Achilles Tendon Assessed with Sonoelastography: Histologic Agreement 1

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Purpose:

To compare and determine the level of agreement of findings at conventional B-mode ultrasonography (US) and sonoelastography of the Achilles tendon with findings at histologic assessment.

Materials and Methods:

This study was conducted with the approval of the institutional review boards, and all cadavers were in legal custody of the study institution. Thirteen Achilles tendons in 10 cadavers (four male, six female; age range, 70–90 years) were examined with B-mode US and sonoelastography. B-mode US grading was as follows: Grade 1 indicated a normal-appearing tendon with homogeneous fibrillar echotexture; grade 2, a focal fusiform or diffuse enlarged tendon; and grade 3, a hypoechoic area with or without tendon enlargement. Sonoelastography grading was as follows: Grade 1 indicated blue (hardest) to green (hard); grade 2, yellow (soft); and grade 3, red (softest). Twenty-five biopsy specimens from representative lesions of the middle and distal thirds of the Achilles tendons were evaluated histologically. The concordance of B-mode US grading compared with sonoelastographic grading was assessed by using k analysis.

Results:

With B-mode US and sonoelastography, all 11 tendon thirds of histologically normal tendons were verified as normal (grade 1). Sonoelastography depicted 14 of 14 (100%) tendon thirds with histologic degeneration (grade 2 or 3), whereas B-mode US could depict only 12 of 14 (86%) lesions (grade 2 or 3). Only moderate agreement between B-mode US and sonoelastography was seen (k = 0.52, P , .001).

Conclusion:

Sonoelastography might help predict signs of histopathologic degeneration of Achilles tendinosis, potentially more sensitively than B-mode US.  RSNA, 2013

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 From the Department of Diagnostic Radiology (A.S.K., M.T., R.F., G.M.F., M.K., W.R.J.), Department of Anatomy, Histology and Embryology–Division of Clinical and Functional Anatomy (B.M.), and Department of Anatomy, Histology and Embryology (G.K.), Medical University Innsbruck, Anichstrasse 35, 6020 Innsbruck, Austria; and Department of Orthopaedic Surgery, Graduate School of Medicine, University of Tokyo, Tokyo, Japan (H.M.). Received September 8, 2012; revision requested October 18; revision received November 21; accepted December 5; final version accepted December 18. Address correspondence to H.M. (e-mail: [email protected]).  RSNA, 2013

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Imaging

Andrea S. Klauser, MD Hideaki Miyamoto, MD Mario Tamegger, MD Ralph Faschingbauer, MD Bernhard Moriggl, MD, PhD Guenther Klima, MD Gudrun M. Feuchtner, MD, PhD Martin Kastlunger, MD Werner R. Jaschke, MD, PhD

Original Research  n  Musculoskeletal

Achilles Tendon Assessed with Sonoelastography: Histologic Agreement1

MUSCULOSKELETAL IMAGING: Sonoelastographic versus Histologic Findings in Achilles Tendon

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chilles tendon disorders frequently occur in athletes, as well in the general population. The incidence rate of Achilles tendinopathy is 1.85 per 1000 patients registered with general practitioners (1). Conventional B-mode ultrasonography (US) has been used as a first-line approach for assessing Achilles tendon disorders (2). However, the diagnostic accuracy of B-mode US alone for these disorders is somewhat controversial (3–6). Sonoelastography is a US technique for evaluating soft-tissue elasticity (7). In breast and thyroid disease, sonoelastography has already shown high diagnostic accuracy, with histologic assessment as the reference standard (8,9). De Zordo et al (10) have reported that sonoelastography depicts abnormal changes in symptomatic Achilles tendons more sensitively than does US. Sonoelastography demonstrates 93% of the tendons in healthy volunteers to be hard and shows distinct softening in 57% of patients in the clinic (10). When clinical diagnosis is used as the reference standard, sonoelastography shows sensitivity of 94%, specificity of 99%, and accuracy of 97% (10). However, agreement between sonoelastographic and histologic findings in the Achilles tendon is still unclear. Thus, the aim of this study was to correlate conventional B-mode US and sonoelastographic findings in Achilles tendons with findings at histologic assessment.

