Original Article
Sonoelastographic Findings of Carpal Tunnel Injection Sonoelastografische Befunde nach Karpaltunnel Injektion
Authors
A. S. Klauser1, H. Miyamoto2, C. Martinoli3, A. S. Tagliafico4, J. Szantkay5, G. Feuchtner1, W. Jaschke1
Affiliations
1
3 4 5
The Department of Diagnostic Radiology, Medical University Innsbruck, Austria Orthopaedic Surgery, The University of Tokyo, TOKYO, Japan Department of Radiology R, University of Genoa, Genova, Italy Department of Experimental Medicine, University of Genoa, Genova Radiation Therapy, Medical University Innsbruck, Austria
Key words
Abstract
Zusammenfassung
"
!
!
Purpose: The objectives of this study were to compare sonoelastographic color findings of the perineural area between carpal tunnel syndrome patients and healthy volunteers, and to analyze elastographic findings in that area before and immediately after intracarpal tunnel injection in carpal tunnel syndrome patients. Materials and Methods: We studied both hands of 15 healthy volunteers (7 men, 8 women; mean age: 60.1 years, range: 41 – 88 years) and 72 hands from 70 patients with symptomatic carpal tunnel syndrome (24 men, 46 women; mean age: 54.2 years, range: 24 – 83 years). Sonoelastographic color distribution was assessed in the perineural area between the median nerve and adjacent flexor tendons. The color elastograms were graded using the following system: Grade 1 as red (softest), grade 2 as yellow (soft), grade 3 as green (hard), grade 4 as blue (hardest). The patients were treated with corticosteroid injection and were reassessed with sonoelastography immediately after the injection. Results: The median color grading in the perineural area of carpal tunnel syndrome patients was grade 3 (3.1 ± 0.3, mean ± 95 % Cl), which was stiffer than that of healthy volunteers (grade 1, 1.9 ± 0.4) (p < 0.0001). Immediately after injection, the diffusion of the injected fluid was observed as having a softer appearance (grade 1, 1.4 ± 0.2) (p < 0.0001). Conclusion: The perineural area surrounding the median nerve in carpal tunnel syndrome patients was stiffer than that in healthy volunteers. Diffusion of the injected fluid in the carpal tunnel was seen as a softer finding after injection in real time using sonoelastography.
Ziel: Das Ziel der Studie ist ein Vergleich von sonoelastografischen Befunden des perineuralen Gewebes in Patienten mit Karpaltunnel Syndrom und Normalprobanden, und weiter die Analyse sonoelastografischer Veränderungen unmittelbar nach Infiltration des Karpaltunnels. Material und Methoden: Es wurden beide Hände von 15 Normalprobanden (sieben Männer, acht Frauen; im Mittel 60,1 Jahre, im Alter von 41 – 88) und 72 Hände von 70 Patienten mit Karpaltunnel Syndrom (24 Männer, 46 Frauen; im Mittel 54,2 Jahre, im Alter von 24 – 83) mittels Sonoelastografie untersucht. Das perineurale Gewebe zwischen Nervus medianus und Fingerflexorensehnen wurde folgend beurteilt; Grad 1 als rot (weich), Grad 2 als gelb (mittelweich), Grad 3 als grün (mittelhart), Grad 4 als blau (hart). Die Patienten wurden sonografisch gezielt mit Korikosteroid infiltriert und infolge darauf unmittelbar wieder mittels Sonoelastografie untersucht. Ergebnisse: Das Grading mittels Sonoelastografie in Patienten mit Karpaltunnel Syndrom ergab 3; 3,1 ± 0,3 (medianer Mittelwert ± 95 % Cl), deutlich härter als das der Normalprobanden (Grad 1; 1,9 ± 0,4) (p < 0,0001). Unmittelbar nach Infiltration zeigte sich eine Verteilung der infiltrierten Medikamentation, was zu einem deutlich weicherem Erscheinungsbild führte (Grad 1; 1,4 ± 0,2) (p < 0,0001). Schlussfolgerung: Das perineurale Gewebe um den Nervus medianus zeigte sich deutlich härter in Patienten mit Karpaltunnel Syndrom als in Normalprobanden. Nach Infiltration zeigte sich eine weichere Darstellung des Karpaltunnels in der sonoelastografischen Untersuchung.
● sonoelastography ● carpal tunnel syndrome ● steroid injection ● ultrasound ● nervous-peripheral ● hand " " " " "
received accepted
3.12.2013 13.11.2014
Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1385836 Published online: 2015 Ultraschall in Med © Georg Thieme Verlag KG Stuttgart · New York · ISSN 0172-4614 Correspondence Dr. Hideaki Miyamoto Orthopaedic Surgery, The University of Tokyo 7-3-1, Hongo, Bunkyo-ku, Tokyo 113–8655, JAPAN 113–8655 TOKYO Japan Tel.: ++ 81/3/38 15 54 11 Fax: ++ 81/3/38 15 54 11 [email protected]
Klauser AS et al. Sonoelastographic Findings of … Ultraschall in Med
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2
Original Article
Introduction !
Materials and Methods !
