Shear-wave elastography: a new potential method to diagnose ulnar neuropathy at the elbow

Shear-wave elastography: a new potential method to diagnose ulnar neuropathy at the elbow Objectives The primary aim of this study was to verify if shear-wave elastography (SWE) can be used to diagnose ulnar neuropathy at the elbow (UNE). The secondary objective was to compare the cross-sectional areas (CSA) of the ulnar nerve in the cubital tunnel and to determine a cut-off value for this parameter accurately identifying persons with UNE. Methods The study included 34 patients with UNE (mean age, 59.35 years) and 38 healthy controls (mean age, 57.42 years). Each participant was subjected to SWE of the ulnar nerve at three levels: in the cubital tunnel (CT) and at the distal arm (DA) and mid-arm (MA). The CSA of the ulnar nerve in the cubital tunnel was estimated by means of ultrasonographic imaging. Results Patients with UNE presented with significantly greater ulnar nerve stiffness in the cubital tunnel than the controls (mean, 96.38 kPa vs. 33.08 kPa, p < 0.001). Ulnar nerve stiffness of 61 kPa, CT to DA stiffness ratio equal 1.68, and CT to MA stiffness ratio of 1.75 provided 100% specificity, sensitivity, positive and negative predictive value in the detection of UNE. Mean CSA of the ulnar nerve in the cubital tunnel turned out to be significantly larger in patients with UNE than in healthy controls (p <0.001). A weak positive correlation was found in the UNE group between the ulnar nerve CSA and stiffness (R = 0.31, p =0.008). Conclusions SWE seems to be a promising, reliable and simple quantitative adjunct test to support the diagnosis of UNE. Key Points � SWE enables reliable detection of cubital tunnel syndrome � Significant increase of entrapped ulnar nerve stiffness is observed in UNE � SWE is a perspective screening tool for early detection of compressive neuropathies . . . . Keywords Elastography Cubital tunnel syndrome Ulnar nerve Ulnar nerve entrapment syndrome Ulnar neuropathies Abbreviations MA Mid-arm CSA Cross-sectional areas MRI Magnetic resonance imaging CT Cubital tunnel ROI Region of interest DA Distal arm SWE Shear-wave elastography EMG Electromyography UNE Ulnar neuropathy at the elbow FCU Flexor carpi ulnaris US Ultrasonography * Bartłomiej Noszczyk Introduction noszczyk@melilot.pl Cubital tunnel syndrome, also referred to as ulnar neuropathy Department of Radiology, Medical Centre of Postgraduate at the elbow (UNE), is the second most common peripheral Education, Gruca Orthopaedic and Trauma Teaching Hospital, entrapment neuropathy after carpal tunnel syndrome. It can be Otwock, Poland 2 defined as a compression of the ulnar nerve at the level of the Department of Plastic and Reconstructive Surgery, Medical Centre of elbow or in its direct proximity [1–4]. The ulnar nerve may be Postgraduate Education, Prof. W. Orlowski Memorial Hospital, Czerniakowska 231 Street, 00-416 Warsaw, Mazowieckie, Poland compressed at the cubital tunnel inlet by the medial intermuscular septum and an aponeurotic band referred to as Department of Applied Pharmacy and Bioengineering, Medical University of Warsaw, Warsaw, Poland the arcade of Struthers. Moreover, the nerve may be entrapped Eur Radiol in the tunnel by the Osborne's band, a retinaculum that extends During recent years, sonoelastography, a relatively new from the medial epicondyle to the olecranon, and by the apo- imaging technology to quantify tissue stiffness, has been neurosis of the flexor carpi ulnaris (FCU); this is postulated to gaining a growing interest of researchers and healthcare pro- be the most common site of the entrapment [5–7]. Finally, the fessionals. Since its introduction by Ophir and colleagues in ulnar nerve may be compressed distally, at the tunnel outlet, 1991, sonoelastography has evolved considerably and found by the two heads of the FCU muscle [7]. application in many clinical disciplines; other potential uses of Idiopathic neuropathy seems to be the most common sonoelastography are still a subject of ongoing research [32, cause of UNE among many potential aetiological factors 33]. One highly promising application of sonoelastography, in of this condition [7, 8]. Ulnar neuropathy may also result particular shear-wave elastography (SWE), is the evaluation from habitual elbow flexion, acute or repetitive trauma, of peripheral nerve elasticity in patients with entrapment syn- excessive strain, presence of mass-like lesions, degenera- dromes. Several authors reported the use of elastography in tive arthritis and snapping triceps syndrome. The list of the diagnosis of median, sciatic and tibial compressive neu- intrinsic aetiological factors includes diseases of the thy- ropathies [34–43]. However, to the best of our knowledge, roid, diabetes mellitus, alcohol abuse, rheumatoid arthritis potential application of this technique as a method to detect and other systemic inflammatory diseases, to mention a UNE has not been studied thus far. few [5, 7, 9–11]. The aim of this study was to use SWE for the quantification Because of its high incidence in the general population and of ulnar nerve elasticity in patients with UNE and in healthy a broad spectrum of symptoms that may interfere with pa- controls, and to verify if this technique may find application in tients’ ability to work and their activities of daily living, clinical practice as an instrument to detect compressive UNE constitutes a significant clinical problem [7, 8, 12]. A neuropathy. number of healthcare professionals with various specialities, among them general practitioners, plastic surgeons, orthopae- dic surgeons and neurologists, are involved in the evaluation Materials and methods of UNE. Although no consensus regarding a management algorithm for UNE has been reached thus far, a recent meta- Study protocol analysis conducted by Mowlavi et al. demonstrated that clin- ical work-up