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Hand Surgery, Vol. 18, No. 2 (2013) 203208 © World Scientific Publishing Company DOI: 10.1142/S021881041350024X

MEDIAN NERVE DEFORMATION DURING FINGER MOTION IN CARPAL TUNNEL SYNDROME: CORRELATION BETWEEN NERVE CONDUCTION AND ULTRASONOGRAPHIC INDICES Yuichi Yoshii, Tomoo Ishii and Shinsuke Sakai Department of Orthopaedic Surgery Endowed Department of Human Resources Development for Community Medicine Tokyo Medical University Ibaraki Medical Center, Ami 300-0395, Japan Received 18 December 2012; Revised 28 February 2013; Accepted 28 February 2013 ABSTRACT To compare the median nerve deformation indices between carpal tunnel syndrome (CTS) patients and controls, 60 wrists of asymptomatic volunteers and 40 wrists of idiopathic CTS patients were evaluated by ultrasound. CTS was diagnosed through clinical findings and nerve conduction studies. Deformation indices, which were determined by the ratios of the nerve cross-sectional area, perimeter, aspect ratio, and circularity in finger extension and flexion positions, were measured. The deformation indices were compared between patients and controls. The correlation coefficients between distal motor latency and deformation indices were measured in CTS patients. There were significant differences between patients and controls in the deformation indices of perimeter, aspect ratio, and circularity. There was a mild correlation between distal latency and deformation indices of the perimeter and circularity (correlation coefficient 0.315 and 0.342). The deformation indices of perimeter and circularity might be useful to identify the nerve conduction severity of CTS. Keywords: Carpal Tunnel Syndrome; Median Nerve; Nerve Conduction; Deformation; Ultrasound.

alteration of the echogenicity of the flexor tendons and flexor retinaculum, synovial proliferation and the flattening of the median nerve in the carpal tunnel.16 Although these findings may distinguish patients with carpal tunnel syndrome from normal subjects, there have been few attempts to detect the material property change of the median nerve in CTS on the basis of ultrasound images. In previous studies, we established the ultrasound method to observe the movement of the structures in the carpal tunnel during finger motion.7 It was suggested that several ultrasound indices can be used to estimate the condition of the disease.8

INTRODUCTION Carpal tunnel syndrome (CTS) is a compression neuropathy of the median nerve at the wrist. The diagnosis of carpal tunnel syndrome is mostly clinically, and is usually confirmed with nerve conduction studies. Recently, the use of ultrasonography for diagnosing CTS has been extensively studied. The principal advantages of ultrasonography are its low cost, non-invasiveness, and the possibility of dynamic imaging. Cross-sectional ultrasound imaging has been proposed as an adjunct for the diagnosis of carpal tunnel syndrome. Static ultrasonography can detect pathological changes such as the thickening and

Correspondence to: Dr. Yuichi Yoshii, Department of Orthopaedic Surgery, Tokyo Medical University Ibaraki Medical Center, 3-20-1 Chuo, Ami, Inashiki, Ibaraki, 300-0395, Japan. Tel: (þ81) 29-887-1161, Fax: (þ81) 29-888-8303, E-mail: [email protected] 203

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Using this technique, we assessed the potential of ultrasound indices to determine the severity of CTS. The objective of this study was to compare the median nerve ultrasonographic indices of CTS patients and healthy controls, and to assess the potential correlation between median nerve deformation indices and the clinical severity of CTS. We hypothesised that there would be a correlation between median nerve deformation indices in the ultrasound and the clinical severity of carpal tunnel syndrome.

METHODS This study protocol was approved by our Institutional Review Board. Sixty wrists of 30 asymptomatic volunteers (25 women, five men, age range 2264 with a mean age of 42.8 years) and forty wrists of 27 patients with idiopathic carpal tunnel syndrome (21 women, six men, age range 4385 with a mean age of 60.6 years) were evaluated by ultrasound. The patients were excluded if they reported a history of cervical radiculopathy, rheumatoid arthritis, osteoarthritis, degenerative joint disease, flexor tendinitis, gout, hemodialysis, obesity, sarcoidosis, amyloidosis, or traumatic injuries to the arm. Participants were given a brief description of the purpose of the research and the testing procedures during the initial contact. Written consent was obtained from all study participants. Carpal tunnel syndrome was diagnosed by both clinical findings and nerve conduction studies. According to Hamada’s classification,9 each of the CTS patients was classified into stage I, II or III. Each stage is defined by the weakness of the thenar muscles, i.e. stage I: no weakness of the thenar muscle, stage II: mild weakness of the thenar muscle but no obstruction for thumb opposition, stage III: severe weakness of the thenar muscle with obstruction of thumb opposition. Nerve conduction studies were performed by an experienced clinical technologist. The technologist was blinded to the other findings. Distal motor latency was recorded at 7 cm proximal to the abductor pollicis brevis motor point.