This study was conducted with the approval of the Institutional Review Boards of our institution, and all participants provided oral and written informed consent. SEL examination was performed with a 5 – 18 MHz linear-array transducer (HI VISION Preirus, Hitachi Aloka Medical, Ltd, Tokyo). The subjects were asked to sit in front of an examination table with the elbow at 90˚ of flexion and the hand in supination. Fingers were relaxed with slight flexion of the wrist during the measurement. The proximal inlet of the carpal tunnel at the scaphoid-pisiform bone level was scanned on an axial plane when using SEL, exactly where the injection was performed under B-mode US guidance. We assessed the color distribution of the perineural area surrounded by the transverse carpal ligament " Fig. 1). and adjacent flexor tendons using SEL (● The elastograms were constructed using the same optimal settings throughout the study, as previously described by Havre et al. [15]. The elastogram is presented in color coding superimposed on a B-mode image in a dual screen setting side by side with the B-mode image. The rate of transducer movement when studying parameters was 100 cycles/min. The amplitude was not measured, but strain in the ROI was approximately in the range of 0.1 % to 2 % [15]. The color code indicated the relative stiffness of the tissues within the ROI and ranged from red (soft) to blue (hard). Green and yellow indicated medium elasticity. The strain indicator on the lateral part of the screen was expressed and indicated whether the displacement was sufficient to obtain adequate strain within the ROI. The probe was held perpendicular to the palm with appropriate pressure to avoid shifting of the elastogram referring to the strain indicator. We selected the ROI including the whole intracarpal tunnel with subcutaneous layer and carpal bone surfaces. For each examination, SEL was performed in both the transverse
Klauser AS et al. Sonoelastographic Findings of … Ultraschall in Med
Fig. 1 Axial conventional B-mode ultrasound image at the proximal inlet of the carpal tunnel. We evaluated sonoelastographic color distribution in the perineural area surrounding the median nerve (dotted area except for nerve). FCR = flexor carpi radialis, S = scaphoid bone, U = ulnar artery, P = pisiform bone, T = flexor digitorum tendon. Abb. 1 Axiales konventionelles B-Bild am proximalen Eingang des Karpaltunnels. Wir beurteilten die sonoelastografische Farbverteilung im perineuralen Bereich um den Nervus medianus (gepunkteter Bereich ohne Nerv). FCR = Flexor carpi radialis, S = Os scaphoideum, U = A. ulnaris, P = Os pisiforme, T = Flexor digitorum, Tendo.
and longitudinal planes. At least three compression-relaxation cycles were applied until reproducible findings were confirmed on both the longitudinal and transverse planes. The images were stored as cine-loops in the memory of the ultrasound system. Representative SEL images were chosen from the middle of each compression-decompression cycle. The color elastograms of the perineural area in the carpal tunnel were graded using the following system: grade 1 (softest), red coloring in the perineural area; grade 2 (soft), mainly yellow; grade 3 (hard), mainly green; " Fig. 2). grade 4 (hardest), mainly blue (● As a preliminary examination, we investigated the reproducibility of SEL color grading in the perineural area by interobserver agreement. The participants consisted of 14 hands of 11 healthy subjects (4 men, 7 women; mean age: 56.5 years, range: 49 – 80 years) and 12 hands of 10 CTS patients (2 men, 8 women; mean age: 53.1 years, range: 42 – 74 years). Two independent raters conducted this preliminary study. Rater A was a musculoskeletal radiologist with four years of experience in SEL. Rater B was trained in the musculoskeletal SEL for two years of experience. Both rater A and rater B were blinded to the medical history of subjects and also blinded to the SEL findings made by the other rater, and assessed the recorded SEL images after the examination. We obtained data of the control group and patient group. The control group consisted of both hands of 15 healthy volunteers (7 men, 8 women; mean age: 60.1 years, range: 41 – 88 years). Exclusion criteria comprised the presence of scar tissue in the wrist from prior trauma or surgery, joint disorders such as rheumatoid arthritis, a bifidus median nerve, or CTS symptoms. The patient group consisted of 72 hands from 70 patients with symptomatic CTS (24 men, 46 women; mean age: 54.2 years, range: 24 – 83 years). The diagnosis of CTS was confirmed when both electrodiagnostic testing was positive and an increased cross-sectional area of the median nerve in B-mode US was present (> 11 mm2) [16] besides CTS symptoms. The exclusion criteria for the patient group comprised the presence of scarring in the wrist from prior trauma or surgery, joint disorders such as rheumatoid arthritis, or a bifidus median nerve. Pa-
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Carpal Tunnel Syndrome (CTS) is a compression neuropathy of the median nerve at the level of the wrist. The prevalence of CTS has been estimated to be 50 cases per 1000 subjects per year [1]. The main symptoms of CTS include numbness and tingling in the area of the median nerve distribution and weakness of the thumb opposition. Local corticosteroid injection has shown verified clinical improvement in symptoms for nonsurgical treatment of CTS [2]. One of the causes of CTS is believed to be pathological fibrosis and thickening of the subsynovial connective tissue (SSCT) that connects the flexor tendons to the median nerve [3]. Ultrasound (US) is widely utilized as a first-line approach for the evaluation of the carpal tunnel contents because of the advantages of real-time assessment [4, 5] and consecutive US-guided injections [6]. Sonoelastography (SEL) is a recently developed modality that can assess the elasticity of soft tissue with a color distribution elastogram via US imaging. SEL has already provided characteristic findings in musculoskeletal disorders [7, 8] including the Achilles tendon [9], lateral epicondylitis [10], and carpal tunnel syndrome [11 – 14]. The objectives of this study were to compare sonoelastographic color findings of the perineural area surrounding the median nerve between CTS patients and healthy volunteers, and to analyze findings in that area before and immediately after intracarpal tunnel injection using SEL.
Original Article
Fig. 2 Clinical examples of the color grading system of the perineural area surrounding the median nerve. a Schematic presentation of the axial image (TCL: transverse carpal ligament, MN: median nerve, FT: flexor tendon). Abb. 2 Klinische Beispiele des Farbgraduierungssystems im perineuralen Bereich um den Nervus medianus. a Schematische Darstellung des axialen Bildes (TCL: Retinaculum flexorum, MN: Nervus medianus; FT: Flexorensehne).
