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ORIGINAL RESEARCH
Real-time Sonoelastography of the Quadriceps Tendon in Patients Undergoing Chronic Hemodialysis Mehmet A. Teber, MD, Törel Oğur, MD, Alper Bozkurt, MD, Bülent Er, MD, Aynur Turan, MD, Mutlu Gülbay, MD, İbrahim Akdağ, MD Objectives—This study aimed to compare sonoelastographic findings for the quadriceps tendon in patients with chronic renal failure who were in a dialysis program to findings in a control group. Methods—Fifty-three randomly allocated patients (mean age, 54.3 years; range, 27–86 years) with chronic renal failure who were in a dialysis program 3 days a week between January and May 2012 were included. The measurements were performed in both knees of 53 patients undergoing dialysis and 25 individuals in the control group. The tendons were classified as follows: type 1, very stiff tissue (blue); type 2, stiff tissue (blue-green); and type 3, intermediate tissue (green-yellow) according to color mapping. Results—The mean quadriceps tendon thicknesses in the patient group were 4.9 mm (range, 1.9–6.5 mm) for the right knee and 4.9 mm (1.4–6.5 mm) for the left knee; the values in the control group were 5.4 mm (3.6–7.0 mm) for the right knee and 5.4 mm (3.4–7.0 mm) for the left knee. The mean elasticity scores in the patient group were 3.14 (1.03–5.23) for the right knee and 3.33 (1.29–5.00) for the left knee; in the control group, the values were 3.79 (1.73–5.23) and 3.69 (1.23–5.53) for the right and left knees, respectively (right knee, P = .025; left knee, P = .018; Mann-Whitney U test). The quadriceps tendons were significantly thinner in the patient group (right knee, P = .054; left knee, P = .015; Mann-Whitney U test). Conclusions—Quadriceps tendons in patients with chronic renal failure are thinner and have lower elasticity scores compared to controls. Key Words—chronic renal failure; hemodialysis; musculoskeletal ultrasound; quadriceps tendon; sonoelastography
Received March 5, 2014, from the Departments of Radiology (M.A.T., T.O., A.B., A.T., M.G.) and Nephrology (B.E., İ.A.), Etlik Ihtisas Training and Research Hospital, Etlik, Ankara, Turkey. Revision requested April 7, 2014. Revised manuscript accepted for publication July 22, 2014. Address correspondence to Mehmet A. Teber, MD, Department of Radiology, Ataturk Training and Research Hospital, Eski¸sehir Yolu Üzeri, 06800 Bilkent, Ankara, Turkey. E-mail: [email protected] doi:10.7863/ultra.34.4.671
I
n the literature, spontaneous quadriceps tendon ruptures are reported in patients with chronic renal failure. There are generally predisposing factors, such as unnoticed recurrent microtrauma or degenerative changes, in most cases. Conditions such as hyperparathyroidism and metabolic acidosis due to chronic renal failure may cause tendon degeneration.1–4 Immediate diagnosis of tendon rupture and differential diagnosis of partial or complete rupture is necessary for accurate diagnosis. Although partial ruptures rarely necessitate surgery, complete ruptures require surgery. Delayed diagnosis and the absence of appropriate treatment would cause prolonged disability, weakness of extensor mechanisms, and joint instability.5,6
©2015 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2015; 34:671–677 | 0278-4297 | www.aium.org
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Teber et al—Sonoelastography of the Quadriceps Tendon With Chronic Hemodialysis
Sonography may be used to evaluate musculoskeletal disorders, in addition to radiography and magnetic resonance imaging. Acute rupture of the quadriceps tendon can be easily diagnosed by clinical examination. Sonography is an affordable and easily performed diagnostic tool for confirmation of the diagnosis of partial versus complete tears.5 Sonoelastography, which was first described by Ophir et al,7 is defined as measurement of the deformation response of tissue to external force or pressure applied by the ultrasound transducer. Depending on the molecular structure, each tissue or lesion behaves in a different manner. The response of stiff tissue is different from that of elastic and soft tissue. Although soft tissue becomes more deformed when pressure is applied, stiff tissue becomes less deformed. This information is reflected on the monitor as a color spectrum. Although it can be changed, blue denotes stiff regions; red denotes soft regions; and green denotes intermediate values.8 Sonoelastography is a sonographic method that has started to be used recently. The first clinical applications were in benign-malignant differentiation of tumors. Although sonoelastography is used more frequently in breast and thyroid examinations, its use in the musculoskeletal system is still considered new but has increased in recent years.9–12 In the evaluation of a quadriceps tendon rupture of the knee, assessment with sonography is one of the first approaches, in addition to clinical evaluation and radiography.2 No elastographic studies about the quadriceps tendon and its rupture were found in the literature. Therefore, this study aimed to compare sonoelastographic findings for the quadriceps tendon in patients with chronic renal failure who were in a dialysis program to findings in a control group.