Japan) equipped with a LA332 3.5/10 MHz Hi-Definition linear array transducer was set to a depth of 20 mm. The ultrasound evaluation was performed by an orthopaedic surgeon trained in the image acquisition procedure. The transducer was placed parallel to the wrist crease (proximal carpal tunnel), with the wrist in the neutral position. To minimise compression to the carpal tunnel contents, the transducer was applied to the skin without additional pressure. The transducer was maintained perpendicular to the surface skin of the wrist crease with reference to a protractor attached to the table. The median nerve was identified by cross-sectional and longitudinal ultrasonographic imaging during the flexion and the extension of the fingers. The participants were asked to flex and extend all four fingers together (index, middle, ring and little), moving from full (0 degrees at each finger joint) finger extension to the maximum flexion (i.e., until the fingertip touch to the palm). They were also asked to move continuously and repeatedly. Before the data collection began, participants practiced the motion with the examiner. Five cycles of motion were recorded. We evaluated both the left and right wrists in the healthy volunteers, but only the affected side in the CTS patients.

Image Analysis Using Analyze 10.0 Software (Biomedical Imaging Resource, Mayo Clinic, Rochester, MN), the recorded images were reviewed and the initial and final frames of the motion for the extension and flexion positions were chosen. Based on these images, the median nerve was outlined for both the extension and the flexion positions (Fig. 1). Then, based on the imaged

Image Acquisition Procedure The image acquisition procedure has been described previously.7 In brief, the subjects were asked to sit with the elbow flexed and the forearm supinated for the image acquisition. The forearm of the examinee was secured to a custom-made table with the wrist in the neutral position. An ultrasound scanner (Mylab Five, Hitachi Medical Corporation, Tokyo,

Fig. 1

Picture of the ultrasound image.

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determined by the ratio of the flexion position and extension position for each parameter, was calculated.

Statistical Analysis Fig. 2

Formula of the circularity.

median nerve; area, perimeter, aspect ratio of minimum enclosing rectangle and circularity were measured. To determine the minimum enclosing rectangle, the algorithm was started by fitting the smallest possible tangential enclosing rectangle to the image and measuring the area of the rectangle. The image was then rotated in 1 degree steps over a range of 90 degrees, recalculating the rectangle area at each step. The characteristics of the smallest rectangle found over the search range were defined as the minimum enclosing rectangle. The aspect ratio of the minimum enclosing rectangle was defined as the ratio of the minor axis length divided by the major axis length. We also measured the circularity as a compactness measure. It is the ratio of the area of the shape to the area of a circle (the most compact shape) which has the same perimeter. Thus, it was defined as (nerve perimeter)2/ (nerve area  4 ), mathematically (Fig. 2). Thus, a perfect circle would have a circularity equal to 1. In addition, the deformation index, which was defined as the value of the flexion position divided by the value of the extension position, was measured for each parameter. The average of the five pieces of data was calculated for each parameter and used for further analysis. Additionally, a deformation index, which was

Table 1

The results were expressed as means þ= standard deviations. To compare the deformation indices between the patients and the controls, Student’s t-test was used. A paired t-test was used to compare finger flexion and extension positions. The correlation coefficients between the clinical classification and the ultrasound indices were measured with Spearman’s correlation test. In addition, correlation coefficients between the distal motor latency and ultrasound indices were measured with Pearson’s correlation test. The p values of < 0:05 were considered significant. All analyses were performed by Statcel QC software (OMS publishing Inc., Saitama, Japan).