Demographic data for healthy volunteers and CTS patients.
characteristics
healthy
CTS patients
Results !
p-value
Preliminary concordance for the SEL grading system of the perineural area
volunteers 54.2 ± 14.1
0.17
females/ all participants (%)
8/15 (53 %)
46/70 (66 %)
0.39
dominant hands/ all hands
15/30 (50 %)
42/72 (46 %)
0.51
Interobserver agreement for the SEL grading of the perineural area between rater A and B was good with a weighted Kappa value of 0.69 ± 0.3 (mean ± 95 %Cl) (p = 0.012) in healthy volunteers and 0.65 ± 0.3 (p = 0.026) in CTS patients.
Values are presented as mean ± SD or number (%). CTS = carpal tunnel syndrome
SEL findings of the perineural area in healthy volunteers
mean age ± SD (years)
60.1 ± 13.2
tients who had a history of steroid injection into the carpal tun" Table 1 nel within 6 months of the study were also excluded. ● shows the baseline characteristics of the control subjects and CTS patients included in this study. In the case of CTS patients, a solution consisting of a mixture of 30 mg (3 ml) of triamcinolone acetonide and 0.5 ml of 2 % mepivacaine (total fluid amount: 3.5 ml) was injected into the adjacent space surrounding the median nerve under B-mode US guidance. The needle was advanced from the ulnar side close to the median nerve into the carpal tunnel, and then the solution was injected. The SEL re-examination was performed immediately after the injection. All therapeutic injections and SEL examinations were performed by a senior radiologist with ten years of experience in musculoskeletal ultrasound. The recorded pre- and post-injection SEL images in this advanced examination were evaluated by rater A, who was blinded to the diagnosis.
Statistical analysis The concordance of SEL grading compared between the two raters was assessed using the weighted Kappa analysis for the preliminary examination. We used the Mann-Whitney U test and Fisher’s exact test to compare demographic data between healthy volunteers and CTS patients. The Wilcoxon t-test was used for the comparison of the color grading before and after the corticosteroid injection in CTS patients. Values of p < 0.05 were considered significant.
In healthy volunteers, the median color grading of the perineural area was grade 1 (1.9 ± 0.6, mean ± 95 %Cl) and grade 1 (1.9 ± 0.6) for men and women, respectively. The median color grading of the perineural area was grade 2 (2.1 ± 0.6) and grade 1 (1.7 ± 0.6) for dominant and non-dominant hands, respectively. There was no significant difference in either gender (p = 0.56) or dominant side (p = 0.36). A representative SEL image of a healthy volunteer " Fig. 3. is shown in ●
SEL findings of the perineural area in CTS patients The median color grading of the perineural area in the CTS patients was grade 3 (3.1 ± 0.3), which was significantly higher than that of the healthy volunteers (grade 1, 1.9 ± 0.4) (p < 0.0001). After corticosteroid injection patients were re-examined immediately, and the median color grading of the perineural area had decreased to grade 1 (1.4 ± 0.2) (p < 0.0001). Representative SEL images of a CTS " Fig. 4. SEL findings of the adjacent nerve patient are shown in ● area in healthy volunteers and CTS patients are summarized in ●" Table 2.
Discussion !
Using elastographic color grading assessment, the reported interobserver variability was good or excellent with a Kappa value of 0.64 – 0.82 in clinical practices [17 – 19]. Our preliminarily examination showed good inter-observer variability with a Kappa value of 0.69 in healthy volunteers and 0.65 in CTS patients. Several authors have reported that the median nerve in CTS patients was stiffer than that in healthy volunteers [11, 12], and that the stiffness of the transverse carpal ligament and intracarpal tunnel contents surrounding the median nerve contributed to CTS symptoms [13, 14]. Our results demonstrated a significantly
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Table 1
Fig. 3 52-year-old healthy female volunteer. a Axial conventional B-mode ultrasound image at the proximal inlet of the carpal tunnel. FCR = flexor carpi radialis, S = scaphoid bone, U = ulnar artery, P = pisiform bone, T = flexor digitorum tendon. b Sonoelastography image at the same level. The main color distribution in the perineural area showed red, assessed as grade 1. Abb. 3 52-jährige gesunde Probandin. a Axiales konventionelles B-Bild am proximalen Eingang des Karpaltunnels. FCR = Flexor carpi radialis, S = Os scaphoideum, U = A. ulnaris, P = Os pisiforme, T = Flexor digitorum, Tendo. b Sonoelastografie-Bild auf gleicher Höhe. Die Hauptfarbgebung im perineuralen Bereich war rot, beurteilt als Grad 1.
increased stiffness of the perineural area in CTS patients when compared to healthy volunteers. Anatomically, the perineural area between the median nerve and adjacent flexor tendons consists of SSCT [3]. SSCT in CTS patients included increased collagen density and fiber size, vascular sclerosis, and fibrosis when compared with that in healthy controls [20, 21]. Our results may reflect these morphological changes of the area surrounding the median nerve by showing a stiffer SEL appearance compared to healthy volunteers. The diffusion of the injected fluid was depicted as an obviously softer SEL appearance around the median nerve. SSCT is thought to be responsible for the median nerve tethering, leading to a disturbance of the epineural blood flow [22]. Besides the primary effect of locally injected corticosteroid in altering the action of cytokines and pain [23], the injected solution might peel adhesion between the median nerve and surrounding soft tissues to improve the ischemic condition mechanically. This study has several limitations. Some SEL methods can assess soft tissue elasticity as absolute values (e. g., estimated Young´s modulus, semi-quantitative values of strain ratio) instead of the qualitative color grading analysis that we used. However, the examined area was too small and irregular to place ROIs for strain ratio calculation, and therefore we used the subjective color grading analysis. We did not investigate the long-term effect of the corticosteroid injection on the stiffness in the carpal tunnel with longterm follow-up.