Materials and Methods Patients and Control Participants The study was approved by the Institutional Review Board, and informed oral and written consent was obtained from all patients and volunteers. Fifty-three randomly selected patients (mean age, 54.3 years; range, 27–86 years) with chronic renal failure who were in a dialysis program 3 days a week between January and May 2012 were included in the study. Twenty-five healthy individuals who had no rheumatologic disease (mean age, 48.6 years; range, 26–69 years) constituted the control group. Patients and control participants who had a history of tendon rupture or who were known to have diagnoses of systemic inflammatory diseases such as rheumatoid arthritis and spondyloarthritis were not included. The measurements were performed in both knees of the 53 patients and 25 control participants. Data regarding their diseases were recorded. In both groups, the participants’ body heights and weights were obtained, and the body mass index was calculated by the following formula: body mass index = weight (kilograms)/height (square meters).
Figure 2. B-mode and sonoelastographic images of the distal part of the quadriceps tendon. A, Type 1: tendons appear homogeneously stiff, with normally appearing tendons in shades of blue (continued). A
Figure 1. Sonoelastographic measurements at the distal part of the tendon.
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Sonography Sonographic assessment was performed by using a freehand compression technique with a real-time strain sonoelastographic scanner (LOGIQ E9; GE Healthcare, Milwaukee, WI) by 2 radiologist who were experienced in musculoskeletal sonography. A 6–15-MHz linear transducer compatible with elastography was used. The examinations were performed with the patients in a supine position while the thigh and the legs were in flexion at approximately 45°, keeping the foot on the floor. Tendon thickness and elastographic measurements were performed proximal to the patellar insertion of the tendon. The tendon thicknesses were measured by taking the anteroposterior sizes in the longitudinal axis. Real-time sonoelastographic images were obtained in the same position while the tendon was in the longitudinal plane. While the conventional B-mode sonograms were displayed on the left side of the screen, the color sonoelastographic images were displayed on right side. An attempt was made to standardize the pressure to the quadriceps according to a visual scale, which was accepted as real time on the sonographic screen. The sonoelastographic measurements were obtained by taking the quantitative values from circular measurement areas that were placed at 3 dif-
ferent points in the distal part of the tendon (Figure 1). They were obtained from the B-mode image in this frame interval, which showed that the applied pressure was optimal. These images were recorded to a hard disk for analysis and archives. The images obtained during the compression phase in the longitudinal plane were visually examined by 2 radiologists in consensus for the tendon image and sonoelastographic pattern definition. The tendons were classified as follows: type 1, very stiff tissue (blue); type 2, stiff tissue (blue-green); and type 3, intermediate tissue (green-yellow and red) according to color mapping (Figure 2). Statistical Analysis The statistical analysis was conducted by using SPSS version 20 software (IBM Corporation, Armonk, NY). The compatibility of the variables to a normal distribution was investigated by visual (histogram and probability graphics) and analytic (Kolmogorov-Smirnov and ShapiroWilk tests) methods. For the statistical analysis, the intergroup variables were compared by the Mann-Whitney U test as the variables did not completely show a normal distribution, and there were ordinal variables. Significance levels were set at P < .05.
Figure 2. (continued) B, Type 2: tendons appear considerably inhomogeneous, in blue to green. C, Type 3: tendons appear inhomogeneous, in green-yellow to red, indicating structurally impaired tendons. B
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C
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Results The patient group consisted of 21 men (39.6%) and 32 women (60.4%); the control group included 5 men (20%) and 20 women (80%). The average duration of hemodialysis treatment was 7.6 years (range, 1–20.5 years) for the patient group. The mean quadriceps tendon thicknesses in the patient group were 4.9 mm (range, 1.9–6.5 mm) for the right knee and 4.9 mm (1.4–6.5 mm) for the left knee; the values in the control group were 5.4 mm (3.6–7.0 mm) for the right knee and 5.4 mm (3.4–7.0 mm) for the left knee. Thus, the quadriceps tendons were significantly thinner in the patient group (right knee, P = .054; left knee, P = .015; Mann-Whitney U test). The mean elasticity scores in the patient group were 3.14 (1.03–5.23) for the right knee and 3.33 (1.29–5.00) for the left knee; in the control group, the values were 3.79 (1.73–5.23) and 3.69 (1.23–5.53) in the right and left knees, respectively. When the results were compared, the elasticity scores were significantly lower in the patient group (right knee, P = .025; left knee, P = .018; MannWhitney U test). Similarly, radiologist classification of the tendon elasticity according to the color map showed a significant difference between the patient and control groups (right knee, P < .001; left knee, P = .018; MannWhitney U test). Although most of the sonoelastographic images of the quadriceps tendons were classified as type 1 by both radiologists in both groups, there were no type 3 tendons in the control group, in contradistinction to the patient group (Table 1). There was no clear correlation between the duration of the hemodialysis treatment and tendon thickness. Additionally, no clear correlation was shown between the body mass index and tendon thickness in both groups (Mann-Whitney U test).