RESULTS A summary of the deformation indices is shown in Tables 1 and 2 where it can be seen that the area of the median nerve was greater in the CTS patients (in both extension and flexion positions) than in the controls (p < 0:01). The perimeter was greater in the extension position (p < 0:05), and the circularity was smaller in the flexion positions of CTS patients (p < 0:01). Also in CTS patients, the aspect ratio was found to be smaller in the finger extension position (p < 0:05), but greater in the finger flexion position (p < 0:01). In the results of the deformation indices, the aspect ratio increased and the circularity decreased in the CTS patients. The perimeter and circularity increased, and the aspect ratio decreased in the

The Results of the Ultrasonographic Indices.

Area, mm2 (SD)

Perimeter, mm (SD)

Aspect Ratio (SD)

Finger extension position CTS patients Controls

14.9 (4.5) 11.8 (2.3) a **

18.1 (4.8) b 16.6 (1.8) b *

0.30 (0.05) b 0.32 (0.04) b *

1.97 (0.26) b 1.90 (0.20) b

Finger flexion position CTS patients Controls

15.0 (4.8) 12.1 (2.4) a **

17.5 (4.8) b 18.4 (1.9) b

0.34 (0.08) b 0.26 (0.03) b **

1.85 (0.29) b 2.28 (0.23) b **

Note: *p < 0:05 between CTS patients and controls. **p < 0:01 between CTS patients and controls. a p < 0:05 between finger extension position and flexion position. b p < 0:01 between finger extension position and flexion position.

Circularity (SD)

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Table 2

CTS patients Controls

The Results of the Deformation Indices. Area

Perimeter

Aspect Ratio

Circularity

1.00 (0.08) 1.02 (0.08)

0.96 (0.06) 1.11 (0.06)*

1.12 (0.26) 0.81 (0.12)*

0.94 (0.11) 1.20 (0.13)*

Note: *p < 0:01 between CTS patients and controls.

Table 3

The Results of Correlation Coefficients. Area

Clinical severity Finger extension position Finger flexion position Deformation index

0.20 0.17 0.04

Nerve conduction Finger extension position 0.31* Finger flexion position 0.27 Deformation index 0.10

Perimeter Aspect Ratio Circularity 0.06 0.07 0.07 0.29 0.34* 0.32*

0.10 0.04 0.18 0.01 0.19 0.20

0.16 0.20 0.01 0.02 0.30 0.34*

Note: *significant correlation, p < 0:05.

controls. There were significant differences between CTS patients and controls in the deformation indices of perimeter, aspect ratio, and circularity (p < 0:01). The correlation coefficients for the clinical severity and nerve conduction studies are shown in Table 3. Four of the patients were excluded, because the motor wave of the thenar muscle could not be detected. The perimeter and circularity deformation indices were mildly correlated with distal motor latency (correlation coefficient 0.315 and 0.342, p < 0:05). There were no significant correlations between the clinical classification and the ultrasound indices.

DISCUSSION In this study, we showed that there is a possibility that the median nerve deformation indices have the potential to distinguish carpal tunnel syndrome patients from healthy controls. In addition, we showed that there may be a relationship between the median nerve ultrasound indices and the nerve conduction severity of carpal tunnel syndrome. There have been several studies which suggested that there may be some deformation of the shape of the median nerve during finger motion.7,8 Since the carpal tunnel is a closed space, the median nerve gets compressed by other tendons. Normally, the median nerve and flexor tendons are connected