is crucial to establish the diagnosis, to determine Protocol of the study was approved by the local bioethics the severity of ulnar neuropathy and to choose an appropriate committee, and written informed consent was sought from treatment strategy [12]. The diagnosis is based primarily on all participants. A plastic surgeon assigned the study subjects detailed analysis of medical history and physical examination. to one of two groups, based on the inclusion criteria presented According to many authors, electrodiagnostic studies consti- in Table 1. tute an essential component of the evaluation, as they can be Each study participant was subjected to US and SWE, both used to confirm the diagnosis and to assess the severity of conducted with a Toshiba iAplio 900 ultrasonograph equipped nerve damage. Additional tests, such as ultrasonography with a 5-18 MHz transducer (Canon Medical Systems). Both (US), plain film radiography and magnetic resonance imaging US and SWE were carried out during the same visit, by the (MRI), are recommended in patients with vague clinical pre- same radiologist with more than 4 years of experience in both sentation or during preoperative work-up [1, 5–7, 13–25]. diagnostic methods, blinded to subjects’ clinical history, phys- Based on published evidence we can expect that also diffusion ical and results of electrodiagnostic testing (EDX). The exam- tensor imaging may be soon added to the peripheral nerve ination was performed in a seated position, with the subject assessment armamentarium [26–31]. facing the examiner. The examined arm was kept downwards Table 1 Inclusion criteria of the UNE group Control group study UNE symptoms present on physical examination No evidence of UNE symptoms on physical examination UNE confirmed by EDX UNE excluded by EDX No history of elbow surgery No history of humeral or ulnar fracture No systemic neurological disorder No thyroid disorder No diabetes mellitus No current pregnancy EDX, Electrodiagnostic testing; UNE, Ulnar neuropathy at the elbow Eur Radiol alongside the trunk, with flexed elbow and forearm resting on nerve was always positioned in the centre of the 1x1 cm Q-box, the knee in a supine position. To control and minimise the set in such way that no underlying bone surfaces were captured pressure applied onto skin surface, an even layer of hydrogel on longitudinal ultrasonographic scans. Shear modulus data for was applied onto the examined area. the selected circular region of interest (ROI, 2 mm in diameter) During B-mode US examination of the cubital tunnel, the were acquired automatically by the ultrasonographic software; transducer was maintained perpendicularly to the ulnar nerve. the results were expressed in kilopascals (kPa). Representative Transverse cross-sections of the ulnar nerve were acquired at elastographic images are presented in Fig. 2. medial epicondyle level to determine the cross-sectional area of the nerve (CSA, in mm ). To measure the CSA, the ulnar Statistical analysis nerve margin was traced along the inner border of perineural echogenic rim, corresponding to the perineurium around the Normal distribution of the study variables was verified with hypoechoic nerve. Shapiro-Wilk test. Statistical characteristics of continuous var- Ulnar nerve stiffness was measured at three levels labelled iables were presented as means, medians and ranges. The with a skin marker prior to the examination: in the cubital tunnel characteristics of qualitative variables were shown as numbers at the level of medial epicondyle and at a posteromedial aspect and percentages. The significance of intergroup differences in of the arm, 5 cm and 10 cm proximally to the cubital tunnel inlet the statistical characteristics of continuous variables was ver- (i.e. on the distal and mid-arm, respectively) (Fig. 1). The course ified with Mann-Whitney U-test and Kruskal-Wallis test with of the ulnar nerve at each level was localised on B-mode scans. Dunn post-hoc tests, whereas the significant of intragroup Then, the transducer was rotated 90 degrees to obtain SWE- differences was tested with Wilcoxon signed-rank test. mode images of the nerve in a longitudinal axis. The transducer Diagnostic accuracy of ulnar nerve stiffness and CSA in the was always kept parallel to skin surface, and special attention detection of UNE was verified by means of receiver operating was paid to minimise the pressure and to avoid a disruption of characteristic (ROC) analysis. Sensitivity, specificity, positive the hydrogel layer. Nerve stiffness at each level was measured and negative predictive value (PPV and NPV, respectively) of three times with 2-3 min intervals and mean measurement was each potential predictor of UNE were calculated, along with used for further processing; during the examination, the ulnar 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 statisti- cal significance set at p ≤ 0.05. Results UNE group included 34 patients with mean age of 59.35 years (range, 36-85 years), among them six men (mean age, 62 years; range, 48-85 years) and 28 women (mean age, 58,79 years; range, 36-80 years), with confirmed ulnar compressive neuropathy at the elbow level. Control group comprised 38 healthy volunteers with mean age of 57.42 years (range, 38-84 years), among them three men (mean age, 53.67 years; range, 38-75 years) and 35 women (mean age, 57.74 years; range, 38-84 years), in whom UNE was excluded based on the re- sults of physical examination and EDX. The CSA of the ulnar nerve at the cubital tunnel level turned out to be significantly larger in patients with UNE than 2 2 in the controls (mean, 9.03 mm ;median, 8mm ;range, 5-18 2 2 2 2 mm vs. mean, 6.47 mm ;median, 6 mm ;range, 3-9 mm ; p < 0.001). The cut-off value for the CSA of the ulnar nerve at the cubital tunnel level, which most accurately distinguished between the individuals with the entrapment neuropathy and