Discussion It is believed that tendon defects are multifactorial. Together with recurrent microtraumas and hypoxia, vascular changes and mucoid, calcified, and lipoid degenerations may lead to microscopic changes, tendon thickening, partial ruptures, and full-thickness ruptures. The clinical differentiation of tendinopathy, partial ruptures, and even peritendinitis may be difficult; therefore, sonography and magnetic resonance imaging are mainly used in imaging.11,13,14 Quadriceps tendon rupture generally occurs by direct or indirect injury during overflexion, which develops from strain against quadriceps contraction during knee stumbling, falling down stairs, or attempts to avoid falling, for 674
example. Rupture of a healthy tendon is rare. However, if the tendon weakens due to degenerative changes from aging, fatty infiltration in obese patients, and various diseases and conditions (eg, steroid therapy, systemic lupus erythematosus, chronic renal failure, diabetes mellitus, syphilis, tuberculosis, tumor infiltration, chronic anemia, atherosclerosis, rheumatoid arthritis, gout, and secondary parathyroidism), it may rupture under relatively lower stress conditions.5,15–19 Large tendon rupture is a rare but catastrophic condition in patients undergoing dialysis. Malnutrition, insufficient dialysis, amyloidosis, chronic acidosis, and hyperparathyroidism are included among the various pathogeneses of the rupture. Jones and Kjellstrand20 investigated their own patients and cases in the literature and found that 44 patients undergoing dialysis (42 hemodialysis and 2 peritoneal dialysis) with tendon rupture were younger and had received dialysis treatment for a longer period; the patients were not malnourished yet had higher parathyroid hormone levels. Furthermore, they reported that steroid use in the patients with rupture was higher than in the control group.20 Similarly, in a study by Morein et al,21 which was conducted in patients with chronic renal failure who were receiving hemodialysis treatment, they mentioned that tendon rupture was more frequent in younger patients who received dialysis for a longer period, and weakness in the tendons was related to time. Patients with limited clinical extension of the knee and those with pain and edema in the proximal patella should be suspected of having complete or partial quadriceps tendon rupture. However, since the physical treatment is limited in patients with severe pain and diffuse edema in the suprapatellar area, the diagnosis is generally unnoticed.5,15,16 Direct knee radiography is an inexpensive tool for diagnosis. On the other hand, it frequently shows nonspecific changes and only indirect findings of rupture. The findings that are observed on plain radiography are soft tissue swelling, knee effusions, calcifications, inferior Table 1. Sonoelastographic Findings for Right and Left Knees According to the Color Scale Color Type Patients 1 2 3 Controls 1 2 3
Right, n (%)
Left, n (%)
27 (50.9) 16 (30.2) 10 (18.9)
33 (62.3) 17 (32.0) 3 (5.7)
23 (92.0) 2 (8.0) 0
22 (88.0) 3 (12.0) 0
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extension of the patella, forward tilting of the patella, and disruption of the quadriceps silhouette. Sonography is another inexpensive method that can be performed at the bedside and used for diagnosis of tendon rupture. Magnetic resonance imaging is a more expensive method that is also used for diagnosis of tendon rupture. It is especially useful for preoperative details, as it allows better visualization of the anatomic details and the soft tissue, together with the rupture size and correct location.6,22–24 High-frequency ultrasound transducers are necessary because of the superficial locations of the tendons. Recently, high-frequency transducers with optimal spatial and contrast resolution that can increase to 15 to 17 MHz and are dedicated to musculoskeletal examinations have been developed. The transducer can be used directly over the skin, or a standoff pad placed in the middle might be useful for the most superficial structures.5,25 When the probe is placed correctly to enable the sound from the transducer to arrive perpendicularly at the tendon, higher echogenicity according to the muscle tissue, which contains fine parallel echogenicity, can be observed. Tendons consist of longitudinally arranged collagen fibrils and are surrounded by a peritendinous sheath. On sonography, the peritendinous sheath is observed as echogenic lines located on both sides of the tendon.26–28 In a study by Bianchi et al,5 they mentioned that the sensitivity and specificity of sonography were high (100% for sonographic diagnosis of complete tears) in the evaluation of quadriceps tendon rupture, and it should be used for management of the diagnosis and treatment. As edema, hemorrhage, mucoid degeneration, and partial ruptures can be seen as isoechoic changes, differentiation of tendon changes on musculoskeletal imaging might be difficult.9,29–32 Because of their advantages and limitations in the evaluation of musculoskeletal diseases, sonography and sonoelastography are currently used frequently in routine practice.12 There are several different sonoelastographic techniques, such as compression strain imaging, shear wave or real-time shear velocity imaging, vibration sonoelastography, and acoustic radiation force sonoelastography. In this study, we used strain elastography, also described as compression elastography, sonoelastography, and real-time elastography.8,33 This technique depends on the principle that tissue compression produces strain.34 This strain is lower in stiff tissue, which has increased cellularity, such as tumors, and is greater in soft tissue. Inflammation and tumors that cause changes in tissue elasticity have been evaluated by sonoelastography more frequently in breast, thyroid, and prostate cancers and for lymph node characterization.
