Quantification of muscle tone using shear-wave velocity during anaesthesia induction: a prospective observational study

doi:10.21203/rs.3.rs-1948429/v1

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Quantification of muscle tone using shear-wave velocity during anaesthesia induction: a prospective observational study

https://doi.org/10.21203/rs.3.rs-1948429/v1

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Purpose

Shear-wave elastography is a non-invasive ultrasound method that provides quantitative information on the elasticity of soft tissues. However, a universal velocity scale for quantification has yet to be developed. This study aimed to determine the shear-wave velocities (SWVs) of the abdominal muscles during anaesthesia induction for future development of a universal scale.

Methods

We enrolled 75 adult patients who received elective surgery with an American Society of Anesthesiologists physical status of I–III from December 2018 to March 2021. We measured and calculated the SWVs before and after opioid administration (baseline at rest and opioid-induced rigidity condition) and after muscle relaxant administration (zero reference condition). The SWV value was adjusted for subcutaneous fat thickness using our proposed corrections. The SWVs after the adjustment were compared among the values at baseline, opioid-induced rigidity, and complete muscle relaxation using one-way repeated-measures analysis of variance and post-hoc Tukey–Kramer tests. Significance was set at p < 0.05.

Results

The SWVs in the baseline, opioid-induced rigidity, and complete muscle relaxation conditions after adjustment were 2.08 ± 0.48, 2.41 ± 0.60, and 1.79 ± 0.30 m/s, respectively (p < 0.001 for all comparisons).

Conclusion

The SWV as reference was 1.8 m/s, and the SWVs at rest and opioid-induced rigidity were ~ 10% and ~ 30% higher than the reference, respectively. SWV adjusted for subcutaneous fat thickness may be a scale point for the assessment of muscle tone.

Clinical trial registration:

UMIN Clinical Trials Registry identifier UMIN000034692, registered on October 30th, 2018

muscle stiffness

shear-wave elastography

neuromuscular blockade

general anaesthesia

Assessing muscle stiffness is essential for medical care. Overexercise or poor posture causes chronic muscle tightness and affects daily activities and quality of life [1]. In orthopaedic and rehabilitation medicine, sprains and strains are the most common causes of muscle stiffness [2]. Pain, anxiety, and depression cause increased muscle tension, which leads to significant myofascial pain [3]. Muscle weakness has also been observed during medical care. Neuromuscular disorders, hypothyroidism, and electrolyte imbalance result in muscle weakness [4–6]. Sarcopenia is a progressive skeletal muscle disorder involving accelerated loss of muscle mass and function and is associated with increased adverse outcomes, including falls, functional decline, frailty, and mortality [7]. In intensive care, intensive care unit-acquired weakness after long-term mechanical ventilation is a strong risk factor for death [8]. Thus, physicians need to quantitatively determine muscle stiffness or weakness in patients.

Shear-wave elastography is a non-invasive ultrasound method that provides quantitative information on the elasticity of soft tissues [9]. This method uses an acoustic pulse to produce shear waves that propagate perpendicularly to the muscle. Previous research has reported a linear relationship between shear-wave velocity and muscle stiffness [10]. A faster velocity reflects increased muscle tone [11]. However, a universal velocity scale for quantitative assessment by healthcare providers has not yet been developed.

In this study, we investigated two situations: opioid-induced muscle rigidity and complete muscle relaxation. Opioid-induced muscle rigidity is called lead-pipe rigidity during anaesthetic induction for surgery and wooden chest syndrome in intensive care [12, 13]. In addition, completely relaxed muscles are produced by administering muscle relaxants during anaesthetic induction. This study aimed to measure shear-wave velocities in these situations and to determine a universal scale for the quantitative assessment of muscle tone. This study was prepared according to the STROBE statement [14].

