Shear-wave elastography in the diagnosis of ulnar tunnel syndrome

Accepted Manuscript

Shear wave elastography in the diagnosis of the ulnar tunnel syndrome. Ł Paluch , BH Noszczyk , J Walecki , K Osiak , M Kicinski , ´ P Pietruski PII: DOI: Reference:

S1748-6815(18)30311-5 https://doi.org/10.1016/j.bjps.2018.08.018 PRAS 5784

To appear in:

Journal of Plastic, Reconstructive & Aesthetic Surgery

Received date: Revised date: Accepted date:

29 May 2018 14 August 2018 19 August 2018

Please cite this article as: Ł Paluch , BH Noszczyk , J Walecki , K Osiak , M Kicinski , P Pietruski , ´ Shear wave elastography in the diagnosis of the ulnar tunnel syndrome., Journal of Plastic, Reconstructive & Aesthetic Surgery (2018), doi: https://doi.org/10.1016/j.bjps.2018.08.018

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ACCEPTED MANUSCRIPT Shear wave elastography in the diagnosis of the ulnar tunnel syndrome.

Ł Paluch 1, BH Noszczyk 2, J Walecki 1, K Osiak 2, M Kiciński 3, P Pietruski 2,4

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Department of Radiology, Gruca Orthopedic and Trauma Teaching Hospital, Medical Centre

2

Department of Plastic Surgery, Prof. W. Orlowski Memorial Hospital, Medical Centre of

Postgraduate Education, Warsaw, Poland 3

Trauma and Orthopedics Department, Gruca Orthopedic and Trauma Teaching Hospital,

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Medical Centre of Postgraduate Education, Otwock, Poland 4

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of Postgraduate Education, Otwock, Poland

Department of Applied Pharmacy and Bioengineering, Medical University of Warsaw,

Corresponding author: Bartłomiej Noszczyk, MD.

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Warsaw, Poland

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Department of Plastic Surgery, Centre of Postgraduate Medical Education, Prof. W. Orlowski Memorial Hospital

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Czerniakowska 231 Street 00-416 Warsaw, Poland

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E-mail address: [email protected] Phone number: +48 602 795 165

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Fax number +48 22 62 96 969

Funding:

The authors received no financial support for the research, authorship, and publication of this article.

The paper was not presented (or submitted for presentation) at any meeting.

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ACCEPTED MANUSCRIPT Summary

An interesting alternative to traditional diagnostic techniques of the upper extremity nerve entrapments might be provided by an ultrasound elastography that started to gain attention in recent research. The aim of this preliminary study was to verify if quantitative analysis of

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ulnar nerve stiffness with shear-wave elastography can be used to diagnose the ulnar tunnel syndrome, an ulnar nerve neuropathy at the Guyon’s canal. The study included 46 patients (39 women) and 39 healthy controls (34 women). All diagnoses in patients and controls were confirmed with nerve conduction studies. Measurements of nerve stiffness were taken at three

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levels: in Guyon’s canal (G) and at distal (DF) and mid-forearm (MF). Additionally, ulnar nerve cross-sectional area at the canal’s level was determined by means of ultrasonography. Patients with the ulnar tunnel syndrome presented with significantly greater nerve stiffness

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than the controls (mean, 99.41 kPa vs. 49.08 kPa, P <0.001). No significant intergroup differences were found in the nerve elasticity at DF and MF (P <0.836 and P < 0.881,

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respectively). Ulnar nerve stiffness value of 80 kPa, and G:DF and G:MF ratios equal to 1.5 provided 100% sensitivity, specificity, positive and negative predictive value in the detection

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of the syndrome. Mean nerve cross-sectional area in the Guyon's canal was significantly

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greater in patients than in the controls (4.63 mm2, range, 2-7 mm2 vs. 3.23 mm2, range, 2-5 mm2, P <0.001). In conclusion, we believe that shear-wave elastography has a potential to

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become a useful adjunct diagnostic test for the ulnar tunnel syndrome.