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Chronic tendinopathy consists of collagen defects that lead to softening and weakening of the tendon and, ultimately, ruptures or tears.27 Sonoelastography is a sensitive imaging technique that is helpful for correct in vivo measurement of hidden changes in the stiffness of the tendon. Initially, elasticity evaluations using sonoelastography were conducted in healthy volunteers with normal Achilles tendon characteristics. In these evaluations, tendons were found to be stiff structures. On the other hand, it was demonstrated that diseased tendons behaved more softly on sonoelastography as correlated with conventional sonographic findings in symptomatic patients.11,35 Healthy tendons possess a stiff structure (blue and green), but yellow and red areas are seen in prominently softening diseased tendons.11 In this study, when the control and patient groups were compared, it was found that tendon stiffness decreased more in the patient group; this change was statistically significant; and heterogeneity developed in the color mapping. However, no case of rupture was detected in the patient group; furthermore, in our clinic, no records of rupture were observed in the patients. We believe that this situation was due to the fact that the patients were under close follow-up in terms of acidosis and hyperparathyroidism, and they continued dialysis regularly. However, we also believe that a controlled study with patients who cannot continue dialysis regularly and who have lability in laboratory results would be more informative. There may be some errors in the practice of sonoelastography. The pressure that is applied to the skin with the freehand technique should be moderate. Due to the nonlinear properties of tissue elasticity, application of high and very low pressures should be avoided. A visual indicator on the screen could assist in achieving an optimal pressure interval, which would be helpful for decreasing variability between practitioners.11 The size of the sonoelastographic window affects the elastogram because sonoelastography calculates the mean elasticity of each image match. As a larger window contains more soft tissue than a smaller window, it portrays the tendon that it surrounds as a more stiff structure (bluer); therefore, standardization of the box is useful.11 In summary, the first results of initial sonoelastography used in musculoskeletal disorders demonstrated that the elastic properties of normal tendons changed in pathologic conditions, and there was substantial intratendinous softening.11 This new technique could be used in addition to conventional sonography to increase diagnostic accuracy. Additionally, it can be used as a potential imaging device for encouraging athletes to change their exercise regimens to prevent tendon injuries.11,29
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This study had a few limitations. First, our study population was relatively small. Second, the patient and control groups did not have a balanced sex distribution. Third, in terms of transducer pressure application, sonoelastography has relatively high operator dependency. Additionally, 2 radiologists who had performed the examinations prospectively assessed the quality and types of elasticity images. However, interobserver variability and intraobserver variability were not assessed in our study. Magnetic resonance imaging is often recommended as a safe and reliable diagnostic tool for visualizing a quadriceps tendon; however, there is no reference standard for evaluation of the quadriceps tendon by sonoelastography for comparative investigations. In conclusion, sonoelastography is a reliable and accurate imaging method, especially in sonographic tendinopathy and for diagnosis of both existing and potential ruptures.17 Magnetic resonance imaging and sonography are commonly used modalities in routine clinical practice. When compared with magnetic resonance imaging, sonography is an inexpensive and easily used modality,17 and it may be useful for diagnosis of musculoskeletal abnormalities. Its major advantages are that it provides dynamic evaluation of structures, is relatively inexpensive, does not involve radiation, and can be widely used.26,36 Moreover, sonoelastography provides additional information and is expected to be widely used in the musculoskeletal area, parallel to the increase in experience with interpretation of elastographic data and artifacts.17
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Anderson WE III, Habermann ET. Spontaneous bilateral quadriceps tendon rupture in a patient on hemodialysis. Orthop Rev 1988; 17:411–414. Harcke HT, Grissom LE, Finkelstein MS. Evaluation of the musculoskeletal system with sonography. AJR Am J Roentgenol 1988; 150:1253– 1261. Shah MK. Simultaneous bilateral quadriceps tendon rupture in renal patients. Clin Nephrol 2002; 58:118–121. Kazimoğlu C, Yağdi S, Karapinar H, Sener M. Bilateral quadriceps tendon rupture and coexistent femoral neck fracture in a patient with chronic renal failure [in Turkish]. Acta Orthop Traumatol Turc 2007; 41:393–396. Bianchi S, Zwass A, Abdelwahab IF, Banderali A. Diagnosis of tears of the quadriceps tendon of the knee: value of sonography. AJR Am J Roentgenol 1994; 162:1137–1140. Walker LG, Glick H. Bilateral spontaneous quadriceps tendon ruptures: a case report and review of the literature. Orthop Rev 1989; 18:867–871. Ophir J, Céspedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 1991; 13:111–134.