Klauser AS et al. Sonoelastographic Findings of … Ultraschall in Med
Fig. 4 56-year-old female with carpal tunnel syndrome. a Axial conventional B-mode ultrasound image at the proximal inlet of the carpal tunnel. FCR = flexor carpi radialis, S = scaphoid bone, U = ulnar artery, P = pisiform bone, T = flexor digitorum tendon. b Sonoelastography image at the same level. The main color distribution in the perineural area was green, assessed as grade 3. c Sonoelastography image immediately after ultrasoundguided injection. The main color distribution of the injected fluid was red (stars) showing pronounced softening around the median nerve, assessed as grade 1. Abb. 4 56-jährige Frau mit Karpaltunnelsyndrom. a Axiales konventionelles B-Bild am proximalen Eingang des Karpaltunnels. FCR = Flexor carpi radialis, S = Os scaphoideum, U = A. ulnaris, P = Os pisiforme, T = Flexor digitorum, Tendo. b Sonoelastografisches Bild auf gleicher Höhe. Die Hauptfarbgebung im perineuralen Bereich war grün, beurteilt als Grad 3. c Sonoelastografisches Bild unmittelbar nach US-gestützter Injektion. Die Hauptfarbgebung der injizierten Flüssigkeit war rot (Sterne) und zeigte ein Weicherwerden um den Nervus medianus, beurteilt als Grad 1.
We concluded that the perineural area surrounding the median nerve in CTS patients was stiffer than that in healthy volunteers. We were able to assess the diffusion of the injected fluid in the carpal tunnel with softer findings after injection in real time using SEL.
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Original Article
Original Article
Table 2
Color grading of the perineural area.
healthy hands (n = 30)
CTS hands (n = 72)
CTS hands after injection (n = 72)
median
mean ± 95 %Cl
median
mean ± 95 %Cl
p-value1
median
mean ± 95 %Cl
p-value2
grade 1
1.9 ± 0.4
grade 3
3.1 ± 0.3
< 0.0001
grade 1
1.4 ± 0.2
< 0.0001
distribution grade 4 blue (hardest)
2 (6.7 %)
35 (49 %)
2 (2.7 %)
grade 3 green (hard)
9 (30 %)
20 (28 %)
9 (13 %)
grade 2 yellow (soft)
2 (6.7 %)
5 (6.9 %)
2 (2.7 %)
grade 1 red (softest)
17 (57 %)
12 (17 %)
59 (82 %)
References 01 Keith MW, Masear V, Chung KC et al. American Academy of Orthopaedic Surgeons Clinical Practice Guideline on diagnosis of carpal tunnel syndrome. J Bone Joint Surg Am 2009; 91: 2478 – 2479 02 Marshall S, Tardif G, Ashworth N. Local corticosteroid injection for carpal tunnel syndrome. Cochrane Database Syst Rev 2007; 18: CD001554 03 Ettema AM, Amadio PC, Zhao C et al. A histological and immunohistochemical study of the subsynovial connective tissue in idiopathic carpal tunnel syndrome. J Bone Joint Surg Am 2004; 86: 1458 – 1466 04 Klauser AS, Tagliafico A, Allen GM et al. Clinical indications for musculoskeletal ultrasound: a Delphi-based consensus paper of the European Society of Musculoskeletal Radiology. Eur Radiol 2012; 22: 1140 – 1148 05 Girtler MT, Krasinski A, Dejaco C et al. Feasibility of 3D ultrasound to evaluate upper extremity nerves. Ultraschall in Med 2013; 34: 382 – 387 06 Grassi W, Farina A, Filippucci E et al. Intralesional therapy in carpal tunnel syndrome: a sonographic-guided approach. Clin Exp Rheumatol 2002; 20: 73 – 76 07 Cosgrove D, Piscaglia F, Bamber J et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall in Med 2013; 34: 238 – 253 08 Bamber J, Cosgrove D, Dietrich CF et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall in Med 2013; 34: 169 – 184 09 Klauser AS, Miyamoto H, Tamegger M et al. Achilles Tendon Assessed with Sonoelastography: Histologic Agreement. Radiology 2013; 267: 837 – 842 10 De Zordo T, Lill SR, Fink C et al. Real-time sonoelastography of lateral epicondylitis: comparison of findings between patients and healthy volunteers. Am J Roentgenol Am J Roentgenol 2009; 193: 180 – 185 11 Orman G, Ozben S, Huseyinoglu N et al. Ultrasound elastographic evaluation in the diagnosis of carpal tunnel syndrome: initial findings. Ultrasound Med Biol 2013; 39: 1184 – 1189