Keywords: shear wave elastography, ulnar nerve, Guyon’s canal, ulnar tunnel syndrome, nerve entrapments, wrist

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ACCEPTED MANUSCRIPT Introduction

Ulnar tunnel syndrome (UTS) also referred as a Guyon’s canal syndrome results from a compressive neuropathy of ulnar nerve at the level of the Guyon's canal, a space in the hypothenar region of the wrist limited radially by the hamate, volarly by the volar carpal

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ligament, ulnarly by the pisiform and flexor carpi ulnaris, and dorsally by the transverse carpal ligament (1). Although the exact incidence and prevalence of UTS have not been

reported, this condition is believed to be the third most common nerve entrapment syndrome in the upper extremity, after carpal tunnel syndrome (CTS) and the ulnar neuropathy at the

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elbow (UNE)cubital tunnel syndrome (11).

UTS may be triggered by the number of factors, among which ulnar nerve compression at the

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wrist by a space-occupying lesion, such as a ganglion, is the most common. Other causes of UTS include acute or repetitive trauma (often referred to as "hypothenar hammer syndrome"), hamate hook fractures, anomalies of hypothenar muscles and ulnar artery pathologies (11,2).

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Also, a long-distance cycling has been implicated as a risk factor of UTS (3). Moreover, the

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incidence of UTS is known to correlate strongly with the occurrence develpoment of CTS,

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since the transverse carpal ligament constitutes a boundary of both canals. As a result, increased strain within the carpal tunnel can be transmitted to the Guyon's canal, contributing

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to ulnar neuropathy (4).

UTS is typically characterized by a history of paresthesia in the small and ring fingers, ulnarsided pain, and a decrease in grip strength with hypothenar muscle atrophy (11,22). However,

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due to the unique structure of the Guyon's canal and its several possible anatomic variations,

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the symptoms may be purely motor, purely sensory or mixed, depending on the site of ulnar

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ACCEPTED MANUSCRIPT nerve compression (5). Considering this, as well as the fact that the symptoms of UTS may resemble those of cubital tunnel syndromeUNE, establishing clinical diagnosis solely based on patient history and physical findings may be sometimes challenging. In such cases, additional tests, such as imaging and electrodiagnostic studies (EDX), should be considered

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during the preoperative work-up (6,7).

Similar to other entrapment syndromes, UTS eventually leads to structural changes in the compressed nerve. Ulnar nerve at the wrist level becomes swollen and fibrotic, which affects its hardness (8,9). These changes can be objectively evaluated with ultrasound (US)

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elastography which hence may become a new method to diagnose UTS. Developed by Ophir and colleagues in 1991, elastography is suitable for the evaluation of tissue elasticity, i.e. the ability to resume original shape and size after being exposed to strain or compression with an

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external force (10,11). Since being first introduced, elastography has found multiple clinical applications and its usefulness in other medical disciplines is still a subject of extensive

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research (12,13,14). One potential application of elastography can be an evaluation of peripheral neuronal tissue elasticity in patients with compartment syndromes. Several recent studies

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documented a usefulness of elastography in the evaluation of median nerve in persons with

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CTS (15,16,17). However, to the best of our knowledge elastography still has not been studied

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as a method to determine the elasticity of ulnar nerve at the wrist level.

The aim of this study was to verify if UTS can be diagnosed based on quantitative analysis of ulnar nerve stiffness with shear-wave elastography (SWE). Moreover, we compared crosssectional area (CSA) of the ulnar nerve at the Guyon’s canal level in patients with UTS and healthy controls, to establish an accurate cut-off value for this parameter for the ultrasonographic examination.

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Materials and Methods Study participants

Protocol of the study was approved by the Bioethical Committee of the Medical Centre of

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Postgraduate Education in Warsaw (no. 42/PB/2017), and written informed consent was sought from all patients and healthy volunteers. The study participants were divided into two groups. UTS group included 46 patients with mean age of 62.70 years (range, 25-85 years), among them 7 men with mean age of 65.14 years (range, 54-75 years) and 39 women with

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mean age of 62.26 years (range, 25-85 years). All the patients were diagnosed with idiopathic, compressive neuropathy of ulnar nerve at the wrist level (22 on the right side and 24 on the left side) based on physical examination and EDX. Control group was comprised of 39

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healthy volunteers with the mean age of 60.05 years (range, 41-93 years), among them 5 men with mean age of 69.60 years (range, 52-81 years) and 34 women with mean age of 58.65

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years (range, 41-93 years). All the controls were free from clinical signs and symptoms of UTS, and presence of this condition was excluded based on physical examination and EDX.

