Abstract
Background
Different methods have been proposed to study skeletal muscle mass in sarcopenia diagnosis, although all have inherent drawbacks. The aim of this study was to evaluate the utility of muscle ultrasound in muscle assessment by studying its correlation with dual-energy x-ray absorptiometry (DXA) and calf circumference (CC), cut-off values for ultrasound-based detection of low muscle mass, and the correlation with muscle performance.
Methods
Fifty-seven participants older than 70 years, underwent a muscle ultrasound study, DXA, calf circumference (CC) and functional assessment. Ultrasound measurements were taken in the femoral quadriceps (transverse plane) and in the medial gastrocnemius (transverse and longitudinal planes). Muscle function was assessed by gait speed, Short Physical Performance Battery (SPPB) and grip strength.
Results
Median age was 78.9 years (IQR 74.9–81.9), and 33 were women (57.9%). We found good correlation between muscle thickness of gastrocnemius muscle in transverse and longitudinal plane and appendicular lean mass measured by DXA (r=0.546 and r=0.689 respectively) and good correlations between muscle thickness of gastrocnemius in transverse and longitudinal plane with CC (r=0.651 and r=0.447 respectively). The thickness of gastrocnemius medialis optimal cut-off points for low muscle mass were 18,5mm in the transverse plane (Sensitivity: 77,8%, Specificity: 77,1%), and 17.3mm in the longitudinal plane (Sensitivity: 100%, Specificity: 68.8%). Muscle thickness was also significantly correlated with gait speed, SPPB and grip strength.
Conclusions
Measures of gastrocnemius medialis thickness obtained by ultrasound are reliable and correlate well with DXA and CC values and muscle performance.
Key words: Ultrasound, dual-energy x-ray absorptiometry, aging, muscle mass and muscle performance
Introduction
Sarcopenia is an involuntary loss of skeletal muscle mass accompanied by loss of strength and/or physical performance. Loss of lean mass occurs gradually starting in the fourth decade of life and can be accelerated by other factors, such as sedentary lifestyle and nutritional disorders (1). The presence of sarcopenia is related to medium- and long-term adverse events, such as falls, functional decline, disability, loss of quality of life, and risk of institutionalization (2, 3, 4). In addition, sarcopenia is considered the central manifestation of frailty (5).
In 2019, the European Working Group on Sarcopenia in Older People (EWGSOP) published a consensus document, which addressed operational diagnostic criteria and diagnostic tools to reach the diagnosis (6). Different methods (magnetic resonance imaging [MRI] (7), computed tomography [CT] (7), dual X-ray absorptiometry [DXA] (6, 7), and bioelectrical impedance analysis [BIA] (8) have been proposed to study skeletal muscle mass in the diagnosis of sarcopenia. However, assessments are hampered by the inherent drawbacks of currently available tools (3, 6).
Magnetic resonance imaging (MRI) is currently considered the gold standard, since it enables accurate assessment of muscle mass, by identifying qualitative and quantitative changes with minimum exposure to low radiation. However, since high costs make it less accessible in practice, it is used almost exclusively for research purposes (7).
Computed tomography (CT) also enables accurate evaluation of muscle mass, although the inconvenience of radiation and high costs make it less accessible for diagnosis of sarcopenia (7).
Dual X-ray absorptiometry (DXA) is a low-radiation technique that is widely used in routine clinical practice to estimate appendicular lean muscle mass. However, it does not provide qualitative data (e.g., fat infiltration, atrophy, fibrosis, and vascularization), which are increasingly valued in the assessment of sarcopenia. Despite these drawbacks, DXA is currently the most widely recommended technique in clinical practice for sarcopenia diagnosis (6, 7).
Bioelectrical impedance analysis (BIA) is used to estimate body composition based on electrical conductivity. It is also an inexpensive, accessible, and easy-to-use method that allows quick measurement in both ambulatory and bedridden subjects, although it may overestimate or underestimate values in certain clinical processes (9). Anthropometric data, especially calf circumference, is accessible and inexpensive so, although it is as an indirect measurement, some authors have proposed it as a surrogate marker of muscle mass for diagnosing sarcopenia (10, 11) so it could be used in settings where there is no other alternative.