12 Miyamoto H, Halpern EJ, Kastlunger M et al. Carpal tunnel syndrome: diagnosis by means of median nerve elasticity–improved diagnostic accuracy of US with sonoelastography. Radiology 2014; 270: 481 – 486 13 Miyamoto H, Miura T, Morizaki Y et al. Comparative Study on the of Transverse Carpal Ligament between Normal Subjects and Carpal Tunnel Syndrome Patients. Hand Surg 2013; 18: 209 – 214 14 Miyamoto H, Siedentopf C, Kastlunger M et al. Intracarpal tunnel contents: evaluation of the effects of corticosteroid injection with sonoelastography. Radiology 2014; 270: 809 – 815 15 Havre RF, Elde E, Gilja OH et al. Freehand real-time elastography: impact of scanning parameters on image quality and in vitro intra- and interobserver validations. Ultrasound Med Biol 2008; 34: 1638 – 1650 16 Klauser AS, Halpern EJ, De Zordo T et al. Carpal tunnel syndrome assessment with US: value of additional cross-sectional area measurements of the median nerve in patients versus healthy volunteers. Radiology 2009; 250: 171 – 177 17 Merino S, Arrazola J, Cárdenas A et al. Utility and interobserver agreement of ultrasound elastography in the detection of malignant thyroid nodules in clinical care. AJNR Am J Neuroradiol 2011; 32: 2142 – 2148 18 Ragazzoni F, Deandrea M, Mormile A et al. High diagnostic accuracy and interobserver reliability of real-time elastography in the evaluation of thyroid nodules. Ultrasound Med Biol 2012; 38: 1154 – 1162 19 Thomas A, Fischer T, Frey H et al. Real-time elastography–an advanced method of ultrasound: First results in 108 patients with breast lesions. Ultrasound Obstet Gynecol 2006; 28: 335 – 340 20 Jinrok O, Zhao C, Amadio PC et al. Vascular pathologic changes in the flexor tenosynovium (subsynovial connective tissue) in idiopathic carpal tunnel syndrome. J Orthop Res 2004; 22: 1310 – 1315 21 Oh J, Zhao C, Zobitz ME et al. Morphological changes of collagen fibrils in the subsynovial connective tissue in carpal tunnel syndrome. J Bone Joint Surg Am 2006; 88: 824 – 831 22 Vanhees M, Morizaki Y, Thoreson AR et al. The effect of displacement on the mechanical properties of human cadaver subsynovial connective tissue. J Orthop Res 2012; 30: 1732 – 1737 23 Dahl J, Hammert WC. Overview of injectable corticosteroids. J Hand Surg Am 2012; 37: 1715 – 1717
Klauser AS et al. Sonoelastographic Findings of … Ultraschall in Med
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CTS = carpal tunnel syndrome. Grade 1: red (softest), grade 2: yellow (soft tissue), grade 3: green (hard tissue), grade 4: blue (hardest tissue). Values are presented as numbers (%). 1 Difference of the color grading between healthy volunteers and CTS patients. 2 Difference of the color grading before and after corticosteroid injection in CTS patients.
Sonoelastographic Findings of Carpal Tunnel Injection Sonoelastografische Befunde nach Karpaltunnel Injektion
Authors
A. S. Klauser1, H. Miyamoto2, C. Martinoli3, A. S. Tagliafico4, J. Szantkay5, G. Feuchtner1, W. Jaschke1
Affiliations
1
3 4 5
The Department of Diagnostic Radiology, Medical University Innsbruck, Austria Orthopaedic Surgery, The University of Tokyo, TOKYO, Japan Department of Radiology R, University of Genoa, Genova, Italy Department of Experimental Medicine, University of Genoa, Genova Radiation Therapy, Medical University Innsbruck, Austria
Key words
Abstract
Zusammenfassung
"
!
!
Purpose: The objectives of this study were to compare sonoelastographic color findings of the perineural area between carpal tunnel syndrome patients and healthy volunteers, and to analyze elastographic findings in that area before and immediately after intracarpal tunnel injection in carpal tunnel syndrome patients. Materials and Methods: We studied both hands of 15 healthy volunteers (7 men, 8 women; mean age: 60.1 years, range: 41 – 88 years) and 72 hands from 70 patients with symptomatic carpal tunnel syndrome (24 men, 46 women; mean age: 54.2 years, range: 24 – 83 years). Sonoelastographic color distribution was assessed in the perineural area between the median nerve and adjacent flexor tendons. The color elastograms were graded using the following system: Grade 1 as red (softest), grade 2 as yellow (soft), grade 3 as green (hard), grade 4 as blue (hardest). The patients were treated with corticosteroid injection and were reassessed with sonoelastography immediately after the injection. Results: The median color grading in the perineural area of carpal tunnel syndrome patients was grade 3 (3.1 ± 0.3, mean ± 95 % Cl), which was stiffer than that of healthy volunteers (grade 1, 1.9 ± 0.4) (p < 0.0001). Immediately after injection, the diffusion of the injected fluid was observed as having a softer appearance (grade 1, 1.4 ± 0.2) (p < 0.0001). Conclusion: The perineural area surrounding the median nerve in carpal tunnel syndrome patients was stiffer than that in healthy volunteers. Diffusion of the injected fluid in the carpal tunnel was seen as a softer finding after injection in real time using sonoelastography.