Fig. 1 Ulnar nerve segments subjected to elastographic examination. A, 2 without was 10 mm ; ROC analysis demonstrated that this Cubital tunnel at medial epicondyle level; B, Posteromedial arm, 5 cm value provided 38.2% sensitivity, 100% specificity, 100% proximally to the cubital tunnel inlet (distal arm level); C, Posteromedial arm, 10 cm proximally to the cubital tunnel inlet (mid-arm level) PPV and 64.4% NPV in the detection of UNE (Fig. 3). Eur Radiol Fig. 2 Elastographic presentation of ulnar nerve at the elbow level in (A) healthy individual (low SWE value), and (B) in patient with compressive neuropathy (high SWE value) The results of SWE measurements are summarised in obtained for the CT to DA ratio of 1.68, and CT to MA ratio Table 2. In any patient the differences between measurements of 1.75 (Fig. 3). that were repeated at each level with 3 minutes intervals did A weak positive correlation was found in the UNE group not exceed 2 kPa (SD ≥ 1.15). Compared to the controls, between the CSA of the ulnar nerve and its stiffness at the site patients with UNE presented with significantly greater ulnar of compression (R = 0.31, p = 0.008). Moreover, the CSA of nerve stiffness at each examined level. In the UNE group, the ulnar nerve correlated significantly with the values of CT mean ulnar nerve stiffness at the entrapment site in the cubital to DA (R = 0.31, p = 0.007) and CT to MA ratios (R = 0.30, p tunnel (96.38 kPa) was significantly greater than at the distal =0.010). arm and mid-arm (38.79 kPa and 39.06 kPa, respectively; p < 0.001). In the healthy controls, no statistically significant dif- ferences were found in ulnar nerve stiffness at various levels Discussion (p =0.779). Aside from the comparison of crude SWE parameters for We hypothesised that SWE can be used for an objective eval- the entrapment site, we also analysed their normalised values, uation of oedema and fibrosis associated with ulnar nerve obtained by dividing ulnar nerve stiffness at the cubital tunnel compression. The study showed clearly that patients with level (CT) by its stiffness at the distal arm (CT to DA ratio) or UNE presented with significantly greater ulnar nerve stiffness mid-arm (CT to MA ratio). The values of both ratios turned at the cubital tunnel level than healthy controls (mean, out to be significantly higher in patients with UNE than in the 96.38 kPa vs. 33.08 kPa). Furthermore, stiffness of the ulnar controls (p <0.001) (Table 3). nerve in UNE patients turned out to be significantly greater at ROC curves illustrating the diagnostic accuracy of the entrapment site than at the mid- and distal arm; however, a elastographically determined ulnar nerve stiffness at the similar relationship was not observed in the controls. ROC cubital tunnel level, CT to DA and CT to MA ratios in the analysis demonstrated that UNE could be accurately diag- detection of UNE are presented in Fig. 3. Ulnar nerve stiffness nosed whenever stiffness of the ulnar nerve at the entrapment at the cubital tunnel level equal 61 kPa provided 100% spec- site equalled 61 kPa or more. However, recall that ulnar nerve ificity, sensitivity, PPV and NPV in the detection of UNE. stiffness may vary from patient to patient due to the modula- Equally excellent indices of diagnostic accuracy were also tory effect of additional factors, such as sex, age, BMI, Eur Radiol Fig. 3 ROC curve illustrating diagnostic accuracy of (A) the cross-sectional area of ulnar nerve (10 mm ), (B) ulnar nerve stiffness at the entrapment site (61 kPa), (C) CT to DA ratio (1.68), and (D) CT to MA ratio (1.75) in the detection of UNE occupation, and upper limb physiognomy. Thus, to boost the with CTS than in the controls. Moreover, ROC analysis dem- diagnostic accuracy of SWE, instead of using the crude value onstrated that the cut-off values for CT to DA and CT to MA of ulnar nerve stiffness at the entrapment site, we recommend ratios (1.68 and 1.75, respectively) accurately distinguished a normalised value of this parameter; dividing ulnar nerve between patients with compressive ulnar neuropathy and stiffness at the entrapment site by the stiffness of its intact without. segment, one can eliminate individual variability in the As mentioned before, the diagnosis of UNE is based pri- elastographic parameters. In this study, we divided ulnar nerve marily on medical history and physical examination. stiffness at the entrapment site by its stiffness at the distal and Although this diagnosis is usually confirmed by EDX, US mid-arm, obtaining CT to DA and CT to MA ratios, respec- due to recent implementation of high-frequency transducers tively. Similar to the crude value of ulnar nerve stiffness, also enabling high-resolution images of peripheral nerves is the values of both ratios were significantly higher in patients emerging as a complementary method to evaluate patients Eur Radiol Table 2 Elastographic estimates of ulnar nerve stiffness (in kPa) in healthy volunteers (control group) and patients with confirmed cubital tunnel syndrome (UNE group) Ulnar nerve SWE value Control group (n=38) UNE group (n=34) p Mean Median Range SD Mean Median Range SD Cubital tunnel level 33.08 31 19-51 10.13 96.38 98 61-121 9.62 <0.001* Distal arm level 33.32 33 21-51 9.13 38.79 36,5 21-65 11.33 0.041 Mid-arm level 33.18 31 19-52 8.82 39.06 36 20-61 10.45 0.009 *Statistically significant intergroup difference with compressive neuropathies, e.g. UNE [5, 7, 15, 17, 22–25, result can be considered reliable only if conducted by an ex- 44, 45]. The hallmark sonographic features of entrapment perienced examiner. neuropathy include enlargement of the nerve, its hypoechoic Our findings are consistent with the results of other studies swelling proximal to the compression site, loss of normal fas- that analysed potential application of elastography in the eval- cicular pattern and, not infrequently, oedema of