Finally, ultrasound (US) is a relatively inexpensive method that is accessible to clinicians, is easily performed at the bedside, and provides the possibility of evaluating not only quantitative parameters but also qualitative characteristics of the muscle. Furthermore, it enables periodic evaluation and monitoring of changes. The main limitation is that the results depend on the experience of the operator, appropriate calibration of the equipment, and standardization of the procedure so that it becomes reproducible. US has been suggested to be useful in the diagnosis of sarcopenia and interestingly, in monitoring the effects of treatment and interventions on muscles. The muscle can be measured anatomically by thickness (mm), length (mm), area (mm2), and pennation angle (angle of insertion of the muscle fiber into the aponeurosis). Previous studies reveal that the first two measurements are especially useful. In addition, US makes it possible to assess qualitative characteristics, such as degree of atrophy, muscle fibrosis, fatty infiltration, and vascularization. It also enables assessment of other structures (such as subcutaneous and intramuscular fat) and their relationship with muscle. Since loss of function is associated mainly with the muscles of the lower extremities, these parameters form the basis for our assessment of sarcopenia (8, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21). Quadricps femoris is the only extensor muscle in the lower limbs that links quadriceps femoris and vastus intermedius to functional capacity in older adults. The gastrocnemius is a powerful muscle, and its function is flexion and extension of the foot, so it is crucial for standing, walking, or running. Both muscles are easily recognized by US (superficial and straight muscle path), so non-expert operators can measure the function of these muscles with no difficulties and they both are mainly made of type II fibers which are specially reduced during sarcopenia.
Therefore, US might be an interesting tool for assessing muscle characteristics at lower limbs, and eventually used to detect the changes that occur with ageing and sarcopenia.
The aim of this study was to assess correlations between data obtained by US (muscular thickness of vastus intermedius and rectus femoris, cross-sectional thickness of the gastrocnemius medialis, length of the gastrocnemius medialis muscle fiber and pennation angle of gastrocnemius medialis) and other measures of muscle mass (appendicular lean mass estimated by DXA and CC). Additionally, cut-off values for ultrasound-based detection of low muscle mass, intra e inter-observator correlation and the correlation with functional performance.
Materials and Methods
Study design and study population
We performed an observational, descriptive, cross-sectional study. The study was approved by the Research Committee of Infanta Sofía University Hospital in March 2018. Data were obtained from May to September 2018. All participating subjects were informed of the characteristics of the study and gave their written informed consent for participation.
Participants were older than 70 years and were able to walk independently (measured using the Functional Ambulatory Classification [FAC] scale ≥ 3). The exclusion criteria included serious or unstable acute illness, hospitalization, a history of neuromuscular or muscular disease, fracture or lower limb surgery in the previous three months, pacemaker, prosthesis in the lower limbs, and/or terminal illness, including advanced dementia (Global Deterioration Scale score of 7), and severe sensory deficiency and/or severe cognitive impairment that prevented correct performance of the functional tests.
Protocol and study variables
Participants who met the selection criteria underwent a muscle US study, functional assessment, and DXA.
We collected demographic variables (age, sex, and race), anthropometric parameters (weight, height, body mass index [BMI], and calf circumference [CC]). Regarding CC, cutoff point of < 31cm for screening sarcopenia was used as recommend (6, 22)
It was also collected information on physical activity (number of hours of exercise per week), usual treatment (statins, corticosteroids, estrogens, and thyroid hormone) and clinical history (diabetes, hypertension, smoking and/or alcohol consumption, liver disease, heart failure, and/or respiratory disease).
