrated by Kubo 49 , and as confirmed in our study.
Detecting changes in muscle architecture is of extreme importance, since these alterations have an impact on the mechanical behaviour of muscles Our study confirmed the presence of a significant correlation between muscle ultrasound characteristics and measures of muscle function.
Moreover, we found a significant correlation between muscle ultrasound aspects and nutritional status evaluated with the MNA-SF. Malnutrition, particularly when disease-associated, is known to be associated with alterations in body composition and reductions in fat free mass Both the European Society of Clinical Nutrition and Metabolism 52 and the Global Leadership Initiative on Malnutrition 53 guidelines recommend the evaluation of fat free mass as a diagnostic criterion for malnutrition.
Therefore, the association of a malnutrition screening tool with impaired measures of muscle mass and quality is not surprising. Muscle ultrasound is a simple and non-expensive tool to assess skeletal muscle characteristics, and could be a valuable instrument for the screening of malnutrition.
Our finding is in line with the study by Mateos-Angulo et al. Compared to the study of Minetto et al. However, Minetto et al. considered a small sample 44 people of institutionalized pre-frail and frail older adults mean age Our data on muscle thickness are more in line with the findings of Kubo et al.
Differently from Kubo, the median values of the pennation angle, were higher in our sample Anyway, the measurement of the pennation angle is strongly influenced by the pressure that the sonographer exerts on the muscle, and further data are needed to define normal and pathological values of this parameter in older people.
Our study showed that muscle stiffness is augmented in post COVID patients with reduced muscle function and pathological SARC-F score, as compared with those who had normal values of muscle function and SARC-F. Since we measured muscle stiffness with muscles in a resting condition, our finding refers to passive muscle stiffness.
Passive muscle stiffness is an important characteristic, since it regulates the interactions between body and environment. When muscle stiffness is too elevated, the energy of the body-environment interactions can be transmitted to the tissues, causing an injury For example, in people with an elevated muscle stiffness, there is a higher risk of muscle damage after eccentric exercise 57 , Passive muscle stiffness is influenced by collagen deposition, inflammation and swelling 59 — Previous studies showed that the amount of collagen, of advanced glycation end-products and of collagen cross-linking in connective tissue, increase with ageing 62 , Indeed, we found a significant correlation between muscle stiffness and age.
In addition to increasing muscle stiffness [as demonstrated in aged 64 and sarcopenic muscles 65 ], the alterations of the extracellular matrix may also favour muscle mass decrease.
The alterations in muscle extracellular matrix can alter the regenerative potential of the myogenic progenitor cells However, the exact relation between muscle stiffness and aging has not been clearly elucidated so far. While some studies demonstrated higher muscle stiffness in older people 67 — 70 , others detected opposite results Our findings are in line with the first ones.
In this study we identified possible muscle ultrasound parameters cut-offs, for probable sarcopenia. Muscle ultrasound is a non-invasive, little expensive and low time-consuming technique.
As such, it could potentially be considered an optimal screening test for probable sarcopenia. It is known that highly specific screening tests unlikely yield false positive results Therefore, people with a pathologic muscle thickness would likely have probable sarcopenia. Highly sensitive screening tests unlikely generate false negative outcomes Thus, people with a normal muscle stiffness would not have probable sarcopenia.
These results indicate that muscle ultrasound has a low accuracy in detecting probable sarcopenia, compared to the gold standard hand grip test. Anyway, these results refer to a preliminary and reduced sample, and could be improved by future wider studies.
Moreover, muscle ultrasound could be used as a complementary technique to hand grip test to assess the morphologic characteristics of skeletal muscle in patients with probable sarcopenia.
Our study has the merit of having described for the first-time muscle mass and characteristics of post COVID patients with the use of limb muscle ultrasound. Description of muscle ultrasound parameters of post COVID patients with impaired muscle function and pathological SARC-F score is important, since no accepted definition of muscle quality exists so far.
Characterizing the changes of muscle architecture through a non-invasive and easy to use tool as echography would provide information to better define muscle quality.
Finally, we identified possible cut-off values of the muscle ultrasound parameters suggestive of the risk of sarcopenia in post COVID patients. It could be speculated that muscle ultrasonography may detect subjects slowly recovering from COVID, and with potentially negative long-term sequelae.
Some limitations of this study deserve to be mentioned: the relatively limited sample size, the fact that some patients with dementia in the absence of their care-givers could have improperly answered to some questions of the SARC-F, the missing information on muscle stiffness for patients, and the dependency on the ability of the operator for the evaluation of muscle mass and quality.
However, the main aim of our study was to characterize muscle mass and quality by muscle ultrasound in a population prone to skeletal muscle impairment 19 , 20 , and to assess the association of ultrasound parameters with established tools for the assessment of the risk of sarcopenia.
Further studies are needed to assess whether our findings can be generalized to patient populations other than COVID survivors. Finally, an important limit is that we did not compare ultrasound muscle characteristics against reference methods for measuring fat free mass, such as dual-energy X-ray absorptiometry, CT or MRI.
In the future, wider, multicenter studies will help better define the role of ultrasound for the evaluation of muscle quantity and quality, and correlate these data to relevant clinical outcomes. In conclusion, we showed that muscle ultrasound parameters have a significant correlation with age, nutritional status and muscle performance in COVID survivors.
Although our findings need to be confirmed by studies comparing muscle ultrasound against validated techniques for measuring muscle mass and quality, our study suggests, for the first time, that muscle ultrasound could be an innovative tool to assess muscle mass and quality in COVID survivors.
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation. The studies involving human participants were reviewed and approved by San Raffaele University Hospital Ethics Committee protocol no. All authors made substantial contributions to all of the following: 1 the conception and design of the study, or acquisition of data, or analysis and interpretation of data, 2 drafting the article or revising it critically for important intellectual content, 3 final approval of the version to be submitted.
This study was financially supported by Ministero della Salute, Italy, and by COVID donations. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
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