adjacent soft uation of compression neuropathies; also, those studies dem- tissues [7, 13, 20, 22, 23]. US is also suitable for the detection onstrated that compression may contribute to greater stiffness of space-occupying masses. Importantly, during the examina- of the entrapped nerve [34–43]. In our opinion, SWE consti- tion, ultrasonographic images of the affected limb can be com- tutes a valuable supplement to ultrasonographic examination pared with those of the contralateral extremity. High- of peripheral nerves, also in patients with UNE [14]. resolution US was shown to be more cost- and time- Elastography is both a time- and cost-effective method with effective than MRI, and its availability is markedly higher. a relatively steep learning curve. Elastographic findings add Noticeably, US can be used for both static and dynamic as- considerably to the results of US, providing quantitative data sessment of the ulnar nerve; this may be particularly helpful in on the nerve stiffness during both static and dynamic exami- patients with nerve subluxation or snapping triceps syndrome nation. In addition, it can determine the level of nerve entrap- [ 5 , 7]. Previous studies demonstrated that ment. In the future, with its growing availability in routine ultrasonographically determined ulnar nerve CSA was a fea- clinical practice, SWE may be used for the monitoring of sible indicator for UNE [5, 25, 46]; ulnar nerve CSA at the treatment outcomes in UNE patients. The numerous advan- elbow level equal to 8.3 mm provided high specificity and tages of SWE make it a perspective screening tool for early sensitivity in the detection of ulnar nerve entrapment [5, 17, detection of compressive neuropathies, with potential applica- 24, 25]. Our findings seem to be consistent with these obser- tion in occupational medicine. Prompt introduction of ade- vations. Not only did the mean CSA of the ulnar nerve at the quate preventive measures in persons at risk or implementa- cubital tunnel level turn out to be significantly larger in pa- tion of conservative treatment in individuals with early stages tients with UNE than in healthy controls (9.03, range, 5-18 of the neuropathy may prevent its long-term consequences, 2 2 mm vs. 6.47, range, 3-9 mm ), but also a significant positive such as chronic disability. correlation was found between this parameter and the The main limitation of this study may stem from the fact elastographically determined ulnar nerve stiffness at the en- that ulnar nerve stiffness was determined by one radiologist, trapment site. The latter observation seems to confirm the and thus, we were unable to estimate inter-observer reliability applicability of SWE to UNE diagnosis. The principal draw- of the results. During the course of another study, which is back of peripheral nerve ultrasonography is the lack of a soon to be conducted at our centre, we will analyse both inter- standardised examination protocol (examination technique, and intra-observer reliability of SWE measurements taken at type of transducer, wave frequency) [7]. Moreover, the exam- various levels of ulnar and median nerves. Interestingly, pa- ination is to a large degree operator-dependent, and thus, its tients from UNE group presented with significantly greater Table 3 Normalised values of Ulnar nerve SWE ratio Control group (n=38) UNE group (n=34) p ulnar nerve stiffness (ratios) in healthy volunteers (control group) Median Range Median Range and patients with confirmed cubital tunnel syndrome (UNE Cubital tunnel level : Distal arm level 1.0 0.8-1.2 2.8 1.7-4.0 <0.001* group) Cubital tunnel level : Mid-arm level 1.0 0.7-1.2 2.7 1.7-4.1 <0.001* *Statistically significant intergroup difference Eur Radiol Statistics and biometry One of the authors has significant statistical ulnar nerve stiffness proximally to the compression site than expertise. the controls. Because of the preliminary characteristic of our study and lack of evidence from similar study, we are unable Informed consent Written informed consent was obtained from all sub- to provide an unequivocal explanation for this phenomenon. jects (patients) in this study. The exact pathophysiology of compressive neuropathy is still not fully understood. It is commonly accepted that increased Ethical approval Institutional Review Board (The Bioethical Committee of the Medical Centre of Postgraduate Education in pressure on a peripheral nerve affects its microcirculation and, Warsaw) approval was obtained. therefore, blood supply. Resultant epineural ischaemia con- tributes to impaired venous outflow and stasis. Chronic com- Methodology pression may predispose to capillary leakage and neural oede- � prospective ma, which further aggravates the harmful effects of the prima- � diagnostic or prognostic study � multicentre study ry causal factor. With time, this mechanism induces inflam- mation, fibrosis, demyelination and eventually, after a Open Access This article is distributed under the terms of the Creative remyelination failure, axonal integrity loss [7, 47–49]. Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, Perhaps, this process involves the segment located proximally distribution, and reproduction in any medium, provided you give appro- to the compression site to a larger degree than previously priate credit to the original author(s) and the source, provide a link to the supposed, which manifests as greater stiffness of the nerve, Creative Commons license, and indicate if changes were made. likewise in our series. This would suggest that elastography may be a highly sensitive test to detect structural anomalies in peripheral nerves. This issue definitively needs to be ad- dressed in future studies. 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Shear-wave elastography: a new potential method to diagnose ulnar neuropathy at the elbow