Assessment of muscle function was based on several parameters: (1) short physical performance battery (SPPB), which measures balance, walking speed, and strength in lower limbs and is scored from zero to 12 (worst to best score) as described by Puthoff (18) and (2) grip strength as measured using a hand dynamometer (KERN & SOHN GmbH, Balingen, Germany, Model; Elect WOC11007248) following a standard protocol (patient preferably in sitting position in the dominant hand with the elbow at 90°). Maximum force was considered to be the highest value of three measurements separated by 1 min between each measurement.
Whole body DXA imaging was obtained using GE Healthcare Lunar Prodigy Advance DXA Scan at Infanta Sofía University Hospital following usual recommendations of protocol. The body composition data collected included absolute lean mass (Kg) of whole body, trunk, and limbs, total body fat and absolute bone masses (Kg), and percentage of fat mass (%). Appendicular lean mass (ALM) was the sum of lean mass from both arms and legs. Low muscle mass was established by appendicular lean body mass (ALM) as measured by DXA, and the selected cut-off points were recommended by Foundation for the National Institutes of Health Foundation (FNIH) Sarcopenia Project: (1) < 19.75 kg in men and (2) < 15.02 kg in women.
Assessment of muscle structure by ultrasound
The US study was carried out using a General Electric Logic F6 device with a linear probe (11.5 MHz) and abundant transducer gel to obtain the best-quality image with minimum pressure on the muscle.
The measurements were recorded three times by two different operators in B mode in the transverse plane of the femoral quadriceps and in the transverse and longitudinal planes of the gastrocnemius medialis. The quadriceps was assessed with the patient in a supine position with lower limbs relaxed. The area selected for study was the anterior thigh of the dominant side with the probe placed perpendicular to the longitudinal axis of the femoral quadriceps at the level of the midpoint of the distance between the greater trochanter and the external femoral condyle. This point corresponded to the thickest part of the rectus femoris muscle. The hyperechoic image corresponding to the cortex of the femur was taken as a bone reference and placed at the bottom of the screen. Subsequently, the image was centered by differentiating the subcutaneous cellular tissue, the rectus femoris, the vastus intermedius, and the lower part the cortex of the femur. For the transverse and longitudinal slices of the gastrocnemius medialis, the patient was in the prone position or sitting without exerting pressure on the legs, thus allowing maximum relaxation of the gastrocnemius. The probe was located at the junction of the proximal third and the calf, which is the point of maximum thickness of the gastrocnemius medialis on its inner face.
Thigh measurements were obtained as described below:
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Thickness of subcutaneous cellular tissue (mm): distance from the surface of the skin to the deepest edge of the subcutaneous cellular tissue.
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Muscular thickness of the anterior femoral compartment (vastus intermedius and rectus femoris): distance in mm between the most superficial fascia of the rectus femoris muscle and the cortex of the femur, including the vastus intermedius and the rectus femoris.
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Thickness of the rectus femoris muscle (relaxed and contracted): distance in mm between the superficial and deep fascia of the rectus femoris with the muscle relaxed. Subsequently, the patient is asked to contract the thigh by raising the leg approximately 15° with respect to the stretcher without flexing the knee. Once again, the measurement is taken with the muscle contracted, thus revealing an increase in length with respect to the measurement with the muscle relaxed.
Measurements of the gastrocnemius medialis included several areas (Figure 1):
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Thickness of subcutaneous cellular tissue: distance in mm from the skin surface to the deepest edge of the subcutaneous cellular tissue.
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Cross-sectional thickness of the gastrocnemius medialis in the transverse and longitudinal planes: distance in mm between the superficial and deep fascia of the muscle, both in the transverse plane and in the longitudinal plane.
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Length of the gastrocnemius medialis muscle fiber: a longitudinal slice enables us to visualize the muscle fibers that run through the muscle belly so that we can measure its length in mm from the superficial to the deep fascia.
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Pennation angle: the angle between the fascicles and the internal aponeurosis, reflects the orientation of the muscle fibers in relation to the connective tissue/tendon. The pennation angle will therefore affect the transmission of force to tendons and bones.
Figure 1.