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26. Kaplan PA, Matamoros A Jr, Anderson JC. Sonography of the musculoskeletal system. AJR Am J Roentgenol 1990; 155:237–245. 27. Dillehay GL, Deschler T, Rogers LF, Neiman HL, Hendrix RW. The ultrasonographic characterization of tendons. Invest Radiol 1984; 19:338– 341. 28. Fornage BD. The hypoechoic normal tendon: a pitfall. J Ultrasound Med 1987; 6:19–22. 29. Garra BS, Cespedes EI, Ophir J, et al. Elastography of breast lesions: initial clinical results. Radiology 1997; 202:79–86. 30. Itoh A, Ueno E, Tohno E, et al. Breast disease: clinical application of US elastography for diagnosis. Radiology 2006; 239:341–350. 31. Lyshchik A, Higashi T, Asato R, et al. Thyroid gland tumor diagnosis at US elastography. Radiology 2005; 237:202–211. 32. Lyshchik A, Higashi T, Asato R, et al. Cervical lymph node metastases: diagnosis at sonoelastography—initial experience. Radiology 2007; 243:258–267. 33. Drakonaki E, Allen GM, Wilson DJ. Ultrasound elastography for musculoskeletal applications. Br J Radiol 2012; 85:1435–1445. 34. Palmeri ML, Nightingale KR. What challenges must be overcome before ultrasound elasticity imaging is ready for the clinic? Imaging Med 2011; 3:433–444. 35. Sharma P, Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact 2006; 6:181–190. 36. Erickson SJ. Sonography of the foot and ankle. Foot Ankle Clin2000; 5:29– 48, v.
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ORIGINAL RESEARCH
Real-time Sonoelastography of the Quadriceps Tendon in Patients Undergoing Chronic Hemodialysis Mehmet A. Teber, MD, Törel Oğur, MD, Alper Bozkurt, MD, Bülent Er, MD, Aynur Turan, MD, Mutlu Gülbay, MD, İbrahim Akdağ, MD Objectives—This study aimed to compare sonoelastographic findings for the quadriceps tendon in patients with chronic renal failure who were in a dialysis program to findings in a control group. Methods—Fifty-three randomly allocated patients (mean age, 54.3 years; range, 27–86 years) with chronic renal failure who were in a dialysis program 3 days a week between January and May 2012 were included. The measurements were performed in both knees of 53 patients undergoing dialysis and 25 individuals in the control group. The tendons were classified as follows: type 1, very stiff tissue (blue); type 2, stiff tissue (blue-green); and type 3, intermediate tissue (green-yellow) according to color mapping. Results—The mean quadriceps tendon thicknesses in the patient group were 4.9 mm (range, 1.9–6.5 mm) for the right knee and 4.9 mm (1.4–6.5 mm) for the left knee; the values in the control group were 5.4 mm (3.6–7.0 mm) for the right knee and 5.4 mm (3.4–7.0 mm) for the left knee. The mean elasticity scores in the patient group were 3.14 (1.03–5.23) for the right knee and 3.33 (1.29–5.00) for the left knee; in the control group, the values were 3.79 (1.73–5.23) and 3.69 (1.23–5.53) for the right and left knees, respectively (right knee, P = .025; left knee, P = .018; Mann-Whitney U test). The quadriceps tendons were significantly thinner in the patient group (right knee, P = .054; left knee, P = .015; Mann-Whitney U test). Conclusions—Quadriceps tendons in patients with chronic renal failure are thinner and have lower elasticity scores compared to controls. Key Words—chronic renal failure; hemodialysis; musculoskeletal ultrasound; quadriceps tendon; sonoelastography
Received March 5, 2014, from the Departments of Radiology (M.A.T., T.O., A.B., A.T., M.G.) and Nephrology (B.E., İ.A.), Etlik Ihtisas Training and Research Hospital, Etlik, Ankara, Turkey. Revision requested April 7, 2014. Revised manuscript accepted for publication July 22, 2014. Address correspondence to Mehmet A. Teber, MD, Department of Radiology, Ataturk Training and Research Hospital, Eski¸sehir Yolu Üzeri, 06800 Bilkent, Ankara, Turkey. E-mail: [email protected] doi:10.7863/ultra.34.4.671
I
n the literature, spontaneous quadriceps tendon ruptures are reported in patients with chronic renal failure. There are generally predisposing factors, such as unnoticed recurrent microtrauma or degenerative changes, in most cases. Conditions such as hyperparathyroidism and metabolic acidosis due to chronic renal failure may cause tendon degeneration.1–4 Immediate diagnosis of tendon rupture and differential diagnosis of partial or complete rupture is necessary for accurate diagnosis. Although partial ruptures rarely necessitate surgery, complete ruptures require surgery. Delayed diagnosis and the absence of appropriate treatment would cause prolonged disability, weakness of extensor mechanisms, and joint instability.5,6
©2015 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2015; 34:671–677 | 0278-4297 | www.aium.org
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Teber et al—Sonoelastography of the Quadriceps Tendon With Chronic Hemodialysis
Sonography may be used to evaluate musculoskeletal disorders, in addition to radiography and magnetic resonance imaging. Acute rupture of the quadriceps tendon can be easily diagnosed by clinical examination. Sonography is an affordable and easily performed diagnostic tool for confirmation of the diagnosis of partial versus complete tears.5 Sonoelastography, which was first described by Ophir et al,7 is defined as measurement of the deformation response of tissue to external force or pressure applied by the ultrasound transducer. Depending on the molecular structure, each tissue or lesion behaves in a different manner. The response of stiff tissue is different from that of elastic and soft tissue. Although soft tissue becomes more deformed when pressure is applied, stiff tissue becomes less deformed. This information is reflected on the monitor as a color spectrum. Although it can be changed, blue denotes stiff regions; red denotes soft regions; and green denotes intermediate values.8 Sonoelastography is a sonographic method that has started to be used recently. The first clinical applications were in benign-malignant differentiation of tumors. Although sonoelastography is used more frequently in breast and thyroid examinations, its use in the musculoskeletal system is still considered new but has increased in recent years.9–12 In the evaluation of a quadriceps tendon rupture of the knee, assessment with sonography is one of the first approaches, in addition to clinical evaluation and radiography.2 No elastographic studies about the quadriceps tendon and its rupture were found in the literature. Therefore, this study aimed to compare sonoelastographic findings for the quadriceps tendon in patients with chronic renal failure who were in a dialysis program to findings in a control group.
