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Hand Surgery, Vol. 18, No. 2 (2013) 193202 © World Scientific Publishing Company DOI: 10.1142/S0218810413500238
Hand Surg. 2013.18:193-202. Downloaded from www.worldscientific.com by UNIVERSITY OF NEW ENGLAND LIBRARIES on 01/24/15. For personal use only.
MID-MOTION DEFORMATION OF MEDIAN NERVE DURING FINGER FLEXION: A NEW INSIGHT INTO THE DYNAMIC AETIOLOGY OF CARPAL TUNNEL SYNDROME Kyrin Liong,* Amitabha Lahiri,† Shujin Lee,‡ Dawn Chia,§ Arijit Biswas§,¶ and Heow Pueh Lee* *Department
of Mechanical Engineering National University of Singapore 9 Engineering Drive 1 Block EA, 07-08, Singapore 117576
†Department
of Hand and Reconstructive Microsurgery National University Hospital 5 Lower Kent Ridge Road Main Building 1, Level 2, Singapore 119074
‡Division
of Plastic, Reconstructive and Aesthetic Surgery National University Hospital 5 Lower Kent Ridge Road Kent Ridge Wing 2, Level 4, Singapore 119074 §
Department of Obstetrics and Gynecology National University Hospital 5 Lower Kent Ridge Road Kent Ridge Wing 2, Level 3, Singapore 119074 ¶
Department of Obstetrics and Gynecology Yong Loo Lin School of Medicine National University of Singapore 1E Lower Kent Ridge Road NUHS Tower Block, Level 12, Singapore 119228 Received 31 October 2012; Revised 17 December 2012; Accepted 18 December 2012 ABSTRACT Carpal tunnel syndrome (CTS) exists in a spectrum of severity and symptoms with a dynamic component. We aim to study dynamic nerve-tendon interrelationships in normal and mild CTS wrists during a fist motion, with dynamic ultrasound. We observed that in normal wrists, the nerve arcs in an ulnar-volar direction and changes from a circular shape to a flat oval during motion. In CTS Correspondence to: Dr. Kyrin Liong, Department of Mechanical Engineering, National University of Singapore, 9 Engineering Drive 1, Block EA, 07-08, Singapore 117576. Tel: (þ65) 6516-2235, Fax: (þ65) 6779-1459, E-mail: [email protected] 193
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candidates, however, the curvature and distance of the nerve’s path are reduced, while nerve shape remains relatively constant. In all candidates, the nerve is compressed against the flexor retinaculum, with the nerve subject to less compression in normal candidates as it moves dorsally into a recess. These findings suggest that besides mechanical compression from increased carpal tunnel contents alone, a decrease in nerve gliding movement may lead to CTS symptomatology. Furthermore, we identified that maximum nerve deformation occurs mid-motion, supporting the use of wrist splints for symptom relief. Keywords: Median Nerve; Carpal Tunnel Syndrome; Ultrasonographic Examination; Aetiology.
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INTRODUCTION While carpal tunnel syndrome (CTS) is the most common peripheral compressive neuropathy, its exact aetiopathogenesis is unknown.1 Symptoms vary from largely asymptomatic in mild CTS cases to the classic triad of pain, tingling and numbness in the median nerve distribution in more severe cases.2 Unfortunately, it is still unknown why CTS symptoms may sometimes be dynamic and fleeting. Furthermore, the release of mechanical obstruction with transverse carpal ligament (TCL) release over the median nerve can be associated with incomplete symptom relief 3,4 and it is possible that other factors, such as impaired nerve-tendon dynamics,5 may also contribute to the aetiopathogenesis of CTS. Dynamic ultrasound (US) is a modality that is well established in obstetric diagnosis and we aim to utilise this modality for performing in vivo, non-invasive, and real-time assessment for the study of the nerve-tendon dynamics in normal wrists, and compare this to mild CTS wrists, diagnosed by clinical symptoms using the Boston Carpal Tunnel Questionnaire (BCTQ). The objective of this study was to compare nerve-tendon dynamics between control and mild CTS candidates by comparison of median nerve displacements and deformation while performing a fist action. Hence, the change in wrist dynamics as CTS develops may be understood. Our null hypothesis was that we would find no difference between normal and mild CTS candidates in nerve displacement and deformation.
METHODS This study was performed in accordance with the guidelines of the institutional review board (IRB) and conforms to the Helsinki Declaraction.
Subjects A convenience sample of 24 candidates was recruited and separated into two groups based on CTS symptomology,
candidates’ medical histories and examination with provocative tests, including Phalen’s test and Durkan’s carpal compression test, and the BCTQ. There was one group of 12 normal individuals and another group of 12 individuals with mild CTS. A normal candidate was defined as one who did not possess any CTS symptoms, including any pain or tingling in the hand and forearm. In addition, to ensure that symptoms were solely a result of CTS, it was ensured that all symptomatic candidates did not possess a history of diabetes, smoking, wrist trauma and/or surgery. The age of the candidates ranged from 30 to 45 years. In the normal group, there were 11 males and one female, and in the mild CTS group, there were six females and six males.
BCTQ: Symptom Severity Score (SSS) and Functional Status Score (FSS) All the subjects were assessed using the BCTQ, encompassing two domains of CTS — ‘symptom severity’ and ‘functional status’. The BCTQ was chosen due to its high reproducibility, validity and sensitivity to any clinical changes.68 Based on the recommended calculations, symptomatic individuals had scores greater than one for either, or both scores. For the asymptomatic individuals, both scores were one.
US Examination We utilised the routine 3D US machine found in our antenatal diagnostic center (General Electric RSM5 14-D 3D/4D linear transducer probe with frequency range of 4.713 MHz and the ‘GE Voluson E8 expert’ US system). The subjects were seated with elbows flexed at 90 degrees and the forearm in a neutral-supine position on a table. The probe was placed at 90 degrees, at the proximal inlet of the carpal tunnel (CT) and the subjects were instructed to gradually flex the digits to full fist and then extend through three cycles. The real-time US videos were recorded and evaluated using digital image morphometry.