Materials and Methods This study was conducted with the approval of the institutional review boards of the study institution (Medical University Innsbruck, Innsbruck, Austria). Written informed consent was provided according to the last wills of the donors, who had dedicated their cadavers to human studies and died between

Advance in Knowledge nn Sonoelastography depicted histologic degeneration in 14 of 14 (100%) tendon thirds of cadaver Achilles tendons, whereas B-mode US depicted it in 12 of 14 (86%) tendon thirds. 838

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September 2009 and March 2011. All cadavers were in legal custody of the Department of Anatomy, Histology and Embryology (Medical University Innsbruck).

Cadavers We examined 13 Achilles tendons in 10 cadavers (four male [mean age, 77 years; range, 70–86 years] and six female [mean age, 81 years; range, 72–90 years]). All cadavers were evaluated within 24 hours after death and were not frozen or embalmed. We had no information on what medical disorders these patients had or whether they had sustained injury to their Achilles tendons. US and Sonoelastography All examinations were performed by using a linear-array transducer with a frequency of 6–14 MHz (EUB-9000; Hitachi Medical, Tokyo, Japan). A 10-mmthick gel pad (Sonar Aid; Geistlich Pharma, Wolhusen, Switzerland) was used. To evaluate the Achilles tendon, we placed the cadaver in the prone position, with the foot hanging off the examination table. The Achilles tendon was divided into the following thirds for systematic evaluation: proximal third (musculotendinous junction), middle third (2–6 cm above insertion at the calcaneus), and distal third (insertion at the calcaneus). In this study we focused on the middle third and the distal third of the tendon. First, conventional B-mode US images were obtained and graded by one radiologist (R.F.) who had more than 8 years of experience in musculoskeletal US. We used the grading system of Archambault et al (11), where grade 1 indicated normal-appearing tendon with homogeneous fibrillar echotexture and parallel margins; grade 2, focal fusiform or diffuse enlarged tendon with bowed margins; and grade 3, hypoechoic area with or without tendon enlargement (12,13). Next, sonoelastography was performed by a second radiologist (A.S.K.) trained in sonoelastography for 5 years. The sonoelastography examiner was blinded to the B-mode results. Sonoelastography was performed by applying

light repetitive compression with the hand-held transducer. The elastogram appeared within a rectangular region of interest (ROI) as a translucent colorcoded real-time image superimposed on the B-mode image. The B-mode image and elastogram were not displayed side-by-side on the screen. 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 showed whether the displacement was sufficient to obtain local strains within the ROI. The elastograms were constructed automatically by using the same optimal settings throughout the study, as previously suggested by Havre et al (14). The probe was held perpendicular to the Achilles tendon, with appropriate pressure to avoid shifting of the elastogram that referred to the strain indicator. We selected the ROI that included a whole thickness of the Achilles tendon with the subcutaneous layer and calcaneus bone surface. For each distal and middle tendon third, sonoelastography was performed in both the transverse and the longitudinal planes. In each plane, at least three compression-relaxation cycles were applied until reproducible findings were confirmed in both longitudinal and transverse planes. Images were stored as cine loops in the memory of the US system. Representative Published online before print 10.1148/radiol.13121936  Content code: Radiology 2013; 267:837–842 Abbreviation: ROI = region of interest Author contributions: Guarantors of integrity of entire study, A.S.K., H.M., M.T., R.F., W.R.J.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, all authors; clinical studies, A.S.K., H.M., G.K., G.M.F., M.K.; experimental studies, A.S.K., H.M., R.F., B.M.; statistical analysis, A.S.K., H.M., G.M.F., M.K.; and manuscript editing, A.S.K., H.M., M.T., B.M., G.K., G.M.F., M.K., W.R.J. Conflicts of interest are listed at the end of this article.

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MUSCULOSKELETAL IMAGING: Sonoelastographic versus Histologic Findings in Achilles Tendon

sonoelastographic images were chosen from the middle of the compressionrelaxation cycle. Sonoelastographic images were graded by using the system of De Zordo et al (15), where grade 1 indicated blue (hardest tissue) to green (hard tissue); grade 2, yellow (soft tissue); and grade 3, red (softest tissue).

the tendon and was fired under US vision control. We performed one biopsy in each middle and distal tendon third in 13 tendons. We obtained 26 biopsy specimens. One biopsy sample was lost in the laboratory; therefore, 25 biopsy specimens were included in this study.