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Medicine & Public Health; Imaging / Radiology; Diagnostic Radiology; Interventional Radiology; Neuroradiology; Ultrasound; Internal Medicine
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Abstract

Objectives The primary aim of this study was to verify if shear-wave elastography (SWE) can be used to diagnose ulnar neuropathy at the elbow (UNE). The secondary objective was to compare the cross-sectional areas (CSA) of the ulnar nerve in the cubital tunnel and to determine a cut-off value for this parameter accurately identifying persons with UNE. Methods The study included 34 patients with UNE (mean age, 59.35 years) and 38 healthy controls (mean age, 57.42 years). Each participant was subjected to SWE of the ulnar nerve at three levels: in the cubital tunnel (CT) and at the distal arm (DA) and mid-arm (MA). The CSA of the ulnar nerve in the cubital tunnel was estimated by means of ultrasonographic imaging. Results Patients with UNE presented with significantly greater ulnar nerve stiffness in the cubital tunnel than the controls (mean, 96.38 kPa vs. 33.08 kPa, p < 0.001). Ulnar nerve stiffness of 61 kPa, CT to DA stiffness ratio equal 1.68, and CT to MA stiffness ratio of 1.75 provided 100% specificity, sensitivity, positive and negative predictive value in the detection of UNE. Mean CSA of the ulnar nerve in the cubital tunnel turned out to be significantly larger in patients with UNE than in healthy controls (p <0.001). A weak positive correlation was found in the UNE group between the ulnar nerve CSA and stiffness (R = 0.31, p =0.008). Conclusions SWE seems to be a promising, reliable and simple quantitative adjunct test to support the diagnosis of UNE. Key Points � SWE enables reliable detection of cubital tunnel syndrome � Significant increase of entrapped ulnar nerve stiffness is observed in UNE � SWE is a perspective screening tool for early detection of compressive neuropathies . . . . Keywords Elastography Cubital tunnel syndrome Ulnar nerve Ulnar nerve entrapment syndrome Ulnar neuropathies Abbreviations MA Mid-arm CSA Cross-sectional areas MRI Magnetic resonance imaging CT Cubital tunnel ROI Region of interest DA Distal arm SWE Shear-wave elastography EMG Electromyography UNE Ulnar neuropathy at the elbow FCU Flexor carpi ulnaris US Ultrasonography * Bartłomiej Noszczyk Introduction noszczyk@melilot.pl Cubital tunnel syndrome, also referred to as ulnar neuropathy Department of Radiology, Medical Centre of Postgraduate at the elbow (UNE), is the second most common peripheral Education, Gruca Orthopaedic and Trauma Teaching Hospital, entrapment neuropathy after carpal tunnel syndrome. It can be Otwock, Poland 2 defined as a compression of the ulnar nerve at the level of the Department of Plastic and Reconstructive Surgery, Medical Centre of elbow or in its direct proximity [1–4]. The ulnar nerve may be Postgraduate Education, Prof. W. Orlowski Memorial Hospital, Czerniakowska 231 Street, 00-416 Warsaw, Mazowieckie, Poland compressed at the cubital tunnel inlet by the medial intermuscular septum and an aponeurotic band referred to as Department of Applied Pharmacy and Bioengineering, Medical University of Warsaw, Warsaw, Poland the arcade of Struthers. Moreover, the nerve may be entrapped Eur Radiol in the tunnel by the Osborne's band, a retinaculum that extends During recent years, sonoelastography, a relatively new from the medial epicondyle to the olecranon, and by the apo- imaging technology to quantify tissue stiffness, has been neurosis of the flexor carpi ulnaris (FCU); this is postulated to gaining a growing interest of researchers and healthcare pro- be the most common site of the entrapment [5–7]. Finally, the fessionals. Since its introduction by Ophir and colleagues in ulnar nerve may be compressed distally, at the tunnel outlet, 1991, sonoelastography has evolved considerably and found by the two heads of the FCU muscle [7]. application in many clinical disciplines; other potential uses of Idiopathic neuropathy seems to be the most common sonoelastography are still a subject of ongoing research [32, cause of UNE among many potential aetiological factors 33]. One highly promising application of sonoelastography, in of this condition [7, 8]. Ulnar neuropathy may also result particular shear-wave elastography (SWE), is the evaluation from habitual elbow flexion, acute or repetitive trauma, of peripheral nerve elasticity in patients with entrapment syn- excessive strain, presence of mass-like lesions, degenera- dromes. Several authors reported the use of elastography in tive arthritis and snapping triceps syndrome. The list of the diagnosis of median, sciatic and tibial compressive neu- intrinsic aetiological factors includes diseases of the thy- ropathies [34–43]. However, to the best of our knowledge, roid, diabetes mellitus, alcohol abuse, rheumatoid arthritis potential application of this technique as a method to detect and other systemic inflammatory diseases, to mention a UNE has not been studied thus far. few [5, 7, 9–11]. The aim of this study was to use SWE for the quantification Because of its high incidence in the general population and of ulnar nerve elasticity in patients with UNE and in healthy a broad spectrum of symptoms that may interfere with pa- controls, and to verify if this technique may find application in tients’ ability to work and their activities of daily living, clinical practice as an instrument to detect compressive UNE constitutes a significant clinical problem [7, 8, 12]. A neuropathy. number of healthcare professionals with various specialities, among them general practitioners, plastic surgeons, orthopae- dic surgeons and neurologists, are involved in the evaluation Materials and methods of UNE. Although no consensus regarding a management algorithm for UNE has been reached thus far, a recent meta- Study protocol analysis conducted by Mowlavi et al. demonstrated