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(A) Raw ultrasound image Fig. 1
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(B) Outlined median nerve
(A) Raw ultrasound (US) image. (B) US image with hyperechogenic rim of median nerve demarcated in white.
US Image Analyses The ultrasonographic video images were digitised with VirtualDub (v1.9.11, GNC General Public License), and images were obtained from every fourth frame of the flexion extension cycle, to include motion from the fingers flexing from a neutral to full-flexion posture. These images were input into ImageJ (v1.44, Public Domain License) and scaled according to the 1 cm grid. The outer hyper-echogenic rim of the median nerve was then outlined in each image (Fig. 1) and its cross-sectional area (CSA) and centroid calculated, so that nerve area and displacement may be tracked. A best-fit second-order polynomial trend line is first applied to the calculated centroidal points (Microsoft Excel 2008, Redmond, WA). The displacement graphs were then input into ImageJ (v1.44, Public Domain License), where displacements were calculated. Deformation measurements — circularity, and aspect ratios, were calculated (Table 1), along with comparative measurements — deformation indices (DI), net deformations Table 1
Statistical Analysis Statistical analyses were performed by GraphPad Prism (v6.0 for Mac, San Diego, CA), which ensured that all data sets, with the exception of the DI and RC of ARMER , conformed to a Gaussian distribution. An unpaired, parametric student’s t-test was performed on Gaussian distributions, and a similar non-parametric test was performed on non-Gaussian distributions, to identify significant changes between the normal and CTS groups. A p value < 0:05 was considered statistically significant.
RESULTS All results are expressed as average value (standard deviation (SD)). Median nerve areas, displacements, and the DI, ND and
Deformation Measurement Quantities, their Associated Formulas, and Significances.
Deformation Measurement Quantity Circularity
(ND) and relative changes (RC) of the nerve in each image (Table 2).
Calculation Circularity ¼
(nerve area 4) (nerve perimeter) 2
Aspect ratio of the minimumenclosing rectangle (ARMER )
The software calculates the minimum-enclosing rectangle (MER) and best-fit ellipse (BFE), respectively, that would fit around the outlined median nerve. The aspect ratio (AR) is then calculated.
Aspect ratio of the best-fit ellipse (ARellip )
AR ¼
Long axis ðof MER or BFEÞ Short Axis
Significance . As this value approaches zero, an
increasingly elongated shape is observed. . An increase in these values implies a
flattening of the nerve throughout the hand motion.
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Table 2
Comparative Measurement Quantities, their Associated Formulas, and Significances.
Comparative Measurement Quantity Deformation Index (DI)
Calculation
Significance . A positive value (> 0) with respect to aspect
Ratio between: . Deformation measurement value that possesses the greatest
deviation from the initial value and, . Initial deformation measurement value.
Net Deformation (ND)
ratio measurements, and a negative value (< 0) with respect to circularity measurement, implies a flattening of the nerve. . The greater the absolute value, the greater the degree of nerve flattening.
Ratio between:
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. Final deformation measurement value, and . Initial deformation measurement value
Relative Change (RC)
Ratio between: . Greatest deviation within the deformation measurement
values, and . Initial deformation measurement value
RC of circularity, ARMER , and ARellip (Table 3) were recorded for all 24 candidates. Of the deformation measurements, ARMER displayed the best discrimination between cases and controls. The following key findings were observed:
(2) In all candidates, the median nerve arcs from mid-wrist in the ulnar-palmar direction and flattens from a circular shape to a flat oval. In mild CTS, however, nerve displacement is significantly reduced (p < 0:01) (Figs. 2 and 3), where the path’s curvature is decreased and exhibits greater linearity. The nerve remains in a flat ovoid shape, experiencing less flattening than normal candidates.
(1) The median nerve in mild CTS candidates was significantly larger than normal candidates (p < 0:001) throughout the fist motion (Table 3).
Table 3 Average Median Nerve Areas (mm2), Displacements (mm) and Deformation Indices (DI), Net Deformation (ND) and Relative Change (RC) of Median Nerve Circularity, ARMER and ARellip for Asymptomatic and Symptomatic Candidates. Median Nerve Characteristic (mm 2 )
Median Nerve Area Median Nerve Displacement (mm) Circularity DI ND RC
Control 9.17 5.12 0.68 0.85 0.32
(0.60) (2.16) (0.12) (0.21) (0.12)
CTS Patients 12.69 2.45 0.80 0.89 0.20
p value
(1.41) (1.36) (0.09) (0.13) (0.09)
< 0:0001 0.001 0.0085 0.2692 0.0073
ARMER
DI ND RC
2.12 (0.52) 1.71 (0.67) 1.12 (0.52)
1.50 (0.35) 1.32 (0.29) 0.50 (0.35)
0.0011 0.0426 0.0011
ARellip
DI ND RC
1.86 (0.50) 1.45 (0.58) 0.86 (0.50)
1.47 (0.27) 1.24 (0.26) 0.47 (0.27)
0.015 0.1362 0.015
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(A)
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(B)
Fig. 2 (A) CTS Symptom severity score (SSS) versus median nerve displacements (mm) during hand fist action. (B) CTS Functional status score (FSS) versus median nerve displacement (mm) during hand fist action. Note: Black columns indicate symptomatic candidates, and grey columns indicate control candidates.
(3) In all candidates, the nerve is subject to direct compression between the flexor tendons and TCL. In 41.67% (five of 12 candidates) of normal candidates, however, extendednerve movement, where the nerve moves in a dorsal-ulnar direction into a recess (Fig. 4), was observed. In mild CTS candidates, only 8.33% (one of 12 candidates) displayed this characteristic. This implies that the nerve is subject to less compression in normal compared to mild CTS subjects.