Cross-sectional image of the gastrocnemius medialis (transverse plane)
Measurement 1: subcutaneous cellular tissue. Measurement 2: gastrocnemius medialis. The soleus muscle is visible at the bottom.
Several steps were taken into account in order to avoid the marked operator dependence that is typical of US. First, the assessment was made using a systematic protocol in order to reduce operator dependence. After placing the patient in the position first operator performed measurements three times (with an interval of 1 min between them) and recorded the results. Next, the second operator performed the same procedure in the same region. The patient was subsequently placed to examine the gastrocnemius region following the same sequence and protocol. Neither observer knew the results obtained by the other observer at the beginning of the assessment.
Statistical analysis
Categorical variables were expressed as frequency (n) and percentage (%). Quantitative variables were expressed as means and standard deviations when the variable was normally distributed and by median and interquartile range (IQR) when the variables were not normally distributed. The intraclass correlation coefficient with its 95% confidence interval (CI) was used to assess intra- and inter-observer correlations. The Spearman rho test was used to assess the correlation between US measurements and appendicular muscle mass. Comparisons between ultrasound measurements were made using the Mann-Whitney test.
The optimal cut-off values for the diagnosis of low muscle mass assessed by US (thickness of gastrocnemius medialis in transverse and longitudinal plane) was established using a ROC Curve. The area under the curve and the sensitivity and specificity values were also calculated.
The statistical analysis was performed using the STATA 13.0 package (StataCorp LP, USA). In all cases, statistical significance was set at p < 0.05.
Results
The study population consisted of 57 community-dwelling participants, of whom 33 were women (57.9%). The median age was 78.9 years (IQR 74.9–81.9). Table 1 shows baseline and demographic characteristics of the participants.
Table 1.
Baseline characteristics in participants
| Characteristics | Total (N=57) |
|---|---|
| Sex female — n (%) | 33 (57.9) |
| Age (years) — median [IQR] | 78.9 [74.9–81.9] |
| Diabetes mellitus- n (%) | 13 (22.8) |
| Hypertension — n (%) | 24 (42.1) |
| COPD — n (%) | 3 (5.3) |
| Abuse of alcohol — n (%) | 1 (1.8) |
| Abuse of tobacco — n (%) | 1 (1.8) |
| Chronic liver disease — n (%) | 0 (0.0) |
| Heart failure — n (%) | 3 (5.4) |
| Exercise less than 2 hours/week- n (%) | 18 (32.7) |
| Treatment with statins — n (%) | 25 (43.9) |
| Treatment with steroids — n (%) | 1 (1.8) |
| Treatment with estrogens — n (%) | 0 (0.0) |
| Treatment with thyroxin — n (%) | 6 (10.5) |
| Weight — (Kg) — median [IQR] | 66.7 [58.0–73.6] |
| Height — (cm) — median [IQR] | 157 [152–162] |
| Body mass index — median [IQR] | 27.1 [25.1–29.2] |
| Body surface — (m2) — median [IQR] | 1.7 [1.6–1.8] |
| Calf Circumference — (cm) — median [IQR] | 35 [32–37] |
Muscle thickness assess by US shows a significant positive correlation with ALM by DXA in both gastrocnemius medialis transverse (r=0.546, p<0.001) and longitudinal planes (r=0.689, p<0.001) (Figure 2).
Figure 2.
Correlation between muscle thickness assess by US and ALM by DXA
Thickness of gastrocnemius medialis ROC curves for low muscle mass (according to to ALM by DXA thresholds) had an area under curve of 0.831, (95% CI; 0.725–0.937) and 0.794 (95% CI: 0.670–0.771) in longitudinal and transverse planes, respectively (figure 3). The thickness of gastrocnemius medialis optimal cut-off points for sarcopenia were 18,5mm in the transverse plane (Sensitivity: 77,8%, Specificity: 77,1%), and 17.3mm in the longitudinal plane (Sensitivity: 100%, Specificity 68.8%).
Figure 3.