that clin- ical work-up is crucial to establish the diagnosis, to determine Protocol of the study was approved by the local bioethics the severity of ulnar neuropathy and to choose an appropriate committee, and written informed consent was sought from treatment strategy [12]. The diagnosis is based primarily on all participants. A plastic surgeon assigned the study subjects detailed analysis of medical history and physical examination. to one of two groups, based on the inclusion criteria presented According to many authors, electrodiagnostic studies consti- in Table 1. tute an essential component of the evaluation, as they can be Each study participant was subjected to US and SWE, both used to confirm the diagnosis and to assess the severity of conducted with a Toshiba iAplio 900 ultrasonograph equipped nerve damage. Additional tests, such as ultrasonography with a 5-18 MHz transducer (Canon Medical Systems). Both (US), plain film radiography and magnetic resonance imaging US and SWE were carried out during the same visit, by the (MRI), are recommended in patients with vague clinical pre- same radiologist with more than 4 years of experience in both sentation or during preoperative work-up [1, 5–7, 13–25]. diagnostic methods, blinded to subjects’ clinical history, phys- Based on published evidence we can expect that also diffusion ical and results of electrodiagnostic testing (EDX). The exam- tensor imaging may be soon added to the peripheral nerve ination was performed in a seated position, with the subject assessment armamentarium [26–31]. facing the examiner. The examined arm was kept downwards Table 1 Inclusion criteria of the UNE group Control group study UNE symptoms present on physical examination No evidence of UNE symptoms on physical examination UNE confirmed by EDX UNE excluded by EDX No history of elbow surgery No history of humeral or ulnar fracture No systemic neurological disorder No thyroid disorder No diabetes mellitus No current pregnancy EDX, Electrodiagnostic testing; UNE, Ulnar neuropathy at the elbow Eur Radiol alongside the trunk, with flexed elbow and forearm resting on nerve was always positioned in the centre of the 1x1 cm Q-box, the knee in a supine position. To control and minimise the set in such way that no underlying bone surfaces were captured pressure applied onto skin surface, an even layer of hydrogel on longitudinal ultrasonographic scans. Shear modulus data for was applied onto the examined area. the selected circular region of interest (ROI, 2 mm in diameter) During B-mode US examination of the cubital tunnel, the were acquired automatically by the ultrasonographic software; transducer was maintained perpendicularly to the ulnar nerve. the results were expressed in kilopascals (kPa). Representative Transverse cross-sections of the ulnar nerve were acquired at elastographic images are presented in Fig. 2. medial epicondyle level to determine the cross-sectional area of the nerve (CSA, in mm ). To measure the CSA, the ulnar Statistical analysis nerve margin was traced along the inner border of perineural echogenic rim, corresponding to the perineurium around the Normal distribution of the study variables was verified with hypoechoic nerve. Shapiro-Wilk test. Statistical characteristics of continuous var- Ulnar nerve stiffness was measured at three levels labelled iables were presented as means, medians and ranges. The with a skin marker prior to the examination: in the cubital tunnel characteristics of qualitative variables were shown as numbers at the level of medial epicondyle and at a posteromedial aspect and percentages. The significance of intergroup differences in of the arm, 5 cm and 10 cm proximally to the cubital tunnel inlet the statistical characteristics of continuous variables was ver- (i.e. on the distal and mid-arm, respectively) (Fig. 1). The course ified with Mann-Whitney U-test and Kruskal-Wallis test with of the ulnar nerve at each level was localised on B-mode scans. Dunn post-hoc tests, whereas the significant of intragroup Then, the transducer was rotated 90 degrees to obtain SWE- differences was tested with Wilcoxon signed-rank test. mode images of the nerve in a longitudinal axis. The transducer Diagnostic accuracy of ulnar nerve stiffness and CSA in the was always kept parallel to skin surface, and special attention detection of UNE was verified by means of receiver operating was paid to minimise the pressure and to avoid a disruption of characteristic (ROC) analysis. Sensitivity, specificity, positive the hydrogel layer. Nerve stiffness at each level was measured and negative predictive value (PPV and NPV, respectively) of three times with 2-3 min intervals and mean measurement was each potential predictor of UNE were calculated, along with used for further processing; during the examination, the ulnar 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 statisti- cal significance set at p ≤ 0.05. Results UNE group included 34 patients with mean age of 59.35 years (range, 36-85 years), among them six men (mean age, 62 years; range, 48-85 years) and 28 women (mean age, 58,79 years; range, 36-80 years), with confirmed ulnar compressive neuropathy at the elbow level. Control group comprised 38 healthy volunteers with mean age of 57.42 years (range, 38-84 years), among them three men (mean age, 53.67 years; range, 38-75 years) and 35 women (mean age, 57.74 years; range, 38-84 years), in whom UNE was excluded based on the re- sults of physical examination and EDX. The CSA of the ulnar nerve at the cubital tunnel level turned out to be significantly larger in patients with UNE than 2 2 in the controls (mean, 9.03 mm ;median, 8mm ;range, 5-18 2 2 2 2 mm vs. mean, 6.47 mm ;median, 6 mm ;range, 3-9 mm ; p < 0.001). The cut-off value for the CSA of the ulnar nerve at the cubital tunnel level, which most accurately distinguished between the individuals with