Materials and Methods Patients and Control Participants The study was approved by the Institutional Review Board, and informed oral and written consent was obtained from all patients and volunteers. Fifty-three randomly selected patients (mean age, 54.3 years; range, 27–86 years) with chronic renal failure who were in a dialysis program 3 days a week between January and May 2012 were included in the study. Twenty-five healthy individuals who had no rheumatologic disease (mean age, 48.6 years; range, 26–69 years) constituted the control group. Patients and control participants who had a history of tendon rupture or who were known to have diagnoses of systemic inflammatory diseases such as rheumatoid arthritis and spondyloarthritis were not included. The measurements were performed in both knees of the 53 patients and 25 control participants. Data regarding their diseases were recorded. In both groups, the participants’ body heights and weights were obtained, and the body mass index was calculated by the following formula: body mass index = weight (kilograms)/height (square meters).
Figure 2. B-mode and sonoelastographic images of the distal part of the quadriceps tendon. A, Type 1: tendons appear homogeneously stiff, with normally appearing tendons in shades of blue (continued). A
Figure 1. Sonoelastographic measurements at the distal part of the tendon.
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Sonography Sonographic assessment was performed by using a freehand compression technique with a real-time strain sonoelastographic scanner (LOGIQ E9; GE Healthcare, Milwaukee, WI) by 2 radiologist who were experienced in musculoskeletal sonography. A 6–15-MHz linear transducer compatible with elastography was used. The examinations were performed with the patients in a supine position while the thigh and the legs were in flexion at approximately 45°, keeping the foot on the floor. Tendon thickness and elastographic measurements were performed proximal to the patellar insertion of the tendon. The tendon thicknesses were measured by taking the anteroposterior sizes in the longitudinal axis. Real-time sonoelastographic images were obtained in the same position while the tendon was in the longitudinal plane. While the conventional B-mode sonograms were displayed on the left side of the screen, the color sonoelastographic images were displayed on right side. An attempt was made to standardize the pressure to the quadriceps according to a visual scale, which was accepted as real time on the sonographic screen. The sonoelastographic measurements were obtained by taking the quantitative values from circular measurement areas that were placed at 3 dif-
ferent points in the distal part of the tendon (Figure 1). They were obtained from the B-mode image in this frame interval, which showed that the applied pressure was optimal. These images were recorded to a hard disk for analysis and archives. The images obtained during the compression phase in the longitudinal plane were visually examined by 2 radiologists in consensus for the tendon image and sonoelastographic pattern definition. The tendons were classified as follows: type 1, very stiff tissue (blue); type 2, stiff tissue (blue-green); and type 3, intermediate tissue (green-yellow and red) according to color mapping (Figure 2). Statistical Analysis The statistical analysis was conducted by using SPSS version 20 software (IBM Corporation, Armonk, NY). The compatibility of the variables to a normal distribution was investigated by visual (histogram and probability graphics) and analytic (Kolmogorov-Smirnov and ShapiroWilk tests) methods. For the statistical analysis, the intergroup variables were compared by the Mann-Whitney U test as the variables did not completely show a normal distribution, and there were ordinal variables. Significance levels were set at P < .05.