ROC curve (thickness of gastrocnemius medialis in longitudinal plane (A) and transverse (B) and ALM by DEXA
Cut-off point= 17.3mm (Sensitivity 100%, Specificity 68.8%); AUC 83,1% CI95% (72,5 – 93,7); Cut-off point= 18,5mm (Sensitivity 77.8%, Specificity 77.1%); AUC 79.4% CI95% (67,0 – 91,8)
Muscle thickness assess by US shows a significant positive correlatation with CC in both gastrocnemius medialis transverse (r=0,651, p<0.001) and longitudinal planes (r=0, 447, p<0.001) (figure 4).
Figure 4.
Correlations between muscle thicknesses assess by US in transverse and longitudinal planes and CC
Intraobserver correlation between the 3 measurements for each region shown coefficients ranging from 0.901 to 0.965, except for the measurement of the pennation angle, for which the coefficient was ranging from 0.738 to 0.820. The highest inter-observator coefficients correspond to measures of gastrocnemius medialis in both the transverse plane (r=0.867 CI95% [0.779–0.922]) and longitudinal planes (r=0.838 CI95% [0.733–0.903]).
Finally Gastrocnemius medialis thickness assesses by US show also a significantly and positive shows significant positive correlations with grip strength (Figure 5), SPPB (Figure 6) and gain speed (Figure 7), in both transverse and longitudinal planes.
Figure 5.
Correlations between muscle thickness and grip strength
Figure 6.
Correlations between muscle thickness and SPPB
Figure 7.
Correlations between muscle thickness and gait speed
Discussion
The aim of this study was to evaluate clinical US as a tool for assessing muscle architecture and its implications in the diagnosis of sarcopenia.
US is a non-invasive, low-cost, and accessible technique for assessing the morphology of skeletal muscle and has therefore been widely used in young people in many specialized areas, such as sports medicine, orthopedic surgery, and rehabilitation. These same advantages suggest that it may be a useful method for evaluating muscle characteristics in older patients who have sarcopenia although experience with this indication in this population remains limited or focused on physically robust healthy older adults, so the usefulness of US has yet to be defined in frail older adults or patients at very advanced ages.
The EWGSOP2 working group proposes various techniques for assessing muscle mass and although it considers CT and MRI to be the gold standards, it recommends DXA and BIA in clinical practice (6).
The results of this study suggest that assessment with US of gastrocnemius medialis in transverse and longitudinal planes is comparable to DXA with good correlations [correlations 0.567 and 0.627, respectively]) and calf circumference measure [correlations 0.651 and 0.447, respectively]). It also suggest cut-off points of measures at gastrocnemius medialis in transverse and longitudinal plane, for the diagnosis of low muscle mass (18,5mm and 17,3mm respectively). Finally authors find correlation between US measures and functional performance.
Kuyumcu et al. (23) also reported a significant correlation between DXA and US at the level of the gastrocnemius although their results were lower than ours (r = 0.59 and 0.52 for muscle thickness and fiber length, respectively). Other authors have focused on measuring muscle thickness at different sites with correlations ranging between 0.55 and 0.92. All investigations were conducted in a healthy population, mostly in men and patients with a younger average age (12, 24, 25, 26). Other authors have evaluated the cross-sectional area of the muscle (rectus femoris or vastus lateralis) with correlations ranging between 0.43 and 0.99 (27, 28). Similarly, we did not find a correlation with the pennation angle as reported elsewhere and concluded that this measure should probably not be used in the evaluation of sarcopenia (20).
Regarding intra- and inter-observer correlations, we found good correlation with coefficients greater than 0.8 in both cases at the level of thickness and length of the gastrocnemius medialis. In other studies, inter- and intra-observer reliabilities were estimated between 0.88 and 0.99 for various muscles (9, 29, 30, 31). Ticinesi et al. (8) reviewed published articles on muscle ultrasound and sarcopenia in older adults and analyzed different muscle areas and measurements, suggesting that it was better to measure muscle thickness than the pennation angle or qualitative parameters such as echogenicity, for which findings seem to be more variable.