the entrapment neuropathy and Fig. 1 Ulnar nerve segments subjected to elastographic examination. A, 2 without was 10 mm ; ROC analysis demonstrated that this Cubital tunnel at medial epicondyle level; B, Posteromedial arm, 5 cm value provided 38.2% sensitivity, 100% specificity, 100% proximally to the cubital tunnel inlet (distal arm level); C, Posteromedial arm, 10 cm proximally to the cubital tunnel inlet (mid-arm level) PPV and 64.4% NPV in the detection of UNE (Fig. 3). Eur Radiol Fig. 2 Elastographic presentation of ulnar nerve at the elbow level in (A) healthy individual (low SWE value), and (B) in patient with compressive neuropathy (high SWE value) The results of SWE measurements are summarised in obtained for the CT to DA ratio of 1.68, and CT to MA ratio Table 2. In any patient the differences between measurements of 1.75 (Fig. 3). that were repeated at each level with 3 minutes intervals did A weak positive correlation was found in the UNE group not exceed 2 kPa (SD ≥ 1.15). Compared to the controls, between the CSA of the ulnar nerve and its stiffness at the site patients with UNE presented with significantly greater ulnar of compression (R = 0.31, p = 0.008). Moreover, the CSA of nerve stiffness at each examined level. In the UNE group, the ulnar nerve correlated significantly with the values of CT mean ulnar nerve stiffness at the entrapment site in the cubital to DA (R = 0.31, p = 0.007) and CT to MA ratios (R = 0.30, p tunnel (96.38 kPa) was significantly greater than at the distal =0.010). arm and mid-arm (38.79 kPa and 39.06 kPa, respectively; p < 0.001). In the healthy controls, no statistically significant dif- ferences were found in ulnar nerve stiffness at various levels Discussion (p =0.779). Aside from the comparison of crude SWE parameters for We hypothesised that SWE can be used for an objective eval- the entrapment site, we also analysed their normalised values, uation of oedema and fibrosis associated with ulnar nerve obtained by dividing ulnar nerve stiffness at the cubital tunnel compression. The study showed clearly that patients with level (CT) by its stiffness at the distal arm (CT to DA ratio) or UNE presented with significantly greater ulnar nerve stiffness mid-arm (CT to MA ratio). The values of both ratios turned at the cubital tunnel level than healthy controls (mean, out to be significantly higher in patients with UNE than in the 96.38 kPa vs. 33.08 kPa). Furthermore, stiffness of the ulnar controls (p <0.001) (Table 3). nerve in UNE patients turned out to be significantly greater at ROC curves illustrating the diagnostic accuracy of the entrapment site than at the mid- and distal arm; however, a elastographically determined ulnar nerve stiffness at the similar relationship was not observed in the controls. ROC cubital tunnel level, CT to DA and CT to MA ratios in the analysis demonstrated that UNE could be accurately diag- detection of UNE are presented in Fig. 3. Ulnar nerve stiffness nosed whenever stiffness of the ulnar nerve at the entrapment at the cubital tunnel level equal 61 kPa provided 100% spec- site equalled 61 kPa or more. However, recall that ulnar nerve ificity, sensitivity, PPV and NPV in the detection of UNE. stiffness may vary from patient to patient due to the modula- Equally excellent indices of diagnostic accuracy were also tory effect of additional factors, such as sex, age, BMI, Eur Radiol Fig. 3 ROC curve illustrating diagnostic accuracy of (A) the cross-sectional area of ulnar nerve (10 mm ), (B) ulnar nerve stiffness at the entrapment site (61 kPa), (C) CT to DA ratio (1.68), and (D) CT to MA ratio (1.75) in the detection of UNE occupation, and upper limb physiognomy. Thus, to boost the with CTS than in the controls. Moreover, ROC analysis dem- diagnostic accuracy of SWE, instead of using the crude value onstrated that the cut-off values for CT to DA and CT to MA of ulnar nerve stiffness at the entrapment site, we recommend ratios (1.68 and 1.75, respectively) accurately distinguished a normalised value of this parameter; dividing ulnar nerve between patients with compressive ulnar neuropathy and stiffness at the entrapment site by the stiffness of its intact without. segment, one can eliminate individual variability in the As mentioned before, the diagnosis of UNE is based pri- elastographic parameters. In this study, we divided ulnar nerve marily on medical history and physical examination. stiffness at the entrapment site by its stiffness at the distal and Although this diagnosis is usually confirmed by EDX, US mid-arm, obtaining CT to DA and CT to MA ratios, respec- due to recent implementation of high-frequency transducers tively. Similar to the crude value of ulnar nerve stiffness, also enabling high-resolution images of peripheral nerves is the values of both ratios were significantly higher in patients emerging as a complementary method to evaluate patients Eur Radiol Table 2 Elastographic estimates of ulnar nerve stiffness (in kPa) in healthy volunteers (control group) and patients with confirmed cubital tunnel syndrome (UNE group) Ulnar nerve SWE value Control group (n=38) UNE group (n=34) p Mean Median Range SD Mean Median Range SD Cubital tunnel level 33.08 31 19-51 10.13 96.38 98 61-121 9.62 <0.001* Distal arm level 33.32 33 21-51 9.13 38.79 36,5 21-65 11.33 0.041 Mid-arm level 33.18 31 19-52 8.82 39.06 36 20-61 10.45 0.009 *Statistically significant intergroup difference with compressive neuropathies, e.g. UNE [5, 7, 15, 17, 22–25, result can be considered reliable only if conducted by an ex- 44, 45]. The hallmark sonographic features of entrapment perienced examiner. neuropathy include enlargement of the nerve, its hypoechoic Our findings are consistent with the results of other studies swelling proximal to the compression site, loss of normal fas- that analysed potential application of elastography in the eval- cicular pattern and, not