To develop the universal scale for quantitative assessment of the muscle tone, we first measured and calculated the SWV in three situations. Using the multiple regression model constructed in the current study, we found that female sex and obesity significantly decrease the SWV. In addition, we finally constructed new single regression model and devised a unique adjustment method to improve the measurement accuracy of the SWVs.
The results shown in Fig. 1 indicated the muscle tone levels in the three conditions, which are keystones for the universal scale or quantitative assessment of muscle tone. At baseline condition, the SWV was 1.9 m/s. We assume that it reflects the level of muscle tone at rest, in the patient. Given that the patient was in supine position during measurements, muscle contraction for standing retention and gravity effects are considered negligible [14]. At opioid-induced rigidity conditions, the SWV was 2.2 m/s. However, interpreting this observation is difficult. An earlier report suggested that opioid-induced rigidity was equivalent to muscle stiffness with Parkinsonism [15]. Ding et al. reported that the shear wave velocity in the biceps brachii muscle of patients with Parkinson’s disease was 3.7 m/s [16]. This velocity is relatively faster than our results, and so the interpretation may be controversial. We presume that the measured SWV at opioid-induced rigidity condition is the same as muscle tone when one keeps the abdominal muscles tight.
As shown in Table 2, significant factors affecting the muscle tone were sex and body mass index. These two factors were used in the multiple regression model, but may not be independent of each other. Women have more body fat mass than men [17], and obesity is a state of excessive body fat accumulation [18]. Body fat mass may be the potential factor to decrease SWV. Body fat mass is classified into visceral fat and subcutaneous fat [19]. CT scan, MRI, and dual-energy X-ray absorptiometry quantify the visceral fat [19], while skinholds by using a caliper or ultrasound can measure the subcutaneous fat easily [19, 20]. We hypothesized that subcutaneous fat thickness would be a significant factor to reduce SWV based on the interpretation of multiple regression models (Table 2). We referred to the stored ultrasound images in which velocity was measured, and we retrospectively measured subcutaneous fat thickness. As shown in Fig. 2, in the both male and female patients, simple linear regression was fitted between subcutaneous fat thickness and the SWV. Next, using the regression model in the complete muscle relaxation conditions of the male and female, we adjusted the measured SWVs. The results shown in Fig. 3 indicated that the SWV was 1.8 m/s at reference (i.e., zero point), and that the SWV was 2.0 m/s at rest (~ 10% increase from the reference). In the opioid-induced rigidity condition, the SWV was 2.4 m/s (~ 30% increase from the reference). In all conditions, the individual differences were smaller than those before adjustment (Fig. 3), and the SWVs after the adjustment were thought to be useful at least as controls to assess the abdominal muscle tone.
One of the most important components of the proposed scale is the zero point. The adjusted SWV under the complete muscle relaxation condition, that is approximately 1.8 m/s, can be considered as a reference point. So far, to the best of our knowledge, such a reference velocity has not been reported in the past. We therefore compare shear wave velocity to those in softer organ than fully relaxed muscle. Barr et al. reported that the velocity in the liver was approximately 1.5 m/s [21, 22]. The value of 1.8 m/s may be reasonable reference point on the scale for assessment of muscle tone.
Our proposed adjustment for subcutaneous fat thickness is practical because it can be measured simultaneously with ultrasound manipulation when measuring velocity, and it is reasonable to assume that, for clinical use of SWV, the thicker the subcutaneous fat, the more likely it is that the ultrasound waves emitted by the echo probe will be attenuated by the subcutaneous fat [23]. It is a plausible explanation that thicker subcutaneous fat reduces SWV. Nevertheless, this adjustment may not be appropriate for other parts of the body, such as the neck, shoulders, waist, and lower limbs, where muscle stiffness often happens in clinical practice [10], because the subcutaneous fat thickness in each site varies even in the same individual [13]. Further investigation at the other sites is needed to generalize our proposed scale. If subcutaneous fat thickness-adjusted scales at the other sites are similar to that at the abdominal muscle, its scale may be universal for assessment of the muscle tone in medicine. For example, the adjusted-SWV values can be used to quantify the severity of conditions such as neck stiffness, frozen shoulder, or back stiffness associated with lower back pain, which are prevalent among middle-aged individuals. Measuring the adjusted-SWV values is also beneficial for identifying muscle weakness, such as ICU-acquired muscle weakness. This would be valuable in clinical practices in orthopaedics, rehabilitation, neurology, intensive care, and pain clinics. Moreover, based on the results of this study, SWV and its scale could potentially serve as an alternative to evaluating muscle relaxation during general anaesthesia, instead of train-of-four monitoring. If the surgical site is other than the abdomen and echo probe sterilization can be ensured, muscle relaxation can be evaluated using methods other than train-of-four monitoring, even in abdominal surgeries.
Moreover, at least based on the results of this study, SWV and its scale are possible to serve as an alternative to the evaluation of muscle relaxation using train-of-four monitoring during general anesthesia. If the surgical site is anywhere other than the abdomen and if echo probe sterilization can be ensured even in the abdomen, muscle relaxation can be evaluated using methods other than train-of-four monitoring.
One of the limitations of this study is the variety of anesthesia methods used during anesthesia induction. Inhaled anesthetics, (i.e., sevoflurane and desflurane), potentiate muscle relaxation and are weak muscle relaxants on their own [24]. Although this patient selection bias influences the measurement of the SWV, our regression models showed no statistically significant effect of inhalation anesthetic (Table 2). We guess that the effect of inhalation anesthetic may be small.
The other limitation of this study is that all measurements were by only one sonography examiner. Ultrasonography depends on the operator’s skill and experience and is not reproducible [25]. In the current study, we did not use the other methods in the measurement of the shear wave velocity and subcutaneous fat thickness except for ultrasound sonography. Also, when the examiner measured the subcutaneous fat thickness, he did not estimate the degree of fat infiltration into the abdominal muscle. Indeed, neuromuscular disease, disuse muscle atrophy, or sarcopenia induce the fat-rich muscle [26]. The possibility that the degree of fat content in muscle is related to muscle tone was not examined. As described above, these information biases may involve the present results in the study.
In conclusion, the present results suggest that shear wave elastography allows for quantification of the muscle tone in the abdomen and that significant clinical factors for decreasing SWV were female sex and high body mass index. The SWV adjusted for the subcutaneous fat thickness may be scale points of future universal scale for the assessment of muscle tone.
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