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The right wrist was examined in 22 individuals from the control group and the left in 17.

Patients from the UTS or control group volunteers who had a history of wrist or hand fracture

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or a surgery involving this region suffered from ganglion, systemic neurologic disorder, diabetes mellitus or a thyroid disorder, as well as pregnant women, were excluded from the study.

Study protocol

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ACCEPTED MANUSCRIPT Each participant of the study underwent conventional US followed by US elastographic examination performed on the same day by the same radiologist with more than 4 years of experience in both diagnostic methods, blinded to the subjects' clinical history. The examination was carried out in a seated position with the examined forearm resting on the examiner's knee. Special attention was paid to examine the hand in a neutral position with

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supinated wrist and relaxed semi-flexed fingers, in order to avoid an excessive strain in the Guyon's canal and carpal tunnel.

All US examinations were performed with Toshiba iAplio 900 ultrasonograph with a 5-18

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MHz transducer (Canon Medical Systems). Cross-sectional area (CSA) of the ulnar nerve was determined at transverse scans obtained at the Guyon’s canal level. Stiffness measurements were taken at three levels: at the inlet of the Guyon's canal, and on the forearm, 5 cm (distal

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forearm) and 10 cm (mid-forearm) proximal to the wrist (Fig. 1). During the image acquisition, the examiner gently applied the transducer onto the surface of the skin covered

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with a hydrogel pad, to minimize the risk of compression-related measurement bias. To normalize the SWE values for ulnar nerve at the Guyon's canal level, they were divided by the

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results of elastographic measurements taken at mid-forearm and distal forearm, and expressed

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as G:MF and G:DF ratio, respectively. SWE measurements were repeated three times at each level, always with ulnar nerve positioned in the center of the region of interest (ROI) on a

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sagittal US scan. Shear modulus data for the selected ROI (ulnar nerve) were expressed in kilopascals (kPa) (Fig. 2).

Statistical analyses

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ACCEPTED MANUSCRIPT Normal distribution was verified with Shapiro-Wilk test. Statistical significance of intergroup differences in the values of continuous variables was verified with Mann-Whitney U-test and Kruskal-Wallis test with Dunn post-hoc test. Diagnostic accuracy of US elastographic parameters and CSA in the detection of UTS was verified by receiver operating characteristic (ROC) analysis. Sensitivity, specificity, positive and negative predictive value (PPV and

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NPV, respectively) were calculated for each potential predictor of UTS, along with the area under the ROC curve (AUC) and its 95% confidence interval (95% CI). All calculations were carried out with Statistica 10 package (StatSoft), with the threshold of statistical significance

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set at p ≤0.05.

Results

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The results of SWE measurements taken in patients with UTS and in the controls are presented in Table 1. Patients with UTS presented withhad significantly higher SWE values

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for ulnar nerve at the Guyon’s canal level than the controls (mean, 99.41 kPa vs. 49.08 kPa, P <0.001). No significant intergroup differences were found in ulnar nerve elasticity measured 5

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cm and 10 cm proximal to the wrist (P <0.836 and P < 0.881, respectively). Comparative

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analysis demonstrated that mean values of both G:MF and G:DF ratio were significantly

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higher in patients with UTS than in the controls (P <0.001) (Table 2).

ROC curves for SWE measurements of the ulnar nerve at the wrist level, G:DF and G:MF ratios as the predictors of UTS are shown in Figure 3a. Analysis demonstrated that ulnar nerve SWE value of at least 80 kPa, and SWE G:DF and G:MF ratios equal to 1.5 or higher provided 100% sensitivity, specificity, positive (PPV) and negative predictive value (NPV) in the detection of UTS (Fig. 3b).

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Mean CSA of the ulnar nerve at the Guyon's canal level was significantly greater in patients with UTS than in the controls (4.63 mm2, range, 2-7 mm2 vs. 3.23 mm2, range, 2-5 mm2, P <0.001). ROC analysis demonstrated that CSA of the ulnar nerve at the Guyon's canal level equal to 5 mm2 or greater provided 97.4% specificity, 56.5% sensitivity, 96.3% PPV and

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65.5% NPV in the detection of UTS (Fig. 3c).