Participants

This was a prospective cohort study. The inclusion criteria were age of > 20 years, an American Society of Anesthesiologists (ASA) physical status classification of I–III, and scheduled for elective surgery under general anaesthesia at the Tohoku University Hospital from December 2018 to March 2021. Patients with neuromuscular diseases or allergies to neuromuscular relaxants were excluded. Written informed consent was obtained from all patients before study participation. Information regarding pre-existing medical history, age, sex, height, weight, ASA physical status classification, and type of surgery was collected from the electronic medical record system.

Experimental protocol in induction of general anaesthesia

All patients were placed in supine on an operating table. Electrocardiography, non-invasive blood pressure, body temperature, and oxygen saturation were monitored. Four treatments were applied every 5 min to induce general anaesthesia. First, 6 L/min oxygen was administered to the patient via a face mask. Second, 5 min after the start of pre-oxygenation, 0.5 mg/kg/min continuous infusion of remifentanil was administered intravenously. Third, 5 min after the start of remifentanil administration, general anaesthesia was induced by 0.5–2 mg/kg of propofol. A muscle relaxant (0.8 mg/kg of rocuronium bromide) was administered intravenously to abolish muscle tone. Anaesthesia was maintained with 3–6 mg/kg/h continuous infusion of propofol, 1–2% sevoflurane, or 3% desflurane. Finally, after 5 min of anaesthetic maintenance, the airway was secured by endotracheal intubation, and positive mechanical ventilation was performed in all patients. Muscle tone was evaluated at three time points: 1) oxygen alone before remifentanil administration (baseline), 2) remifentanil administration before propofol administration (opioid-induced rigidity), and 3) after rocuronium administration (complete muscle relaxation). The primary endpoint was the muscle tone during complete muscle relaxation. The secondary endpoints were the muscle tones at both baseline and opioid-induced rigidity.

Ultrasound examination for evaluation of muscle tone

A diagnostic ultrasound system (Acuson S3000, Siemens Medical Solutions USA, Inc., Malvern, PA, USA) with a linear array transducer (9L4, 4–9 MHz, Siemens) was used to evaluate muscle tone. All the measurements were performed by a single examiner (H.S.). An examiner handled the probe without pushing it, scanned the abdominal rectus muscle near the umbilicus, and obtained B-mode images of the horizontal axis at the end of expiration. Next, the examiner selected the virtual touch imaging quantification mode for shear-wave elastography. Three regions of interest were determined at the midpoint between the superficial (ventral) and deep (dorsal) fasciae of the abdominal rectus muscle. The velocity, which reflects muscle elasticity, was measured in each region using shear-wave elastography. On the longitudinal axis, the three velocities were measured in the same manner. The average velocity values in the six regions were calculated as the shear-wave velocity (SWV). The average distance between the superficial and deep fasciae was calculated as the abdominal muscle thickness. The ultrasound image was saved in the JPEG format to prepare for later verification. In this digital image, subcutaneous fat thickness was measured in the same six areas in which the velocity values were measured. We used the mean of the six thickness values in subsequent analysis.

Statistical analysis

Numerical data are presented as mean ± standard deviation. A one-way repeated measures analysis of variance (ANOVA) and a subsequent Tukey–Kramer multiple comparison test were performed to compare the SWVs or abdominal muscle thickness among the three time points in the patients. We also performed a multiple linear regression analysis, with the threshold p-value set to 0.2 to five factors. The three factors that were considered potential confounders were age, sex, and body mass index [15]. The two factors that were considered potential effect modifiers were the surgical procedure and use of inhalational or intravenous anaesthesia. The significant factors were evaluated in subsequent single linear regression models to verify the hypothesis and perform a sensitivity analysis (see the Results section). All analyses were performed using the JMP Pro Version 16 for Windows (SAS Institute Inc., Cary, NC, USA). Significance was set at p < 0.05. The theoretical sample size needed for this study was designed to have a power of 1-β: > 0.9 to detect a difference in one-way ANOVA based on the effect of a 25% change in the standard deviation (0.5 m/s) of SWVs (α < 0.05). Consequently, the sample size was calculated to be 207 measurements (207 measurements / 3 times per patient = 69 patients).