DISCUSSION In this study, our findings provided new insight to the nervetendon dynamics in the normal wrist and into the transition from a normal wrist to that with mild CTS. Specifically, we demonstrated that median nerve movement (p < 0:01) and DIs (p < 0:05) were significantly decreased in CTS patients than in controls.
Median Nerve Displacement During fist action, we observed that all candidates exhibited an arc-like nerve displacement in the volar-ulnar direction, opposite to that of the tendons, moving towards the TCL and flattening in the process (Fig. 3), due to the high compression that occurs within the hand during fist motion. Yoshii et al.5 and Kunze et al.9 reported similar findings in healthy individuals via US and magnetic resonance imaging (MRI), respectively. In our study, we observed that CTS patients exhibited significantly decreased nerve displacement (Table 3) (p < 0:01), in which the displacement arc was relatively linear, as compared to the more pronounced arc present in normal candidates (Fig. 4). The higher linearity of nerve translation in mild CTS subjects causes the nerve to be displaced to an increased
Fig. 3 (A) Median nerve displacement in a CTS symptomatic patient, displaying decreased movement. (B) Median nerve displacement in a normal candidate, displaying increased movement.
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(A) Plain Nerve Movement Fig. 4
(B) Extended Nerve Movement
(A) Plain, volar-ulnar median nerve displacement. (B) Extended, volar-ulnar movement, followed by dorsal-ulnar nerve displacement.
volar position, placing it closer to the TCL. The higher nerve displacements in normal candidates may be attributed to their smaller nerve CSA and less adhesive10,11 and fibrous connective tissue,12,13 both of which increase the nerve’s ability to displace in a pronounced arc, and easily glide into a protected recess away from direct compression between the TCL and tendons. In such instances, the nerve is thus subject to less compression. In mild CTS candidates, however, in addition to the significantly greater nerve CSA (p < 0:001), the stiffer and thicker interstitial matter that is commonly found in idiopathic CTS patients,5,1216 also contributes to the decreased nerve mobility and ability to translate within the CT during fist motion. As the nerve is entrapped and incapable of readjusting itself in mild CTS patients, it is consequently subject to greater compression than in normal candidates. This could account for nerve impingement symptoms that are encountered during hand actions, which cause dynamic compression of the median nerve. Our findings are supported by similar ultrasonographic studies conducted by Lopes et al.,16 Korstanje et al.14 and Erel et al.,17 who demonstrated that CTS patients experience less longitudinal nerve gliding than their normal counterparts. With respect to transverse displacement measurement, Nakamichi and Tachibana18 reported that normal candidates (1.75 (0.49) mm) exhibited greater transverse sliding than symptomatic candidates (0.37 (0.34) mm) during index finger flexion. Their relatively small values could be attributed to the decreased flexor tendon motion in index finger motion as compared to full fist motion, which involves all nine flexor tendons. Conversely, van
Doesburg et al.19 conducted a similar study and reported that CTS patients exhibited greater transverse nerve displacement (2.20 (1.80) mm) than their normal counterparts (1.93 (1.48) mm) during a four-finger curling motion. While comparable to our values, the nerve displacements in the aforementioned studies are calculated by assuming a linear translation of the median nerve from the initial to final motion frame. In our study, it is evident from the dynamic US imaging that this method is inaccurate (Fig. 5). A linear displacement assumption grossly underestimates the movement of the nerve, leading to inaccurate results. This could account for the differing results reported by van Doesburg et al.19
Median Nerve Deformation Measurements In our study, the flattening of the median nerve was consistently greater in the control group as compared to the symptomatic group (p < 0:05), with mild CTS subjects maintaining a fairly constant ovoid median nerve shape during fist motion. Despite its relative ease in motion, the normal median nerve still deforms to a greater extent than that in the symptomatic group, indicating the intrinsic malleability of a normal median nerve. The minimal nerve deformation exhibited by mild CTS candidates may be attributed to the fact that they have begun to experience \minor physiologic changes such as ischemia and fibrosis"8 that would inhibit shape-change. In the ischaemia reperfusion chronic cycle of chronic inflammation, nerve hardening and the hardening of peripheral tissue, which is also
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(A)
(B)
(C) Fig. 5 (A) Median nerve displacement from neutral to a full fist position. (B) Graph of median nerve aspect ratio (minimum enclosing rectangle) vs. time. (C) Graph of median nerve displacement from a neutral to a full fist position. Note: The images and graphs were obtained from an asymptomatic candidate. In (B) and (C), the actual and linear assumption results are indicated, where the latter describes the relationship between the initial and final frames of motion.
caused by oedema and operational scarring, result. This ultimately leads to a stiffer nerve that is less malleable and increasingly resistant to deformation, as demonstrated here. The increased nerve stiffness in such candidates might predispose him to localised pressure points on the nerve,5 possibly leading to increased severity of CTS symptoms. Numerous studies concur with our findings. Impink et al.,8 Altinok et al.,20 Wong et al.21 and Buchberger et al.22 reported a greater flattening ratio in normal candidates than CTS patients
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via US. In particular, Yesildag et al.23 reported average ND ratios of ARMER values of 2.9 (0.5) and 2.5 (0.5) for control and CTS candidates, respectively, and are comparable to our findings. Despite these concurring findings, other studies have suggested otherwise. Van Doesburg et al.24 utilised dynamic US to study healthy and CTS candidates performing a four-finger curling motion, and reported average ARMER values of 1.06 (5.26) and 1.03 (9.09) respectively. Sarria et al.,25 however, reported no significant differences between the two groups. These studies may have presented differing results due to the different methods in which median nerve flattening (ARellip or ARMER ) was calculated. More importantly, in studies such as those conducted by van Doesburg et al.24 and Allman et al.,26 where median nerve changes were observed, the manner in which nerve deformation was quantified may have produced misleading results. In these studies, only the initial and final frames of motion were obtained, and the ND was determined. From our analysis, we observed that maximum nerve deformation often occurs during mid-movement, instead of the end of the movement (Fig. 3). Therefore, utilising a ND calculation as opposed to DI or RC as a comparison between groups may result in possible misinterpretation of nerve deformation as p values are much higher when utilising ND (Table 3) — which may lead readers to believe that there are no significant differences between the groups, when in fact, there are. Due to these differing results and the malleability of the median nerve, it has been suggested that ARMER may be a poor predictor of CTS symptom prevalence.21,23,27 Nonetheless, we believe by observing decreased nerve displacement in addition to decreased nerve deformation and increased nerve CSA, CTS may be better diagnosed.