Ziel: Das Ziel der Studie ist ein Vergleich von sonoelastografischen Befunden des perineuralen Gewebes in Patienten mit Karpaltunnel Syndrom und Normalprobanden, und weiter die Analyse sonoelastografischer Veränderungen unmittelbar nach Infiltration des Karpaltunnels. Material und Methoden: Es wurden beide Hände von 15 Normalprobanden (sieben Männer, acht Frauen; im Mittel 60,1 Jahre, im Alter von 41 – 88) und 72 Hände von 70 Patienten mit Karpaltunnel Syndrom (24 Männer, 46 Frauen; im Mittel 54,2 Jahre, im Alter von 24 – 83) mittels Sonoelastografie untersucht. Das perineurale Gewebe zwischen Nervus medianus und Fingerflexorensehnen wurde folgend beurteilt; Grad 1 als rot (weich), Grad 2 als gelb (mittelweich), Grad 3 als grün (mittelhart), Grad 4 als blau (hart). Die Patienten wurden sonografisch gezielt mit Korikosteroid infiltriert und infolge darauf unmittelbar wieder mittels Sonoelastografie untersucht. Ergebnisse: Das Grading mittels Sonoelastografie in Patienten mit Karpaltunnel Syndrom ergab 3; 3,1 ± 0,3 (medianer Mittelwert ± 95 % Cl), deutlich härter als das der Normalprobanden (Grad 1; 1,9 ± 0,4) (p < 0,0001). Unmittelbar nach Infiltration zeigte sich eine Verteilung der infiltrierten Medikamentation, was zu einem deutlich weicherem Erscheinungsbild führte (Grad 1; 1,4 ± 0,2) (p < 0,0001). Schlussfolgerung: Das perineurale Gewebe um den Nervus medianus zeigte sich deutlich härter in Patienten mit Karpaltunnel Syndrom als in Normalprobanden. Nach Infiltration zeigte sich eine weichere Darstellung des Karpaltunnels in der sonoelastografischen Untersuchung.
● sonoelastography ● carpal tunnel syndrome ● steroid injection ● ultrasound ● nervous-peripheral ● hand " " " " "
received accepted
3.12.2013 13.11.2014
Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1385836 Published online: 2015 Ultraschall in Med © Georg Thieme Verlag KG Stuttgart · New York · ISSN 0172-4614 Correspondence Dr. Hideaki Miyamoto Orthopaedic Surgery, The University of Tokyo 7-3-1, Hongo, Bunkyo-ku, Tokyo 113–8655, JAPAN 113–8655 TOKYO Japan Tel.: ++ 81/3/38 15 54 11 Fax: ++ 81/3/38 15 54 11 [email protected]
Klauser AS et al. Sonoelastographic Findings of … Ultraschall in Med
Downloaded by: Rutgers University. Copyrighted material.
2
Original Article
Introduction !
Materials and Methods !
This study was conducted with the approval of the Institutional Review Boards of our institution, and all participants provided oral and written informed consent. SEL examination was performed with a 5 – 18 MHz linear-array transducer (HI VISION Preirus, Hitachi Aloka Medical, Ltd, Tokyo). The subjects were asked to sit in front of an examination table with the elbow at 90˚ of flexion and the hand in supination. Fingers were relaxed with slight flexion of the wrist during the measurement. The proximal inlet of the carpal tunnel at the scaphoid-pisiform bone level was scanned on an axial plane when using SEL, exactly where the injection was performed under B-mode US guidance. We assessed the color distribution of the perineural area surrounded by the transverse carpal ligament " Fig. 1). and adjacent flexor tendons using SEL (● The elastograms were constructed using the same optimal settings throughout the study, as previously described by Havre et al. [15]. The elastogram is presented in color coding superimposed on a B-mode image in a dual screen setting side by side with the B-mode image. The rate of transducer movement when studying parameters was 100 cycles/min. The amplitude was not measured, but strain in the ROI was approximately in the range of 0.1 % to 2 % [15]. The color code indicated the relative stiffness of the tissues within the ROI and ranged from red (soft) to blue (hard). Green and yellow indicated medium elasticity. The strain indicator on the lateral part of the screen was expressed and indicated whether the displacement was sufficient to obtain adequate strain within the ROI. The probe was held perpendicular to the palm with appropriate pressure to avoid shifting of the elastogram referring to the strain indicator. We selected the ROI including the whole intracarpal tunnel with subcutaneous layer and carpal bone surfaces. For each examination, SEL was performed in both the transverse
Klauser AS et al. Sonoelastographic Findings of … Ultraschall in Med
Fig. 1 Axial conventional B-mode ultrasound image at the proximal inlet of the carpal tunnel. We evaluated sonoelastographic color distribution in the perineural area surrounding the median nerve (dotted area except for nerve). FCR = flexor carpi radialis, S = scaphoid bone, U = ulnar artery, P = pisiform bone, T = flexor digitorum tendon. Abb. 1 Axiales konventionelles B-Bild am proximalen Eingang des Karpaltunnels. Wir beurteilten die sonoelastografische Farbverteilung im perineuralen Bereich um den Nervus medianus (gepunkteter Bereich ohne Nerv). FCR = Flexor carpi radialis, S = Os scaphoideum, U = A. ulnaris, P = Os pisiforme, T = Flexor digitorum, Tendo.