Opioid-induced rigidity increased the abdominal muscle tone, and complete muscle relaxation decreased the tone

A total of 75 patients were included in the study. Table 1 summarises the patient demographics. Figure 1 presents the chronological changes in the SWVs. At baseline, the SWV was 1.91 ± 0.51 m/s. At the opioid-induce rigidity, the SWV was 2.24 ± 0.65 m/s, and it was faster than that at baseline (p = 0.0005). At complete muscle relaxation, the SWV was 1.61 ± 0.38 m/s, which was lower than that at baseline (p = 0.0014). In abdominal muscle thickness, no significant difference was observed among the three situations as follows: 0.82 ± 0.18 cm at baseline, 0.82 ± 0.17 cm during opioid-induced rigidity, and 0.82 ± 0.17 cm at complete muscle relaxation (p = 0.98).

Table 1

Patient characteristics
	Patient data
Total number	75
Age (years)	60 ± 16
Sex
Male	29 (39%)
Female	46 (61%)
Body mass index	24 ± 4
ASA-PS
1	7 (9%)
2	50 (67%)
3	18 (24%)
Type of surgery
Abdominal	57 (76%)
Non-abdominal	18 (24%)
Anaesthesia
Inhalational	32 (43%)
Intravenous	43 (57%)
Data are presented as the mean ± standard deviation or number (percentage). ASA-PS, American Society of Anesthesiologists physical status.

Sex and body mass index as significant factors affecting muscle tone

To estimate the effects of the coefficients on SWV and to reduce selection bias, we used three multiple regression models at each time point (Table 2). The female sex was an independent factor in decreasing SWVs in both opioid-induced rigidity and complete muscle relaxation. In addition, a higher body mass index was an independent factor in decreasing SWVs at all the time points.

Table 2

Multivariate models for muscle tone values during anaesthesia induction
	Baseline			Opioid-induced rigidity			Complete muscle relaxation
	Estimate	95%CI	p value	Estimate	95%CI	p value	Estimate	95%CI	p value
Intercept	3.16	2.36–3.96	< 0.0001	3.76	2.76–4.75	< 0.0001	2.07	1.46–2.68	< 0.0001
Age (years)	−0.0009	−0.10–0.01	0.84	−0.005	−0.02–0.01	0.41	−0.0007	−0.01–0.01	0.83
Female	−0.05	−0.18–0.07	0.40	−0.21	−0.37–0.05	0.01	−0.10	−0.20 – −0.05	0.04
BMI (kg/m²)	−0.05	−0.08 – −0.03	0.0002	−0.05	−0.08 – −0.02	0.002	−0.02	−0.04–0.00	0.04
Abdominal surgery	−0.07	−0.21–0.07	0.31	0.01	−0.16–0.18	0.90	0.006	−0.10–0.11	0.91
Inhalational anaesthesia	0.04	−0.10–0.18	0.59	−0.09	−0.26–0.08	0.30	0.05	−0.06–0.16	0.35
BMI, body mass index; 95%CI,95% confidence interval.

Adjustment for subcutaneous fat thickness reduces individual differences in SWV

As described above, the female sex and high body mass index were significant factors that reduced the SWVs; therefore, we examined whether subcutaneous fat thickness was an alternative potential factor. We constructed a single linear regression model between subcutaneous fat thickness and SWVs in each sex subpopulation. Figure 2 presents the six models at the three time points. The calculated three y-intercepts in the female patients were lower than those in the male patients. The calculated three slopes (i.e. the reduction effect of increasing thickness on the SWVs) in the male patients were higher than those in the female patients. In both the female and male patients, the reduction effect of increasing thickness on SWVs was similar among all the three time points.