infrequently, oedema of adjacent soft uation of compression neuropathies; also, those studies dem- tissues [7, 13, 20, 22, 23]. US is also suitable for the detection onstrated that compression may contribute to greater stiffness of space-occupying masses. Importantly, during the examina- of the entrapped nerve [34–43]. In our opinion, SWE consti- tion, ultrasonographic images of the affected limb can be com- tutes a valuable supplement to ultrasonographic examination pared with those of the contralateral extremity. High- of peripheral nerves, also in patients with UNE [14]. resolution US was shown to be more cost- and time- Elastography is both a time- and cost-effective method with effective than MRI, and its availability is markedly higher. a relatively steep learning curve. Elastographic findings add Noticeably, US can be used for both static and dynamic as- considerably to the results of US, providing quantitative data sessment of the ulnar nerve; this may be particularly helpful in on the nerve stiffness during both static and dynamic exami- patients with nerve subluxation or snapping triceps syndrome nation. In addition, it can determine the level of nerve entrap- [ 5 , 7]. Previous studies demonstrated that ment. In the future, with its growing availability in routine ultrasonographically determined ulnar nerve CSA was a fea- clinical practice, SWE may be used for the monitoring of sible indicator for UNE [5, 25, 46]; ulnar nerve CSA at the treatment outcomes in UNE patients. The numerous advan- elbow level equal to 8.3 mm provided high specificity and tages of SWE make it a perspective screening tool for early sensitivity in the detection of ulnar nerve entrapment [5, 17, detection of compressive neuropathies, with potential applica- 24, 25]. Our findings seem to be consistent with these obser- tion in occupational medicine. Prompt introduction of ade- vations. Not only did the mean CSA of the ulnar nerve at the quate preventive measures in persons at risk or implementa- cubital tunnel level turn out to be significantly larger in pa- tion of conservative treatment in individuals with early stages tients with UNE than in healthy controls (9.03, range, 5-18 of the neuropathy may prevent its long-term consequences, 2 2 mm vs. 6.47, range, 3-9 mm ), but also a significant positive such as chronic disability. correlation was found between this parameter and the The main limitation of this study may stem from the fact elastographically determined ulnar nerve stiffness at the en- that ulnar nerve stiffness was determined by one radiologist, trapment site. The latter observation seems to confirm the and thus, we were unable to estimate inter-observer reliability applicability of SWE to UNE diagnosis. The principal draw- of the results. During the course of another study, which is back of peripheral nerve ultrasonography is the lack of a soon to be conducted at our centre, we will analyse both inter- standardised examination protocol (examination technique, and intra-observer reliability of SWE measurements taken at type of transducer, wave frequency) [7]. Moreover, the exam- various levels of ulnar and median nerves. Interestingly, pa- ination is to a large degree operator-dependent, and thus, its tients from UNE group presented with significantly greater Table 3 Normalised values of Ulnar nerve SWE ratio Control group (n=38) UNE group (n=34) p ulnar nerve stiffness (ratios) in healthy volunteers (control group) Median Range Median Range and patients with confirmed cubital tunnel syndrome (UNE Cubital tunnel level : Distal arm level 1.0 0.8-1.2 2.8 1.7-4.0 <0.001* group) Cubital tunnel level : Mid-arm level 1.0 0.7-1.2 2.7 1.7-4.1 <0.001* *Statistically significant intergroup difference Eur Radiol Statistics and biometry One of the authors has significant statistical ulnar nerve stiffness proximally to the compression site than expertise. the controls. Because of the preliminary characteristic of our study and lack of evidence from similar study, we are unable Informed consent Written informed consent was obtained from all sub- to provide an unequivocal explanation for this phenomenon. jects (patients) in this study. The exact pathophysiology of compressive neuropathy is still not fully understood. It is commonly accepted that increased Ethical approval Institutional Review Board (The Bioethical Committee of the Medical Centre of Postgraduate Education in pressure on a peripheral nerve affects its microcirculation and, Warsaw) approval was obtained. therefore, blood supply. Resultant epineural ischaemia con- tributes to impaired venous outflow and stasis. Chronic com- Methodology pression may predispose to capillary leakage and neural oede- � prospective ma, which further aggravates the harmful effects of the prima- � diagnostic or prognostic study � multicentre study ry causal factor. With time, this mechanism induces inflam- mation, fibrosis, demyelination and eventually, after a Open Access This article is distributed under the terms of the Creative remyelination failure, axonal integrity loss [7, 47–49]. Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, Perhaps, this process involves the segment located proximally distribution, and reproduction in any medium, provided you give appro- to the compression site to a larger degree than previously priate credit to the original author(s) and the source, provide a link to the supposed, which manifests as greater stiffness of the nerve, Creative Commons license, and indicate if changes were made. likewise in our series. This would suggest that elastography may be a highly sensitive test to detect structural anomalies in peripheral nerves. This issue definitively needs to be ad- dressed in future studies. 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European RadiologySpringer Journals

Published: Jun 1, 2018

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