Figure 2. (continued) B, Type 2: tendons appear considerably inhomogeneous, in blue to green. C, Type 3: tendons appear inhomogeneous, in green-yellow to red, indicating structurally impaired tendons. B
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C
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Results The patient group consisted of 21 men (39.6%) and 32 women (60.4%); the control group included 5 men (20%) and 20 women (80%). The average duration of hemodialysis treatment was 7.6 years (range, 1–20.5 years) for the patient group. The mean quadriceps tendon thicknesses in the patient group were 4.9 mm (range, 1.9–6.5 mm) for the right knee and 4.9 mm (1.4–6.5 mm) for the left knee; the values in the control group were 5.4 mm (3.6–7.0 mm) for the right knee and 5.4 mm (3.4–7.0 mm) for the left knee. Thus, the quadriceps tendons were significantly thinner in the patient group (right knee, P = .054; left knee, P = .015; Mann-Whitney U test). The mean elasticity scores in the patient group were 3.14 (1.03–5.23) for the right knee and 3.33 (1.29–5.00) for the left knee; in the control group, the values were 3.79 (1.73–5.23) and 3.69 (1.23–5.53) in the right and left knees, respectively. When the results were compared, the elasticity scores were significantly lower in the patient group (right knee, P = .025; left knee, P = .018; MannWhitney U test). Similarly, radiologist classification of the tendon elasticity according to the color map showed a significant difference between the patient and control groups (right knee, P < .001; left knee, P = .018; MannWhitney U test). Although most of the sonoelastographic images of the quadriceps tendons were classified as type 1 by both radiologists in both groups, there were no type 3 tendons in the control group, in contradistinction to the patient group (Table 1). There was no clear correlation between the duration of the hemodialysis treatment and tendon thickness. Additionally, no clear correlation was shown between the body mass index and tendon thickness in both groups (Mann-Whitney U test).
Discussion It is believed that tendon defects are multifactorial. Together with recurrent microtraumas and hypoxia, vascular changes and mucoid, calcified, and lipoid degenerations may lead to microscopic changes, tendon thickening, partial ruptures, and full-thickness ruptures. The clinical differentiation of tendinopathy, partial ruptures, and even peritendinitis may be difficult; therefore, sonography and magnetic resonance imaging are mainly used in imaging.11,13,14 Quadriceps tendon rupture generally occurs by direct or indirect injury during overflexion, which develops from strain against quadriceps contraction during knee stumbling, falling down stairs, or attempts to avoid falling, for 674
example. Rupture of a healthy tendon is rare. However, if the tendon weakens due to degenerative changes from aging, fatty infiltration in obese patients, and various diseases and conditions (eg, steroid therapy, systemic lupus erythematosus, chronic renal failure, diabetes mellitus, syphilis, tuberculosis, tumor infiltration, chronic anemia, atherosclerosis, rheumatoid arthritis, gout, and secondary parathyroidism), it may rupture under relatively lower stress conditions.5,15–19 Large tendon rupture is a rare but catastrophic condition in patients undergoing dialysis. Malnutrition, insufficient dialysis, amyloidosis, chronic acidosis, and hyperparathyroidism are included among the various pathogeneses of the rupture. Jones and Kjellstrand20 investigated their own patients and cases in the literature and found that 44 patients undergoing dialysis (42 hemodialysis and 2 peritoneal dialysis) with tendon rupture were younger and had received dialysis treatment for a longer period; the patients were not malnourished yet had higher parathyroid hormone levels. Furthermore, they reported that steroid use in the patients with rupture was higher than in the control group.20 Similarly, in a study by Morein et al,21 which was conducted in patients with chronic renal failure who were receiving hemodialysis treatment, they mentioned that tendon rupture was more frequent in younger patients who received dialysis for a longer period, and weakness in the tendons was related to time. Patients with limited clinical extension of the knee and those with pain and edema in the proximal patella should be suspected of having complete or partial quadriceps tendon rupture. However, since the physical treatment is limited in patients with severe pain and diffuse edema in the suprapatellar area, the diagnosis is generally unnoticed.5,15,16 Direct knee radiography is an inexpensive tool for diagnosis. On the other hand, it frequently shows nonspecific changes and only indirect findings of rupture. The findings that are observed on plain radiography are soft tissue swelling, knee effusions, calcifications, inferior Table 1. Sonoelastographic Findings for Right and Left Knees According to the Color Scale Color Type Patients 1 2 3 Controls 1 2 3
Right, n (%)
Left, n (%)
27 (50.9) 16 (30.2) 10 (18.9)
33 (62.3) 17 (32.0) 3 (5.7)
23 (92.0) 2 (8.0) 0
22 (88.0) 3 (12.0) 0
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extension of the patella, forward tilting of the patella, and disruption of the quadriceps silhouette. Sonography is another inexpensive method that can be performed at the bedside and used for diagnosis of tendon rupture. Magnetic resonance imaging is a more expensive method that is also used for diagnosis of tendon rupture. It is especially useful for preoperative details, as it allows better visualization of the anatomic details and the soft tissue, together with the rupture size and correct location.6,22–24 High-frequency ultrasound transducers are necessary because of the superficial locations of the tendons. Recently, high-frequency transducers with optimal spatial and contrast resolution that can increase to 15 to 17 MHz and are dedicated to musculoskeletal examinations have been developed. The transducer can be used directly over the skin, or a standoff pad placed in the middle might be useful for the most superficial structures.5,25 When the probe is placed correctly to enable the sound from the transducer to arrive perpendicularly at the