Biopsy When abnormal softening was seen at sonoelastography, the sonoelastography examiner performed a biopsy, with realtime US guidance, of the softened area seen at sonoelastography. In specimens without abnormal findings at B-mode US or sonoelastography, slices were obtained nonselectively from the central parts of each middle and distal third of the tendon. The biopsy was performed by using a 14-gauge 3 15-cm needle (SuperCore; Inter V Medical Device Technologies, Gainesville, Fla). To avoid oblique tendon biopsy, we made a small longitudinal incision in the overlying skin layers and put the biopsy device into a longitudinal plane. The tip of the needle was advanced to the surface of

Histologic Evaluation The obtained tissue was fixed in 4% formalin. The specimens were embedded in paraffin. The slices were cut at a thickness of 15 mm in a plane parallel to the tendon fibers and at a thickness of 10 mm in planes parallel and perpendicular to the tendon fibers. The 15-mm slices were left unstained for the examination in polarized light. The 10-mm slices were stained with hematoxylineosin (the standard stain), azan (a stain for tissue that contains collagen), and orcein (elastica staining for identification of elastic fibers). The following were considered histopathologic signs of degeneration: thinning of the collagen fibers and voids in the structure of the tissue, termed

Klauser et al

loss of parallel collagen structure; fiber deviation with fluid accumulation, termed loss of fiber integrity; fibroblasts incorporating fat, termed fatty infiltration; and signs of angiogenesis and neovascularization, termed capillary proliferation. Histologic evaluation was performed by one specialized interpreter (G.K.) with 30 years of histologic experience, who was blinded to the US and sonoelastographic findings.

Statistical Analysis The concordance of US grading compared with sonoelastographic grading was assessed by using k analysis. SPSS software, version 13.0 (SPSS, Chicago, Ill), was used for the statistical analysis. P , .05 was considered to indicate a statistically significant difference. Results The findings of the specimens are shown in Tables 1 and 2. At US, 13 tendon thirds were classified as normal (grade 1), nine as grade 2, and three as grade 3. At sonoelastography,

Table 1 Characteristics of All Specimens in Cadavers 1–5 Cadaver and Biopsy No. Cadaver 1   Biopsy 1   Biopsy 2 Cadaver 2   Biopsy 3   Biopsy 4 Cadaver 3   Biopsy 5   Biopsy 6   Biopsy 7   Biopsy 8 Cadaver 4   Biopsy 9   Biopsy 10   Biopsy 11   Biopsy 12 Cadaver 5   Biopsy 13   Biopsy 14   Biopsy 15   Biopsy 16

Side and Tendon Third

US Finding and Grade

Sonoelastographic Finding and Grade

Histologic Findings

Right, middle Right, distal

Enlarged, grade 2 Normal, grade 1

Red, grade 3 Yellow, grade 2

Loss of parallel collagen structure Loss of fiber integrity

Right, middle Right, distal

Hypoechoic, grade 3 Normal, grade 1

Red, grade 3 Red, grade 3

Loss of parallel collagen structure Loss of fiber integrity

Right, middle Right, distal

Normal, grade 1 Enlarged, grade 2

Blue-green, grade 1 Red, grade 3

Left, middle Left, distal

Normal, grade 1 Normal, grade 1

Blue-green, grade 1 Blue-green, grade 1

Normal Loss of parallel collagen structure, loss of fiber integrity, capillary proliferation Normal Normal

Right, middle Right, distal Left, middle Left, distal

Enlarged, grade 2 Enlarged, grade 2 Enlarged, grade 2 Enlarged, grade 2

Red, grade 3 Yellow, grade 2 Red, grade 3 Yellow, grade 2

Loss of fiber integrity Loss of parallel collagen structure Fatty infiltration Loss of fiber integrity

Right, middle Right, distal Left, middle Left, distal

Normal, grade 1 Normal, grade 1 Normal, grade 1 Normal, grade 1

Blue-green, grade 1 Blue-green, grade 1 Blue-green, grade 1 Blue-green, grade 1

Normal Normal Normal Lost in laboratory

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Table 2 Characteristics of All Specimens in Cadavers 6–10 Cadaver and Biopsy No. Cadaver 6   Biopsy 17   Biopsy 18 Cadaver 7   Biopsy 19   Biopsy 20 Cadaver 8   Biopsy 21   Biopsy 22 Cadaver 9   Biopsy 23   Biopsy 24 Cadaver 10   Biopsy 25   Biopsy 26