In our model of the complete muscle relaxation, if we standardize on being male, having a subcutaneous fat thickness of 1.0 cm, which is average in adult Japanese men [15], the predicted SWV was approximately 1.8 m/s (− 0.45 × 1.0 + 2.27). Consequently, we devised the following correction equations, so that the SWV approaches 1.8 m/s, cancelling the effects of being female and subcutaneous fat thickness:

Figure 3 presents the chronological changes in SWVs adjusted for subcutaneous fat thickness. At baseline, the adjusted SWV was 2.08 ± 0.48 m/s. At opioid-induced rigidity, the SWV was 2.41 ± 0.60 m/s, which was faster than that at baseline (p = 0.0001). At complete muscle relaxation, the SWV was 1.79 ± 0.30 m/s, which was lower than that at baseline (p = 0.0006).

To examine the changes in muscle tone after pharmacological intervention, we first measured and calculated SWV in three situations. Using the multiple regression model constructed in the current study, the female sex and obesity were identified to significantly decrease the SWV. In addition, we constructed a new single regression model and devised a unique adjustment method to improve the measurement accuracy of SWVs. We hypothesised that the adjusted SWV values were keystones for the universal scale or quantitative assessment of muscle tone.

The results presented in Fig. 1 showed that shear-wave elastography quantified the abdominal muscle tone. To the best of our knowledge, this is the first report of shear-wave elastography under special conditions of anaesthetic administration. Surprisingly, shear-wave elastography was able to measure and quantify changes in muscle tone, despite the lack of muscle thickening that occurs with muscle contraction. At baseline, the SWV was 1.9 m/s; this may reflect the level of muscle tone at rest in a patient. Considering that the patient was in supine during the measurements, the effects of muscle contraction for standing retention and gravity were considered negligible [16]. Under opioid-induced rigidity conditions, the SWV was 2.2 m/s. However, this observation is difficult to interpret. An earlier report has suggested that opioid-induced rigidity is equivalent to muscle stiffness in Parkinsonism [17]. Ding et al. have reported that the SWV in the biceps brachii muscle of patients with Parkinson’s disease was 3.7 m/s [18]. This velocity is relatively higher than that in our results; therefore, the interpretation may be controversial.

As presented in Table 2, sex and body mass index were significant factors affecting muscle tone. These two factors were used in the multiple regression model; however, they may not be independent of each other. Women have higher body fat mass than men [19], and obesity is a state of excessive body fat accumulation [20]. Body fat mass may be a potential factor in decreasing the SWV, and it is classified as either visceral or subcutaneous [21]. Computed tomography scan, magnetic resonance imaging, and dual-energy X-ray absorptiometry quantify visceral fat [21], while a calliper or ultrasound can easily measure subcutaneous fat through skinfolds [21, 22]. Thus, subcutaneous fat thickness may be a significant factor in reducing SWV based on the interpretation of multiple regression models. We referred to the stored ultrasound images in which the velocity was measured, and we retrospectively measured subcutaneous fat thickness. As presented in Fig. 2, in both the male and female patients, a simple linear regression was fitted between subcutaneous fat thickness and SWV. Next, using the regression model for the complete muscle relaxation conditions of the male and female patients, we adjusted the measured SWVs. The results presented in Fig. 3 indicate 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 the conditions, the individual differences were smaller than those before adjustment; standard deviations were smaller (Fig. 3), and the probability of rejecting the null hypothesis in statistical comparisons was also smaller than that before adjustment. The SWVs after adjustment may be useful as controls to assess abdominal muscle tone. Quantification of the SWV will be possible as a goal when treating muscle stiffness, for example, by lowering it to approximately 2.0 m/s. In rehabilitation medicine, chronological measurement of SWV can be used to quantify the effect of rehabilitation (e.g. passive motion on joint stiffness) [23]. In perioperative or critical care, monitoring of SWVs may be an indicator for reversing opioid overdoses with naloxone. The three values (i.e. 1.8, 2.0, and 2.4 m/s) may be used as scale points for the assessment of muscle tone.