Maximum Nerve Deformation An important observation that was made in this study was that maximum nerve deformation occurs mid-motion (Fig. 5), instead of at the final nerve position, as supposed by previous studies. This suggests a more accurate nerve-tracking technique, as it demonstrates the necessity in tracking the nerve throughout its motion, as opposed to tracking its initial and final positions, and assuming a linear relationship between the two. This observation also has important implications as it validates the use of wrist splints that immobilise wrists to prevent CTS patients from maximally deforming the nerve during hand movements.
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Applications In this study, our comparison of normal to mild CTS candidates allowed us to gain insight into the physiological changes associated with the early stages of CTS. We have found that three main physiological changes occur as CTS begins to develop in subjects: (1) decreased nerve movement possibly due to the commonly associated tethering of the interstitial matter5,10,11; (2) increased median nerve CSA; and (3) stiffer nerve as indicated by a low DI. Hand Surg. 2013.18:193-202. Downloaded from www.worldscientific.com by UNIVERSITY OF NEW ENGLAND LIBRARIES on 01/24/15. For personal use only.
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These observations offer critical insight into the aetiopathogenesis of CTS, and may lead to improved preventive or treatment measures. Our findings also suggest that median nerve displacement may be utilised as an additional discriminatory characteristic that may be observed via dynamic US to indicate the prevalence of CTS symptoms, where a smaller nerve displacement may suggest CTS development. Furthermore, the wide availability of the aforementioned US equipment, albeit in routine obstetrics, makes this modality potentially vital in CTS diagnosis. Such US equipment, that is already readily available, may now be applied in new areas — CTS diagnosis. The availability, portability, low cost of US, and shorter examination times have made US increasingly popular as a complementary5,2831 or a preliminary technique to predict the \likelihood of developing CTS, rather than simply diagnosing it after the fact".32 There has also been increasing evidence that supports the use of US as a primary test in the diagnosis of CTS.31 Buchberger et al.,22 Duncan et al.27 and Allman et al.26 previously described four main characteristics that may be observed in CTS patients via US: (1) increased median nerve CSA at the pisiform level, and, to a lesser extent, at the hamate level; (2) increased swelling ratio, where there is a greater difference between the nerve area at the pisiform level and that at the distal radius; (3) increase in flattening ratio at the hamate level; and (4) increase in palmar bowing of the TCL. Despite these findings, all four characteristics were encountered in less than half of the CTS patients tested. Thus far, increased CSA of the median nerve proximal to the CT inlet or at the level
of the pisiform has proven to be the best predictor of CTS symptom prevalence.21,33,34 We propose that by utilising transverse median nerve displacement in conjunction with median nerve CSA and/or palmar bowing of the TCL, US may be able to accurately diagnose CTS. Nerve displacement and identification are particularly simple in axial imaging, and provides a simpler alternative to swelling ratio measurement, which requires comparison between different levels of the CT. US diagnostic tests are also painless and may therefore be considered in cases where the patients refuse nerve conduction studies.
Limitations Our study has certain limitations. Firstly, the sample size of both control and patient groups were small. A larger sample size that compares CTS severity, age, gender and ethnicity may provide more definitive conclusions with regards to nerve displacement and CTS prevalence. Secondly, no device was employed to ensure that candidates performed the fist action at a similar rate. Nonetheless, all candidates practiced the motion prior to US assessment to ensure the action was performed at a similar speed. Thirdly, a single examiner reviewed the images in our study and we did not assess inter or intra-rater reliability. Fourth, we imaged the proximal CT, and did not image the middle or distal part of the tunnel, as imaging at these sections is often difficult and less reliable due to the thicker subcutaneous tissue and increased palm curvature.
CONCLUSION In conclusion, we have demonstrated that median nerve characteristics — both dynamic and static — differ greatly between normal and mild CTS candidates. Mild CTS patients exhibit increased median nerve CSA, decreased nerve deformation and displacement, in the absence of an extended movement. Due to the commonly associated shear thickening of the interstitial matter in the CT and fibrosis of the median nerve, this also implies that mild CTS patients possess less ability for nerve gliding and movement, and are therefore more susceptible to higher compression, which could further aggravate CTS symptoms. Our findings also revealed that nerve deformation is most severe mid-motion, as opposed to the nerve’s final position. This validates the use of wrist splints to restrain CTS patients’ hand movements, thereby protecting the nerve from maximum compression that occurs mid-motion.
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Our findings also suggest the use of decreased nerve displacement as an additional discriminatory characteristic in dynamic US diagnosis of CTS. In addition, the wide availability of the US equipment utilised in this study further support the use of this modality for dynamic US CTS diagnosis, which could potentially increase the accuracy of CTS diagnosis.
SOURCE OF FUNDING
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The project was not funded by any external funding source.
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28. Padua L, Repeated ultrasound studies may help us understand what’s going on inside the nerve, Muscle Nerve 44:67, 2011. 29. Wiesler ER, Chloros GD, Cartwright MS, Smith BP, Rushing J, Walker FO, The use of diagnostic ultrasound in carpal tunnel syndrome, J Hand Surg Am 31:726732, 2006. 30. Martins RS, Siqueira MG, Sirnplicio H, Agapito D, Medeiros M, Magnetic resonance imaging of idiopathic carpal tunnel syndrome: correlation with clinical findings and electrophysiological investigation, Clin Neurol Neurosurg 110:3845, 2008. 31. Wilder-Smith EPV, Nerve ultrasound: ready for clinical practice? Neurol Asia 17:14, 2012.