by the multilayered connective tissue.10 In carpal tunnel syndrome, the connective tissue is found to be fibrotic and as a result the relative motion of the structures is reduced.1113 This fibrosis may also therefore affect the ability of the median nerve to move out of the way of the tendons during finger motion, resulting in increased compression of the nerve when the hand is active. This may cause a change in the median nerve deformation. In a previous study,8 it was suggested that the deformation indices of the area, perimeter, and circularity could be used to distinguish the CTS patients from the controls. In this study, the perimeter and circularity were consistent with the results of the previous study.8 In addition, the aspect ratio was able to distinguish the patients from the controls in this study. According to the deformation indices, the aspect ratio increased and the circularity decreased (close to circular) in the CTS patients, and the perimeter and circularity increased, and the aspect ratio decreased in the controls. Normally, if the nerve is compressed, it changes the distribution of the fascicles in the nerve. This results in a flattening of the nerve bundle according the direction of compression. This was related to the decrease of the aspect ratio in the finger flexion position of the controls and is a normal alteration during finger motion.7 However, in the case of CTS patients, the aspect ratio was increased in the finger flexion position. This may relate to increased pressure or a different distribution of the median nerve and flexor tendons inside the carpal tunnel. Chronic compression has been known to lead to fibrosis and thickening of the epineurium at the nerve trunk.14 We believe these different characters of deformation indices are reflected in the material property changes of the median nerve. Contrary to a previous study,8 this study did not find a significant difference in the deformation index of median nerve area between patients and controls. Also, there were some differences between the two studies concerning the absolute values of the parameters.8 This may be related to several factors, i.e. the differences in the age distribution, the stage of disease, or the ethnicity of the subjects. In this study, all of the subjects were Asian. In the previous study, the subjects included several different races. Hand size varies according to gender and ethnicity,15 and so this may be one reason for the different results in some of the parameters. Since the deformation indices of perimeter and circularity were consistent with the previous study, we would suggest using those parameters for the evaluations of CTS.

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There was mild correlation between distal motor latency and the deformation indices of the perimeter and the circularity. Several studies reported the correlation of ultrasonographic findings and CTS severity.16,17 It was reported that the swelling of the median nerve at the proximal carpal tunnel was related to the nerve conduction study.18 Also there were some reports which showed the correlation between electrophysiological severity and the cross-sectional area of the median nerve. The median nerve cross sectional area has been used to distinguish CTS patients from controls.19,20 It was reported that the absolute value of the cross-sectional area was increased in the CTS patients and this was consistent in our study. However, the values of the area have varied among reports.1921 One benefit of the deformation index reported in our study is that it was not influenced by proportions of body weight or hand size. Thus, we suggest the deformation indices of perimeter and circularity may be useful to determine the severity of nerve conduction in carpal tunnel syndrome. Unfortunately, there were no significant correlations between the clinical classification and the ultrasound indices. Since Hamada’s classification was designed only for motor function, it may be more useful to use a questionnaire to quantify the clinical symptoms. There are several limitations to our study. First, ultrasound measurements are known to be operator and experience dependent, specifically with regard to transducer placement. An experienced operator is mandatory for accurate acquisition of the image. However, in this study, the transducer was held in position with a custom fixture. Once the transducer was placed in a position, the examiner could focus on the nerve-tendon motion on the screen. This may help to minimise operator dependency. Second, we took the ultrasound images at the proximal edge of the carpal tunnel and did not image at the mid or distal carpal tunnel. While several other studies have used ultrasound measurements of the median nerve at the proximal carpal tunnel diagnostically,2,4 more distal images may also be useful. However, to take images at the mid or distal carpal tunnel requires transducer pressure on the relatively uneven subcutaneous tissues of the palm. This pressure may affect the motion of the immediately subjacent median nerve and flexor tendons. Third, we did not compare sensory nerve conduction of the median nerve to the ultrasound indices. It was excluded because many uncontrollable variables such as room temperature, patient condition and time taken can affect sensory conduction studies. Since the examiner was not a doctor, the needle electrode which may be able to identify a

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more sensitive response could not be used. Finally, it takes time to analyse the images. Although image acquisition can be finished in five minutes, the total time for the image analysis took more than 30 minutes per patient. Future studies should aim to shorten the image analysis time. In conclusion, we have found that the deformation indices of perimeter, aspect ratio and circularity can be useful to distinguish carpal tunnel syndrome patients from healthy controls. In addition, the ultrasound indices of the median nerve might be related to the severity of nerve conduction in carpal tunnel syndrome. This information may be useful to assess the relation between material property and function of the median nerve.

ACKNOWLEDGMENTS The project described was supported by a grant from Japanese Society for Surgery of the Hand (20092012).

