Shear wave elastography of ulnar nerve in arm: An observational study for evaluation of performance

INTRODUCTION

The elasticity of soft tissues is defined as tissue deformability, and is determined by its structure and composition. Ultrasound (US) elastography is a method that can assess the mechanical properties of soft tissue through US imaging. Since its introduction in 1991, US elastography has evolved considerably. It has found clinical application in neoplastic and non-neoplastic disorders, including neuromuscular diseases.^[1-4]

Different elasticity measurement techniques depend on the type of stress applied and the method used to detect tissue deformability. Shear wave elastography (SWE) measures the directional shear wave’s velocity produced by an US pulse. It allows both qualitative color-coded image and quantitative information of elasticity (in kilopascals [kPa]) or shear wave velocity (in cm s⁻¹).^[5]

The introduction of SWE into commercially available US systems has allowed its use in various clinical conditions despite reservation raised by an in vitro study that reported considerable difference in SWV on different transducers and machines, limiting its use with the absolute values.^[6] SWE has been validated in breast, liver, prostate, and thyroid diseases.^[7-12] It also holds promise for several musculoskeletal disorders and has complemented conventional B-mode US and Doppler imaging.^[1,2,13,14] However, there are concerns about using this method for very superficial structures, as a certain depth of US penetration is needed for shear waves to be produced.^[15,16]

Electrodiagnostic studies have been the primary diagnostic modality for providing insight into peripheral nerve dysfunction. Recently elastography has been explored as a non-invasive way to evaluate nerve parenchyma. There have been some reports about the performance of SWE for peripheral nerve pathology, predominantly compressive neuropathy in the median nerve, ulnar nerve, sciatic nerve, and tibial nerve.^[17-19]

The SWE measurements have been reported to be reproducible, with high inter-rater agreement rates for median nerve stiffness.^[17] These arguments support its routine use in suspected entrapment neuropathies. However, these studies also documented a considerable variance in the absolute values of nerve’s stiffness, both in cases and healthy controls.^[17,19] To overcome this limitation, the ratio of measurements at two sites was evaluated, and it provided high accuracy in distinguishing between the two groups.^[19] SWE studies for the ulnar nerve are limited, and data do not establish the role of elastography in the diagnosis of ulnar neuropathy at the elbow.^[20-22] This may be attributed to fewer studies or due to the under performance of this tool in the ulnar nerve.

This study investigates the performance of SWE for the ulnar nerve in the arm regarding its measured value by two different US transducers of the same US system. In vivo reliability in terms of SWE values correlation of two different transducers has not been reported in the literature to the best of our knowledge. The in vitro study reporting difference in SWV by two probes is silent about the correlation of the values obtained by two probes in the same experimental settings.

MATERIAL AND METHODS

Sonographic examinations

Sonographic examinations were performed with SuperSonic Imagine-Aixplorer^®-Innovative UltraFast™ US Imaging system with SuperLinear™ SLH20-6 probe of bandwidth 6–20 MHz and SuperLinear™ SL18-5 probe of bandwidth 5–18 MHz by a radiologist of more than 15 years of experience in peripheral nerve ultrasonography. Examiner was blinded to the clinical condition of the patient.

The examination was done in the supine position with the arm abducted for 15–30°, elbow extended and palm facing the ceiling on the right side. On the left side, it was examined in cobra position. The nerve is relaxed on the right and semi stretched on the left side [Figure 1].

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Figure 1:

Photograph showing the position of the elbow. Extended on the right (a) and flexed on the left (b). Note the position of the probe along the course of ulnar nerve.