and longitudinal planes. At least three compression-relaxation cycles were applied until reproducible findings were confirmed on both the longitudinal and transverse planes. The images were stored as cine-loops in the memory of the ultrasound system. Representative SEL images were chosen from the middle of each compression-decompression cycle. The color elastograms of the perineural area in the carpal tunnel were graded using the following system: grade 1 (softest), red coloring in the perineural area; grade 2 (soft), mainly yellow; grade 3 (hard), mainly green; " Fig. 2). grade 4 (hardest), mainly blue (● As a preliminary examination, we investigated the reproducibility of SEL color grading in the perineural area by interobserver agreement. The participants consisted of 14 hands of 11 healthy subjects (4 men, 7 women; mean age: 56.5 years, range: 49 – 80 years) and 12 hands of 10 CTS patients (2 men, 8 women; mean age: 53.1 years, range: 42 – 74 years). Two independent raters conducted this preliminary study. Rater A was a musculoskeletal radiologist with four years of experience in SEL. Rater B was trained in the musculoskeletal SEL for two years of experience. Both rater A and rater B were blinded to the medical history of subjects and also blinded to the SEL findings made by the other rater, and assessed the recorded SEL images after the examination. We obtained data of the control group and patient group. The control group consisted of both hands of 15 healthy volunteers (7 men, 8 women; mean age: 60.1 years, range: 41 – 88 years). Exclusion criteria comprised the presence of scar tissue in the wrist from prior trauma or surgery, joint disorders such as rheumatoid arthritis, a bifidus median nerve, or CTS symptoms. The patient group consisted of 72 hands from 70 patients with symptomatic CTS (24 men, 46 women; mean age: 54.2 years, range: 24 – 83 years). The diagnosis of CTS was confirmed when both electrodiagnostic testing was positive and an increased cross-sectional area of the median nerve in B-mode US was present (> 11 mm2) [16] besides CTS symptoms. The exclusion criteria for the patient group comprised the presence of scarring in the wrist from prior trauma or surgery, joint disorders such as rheumatoid arthritis, or a bifidus median nerve. Pa-
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Carpal Tunnel Syndrome (CTS) is a compression neuropathy of the median nerve at the level of the wrist. The prevalence of CTS has been estimated to be 50 cases per 1000 subjects per year [1]. The main symptoms of CTS include numbness and tingling in the area of the median nerve distribution and weakness of the thumb opposition. Local corticosteroid injection has shown verified clinical improvement in symptoms for nonsurgical treatment of CTS [2]. One of the causes of CTS is believed to be pathological fibrosis and thickening of the subsynovial connective tissue (SSCT) that connects the flexor tendons to the median nerve [3]. Ultrasound (US) is widely utilized as a first-line approach for the evaluation of the carpal tunnel contents because of the advantages of real-time assessment [4, 5] and consecutive US-guided injections [6]. Sonoelastography (SEL) is a recently developed modality that can assess the elasticity of soft tissue with a color distribution elastogram via US imaging. SEL has already provided characteristic findings in musculoskeletal disorders [7, 8] including the Achilles tendon [9], lateral epicondylitis [10], and carpal tunnel syndrome [11 – 14]. The objectives of this study were to compare sonoelastographic color findings of the perineural area surrounding the median nerve between CTS patients and healthy volunteers, and to analyze findings in that area before and immediately after intracarpal tunnel injection using SEL.
Original Article
Fig. 2 Clinical examples of the color grading system of the perineural area surrounding the median nerve. a Schematic presentation of the axial image (TCL: transverse carpal ligament, MN: median nerve, FT: flexor tendon). Abb. 2 Klinische Beispiele des Farbgraduierungssystems im perineuralen Bereich um den Nervus medianus. a Schematische Darstellung des axialen Bildes (TCL: Retinaculum flexorum, MN: Nervus medianus; FT: Flexorensehne).
Demographic data for healthy volunteers and CTS patients.
characteristics
healthy
CTS patients
Results !
p-value
Preliminary concordance for the SEL grading system of the perineural area
volunteers 54.2 ± 14.1
0.17
females/ all participants (%)
8/15 (53 %)
46/70 (66 %)
0.39
dominant hands/ all hands
15/30 (50 %)
42/72 (46 %)
0.51
Interobserver agreement for the SEL grading of the perineural area between rater A and B was good with a weighted Kappa value of 0.69 ± 0.3 (mean ± 95 %Cl) (p = 0.012) in healthy volunteers and 0.65 ± 0.3 (p = 0.026) in CTS patients.
Values are presented as mean ± SD or number (%). CTS = carpal tunnel syndrome
SEL findings of the perineural area in healthy volunteers
mean age ± SD (years)
60.1 ± 13.2
tients who had a history of steroid injection into the carpal tun" Table 1 nel within 6 months of the study were also excluded. ● shows the baseline characteristics of the control subjects and CTS patients included in this study. In the case of CTS patients, a solution consisting of a mixture of 30 mg (3 ml) of triamcinolone acetonide and 0.5 ml of 2 % mepivacaine (total fluid amount: 3.5 ml) was injected into the adjacent space surrounding the median nerve under B-mode US guidance. The needle was advanced from the ulnar side close to the median nerve into the carpal tunnel, and then the solution was injected. The SEL re-examination was performed immediately after the injection. All therapeutic injections and SEL examinations were performed by a senior radiologist with ten years of experience in musculoskeletal ultrasound. The recorded pre- and post-injection SEL images in this advanced examination were evaluated by rater A, who was blinded to the diagnosis.
Statistical analysis The concordance of SEL grading compared between the two raters was assessed using the weighted Kappa analysis for the preliminary examination. We used the Mann-Whitney U test and Fisher’s exact test to compare demographic data between healthy volunteers and CTS patients. The Wilcoxon t-test was used for the comparison of the color grading before and after the corticosteroid injection in CTS patients. Values of p < 0.05 were considered significant.
In healthy volunteers, the median color grading of the perineural area was grade 1 (1.9 ± 0.6, mean ± 95 %Cl) and grade 1 (1.9 ± 0.6) for men and women, respectively. The median color grading of the perineural area was grade 2 (2.1 ± 0.6) and grade 1 (1.7 ± 0.6) for dominant and non-dominant hands, respectively. There was no significant difference in either gender (p = 0.56) or dominant side (p = 0.36). A representative SEL image of a healthy volunteer " Fig. 3. is shown in ●
SEL findings of the perineural area in CTS patients The median color grading of the perineural area in the CTS patients was grade 3 (3.1 ± 0.3), which was significantly higher than that of the healthy volunteers (grade 1, 1.9 ± 0.4) (p < 0.0001). After corticosteroid injection patients were re-examined immediately, and the median color grading of the perineural area had decreased to grade 1 (1.4 ± 0.2) (p < 0.0001). Representative SEL images of a CTS " Fig. 4. SEL findings of the adjacent nerve patient are shown in ● area in healthy volunteers and CTS patients are summarized in ●" Table 2.