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32. Impink BG, Boninger ML, Walker H, Collinger JL, Niyonkuru C, Ultrasonographic median nerve changes after a wheelchair sporting event, Arch Phys Med Rehab 90:14891494, 2009. 33. Beekman R, Visser LH, Sonography in the diagnosis of carpal tunnel syndrome: a critical review of the literature, Muscle Nerve 27:2633, 2003. 34. Yao L, Gai N, Median nerve cross-sectional area and MRI diffusion characteristics: normative values at the carpal tunnel, Skel Radiol 38:355361, 2009.
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MID-MOTION DEFORMATION OF MEDIAN NERVE DURING FINGER FLEXION: A NEW INSIGHT INTO THE DYNAMIC AETIOLOGY OF CARPAL TUNNEL SYNDROME Kyrin Liong,* Amitabha Lahiri,† Shujin Lee,‡ Dawn Chia,§ Arijit Biswas§,¶ and Heow Pueh Lee* *Department
of Mechanical Engineering National University of Singapore 9 Engineering Drive 1 Block EA, 07-08, Singapore 117576
†Department
of Hand and Reconstructive Microsurgery National University Hospital 5 Lower Kent Ridge Road Main Building 1, Level 2, Singapore 119074
‡Division
of Plastic, Reconstructive and Aesthetic Surgery National University Hospital 5 Lower Kent Ridge Road Kent Ridge Wing 2, Level 4, Singapore 119074 §
Department of Obstetrics and Gynecology National University Hospital 5 Lower Kent Ridge Road Kent Ridge Wing 2, Level 3, Singapore 119074 ¶
Department of Obstetrics and Gynecology Yong Loo Lin School of Medicine National University of Singapore 1E Lower Kent Ridge Road NUHS Tower Block, Level 12, Singapore 119228 Received 31 October 2012; Revised 17 December 2012; Accepted 18 December 2012 ABSTRACT Carpal tunnel syndrome (CTS) exists in a spectrum of severity and symptoms with a dynamic component. We aim to study dynamic nerve-tendon interrelationships in normal and mild CTS wrists during a fist motion, with dynamic ultrasound. We observed that in normal wrists, the nerve arcs in an ulnar-volar direction and changes from a circular shape to a flat oval during motion. In CTS Correspondence to: Dr. Kyrin Liong, Department of Mechanical Engineering, National University of Singapore, 9 Engineering Drive 1, Block EA, 07-08, Singapore 117576. Tel: (þ65) 6516-2235, Fax: (þ65) 6779-1459, E-mail: [email protected] 193
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candidates, however, the curvature and distance of the nerve’s path are reduced, while nerve shape remains relatively constant. In all candidates, the nerve is compressed against the flexor retinaculum, with the nerve subject to less compression in normal candidates as it moves dorsally into a recess. These findings suggest that besides mechanical compression from increased carpal tunnel contents alone, a decrease in nerve gliding movement may lead to CTS symptomatology. Furthermore, we identified that maximum nerve deformation occurs mid-motion, supporting the use of wrist splints for symptom relief. Keywords: Median Nerve; Carpal Tunnel Syndrome; Ultrasonographic Examination; Aetiology.
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INTRODUCTION While carpal tunnel syndrome (CTS) is the most common peripheral compressive neuropathy, its exact aetiopathogenesis is unknown.1 Symptoms vary from largely asymptomatic in mild CTS cases to the classic triad of pain, tingling and numbness in the median nerve distribution in more severe cases.2 Unfortunately, it is still unknown why CTS symptoms may sometimes be dynamic and fleeting. Furthermore, the release of mechanical obstruction with transverse carpal ligament (TCL) release over the median nerve can be associated with incomplete symptom relief 3,4 and it is possible that other factors, such as impaired nerve-tendon dynamics,5 may also contribute to the aetiopathogenesis of CTS. Dynamic ultrasound (US) is a modality that is well established in obstetric diagnosis and we aim to utilise this modality for performing in vivo, non-invasive, and real-time assessment for the study of the nerve-tendon dynamics in normal wrists, and compare this to mild CTS wrists, diagnosed by clinical symptoms using the Boston Carpal Tunnel Questionnaire (BCTQ). The objective of this study was to compare nerve-tendon dynamics between control and mild CTS candidates by comparison of median nerve displacements and deformation while performing a fist action. Hence, the change in wrist dynamics as CTS develops may be understood. Our null hypothesis was that we would find no difference between normal and mild CTS candidates in nerve displacement and deformation.
METHODS This study was performed in accordance with the guidelines of the institutional review board (IRB) and conforms to the Helsinki Declaraction.
Subjects A convenience sample of 24 candidates was recruited and separated into two groups based on CTS symptomology,
candidates’ medical histories and examination with provocative tests, including Phalen’s test and Durkan’s carpal compression test, and the BCTQ. There was one group of 12 normal individuals and another group of 12 individuals with mild CTS. A normal candidate was defined as one who did not possess any CTS symptoms, including any pain or tingling in the hand and forearm. In addition, to ensure that symptoms were solely a result of CTS, it was ensured that all symptomatic candidates did not possess a history of diabetes, smoking, wrist trauma and/or surgery. The age of the candidates ranged from 30 to 45 years. In the normal group, there were 11 males and one female, and in the mild CTS group, there were six females and six males.
BCTQ: Symptom Severity Score (SSS) and Functional Status Score (FSS) All the subjects were assessed using the BCTQ, encompassing two domains of CTS — ‘symptom severity’ and ‘functional status’. The BCTQ was chosen due to its high reproducibility, validity and sensitivity to any clinical changes.68 Based on the recommended calculations, symptomatic individuals had scores greater than one for either, or both scores. For the asymptomatic individuals, both scores were one.