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The course of the ulnar nerve at each level was localized on B-mode scans. The transducer was always kept parallel to the skin surface, and special attention was paid to minimize the pressure and avoid a disruption of the hydrogel layer. Elastographic measurements were taken in a transverse scan and longitudinal scan with both the probes one after the other in the same sitting at the level just above the medial epicondyle and about 7 cm proximal to it.^[23] Shear wave imaging was done in standard setting at 1.1 Hz in 20–6 MHz probe and 2.0 Hz in 18–5 MHz probe. Any abnormal shadowing from superficial structure/septa was avoided. Q-Box was placed at least 5 mm deep to surface, and measurements were taken with an area of the circle being 1 sq mm and SD <4. During the examination, supersonic shear imaging pulse was focused at the nerve stroma by positioning the ulnar nerve in the center of the SWE box and stabilized for 3–4 s to get good SWE map that is stable and not pixelated. Care was taken so that no surface jell layer or underlying bone surfaces were included in the SWE box.^[24,25] Shear modulus data for the Q-Box, (one sq. mm) were acquired automatically by the ultrasonographic software, and the results were recorded in kPa. Representative elastography map is presented in Figure 2.

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Figure 2:

Elastogram map images showing the shear wave elastography box placement and point of measurements in longitudinal plane (a) and transverse plane (b).

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Elastographic measurements were taken at two sites, as mentioned above. In a transverse scan, the shear wave velocity was measured in the nerve stroma, in the peripheral epineurium (marginal), and the subcutaneous fat (as close to deep fascia as possible). In a longitudinal scan, two measurements were taken in the nerve stroma, and the average was calculated, and one measurement was taken in subcutaneous plane. Shear wave elasticity ratio was calculated at each site using the value measured in the nerve stroma and value in subcutaneous fat in longitudinal sonogram as numerator and denominator, respectively. In the transverse sonogram, two ratios were calculated. The first was the ratio between the elasticity values in nerve stroma and epineurium, and second between the values in nerve stroma and subcutaneous fat. Ratio of elasticity measured at mid arm and supracondylar region was also calculated for agreement between two probes.

RESULTS

Fifty-three subjects referred for evaluation of ulnar nerve for different clinical conditions were enrolled. There were 93 sets of measurements of the ulnar nerve (measurements taken on one arm constitutes a set). One set showed significant outliers interfering with results, and was excluded from the analysis. So a total of 92 nerve measurement sets were analyzed. There were 37 males, and 16 females with 25 males and 14 females had both arm measurements, and rest had a measure of single nerves. The ages of the patients ranged from 14 years to 76 years, with a median age of 50 years.

The description of the measurements taken is given in Table 1.

The ICCs for agreement between the values both absolute and ratios were low for almost all parameters studied, with not a single measure having even an ICC of 0.5 [Table 2]. The correlation of agreement between two probes in the longitudinal plane at the midarm was (0.42) with 95% CI 0.26–0.59, and in supracondylar region was 0.42 with 95% CI of 0.23–0.57. ICC for agreement in ratio of elasticity value at two sites between two probes was 0.017 and 0.272 in longitudinal and transverse plane. Pearson’s correlation coefficient for association between values taken in two planes at each site and probes is listed in Table 3.

DISCUSSION

This study has been undertaken to determine the reliability of SWE quantitative imaging in peripheral nerve. The present study was done for the ulnar nerve in arm, as it is one of the most commonly affected neuropathies in clinical practice. The measured value for ulnar nerve elastography has a limited publication.^[21,22] Study by Shin et al., on phantom reported significant difference in SWV on US elastography depending on the machines, transducers, and acquisition depth. However, they did not mention about the strength of correlation between the values obtained by two transducers with other parameters being same.^[6] The research is ongoing with use of elastography in the diagnosis of peripheral nerve lesions especially the median nerve with good outcome in terms of interobserver reliability and repeatability. However, in a review concerning the use of elastography for evaluation of peripheral nerve lesion by Wee et al., the author highlights the paucity of data available in literature to assign any role of elastography for ulnar nerve pathology. They were silent on the reason for the same, as the instrumental limitation as mentioned by Shin et al., are equally relevant for all other nerve as well. They also stressed the need for study on this subject as the future area of interest.^[20]

In the present study, the performance of SWE to measure the elasticity of the ulnar nerve in arm has been evaluated by two different US transducers of the same unit, at the same site and imaging planes, and in the same sitting. Thus, we have avoided inter-observer, inter-instrumental, temporal, and positional factors in this analysis. Chang et al. observed that, of all physical factor extrinsic to US beam, probe pressure is an important determinant to changes the speed of propagation in superficial tissue by increasing the density, and so the propagation speed. This has been overcome in the study design by adequate gel layer avoiding any compression.^[27]