We also compared US results with functional status based on muscle strength and function. We consider these results especially interesting since there is a significant correlation between US findings at gastrocnemius medialis measured in both transverse and longitudinal planes and gait speed, SPPB and handgrip strength.
Sarcopenia affects the whole body, so patients with severe sarcopenia could have lower muscle thickness and structural changes in lower limbs as they are functionally and severely affected. It appears that age-related muscle mass decline does not occur in all anatomic places at the same pace, and lower limb muscles are especially affected by sarcopenia in older population (24). Other authors have also described good correlation between hand grip strength and US measures in lower limbs (32). On the other hand, we need more research to explain why only gastrocnemius medialis measures correlates with the different measures done in the study but could not find this correlation with vastus intermedius and rectus femoris.
The relationship between functional parameters and ultrasound assessment of skeletal muscle has been studied by other authors. Ismail et al. (25) described the relationship between muscle strength and US in 20 subjects, and Abe et al. (24) used gait speed to measure function although neither group took into account both parameters (muscle strength and function), which are key components in the sarcopenia diagnosis. Ticinesi et al. (8) reviewed various studies that evaluated the relationship between muscle ultrasound and loss of function with correlations between 0.5 and 0.8. They found differences in methods as they evaluated other muscles, mainly the rectus femoris and quadriceps and various functional parameters (grip strength, zigzag gait, isometric strength of different muscle groups) mostly in young and healthy persons (20, 24, 26, 28, 31, 32, 33). However, none of these studies assessed the gastrocnemius. We used the recommended criteria (grip strength and SPPB) and cut-off points of the EWGSOP for diagnosing sarcopenia in older patients.
Other authors have studied relationship between echo intensity or qualitative aspects with functional parameters. Wilheim et al. (34) found a relationship between echo intensity of the quadriceps femoris and knee extension power and a 30 sec sit-to stand test in 50 healthy men. Rech et al. (32) described echo intensity that was negatively associated with functional capacity in 45 healthy active women, and Watanabe et al. observed an inverse association between echo intensity and muscle strength in men (21).
We used US to assess muscle structure in the lower limbs in older adults and investigated the association with functional performance. Our study was limited by its sample size and the lack of complementary qualitative parameters in the US evaluation. However, we believe that the results enable us to propose US as a useful tool for estimating muscle mass loss and use as an adjunct diagnostic procedure in sarcopenia diagnosis in older adults.
Using the results of the present study, the authors state that US measurements of the gastrocnemius medialis have good correlation with ALM as estimated by DXA and calf circumference and good relationship with functional performance. They propose cut-off values at gastrocnemius medialis for the diagnosis of low muscle mass.
With a well-defined examination protocol, it is possible to obtain good intra- and inter-observer correlations, which should enable us to extend the use of US in clinical practice without the major limitation of operator dependence.
Acknowledgments
The authors are very grateful to Dr. Esther Dominguez Franjo (Radiology Department) for her role in the DXA study and Carmen Saucedo Díaz (Nurse, Internal Medicine Department), who participated in the clinical evaluation. We also want to thank all the participants of the study for their collaboration, time and dedication for the development of the study. Finally the authors want to thank Dr. Rodriguez-Mañas for his considered review and suggestions to improve the paper.
Disclosure of interest
The authors declare that they have no conflicts of interest concerning this article.
Data statement
The data that support the findings of this study are available on request from the corresponding author (MNA). The data are not publicly available due to the contain information that could compromise the privacy of research patients.
Funding
This research received a funding from Foundation for Biomedical Research and Innovation of Infanta Sofía University Hospital and Henares University Hospital (FIIB HUIS HHEN) for grammar and spell check.
Ethical standards
The authors confirm that this research complies with the current laws of the country in which the study was performed. The study was approved by the Research Committee of Infanta Sofía University Hospital and participants gave informed consent to participate.
Electronic supplementary material
Supplementary material is available for this article at https://doi.org/10.1007/s12603-021-1669-4 and is accessible for authorized users.
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