Discussion

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The primary aim of this study was to verify the applicability of SWE for the detection of ulnar tunnel syndrome, based on comparative analysis of elastographically-determined ulnar nerve stiffness in patients with UTS and in healthy controls. The study demonstrated clearly that

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UTS is associated with a significant increase in ulnar nerve stiffness at the Guyon’s canal inlet. This observation is consistent with the results of a previous studiesy in whichwhere

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patients with CTS presented with a greater stiffness of median nerve at the wrist level than

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compressive neuropathy syndrome might result from a greater strain within the canal, edema

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healthy controls (1515,1616). The lesser elasticity of the nerve in individuals with the

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factors.

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and structural changes of the nerve (e.g. fibrosis), or reflected the influence of all these

Using ROC analysis, we identified the cut-off value for SWE-determined ulnar nerve stiffness (80 kPa), which provided an optimal accuracy and might be useful for clinicians in the detection of UTS. However, our clinical experiences suggest that the diagnosis may be more accurate if normalized values of ulnar nerve stiffness (ratios) are used instead of the raw estimates. Although a recent study has shown that age and BMI have no effect on peripheral

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ACCEPTED MANUSCRIPT nerve SWE (18), factors like patient job or hand volume should be considered important. The stiffness of the nerve, as well as its CSA, may vary depending on sex, age, profession, BMI and hand physiognomies. Since patients with UTS did not differ from healthy controls in terms of ulnar nerve stiffness proximal to the wrist, we used the latter parameter to normalize the stiffness estimates at the Guyon’s canal inlet. The validity of this assumption was

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confirmed on the ROC analysis, as either G:DF or G:MF ratio of at least 1.5 provided an excellent accuracy in the detection of compressive ulnar neuropathy at the Guyon's canal level.

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Clinical presentation of UTS is not always straightforward due to a large variety of possible causal factors and anatomical variations of the Guyon's canal (55). Therefore, preoperative

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work-up frequently includes additional tests. A number of various diagnostic instruments

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have been proposed as adjunct tests to confirm UTS, among them US, plain film radiography, computed tomography and magnetic resonance imaging (MRI) (19,20). For UNE diagnosis the

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diffusion tensor imaging (DTI) tractography has been also proposed (21). At the level of the wrist it enables additional nerve visualization in 3D, supports nerve laceration information (22)

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and increase diagnostic confidence (23). Although DTI has not been described in UTS

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diagnosis, it's a potent non-invasive nerve imaging modality. However, its drawbacks like high costs, troublesome results compilation, lengthy scanning and limited availability imply

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that DTI should be perhaps considered for difficult cases of UTS that require meticulous preoperative planning. However, the specificity and sensitivity of many of these methods in the detection of UTS remain unknown or available evidence in this matter is sparse (6).

EDX is one of theconsidered a most common testsgold standard to for confirmation of the ulnar neuropathy, localize the site of compression (24) and to monitor the progression of the

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ACCEPTED MANUSCRIPT disease over time (25). However, this method has some drawbacks; it is invasive, timeconsuming and needs to be performed by an experienced operator what limits test availability and increases its cost. FinallyMoreover, some authors put the accuracy of EDX into question, pointing that its results are not necessarily consistent with clinical presentation, even in the

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case of an evident peripheral nerve compression (26).

US seems to be the most comprehensive of all imaging studies that have been proposed as diagnostic options in UTS (27). Not only US can detect a presence of a space-occupying

lesion, e.g. ganglion being a common cause of ulnar neuropathy at the wrist level, but also it

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accurately identifies potential anomalous variants of hypothenar muscles and arterial

pathologies (28). US can be used to determine various ulnar nerve characteristics, such as CSA, mobility, structure and echogenicity, and to guide some therapeutic interventions, e.g.

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ganglion aspiration (29). Furthermore, US is less invasive and less costly than EDX, which

diagnosis of UTS.