One of the most important components of the proposed scale was a zero point. The adjusted SWV under the complete muscle relaxation condition, which was approximately 1.8 m/s, can be considered as a reference point. To the best of our knowledge, such a reference velocity has not been previously reported. Therefore, we compared SWV in softer organs to that in fully relaxed muscles. Barr et al. have reported that the velocity in the liver was approximately 1.5 m/s [24, 25]. The value of 1.8 m/s may be a reasonable reference point on the scale for the 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 [26]. A plausible explanation is 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 occurs in clinical practice [27] because the subcutaneous fat thickness at each site varies even in the same individual [15]. Further investigation at other sites is required to generalise the proposed scale. If subcutaneous fat thickness-adjusted scales at other sites are similar to those at the abdominal muscle, the scale may be universal for the assessment of muscle tone in medicine.

One of the limitations of this study is the variety of anaesthesia methods used during anaesthetic induction. Inhaled anaesthetics (i.e., sevoflurane and desflurane) potentiate muscle relaxation and are weak muscle relaxants on their own [28]. Although this patient selection bias may have influenced the measurement of SWV, our regression models demonstrated no significant effects of inhaling anaesthetics (Table 2). Thus, the effects of inhaling anaesthetics may be insignificant.

Another limitation of this study was that all measurements were performed by only one sonographer. Ultrasonography depends on the operator’s skill and experience and is not reproducible [29]. Here, we did not use other methods to measure SWV and subcutaneous fat thickness, except for ultrasound sonography. Moreover, when the examiner measured the subcutaneous fat thickness, he did not estimate the degree of fat infiltration into the abdominal muscle. Neuromuscular disease, disuse atrophy, and sarcopenia induce fat-rich muscles [30]. However, the possible relationship between the degree of fat content in the muscle and muscle tone has not been examined. As described above, these information biases may be related to the results of this study.

In conclusion, our results suggest that shear-wave elastography allows for quantification of abdominal muscle tone and that significant clinical factors for decreasing SWV are the female sex and high body mass index. SWV adjusted for subcutaneous fat thickness may be a scale point in a universal scale for assessing muscle tone that can be developed in the future.

Ethics approval and consent to participate

This study was approved by the Institutional Review Board and Ethics Committee of the Tohoku University School of Medicine (ID#2021-1-1055, approved on October 22, 2018). Written informed consent was obtained from all the study participants.

Consent for publication

Not applicable.

Availability of data and materials

The datasets generated during this study are not publicly available because the institutional review board did not allow uploading of the raw data to the web (only published data). However, the datasets are available from the corresponding author upon reasonable request.

Competing interests

All authors declare no competing interests regarding the publication of this study.

Funding

Authors' contributions in CRediT taxonomy style

Hidehisa Saito: Data curation, Formal analysis, Investigation, Writing - Original draft. Shigekazu Sugino: Funding acquisition, Visualization, Writing – Review and Editing. Shoichiro Moteki: Investigation. Akihiro Kanaya: Methodology, Writing – Review and Editing. Masanori Yamauchi: Conceptualization, Funding acquisition, Methodology, Project administration, Supervision, Writing – Review and Editing.

Acknowledgments

This study was supported by a grant from the Research Project on the Elucidation of Chronic Pain (ref#: 18950309 to M.Y.) from the Japan Agency for Medical Research and Development (AMED), Tokyo, Japan. Presented in part at the 42^nd Annual Meeting of the Japan Society for Clinical Anesthesia, Kyoto, Japan, November 11–12, 2022. The author (H.S.) thanks the staff of the Department of Anesthesiology and Perioperative Medicine, Tohoku University School of Medicine, for providing valuable comments regarding the preparation of this manuscript.

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No competing interests reported.

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Quantification of muscle tone using shear-wave velocity during anaesthesia induction: a prospective observational study

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Version 1

Abstract

Purpose

Methods

Results

Conclusion

Clinical trial registration:

Figures

Introduction

Methods

Participants

Experimental protocol in induction of general anaesthesia

Ultrasound examination for evaluation of muscle tone

Statistical analysis

Results

Opioid-induced rigidity increased the abdominal muscle tone, and complete muscle relaxation decreased the tone

Sex and body mass index as significant factors affecting muscle tone

Adjustment for subcutaneous fat thickness reduces individual differences in SWV

Discussion

Declarations

References

Additional Declarations

Status:

Version 1