Side and Tendon Third

US Finding and Grade

Sonoelastographic Finding and Grade

Histologic Findings

Left, middle Left, distal

Normal, grade 1 Normal, grade 1

Blue-green, grade 1 Blue-green, grade 1

Normal Normal

Left, middle Left, distal

Normal, grade 1 Hypoechoic, grade 3

Blue-green, grade 1 Red, grade 3

Normal Loss of parallel collagen structure, loss of fiber integrity, fatty infiltration, capillary proliferation

Right, middle Right, distal

Hypoechoic, grade 3 Enlarged, grade 2

Red, grade 3 Red, grade 3

Loss of parallel collagen structure Loss of fiber integrity

Left, middle Left, distal

Normal, grade 1 Normal, grade 1

Blue-green, grade 1 Blue-green, grade 1

Normal Normal

Left, middle Left, distal

Enlarged, grade 2 Enlarged, grade 2

Red, grade 3 Yellow, grade 2

Loss of parallel collagen structure Loss of parallel collagen structure

11 tendon thirds were classified as normal (grade 1), four as grade 2, and 10 as grade 3. At histologic assessment, 11 specimens showed normal collagen structure (Fig 1), and 14 specimens showed altered tendon structure. Six of the 14 showed loss of the parallel collagen structure, eight showed loss of the fiber integrity, two showed capillary proliferation, and two showed fatty infiltration (Fig 2). With histologic findings as the reference standard for all tendon thirds, the sensitivity, specificity, positive predictive value, and negative predictive value of B-mode US were 86% (12 of 14), 100% (11 of 11), 100% (12 of 12), and 85% (11 of 13), respectively. The respective values for sonoelastography were 100% (14 of 14), 100% (11 of 11), 100% (14 of 14), and 100% (11 of 11). Histologic agreement of B-mode US and sonoelastographic findings is shown in Table 3. k Analysis showed moderate agreement between B-mode US and sonoelastographic grading (k = 0.52; P , .001) (Table 4).

Discussion Several sonoelastographic methods are commercially available. The appropriate method depends on the stress application. 840

In addition to compression elastography, which we used in this study, shear wave elastography, transient elastography, and acoustic force elastography are available (16–18). These last three might not have been suitable for our study aim because they provide only regional measurements with limited depth or cannot depict anatomic images or elastograms (16–18). In our study, both B-mode US and sonoelastography had high specificities, and sonoelastography depicted histologic degeneration more sensitively than B-mode US did. The concordance between B-mode US and sonoelastographic grading showed moderate agreement. Aström et al (19) investigated histologic agreement with B-mode US findings in Achilles tendinopathy. Bmode US showed abnormal results in 21 of 26 (80.8%) cases with histologic degeneration. Although B-mode US can be used for locating Achilles tendon abnormalities, this method alone is not completely reliable for the diagnosis of Achilles tendon disorders. In our study, two tendon thirds specimens with normal findings at B-mode US and abnormal softening at sonoelastography showed loss of fiber integrity at histologic assessment. On the basis of our results, loss of collagen structure, fatty infiltration, and capillary proliferation in

Achilles tendons may be detectable with B-mode US or sonoelastography; sonoelastography may be able to depict loss of fiber integrity in Achilles tendons with possibly greater sensitivity than B-mode US can. The degenerative sign of loss of fiber integrity is more likely to be associated with pathologic softening (grade 2 or 3) at sonoelastography. This might have clinical importance because in clinically equivocal cases, degenerative change of collagen structure (which softens and weakens the tendon) eventually leads to a partial tendon tear or spontaneous tendon rupture (20,21). Several limitations should be noted. First, we used a subjective color grading system for sonoelastography and did not use objective quantification, such as a strain index. We also did not consider the potential for differences in examiner variability. Drakonaki et al (22) have already shown that the reproducibility of sonoelastography with use of the strain index was helpful in 50 normal Achilles tendons. To minimize color grading bias, we obtained sonoelastographic images from at least three compression-relaxation cycles as entire cine loops rather than still images to avoid temporal fluctuations. We then selected the best-fit B-mode–elastogram images from the middle of each cycle (15).