US Examination We utilised the routine 3D US machine found in our antenatal diagnostic center (General Electric RSM5 14-D 3D/4D linear transducer probe with frequency range of 4.713 MHz and the ‘GE Voluson E8 expert’ US system). The subjects were seated with elbows flexed at 90 degrees and the forearm in a neutral-supine position on a table. The probe was placed at 90 degrees, at the proximal inlet of the carpal tunnel (CT) and the subjects were instructed to gradually flex the digits to full fist and then extend through three cycles. The real-time US videos were recorded and evaluated using digital image morphometry.
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(A) Raw ultrasound image Fig. 1
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(B) Outlined median nerve
(A) Raw ultrasound (US) image. (B) US image with hyperechogenic rim of median nerve demarcated in white.
US Image Analyses The ultrasonographic video images were digitised with VirtualDub (v1.9.11, GNC General Public License), and images were obtained from every fourth frame of the flexion extension cycle, to include motion from the fingers flexing from a neutral to full-flexion posture. These images were input into ImageJ (v1.44, Public Domain License) and scaled according to the 1 cm grid. The outer hyper-echogenic rim of the median nerve was then outlined in each image (Fig. 1) and its cross-sectional area (CSA) and centroid calculated, so that nerve area and displacement may be tracked. A best-fit second-order polynomial trend line is first applied to the calculated centroidal points (Microsoft Excel 2008, Redmond, WA). The displacement graphs were then input into ImageJ (v1.44, Public Domain License), where displacements were calculated. Deformation measurements — circularity, and aspect ratios, were calculated (Table 1), along with comparative measurements — deformation indices (DI), net deformations Table 1
Statistical Analysis Statistical analyses were performed by GraphPad Prism (v6.0 for Mac, San Diego, CA), which ensured that all data sets, with the exception of the DI and RC of ARMER , conformed to a Gaussian distribution. An unpaired, parametric student’s t-test was performed on Gaussian distributions, and a similar non-parametric test was performed on non-Gaussian distributions, to identify significant changes between the normal and CTS groups. A p value < 0:05 was considered statistically significant.
RESULTS All results are expressed as average value (standard deviation (SD)). Median nerve areas, displacements, and the DI, ND and
Deformation Measurement Quantities, their Associated Formulas, and Significances.
Deformation Measurement Quantity Circularity
(ND) and relative changes (RC) of the nerve in each image (Table 2).
Calculation Circularity ¼
(nerve area 4) (nerve perimeter) 2
Aspect ratio of the minimumenclosing rectangle (ARMER )
The software calculates the minimum-enclosing rectangle (MER) and best-fit ellipse (BFE), respectively, that would fit around the outlined median nerve. The aspect ratio (AR) is then calculated.
Aspect ratio of the best-fit ellipse (ARellip )
AR ¼
Long axis ðof MER or BFEÞ Short Axis
Significance . As this value approaches zero, an
increasingly elongated shape is observed. . An increase in these values implies a
flattening of the nerve throughout the hand motion.
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Table 2
Comparative Measurement Quantities, their Associated Formulas, and Significances.
Comparative Measurement Quantity Deformation Index (DI)
Calculation
Significance . A positive value (> 0) with respect to aspect
Ratio between: . Deformation measurement value that possesses the greatest
deviation from the initial value and, . Initial deformation measurement value.
Net Deformation (ND)
ratio measurements, and a negative value (< 0) with respect to circularity measurement, implies a flattening of the nerve. . The greater the absolute value, the greater the degree of nerve flattening.
Ratio between:
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. Final deformation measurement value, and . Initial deformation measurement value
Relative Change (RC)
Ratio between: . Greatest deviation within the deformation measurement
values, and . Initial deformation measurement value
RC of circularity, ARMER , and ARellip (Table 3) were recorded for all 24 candidates. Of the deformation measurements, ARMER displayed the best discrimination between cases and controls. The following key findings were observed:
(2) In all candidates, the median nerve arcs from mid-wrist in the ulnar-palmar direction and flattens from a circular shape to a flat oval. In mild CTS, however, nerve displacement is significantly reduced (p < 0:01) (Figs. 2 and 3), where the path’s curvature is decreased and exhibits greater linearity. The nerve remains in a flat ovoid shape, experiencing less flattening than normal candidates.
(1) The median nerve in mild CTS candidates was significantly larger than normal candidates (p < 0:001) throughout the fist motion (Table 3).
Table 3 Average Median Nerve Areas (mm2), Displacements (mm) and Deformation Indices (DI), Net Deformation (ND) and Relative Change (RC) of Median Nerve Circularity, ARMER and ARellip for Asymptomatic and Symptomatic Candidates. Median Nerve Characteristic (mm 2 )
Median Nerve Area Median Nerve Displacement (mm) Circularity DI ND RC
Control 9.17 5.12 0.68 0.85 0.32
(0.60) (2.16) (0.12) (0.21) (0.12)
CTS Patients 12.69 2.45 0.80 0.89 0.20
p value
(1.41) (1.36) (0.09) (0.13) (0.09)
< 0:0001 0.001 0.0085 0.2692 0.0073
ARMER
DI ND RC
2.12 (0.52) 1.71 (0.67) 1.12 (0.52)
1.50 (0.35) 1.32 (0.29) 0.50 (0.35)
0.0011 0.0426 0.0011
ARellip
DI ND RC
1.86 (0.50) 1.45 (0.58) 0.86 (0.50)
1.47 (0.27) 1.24 (0.26) 0.47 (0.27)
0.015 0.1362 0.015
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(A)
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(B)
Fig. 2 (A) CTS Symptom severity score (SSS) versus median nerve displacements (mm) during hand fist action. (B) CTS Functional status score (FSS) versus median nerve displacement (mm) during hand fist action. Note: Black columns indicate symptomatic candidates, and grey columns indicate control candidates.