There was poor agreement of absolute values of elasticity in two transducers. This is in agreement with the observation by Shin et al.^[6] Similar observation has been reported in Median nerve by Bedewi et al. Moreover, different studies have quoted different value of elasticity in a healthy median nerve.^[17,28,29]

The speed of shear wave propagation decreases at greater source-to-target distances, paralleling the progressive attenuation of the pulses generating the shear waves as they travel within tissues. Thus, lower values are obtained in deeper tissue. Two sites were chosen in present study so as to include a very superficial location, and an intermediate depth. However, the values obtained in our study were not showing any significant lower values in deeper course of the nerve (mid arm) as compared to supracondylar region. This may be attributed to relatively lower depth of both sites in comparison to depth associated with liver elastography in experimental model.^[27,30,31] Moreover, other reason could be that shear waves are expected to meet more architectural disturbances in heterogenous tissue.^[32] On a similar note, Palmeri et al. observed that nerves surrounded by fat typically displaces less and are relatively stiffer than their adjacent tissues. These same nerves can appear more compliant when surrounded by substantial volumes of skeletal muscle.^[33] Thus, more fat surrounding the supracondylar part of ulnar nerve may have compensated for its more superficial location and hence not much of a difference in values at two sites.

The mean values of elasticity were higher in longitudinal plane in both transducers, as compared to transverse plane. A similar observation was made by Paluch et al., attributing such discrepancies to different transducer frequencies and plane of the tissues.^[22,28] At least two categories of anatomical factors strongly influence the propagation of the shear waves, the tissue architecture, and anisotropy. The anisotropy reflects the direction dependence of certain properties. Most of the current knowledge about the effects of anisotropy on the transmission of shear waves derives from an experimental work by Gennisson et al. on an animal model using supersonic shear waves imaging.^[34] Similar anisotropic effect in elasticity has been seen in other tissues. In a study by Arda et al., the mean elasticity value of Achille’s tendon in longitudinal and transverse plane was different with significantly different ranges, consistent with this anisotropic concept of tissue elasticity.^[9]

The ICC of stromal elasticity measured showed mild correlation between the two transducers. However, the level of agreement was higher in longitudinal plane (0.44–0.42) than in transverse plane (0.34–0.21) at both sites. This is similar to observation made by Paluch et al. that measurements from the nerve cross-section are characterized by lower repeatability.^[28]

Use of ratio of the elasticity of nerve tissue and subcutaneous fat has been evaluated in line with the strain ratio equivalent in strain elastography. Our observation shows that the use of elasticity equivalent ratio between the ratio of fat and nerve elasticity values obtained by two probes had poor ICC (<0.3). This lower ICC is in sync with law of statistics where the negative factors are exaggerated in ratio, and so a relatively higher discordance.

The ratio of elasticity of ulnar nerve at mid arm and supracondylar region has been advocated in some of the studies due to the limitations of variability in observation. Paluch et al., proposed wrist to forearm ratios to be independent of patient age or weight and exhibit excellent diagnostic accuracy regardless of where on the forearm the second measurement is taken.^[19] However, our study showed poor ICC 0.017 in longitudinal and 0.272 in transverse plane making this ratio a less reliable tool in case of ulnar nerve in distal arm. This can also be explained with effect of probe frequency, depth, heterogeneity, and anisotropy being significantly high due to its anatomy.

CONCLUSION

Quantitative SWE measurements of the ulnar nerve in the arm by two transducers showed weak interclass correlation, suggesting complex non-linear interaction of instrumentation, anatomy, and tissue architecture. Hence, the absolute values or the ratios of elasticity of ulnar nerve as a diagnostic tool by SWE need to be used with caution.

This study design has some inherent limitations including evaluation by single observer with lack of inter- and intra-observer reliability assessment. Simultaneous study of any deeper nerve could have added much insight and served as control for some of the ambiguity. Methodology could have included measurement with larger Q-Box tool so as to get a better average value.