Discussion !
Using elastographic color grading assessment, the reported interobserver variability was good or excellent with a Kappa value of 0.64 – 0.82 in clinical practices [17 – 19]. Our preliminarily examination showed good inter-observer variability with a Kappa value of 0.69 in healthy volunteers and 0.65 in CTS patients. Several authors have reported that the median nerve in CTS patients was stiffer than that in healthy volunteers [11, 12], and that the stiffness of the transverse carpal ligament and intracarpal tunnel contents surrounding the median nerve contributed to CTS symptoms [13, 14]. Our results demonstrated a significantly
Klauser AS et al. Sonoelastographic Findings of … Ultraschall in Med
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Table 1
Fig. 3 52-year-old healthy female volunteer. a Axial conventional B-mode ultrasound image at the proximal inlet of the carpal tunnel. FCR = flexor carpi radialis, S = scaphoid bone, U = ulnar artery, P = pisiform bone, T = flexor digitorum tendon. b Sonoelastography image at the same level. The main color distribution in the perineural area showed red, assessed as grade 1. Abb. 3 52-jährige gesunde Probandin. a Axiales konventionelles B-Bild am proximalen Eingang des Karpaltunnels. FCR = Flexor carpi radialis, S = Os scaphoideum, U = A. ulnaris, P = Os pisiforme, T = Flexor digitorum, Tendo. b Sonoelastografie-Bild auf gleicher Höhe. Die Hauptfarbgebung im perineuralen Bereich war rot, beurteilt als Grad 1.
increased stiffness of the perineural area in CTS patients when compared to healthy volunteers. Anatomically, the perineural area between the median nerve and adjacent flexor tendons consists of SSCT [3]. SSCT in CTS patients included increased collagen density and fiber size, vascular sclerosis, and fibrosis when compared with that in healthy controls [20, 21]. Our results may reflect these morphological changes of the area surrounding the median nerve by showing a stiffer SEL appearance compared to healthy volunteers. The diffusion of the injected fluid was depicted as an obviously softer SEL appearance around the median nerve. SSCT is thought to be responsible for the median nerve tethering, leading to a disturbance of the epineural blood flow [22]. Besides the primary effect of locally injected corticosteroid in altering the action of cytokines and pain [23], the injected solution might peel adhesion between the median nerve and surrounding soft tissues to improve the ischemic condition mechanically. This study has several limitations. Some SEL methods can assess soft tissue elasticity as absolute values (e. g., estimated Young´s modulus, semi-quantitative values of strain ratio) instead of the qualitative color grading analysis that we used. However, the examined area was too small and irregular to place ROIs for strain ratio calculation, and therefore we used the subjective color grading analysis. We did not investigate the long-term effect of the corticosteroid injection on the stiffness in the carpal tunnel with longterm follow-up.
Klauser AS et al. Sonoelastographic Findings of … Ultraschall in Med
Fig. 4 56-year-old female with carpal tunnel syndrome. a Axial conventional B-mode ultrasound image at the proximal inlet of the carpal tunnel. FCR = flexor carpi radialis, S = scaphoid bone, U = ulnar artery, P = pisiform bone, T = flexor digitorum tendon. b Sonoelastography image at the same level. The main color distribution in the perineural area was green, assessed as grade 3. c Sonoelastography image immediately after ultrasoundguided injection. The main color distribution of the injected fluid was red (stars) showing pronounced softening around the median nerve, assessed as grade 1. Abb. 4 56-jährige Frau mit Karpaltunnelsyndrom. a Axiales konventionelles B-Bild am proximalen Eingang des Karpaltunnels. FCR = Flexor carpi radialis, S = Os scaphoideum, U = A. ulnaris, P = Os pisiforme, T = Flexor digitorum, Tendo. b Sonoelastografisches Bild auf gleicher Höhe. Die Hauptfarbgebung im perineuralen Bereich war grün, beurteilt als Grad 3. c Sonoelastografisches Bild unmittelbar nach US-gestützter Injektion. Die Hauptfarbgebung der injizierten Flüssigkeit war rot (Sterne) und zeigte ein Weicherwerden um den Nervus medianus, beurteilt als Grad 1.
We concluded that the perineural area surrounding the median nerve in CTS patients was stiffer than that in healthy volunteers. We were able to assess the diffusion of the injected fluid in the carpal tunnel with softer findings after injection in real time using SEL.
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Original Article
Original Article
Table 2
Color grading of the perineural area.
healthy hands (n = 30)
CTS hands (n = 72)
CTS hands after injection (n = 72)
median
mean ± 95 %Cl
median
mean ± 95 %Cl
p-value1
median
mean ± 95 %Cl
p-value2
grade 1
1.9 ± 0.4
grade 3
3.1 ± 0.3
< 0.0001
grade 1
1.4 ± 0.2
< 0.0001
distribution grade 4 blue (hardest)
2 (6.7 %)
35 (49 %)
2 (2.7 %)
grade 3 green (hard)
9 (30 %)
20 (28 %)
9 (13 %)
grade 2 yellow (soft)
2 (6.7 %)
5 (6.9 %)
2 (2.7 %)
grade 1 red (softest)
17 (57 %)
12 (17 %)
59 (82 %)
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CTS = carpal tunnel syndrome. Grade 1: red (softest), grade 2: yellow (soft tissue), grade 3: green (hard tissue), grade 4: blue (hardest tissue). Values are presented as numbers (%). 1 Difference of the color grading between healthy volunteers and CTS patients. 2 Difference of the color grading before and after corticosteroid injection in CTS patients.