(3) In all candidates, the nerve is subject to direct compression between the flexor tendons and TCL. In 41.67% (five of 12 candidates) of normal candidates, however, extendednerve movement, where the nerve moves in a dorsal-ulnar direction into a recess (Fig. 4), was observed. In mild CTS candidates, only 8.33% (one of 12 candidates) displayed this characteristic. This implies that the nerve is subject to less compression in normal compared to mild CTS subjects.
DISCUSSION In this study, our findings provided new insight to the nervetendon dynamics in the normal wrist and into the transition from a normal wrist to that with mild CTS. Specifically, we demonstrated that median nerve movement (p < 0:01) and DIs (p < 0:05) were significantly decreased in CTS patients than in controls.
Median Nerve Displacement During fist action, we observed that all candidates exhibited an arc-like nerve displacement in the volar-ulnar direction, opposite to that of the tendons, moving towards the TCL and flattening in the process (Fig. 3), due to the high compression that occurs within the hand during fist motion. Yoshii et al.5 and Kunze et al.9 reported similar findings in healthy individuals via US and magnetic resonance imaging (MRI), respectively. In our study, we observed that CTS patients exhibited significantly decreased nerve displacement (Table 3) (p < 0:01), in which the displacement arc was relatively linear, as compared to the more pronounced arc present in normal candidates (Fig. 4). The higher linearity of nerve translation in mild CTS subjects causes the nerve to be displaced to an increased
Fig. 3 (A) Median nerve displacement in a CTS symptomatic patient, displaying decreased movement. (B) Median nerve displacement in a normal candidate, displaying increased movement.
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(A) Plain Nerve Movement Fig. 4
(B) Extended Nerve Movement
(A) Plain, volar-ulnar median nerve displacement. (B) Extended, volar-ulnar movement, followed by dorsal-ulnar nerve displacement.
volar position, placing it closer to the TCL. The higher nerve displacements in normal candidates may be attributed to their smaller nerve CSA and less adhesive10,11 and fibrous connective tissue,12,13 both of which increase the nerve’s ability to displace in a pronounced arc, and easily glide into a protected recess away from direct compression between the TCL and tendons. In such instances, the nerve is thus subject to less compression. In mild CTS candidates, however, in addition to the significantly greater nerve CSA (p < 0:001), the stiffer and thicker interstitial matter that is commonly found in idiopathic CTS patients,5,1216 also contributes to the decreased nerve mobility and ability to translate within the CT during fist motion. As the nerve is entrapped and incapable of readjusting itself in mild CTS patients, it is consequently subject to greater compression than in normal candidates. This could account for nerve impingement symptoms that are encountered during hand actions, which cause dynamic compression of the median nerve. Our findings are supported by similar ultrasonographic studies conducted by Lopes et al.,16 Korstanje et al.14 and Erel et al.,17 who demonstrated that CTS patients experience less longitudinal nerve gliding than their normal counterparts. With respect to transverse displacement measurement, Nakamichi and Tachibana18 reported that normal candidates (1.75 (0.49) mm) exhibited greater transverse sliding than symptomatic candidates (0.37 (0.34) mm) during index finger flexion. Their relatively small values could be attributed to the decreased flexor tendon motion in index finger motion as compared to full fist motion, which involves all nine flexor tendons. Conversely, van
Doesburg et al.19 conducted a similar study and reported that CTS patients exhibited greater transverse nerve displacement (2.20 (1.80) mm) than their normal counterparts (1.93 (1.48) mm) during a four-finger curling motion. While comparable to our values, the nerve displacements in the aforementioned studies are calculated by assuming a linear translation of the median nerve from the initial to final motion frame. In our study, it is evident from the dynamic US imaging that this method is inaccurate (Fig. 5). A linear displacement assumption grossly underestimates the movement of the nerve, leading to inaccurate results. This could account for the differing results reported by van Doesburg et al.19
Median Nerve Deformation Measurements In our study, the flattening of the median nerve was consistently greater in the control group as compared to the symptomatic group (p < 0:05), with mild CTS subjects maintaining a fairly constant ovoid median nerve shape during fist motion. Despite its relative ease in motion, the normal median nerve still deforms to a greater extent than that in the symptomatic group, indicating the intrinsic malleability of a normal median nerve. The minimal nerve deformation exhibited by mild CTS candidates may be attributed to the fact that they have begun to experience \minor physiologic changes such as ischemia and fibrosis"8 that would inhibit shape-change. In the ischaemia reperfusion chronic cycle of chronic inflammation, nerve hardening and the hardening of peripheral tissue, which is also
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(A)
(B)
(C) Fig. 5 (A) Median nerve displacement from neutral to a full fist position. (B) Graph of median nerve aspect ratio (minimum enclosing rectangle) vs. time. (C) Graph of median nerve displacement from a neutral to a full fist position. Note: The images and graphs were obtained from an asymptomatic candidate. In (B) and (C), the actual and linear assumption results are indicated, where the latter describes the relationship between the initial and final frames of motion.