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together with its wider availability makes it an excellent adjunct method to confirm the

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During recent years, US elastography has been gaining a growing interest as a method to

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detect and to evaluate abnormalities in peripheral neural tissue. Several previous studies documented usefulness of strain elastography and SWE in the evaluation of median, sciatic and tibial neuropathy (1515,30,31). SWE seems to be more promising of the two elastographic

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modalities, as it is operator-independent, highly reproducible and relatively easy to perform. Moreover, contrary to strain elastography which is semi-quantitative at best, SWE provides quantitative estimates of tissue stiffness expressed in kPa (1414). Owing to its examiner-

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independent character and simplicity, SWE may become a widely accepted method to diagnose UTS and cubital tunnel syndromeUNE (32). In our opinion, SWE may also find

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ACCEPTED MANUSCRIPT application as a screening tool to monitor ulnar nerve status in individuals at increased risk of compressive neuropathy, such as long-distance cyclists and pneumatic hammer operators (33). FOur future studies will verify the applicability of SWE for the secondary prevention of UTS and for the monitoring of treatment outcomes.

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Aside from ulnar nerve stiffness, we also analyzed its CSA at the wrist level. While previous studies documented a cut-off value for median nerve CSA that can be used to diagnose CTS, to the best of our knowledge, no similar reference values for ulnar nerve have been published thus far. We demonstrated that mean CSA of the ulnar nerve at the Guyon's canal level was

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significantly greater in patients with UTS than in healthy controls, and this parameter provided a satisfactory accuracy as a predictor of ulnar neuropathy.

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We are well aware of some potential limitations of this study. First, due to the preliminary character of our research, the study group was relatively small. Second, our findings cannot be

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compared with published evidence since to the best of our knowledge, none of the previous studies examined SWE as a method to detect UTS. Third, due to the small size of the study

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group, we did not exclude a potential confounding effect of patient-related factors, such as

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occupation, BMI or hand physiognomies, on ulnar nerve stiffness. FourthThird, the stiffness of ulnar nerve at the wrist level was determined solely at the Guyon's canal inlet, above

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division of the nerve. Finally, owing objective, operator-independent character of SWE, we did not verify inter-rater reliability of the measurements, which also might be considered as a limitation.

Shear-wave elastography has a potential to become a useful adjunct diagnostic test for UTS, or even a primary instrument to detect this condition. Future studies should verify the ability

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ACCEPTED MANUSCRIPT of SWE to grade the severity of UTS, and applicability of this method for the secondary

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Conflict of interest statement: none

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prevention and monitoring of treatment outcomes.

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Funding: none

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Figure legends:

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Figure 1: Ulnar nerve segments subjected to elastographic examination.

Figure 2: Elastographic presentation of the ulnar nerve at the Guyon's canal in a patient with

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UTS (high SWE value).

Figure 3: ROC curve illustrating diagnostic accuracy of (a) at least 80-kPa SWE ulnar nerve stiffness at the site of compression in the detection of UTS, (b) at least 1.5 SWE G:DF ratio

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(A) and at least 1.5 SWE G:MF ratio (B) in the detection of UTS, and (c) at least 5-mm2

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cross-sectional area of ulnar nerve in the detection of UTS.

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ACCEPTED MANUSCRIPT Tables:

Table 1. Elastographic estimates of ulnar nerve stiffness (in kPa) in healthy volunteers

CONTROL GROUP UTS GROUP ULNAR NERVE (n=39)

(n=46)

SWE VALUE

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(control group) and patients with confirmed ulnar tunnel syndrome (UTS group).

P

Range

Median

Range

Ulnar tunnel level

51

20-69

98

80-129

<0.001*

Distal forearm level

50

21-66

49

21-67

0.836

Mid-forearm level

49

23-68

48

22-72

0.881

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Median

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*Statistically significant intergroup difference

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Table 2. Normalized values of ulnar nerve stiffness at the Guyon’s canal inlet in healthy volunteers (control group) and patients with confirmed ulnar tunnel syndrome (UTS group).

(n=39)

ULNAR NERVE SWE RATIO

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CONTROL GROUP UTS GROUP (n=46)

Range

Ulnar tunnel level : Distal forearm level

1.0

0.9-1.1

Ulnar tunnel level : Mid-forearm level

1.0

0.9-1.1

Median

Range

2.0

1.5-4.8

<0.001*

2.0

1.5-4.6

<0.001*

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Median

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*Statistically significant intergroup difference

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