References 1. Buchberger W, Sch€on G, Strasser K, Jungwirth W, Carpal tunnel syndrome: diagnosis with high-resolution sonography, Am J Roentgenol 159:793798, 1992. 2. Duncan I, Sullivan P, Lomas F, Sonography in the diagnosis of carpal tunnel syndrome, Am J Roentgenol 173:681684, 1999. 3. Lee CH, Kim TK, Yoon ES, Dhong ES, Correlation of high-resolution ultrasonographic findings with the clinical symptoms and electrodiagnostic data in carpal tunnel syndrome, Ann Plast Surg 54:2023, 2005. 4. Lee D, van Holsbeeck MT, Janevski PK, Ganos DL, Ditmars DM, Darian VB, Diagnosis of carpal tunnel syndrome. Ultrasound versus electromyography, Radiol Clin North Am 37:859872, 1999. 5. Missere M, Echography and the carpal tunnel syndrome, Radiol Med (Torino) 94:274, 1997. 6. Ferrari FS, Della Sala L, Cozza S, Guazzi G, Belcapo L, Mariottini A, Bolognini A, Stefani P, High-resolution ultrasonography in the study of carpal tunnel syndrome, Radiol Med (Torino) 93:336341, 1997. 7. Yoshii Y, Villarraga HR, Henderson J, Zhao C, An KN, Amadio PC, Ultrasound assessment of the displacement and deformation of the median nerve in the human carpal tunnel with active finger motion, J Bone Joint Surg Am 91:29222930, 2009. 8. van Doesburg MH, Henderson J, Yoshii Y, Mink van der Molen AB, Cha SS, An KN, Amadio PC, Median nerve deformation in differential finger motions: ultrasonographic comparison of carpal tunnel syndrome patients and healthy controls, J Orthop Res 30:643648, 2012. 9. Hamada Y, Ide T, Yamaguchi, Results of conservative and operative treatment of carpal tunnel syndrome, J Jpn Soc Surg Hand 2:156159, 1985.

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10. Guimberteau JC, The sliding system. Vascularized flexor tendon transfers, in New Ideas in Hand Flexor Tendon Surgery, Institut Aquitain De La Main, 2001. 11. Ettema AM, An KN, Zhao C, O’Byrne MM, Amadio PC, Flexor tendon and synovial gliding during simultaneous and single digit flexion in idiopathic carpal tunnel syndrome, J Biomech 41:292298, 2008. 12. Oh J, Zhao C, Zobitz ME, Wold LE, An KN, Amadio PC, Morphological changes of collagen fibrils in the subsynovial connective tissue in carpal tunnel syndrome, J Bone Joint Surg Am 88:824831, 2006. 13. Nakamichi K, Tachibana S, Restricted motion of the median nerve in carpal tunnel syndrome, J Hand Surg Br 20:460464, 1995. 14. Mackinnon SE, Dellon AL, Hudson AR, Hunter DA, A primate model for chronic nerve compression, J Reconstr Microsurg 1:185195, 1985. 15. Manning JT, Churchill AJ, Peters M, The effects of sex, ethnicity, and sexual orientation on self-measured digit ratio (2D:4D), Arch Sex Behav 36:223233, 2007. 16. Kang S, Kwon HK, Kim KH, Yun HS, Ultrasonography of median nerve and electrophysiologic severity in carpal tunnel syndrome, Ann Rehabil Med 36:7279, 2012.

17. Chen SF, Lu CH, Huang CR, Chuang YC, Tsai NW, Chang CC, Chang WN, Ultrasonographic median nerve cross-section areas measured by 8-point \inching test" for idiopathic carpal tunnel syndrome: a correlation of nerve conduction study severity and duration of clinical symptoms, BMC Med Imag 11:22, 2011. 18. Visser LH, Smidt MH, Lee ML, High-resolution sonography versus EMG in the diagnosis of carpal tunnel syndrome, J Neurol Neurosurg Psychiatry 79:6367, 2008. 19. Buchberger W, Sch€on G, Strasser K, Jungwirth W, High-resolution ultrasonography of the carpal tunnel, J Ultrasound Med 10:531537, 1991. 20. Nakamichi K, Tachibana S, Ultrasonographic measurement of median nerve cross-sectional area in idiopathic carpal tunnel syndrome: diagnostic accuracy, Muscle Nerve 26:798803, 2002. 21. Beekman R, Visser LH, Sonography in the diagnosis of carpal tunnel syndrome: a critical review of the literature, Muscle Nerve 27:2633, 2003.

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Median nerve deformation during finger motion in carpal tunnel syndrome: correlation between nerve conduction and ultrasonographic indices.

To compare the median nerve deformation indices between carpal tunnel syndrome (CTS) patients and controls, 60 wrists of asymptomatic volunteers and 4...
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