caused by oedema and operational scarring, result. This ultimately leads to a stiffer nerve that is less malleable and increasingly resistant to deformation, as demonstrated here. The increased nerve stiffness in such candidates might predispose him to localised pressure points on the nerve,5 possibly leading to increased severity of CTS symptoms. Numerous studies concur with our findings. Impink et al.,8 Altinok et al.,20 Wong et al.21 and Buchberger et al.22 reported a greater flattening ratio in normal candidates than CTS patients
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via US. In particular, Yesildag et al.23 reported average ND ratios of ARMER values of 2.9 (0.5) and 2.5 (0.5) for control and CTS candidates, respectively, and are comparable to our findings. Despite these concurring findings, other studies have suggested otherwise. Van Doesburg et al.24 utilised dynamic US to study healthy and CTS candidates performing a four-finger curling motion, and reported average ARMER values of 1.06 (5.26) and 1.03 (9.09) respectively. Sarria et al.,25 however, reported no significant differences between the two groups. These studies may have presented differing results due to the different methods in which median nerve flattening (ARellip or ARMER ) was calculated. More importantly, in studies such as those conducted by van Doesburg et al.24 and Allman et al.,26 where median nerve changes were observed, the manner in which nerve deformation was quantified may have produced misleading results. In these studies, only the initial and final frames of motion were obtained, and the ND was determined. From our analysis, we observed that maximum nerve deformation often occurs during mid-movement, instead of the end of the movement (Fig. 3). Therefore, utilising a ND calculation as opposed to DI or RC as a comparison between groups may result in possible misinterpretation of nerve deformation as p values are much higher when utilising ND (Table 3) — which may lead readers to believe that there are no significant differences between the groups, when in fact, there are. Due to these differing results and the malleability of the median nerve, it has been suggested that ARMER may be a poor predictor of CTS symptom prevalence.21,23,27 Nonetheless, we believe by observing decreased nerve displacement in addition to decreased nerve deformation and increased nerve CSA, CTS may be better diagnosed.
Maximum Nerve Deformation An important observation that was made in this study was that maximum nerve deformation occurs mid-motion (Fig. 5), instead of at the final nerve position, as supposed by previous studies. This suggests a more accurate nerve-tracking technique, as it demonstrates the necessity in tracking the nerve throughout its motion, as opposed to tracking its initial and final positions, and assuming a linear relationship between the two. This observation also has important implications as it validates the use of wrist splints that immobilise wrists to prevent CTS patients from maximally deforming the nerve during hand movements.
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Applications In this study, our comparison of normal to mild CTS candidates allowed us to gain insight into the physiological changes associated with the early stages of CTS. We have found that three main physiological changes occur as CTS begins to develop in subjects: (1) decreased nerve movement possibly due to the commonly associated tethering of the interstitial matter5,10,11; (2) increased median nerve CSA; and (3) stiffer nerve as indicated by a low DI. Hand Surg. 2013.18:193-202. Downloaded from www.worldscientific.com by UNIVERSITY OF NEW ENGLAND LIBRARIES on 01/24/15. For personal use only.
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These observations offer critical insight into the aetiopathogenesis of CTS, and may lead to improved preventive or treatment measures. Our findings also suggest that median nerve displacement may be utilised as an additional discriminatory characteristic that may be observed via dynamic US to indicate the prevalence of CTS symptoms, where a smaller nerve displacement may suggest CTS development. Furthermore, the wide availability of the aforementioned US equipment, albeit in routine obstetrics, makes this modality potentially vital in CTS diagnosis. Such US equipment, that is already readily available, may now be applied in new areas — CTS diagnosis. The availability, portability, low cost of US, and shorter examination times have made US increasingly popular as a complementary5,2831 or a preliminary technique to predict the \likelihood of developing CTS, rather than simply diagnosing it after the fact".32 There has also been increasing evidence that supports the use of US as a primary test in the diagnosis of CTS.31 Buchberger et al.,22 Duncan et al.27 and Allman et al.26 previously described four main characteristics that may be observed in CTS patients via US: (1) increased median nerve CSA at the pisiform level, and, to a lesser extent, at the hamate level; (2) increased swelling ratio, where there is a greater difference between the nerve area at the pisiform level and that at the distal radius; (3) increase in flattening ratio at the hamate level; and (4) increase in palmar bowing of the TCL. Despite these findings, all four characteristics were encountered in less than half of the CTS patients tested. Thus far, increased CSA of the median nerve proximal to the CT inlet or at the level
of the pisiform has proven to be the best predictor of CTS symptom prevalence.21,33,34 We propose that by utilising transverse median nerve displacement in conjunction with median nerve CSA and/or palmar bowing of the TCL, US may be able to accurately diagnose CTS. Nerve displacement and identification are particularly simple in axial imaging, and provides a simpler alternative to swelling ratio measurement, which requires comparison between different levels of the CT. US diagnostic tests are also painless and may therefore be considered in cases where the patients refuse nerve conduction studies.
Limitations Our study has certain limitations. Firstly, the sample size of both control and patient groups were small. A larger sample size that compares CTS severity, age, gender and ethnicity may provide more definitive conclusions with regards to nerve displacement and CTS prevalence. Secondly, no device was employed to ensure that candidates performed the fist action at a similar rate. Nonetheless, all candidates practiced the motion prior to US assessment to ensure the action was performed at a similar speed. Thirdly, a single examiner reviewed the images in our study and we did not assess inter or intra-rater reliability. Fourth, we imaged the proximal CT, and did not image the middle or distal part of the tunnel, as imaging at these sections is often difficult and less reliable due to the thicker subcutaneous tissue and increased palm curvature.
CONCLUSION In conclusion, we have demonstrated that median nerve characteristics — both dynamic and static — differ greatly between normal and mild CTS candidates. Mild CTS patients exhibit increased median nerve CSA, decreased nerve deformation and displacement, in the absence of an extended movement. Due to the commonly associated shear thickening of the interstitial matter in the CT and fibrosis of the median nerve, this also implies that mild CTS patients possess less ability for nerve gliding and movement, and are therefore more susceptible to higher compression, which could further aggravate CTS symptoms. Our findings also revealed that nerve deformation is most severe mid-motion, as opposed to the nerve’s final position. This validates the use of wrist splints to restrain CTS patients’ hand movements, thereby protecting the nerve from maximum compression that occurs mid-motion.
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Our findings also suggest the use of decreased nerve displacement as an additional discriminatory characteristic in dynamic US diagnosis of CTS. In addition, the wide availability of the US equipment utilised in this study further support the use of this modality for dynamic US CTS diagnosis, which could potentially increase the accuracy of CTS diagnosis.
SOURCE OF FUNDING
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The project was not funded by any external funding source.
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