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MUSCULOSKELETAL IMAGING: Sonoelastographic versus Histologic Findings in Achilles Tendon

Figure 1

Figure 2

Figure 1:  Images of normal Achilles tendon (biopsy 7 [Table 1]). A, B-mode US image at midportion of Achilles tendon in longitudinal plane.  = Homogeneous fibrillar pattern graded as normal appearing (grade 1). B, Sonoelastographic image at same level as A.  = Blue-green elastogram area (grade 1) indicates hard tissue, where the biopsy was subsequently performed. C, Histologic image obtained with orcein stain shows parallel collagen fibrils, no fatty infiltration, and no capillary proliferation.

Second, sonoelastographic findings may differ between cadavers and in vivo tendons because of vascular supply, hydration, or temperature. Although our specimens were investigated within 24 hours after death, loss of the physiologic perfusion patterns caused difficulty in the histologic evaluation of edematous changes or

Klauser et al

Figure 2:  Images of degenerative Achilles tendon (biopsy 20 [Table 1]). A, B-mode US image at insertion of Achilles tendon on longitudinal plane. ∗ = Hypoechoic area without tendon enlargement (grade 3). CAL = calcaneus bone. B, Sonoelastographic image at same level as A. ∗ = Red elastogram area (grade 3) appears as abnormal softening, where biopsy was subsequently performed. C, Histologic image obtained with azan stain (special stain for collagen-containing tissue) shows loss of parallel collagen structure, loss of fiber integrity (∗), fatty infiltration (), capillary proliferation (+), and mucoid deposition ().

hemorrhage in our study. In three cadavers, we obtained biopsy specimens from both legs; in the remaining cadavers, we used only one leg because of time restrictions in the anatomy laboratory. We also could evaluate only a small number of cadavers because of the difficulty of producing a larger cadaver series.

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Third, the selection of the ROI may affect the color distribution because the elastogram shows the relative elasticity within the ROI materially. We used a gel pad on the ROI, which can alter the color response of the elastogram and may not give the same results as skin contact. In examining the distal and middle thirds of the Achilles tendon, it 841

MUSCULOSKELETAL IMAGING: Sonoelastographic versus Histologic Findings in Achilles Tendon

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Table 3 Agreement of B-Mode US and Sonoelastographic Findings with Histologic Assessment Histologic Findings US and Sonoelastographic Findings Pathologic (grade 2 or 3) Normal (grade 1)  Total

Pathologic

Normal

Overall

12/14 2/0 14/14

0/0 11/11 11/11

12/14 13/11 25/25

Note.—Data are numbers/numbers of tendon thirds.

Table 4 Concordance between B-Mode US and Sonoelastographic Grading Sonoelastographic Findings US Findings Grade 1 Grade 2 Grade 3  Total

Grade 1

Grade 2

Grade 3

Overall

11 0 0 11

1 3 0 4

1 6 3 10

13 9 3 25

Note.—Data are numbers of tendon thirds.

is difficult to obtain uniform contact between the skin and probe because the lower leg is not a linear structure. Finally, we performed biopsies only for the focal lesions, which were the softest areas at sonoelastography; we did not examine the whole tendon as a specimen. When the biopsy specimen was obtained at the central part of the tendon, a peripheral lesion, such as that related to capillary proliferation, might be missed. For histologic evaluation of Achilles tendons, the whole specimen could better reflect the disease extension than could focal biopsy samples. Sonoelastography can be used to assess the elasticity of soft tissue through conventional B-mode US simultaneously; therefore, it may be preferable in clinical practice as a first-line approach. We conclude that sonoelastography might help predict signs of histopathologic degeneration of Achilles tendinosis potentially more sensitively than can B-mode US. Disclosures of Conflicts of Interest: A.S.K. No relevant conflicts of interest to disclose. H.M. No relevant conflicts of interest to disclose. M.T. No relevant conflicts of interest to disclose. R.F. No relevant conflicts of interest to disclose. B.M. No relevant conflicts of interest to disclose. G.K. No relevant conflicts of interest to disclose. G.M.F.

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No relevant conflicts of interest to disclose. M.K. No relevant conflicts of interest to disclose. W.R.J. No relevant conflicts of interest to disclose.

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