tendon, higher echogenicity according to the muscle tissue, which contains fine parallel echogenicity, can be observed. Tendons consist of longitudinally arranged collagen fibrils and are surrounded by a peritendinous sheath. On sonography, the peritendinous sheath is observed as echogenic lines located on both sides of the tendon.26–28 In a study by Bianchi et al,5 they mentioned that the sensitivity and specificity of sonography were high (100% for sonographic diagnosis of complete tears) in the evaluation of quadriceps tendon rupture, and it should be used for management of the diagnosis and treatment. As edema, hemorrhage, mucoid degeneration, and partial ruptures can be seen as isoechoic changes, differentiation of tendon changes on musculoskeletal imaging might be difficult.9,29–32 Because of their advantages and limitations in the evaluation of musculoskeletal diseases, sonography and sonoelastography are currently used frequently in routine practice.12 There are several different sonoelastographic techniques, such as compression strain imaging, shear wave or real-time shear velocity imaging, vibration sonoelastography, and acoustic radiation force sonoelastography. In this study, we used strain elastography, also described as compression elastography, sonoelastography, and real-time elastography.8,33 This technique depends on the principle that tissue compression produces strain.34 This strain is lower in stiff tissue, which has increased cellularity, such as tumors, and is greater in soft tissue. Inflammation and tumors that cause changes in tissue elasticity have been evaluated by sonoelastography more frequently in breast, thyroid, and prostate cancers and for lymph node characterization.
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Chronic tendinopathy consists of collagen defects that lead to softening and weakening of the tendon and, ultimately, ruptures or tears.27 Sonoelastography is a sensitive imaging technique that is helpful for correct in vivo measurement of hidden changes in the stiffness of the tendon. Initially, elasticity evaluations using sonoelastography were conducted in healthy volunteers with normal Achilles tendon characteristics. In these evaluations, tendons were found to be stiff structures. On the other hand, it was demonstrated that diseased tendons behaved more softly on sonoelastography as correlated with conventional sonographic findings in symptomatic patients.11,35 Healthy tendons possess a stiff structure (blue and green), but yellow and red areas are seen in prominently softening diseased tendons.11 In this study, when the control and patient groups were compared, it was found that tendon stiffness decreased more in the patient group; this change was statistically significant; and heterogeneity developed in the color mapping. However, no case of rupture was detected in the patient group; furthermore, in our clinic, no records of rupture were observed in the patients. We believe that this situation was due to the fact that the patients were under close follow-up in terms of acidosis and hyperparathyroidism, and they continued dialysis regularly. However, we also believe that a controlled study with patients who cannot continue dialysis regularly and who have lability in laboratory results would be more informative. There may be some errors in the practice of sonoelastography. The pressure that is applied to the skin with the freehand technique should be moderate. Due to the nonlinear properties of tissue elasticity, application of high and very low pressures should be avoided. A visual indicator on the screen could assist in achieving an optimal pressure interval, which would be helpful for decreasing variability between practitioners.11 The size of the sonoelastographic window affects the elastogram because sonoelastography calculates the mean elasticity of each image match. As a larger window contains more soft tissue than a smaller window, it portrays the tendon that it surrounds as a more stiff structure (bluer); therefore, standardization of the box is useful.11 In summary, the first results of initial sonoelastography used in musculoskeletal disorders demonstrated that the elastic properties of normal tendons changed in pathologic conditions, and there was substantial intratendinous softening.11 This new technique could be used in addition to conventional sonography to increase diagnostic accuracy. Additionally, it can be used as a potential imaging device for encouraging athletes to change their exercise regimens to prevent tendon injuries.11,29
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This study had a few limitations. First, our study population was relatively small. Second, the patient and control groups did not have a balanced sex distribution. Third, in terms of transducer pressure application, sonoelastography has relatively high operator dependency. Additionally, 2 radiologists who had performed the examinations prospectively assessed the quality and types of elasticity images. However, interobserver variability and intraobserver variability were not assessed in our study. Magnetic resonance imaging is often recommended as a safe and reliable diagnostic tool for visualizing a quadriceps tendon; however, there is no reference standard for evaluation of the quadriceps tendon by sonoelastography for comparative investigations. In conclusion, sonoelastography is a reliable and accurate imaging method, especially in sonographic tendinopathy and for diagnosis of both existing and potential ruptures.17 Magnetic resonance imaging and sonography are commonly used modalities in routine clinical practice. When compared with magnetic resonance imaging, sonography is an inexpensive and easily used modality,17 and it may be useful for diagnosis of musculoskeletal abnormalities. Its major advantages are that it provides dynamic evaluation of structures, is relatively inexpensive, does not involve radiation, and can be widely used.26,36 Moreover, sonoelastography provides additional information and is expected to be widely used in the musculoskeletal area, parallel to the increase in experience with interpretation of elastographic data and artifacts.17
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