MR Imaging of the Medial Collateral Ligament Bursa: Findings in Patients and Anatomic Data Derived from Cadavers

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Michel De Maeseneer 1 Maryam Shahabpour 1 Frans Van Roy 2 Anita Goossens 3 Filip De Ridder 1 Jan Clarijs 2 Michel Osteaux 1 Received October 9, 2000; accepted after revision April 17, 2001. 1 Department of Radiology, Vrije Universiteit russel, Laerbeeklaan 101, 1090 Jette, elgium. Address correspondence to M. De Maeseneer. 2 Department of Experimental Anatomy, Vrije Universiteit russel, Jette, elgium. 3 Department of Pathology, Vrije Universiteit russel, Jette, elgium. AJR 2001;177:911 917 0361 803X/01/1774 911 American Roentgen Ray Society MR Imaging of the Medial Collateral Ligament ursa: Findings in Patients and Anatomic Data Derived from Cadavers OJECTIVE. The purpose of this work was to define the MR imaging findings of fluid collections confined to the medial collateral ligament (MCL) bursa and to correlate these findings with anatomic features shown in cadaveric specimens. MATERIALS AND METHODS. The anatomic location of the MCL bursa was investigated by MR anatomic correlation in seven cadaveric knees. The MR imaging studies and clinical charts of six patients with fluid collections confined to the MCL bursa were reviewed. RESULTS. On anatomic sections, the MCL bursa was located between the superficial and deep portions of the MCL. Separate femoral and tibial compartments were seen in most specimens. CONCLUSION. The anatomy of the MCL bursa is shown with MR imaging in cadaveric specimens and patients. Understanding the compartmentlike distribution of fluid in the MCL bursa at MR imaging allows accurate diagnosis and differentiation from other conditions. ursae are typically interposed between bony surfaces and ligaments or tendons in areas where friction takes place. rantigan and Voshell [1] found evidence of the medial collateral ligament (MCL) bursa in 52 (91%) of 57 dissected knees. Despite this high prevalence, to our knowledge, only one article in the radiological literature refers to the MCL bursa [2]. oth Stuttle [3] and Kerlan and Glousman [4] reported that the clinical condition referred to as MCL bursitis may result when the MCL bursa is inflamed and distended by fluid. These authors consider MCL bursitis an important cause of medial knee pain that should be differentiated from other conditions such as MCL injuries and meniscal tears. The medial supporting structures of the knee can be divided into three layers [5]. Layer I consists of the crural fascia, layer II is made up of the superficial portion of the MCL, and layer III is made up of the joint capsule and the deep portion of the MCL that includes the meniscotibial and meniscofemoral extensions. Along the anterior edge of the superficial portion of the MCL, layer II is discontinuous. The discontinuity in layer II and the presence of the MCL bursa allow the MCL to glide over the bony surfaces of the tibia and femur with knee flexion [1, 5] (Figs. 1 and 2). Along the posterior third of the medial side of the knee, the superficial and deep portions of the MCL are fused and tend to fold rather than glide over the bony surfaces when the knee is flexed [1, 5]. The MCL bursa may become apparent at MR imaging when filled with fluid [2]. The purpose of our study was to describe the normal imaging anatomy of the MCL bursa by using cadaveric correlation and contrast opacification of the bursa. The second aim of our article was to evaluate the clinical and MR imaging findings in patients with fluid collections confined to the MCL bursa. Materials and Methods Cadaveric Study Seven cadaveric knees were obtained from nonembalmed fresh cadavers and were immediately deep-frozen at 30 C. The knees belonged to three men and four women whose age at death ranged from 50 to 91 years. The specimens were thawed in saline solution at room temperature for 18 hr before imaging. In six specimens, MR images were obtained in the transverse and coronal imaging planes with a 1.5-T clinical system (Vision; Siemens, Erlangen, Germany). The specimens were placed in supine position in a dedicated knee coil. The imaging parameters are listed in Table 1. In two specimens, we attempted to inject the MCL bursa with a mixture of dye and contrast agent. A mixture of 1 ml of dye and 10 ml of gadopentatate dimeglumine solution (Magnevist [1 ml in 200 ml of saline solution]; Schering, erlin, Germany) was injected into the MCL bursa using sonographic guidance (Prosound 5500 [7.5-Mhz probe]; Aloka, Tokyo, AJR:177, October 2001 911

De Maeseneer et al. Japan). For injection of the MCL bursa, an 18-gauge spinal needle was advanced obliquely through the skin until the needle tip was positioned deep in relation to the superficial portion of the MCL. The needle was placed at about 1.5 cm above and below the level of the joint space, adjacent to the femoral cortex and tibial cortex, respectively. Filling of the bursa could be observed in real time using sonography. Subsequently, MR images were obtained using the parameters listed in Table 1. Fig. 1. Line drawing represents anteromedial aspect of knee. Clamp (C) elevates anterior edge of superficial portion of medial collateral ligament (MCL). MCL bursa (black area) is seen between superficial (S) and deep MCL. Meniscofemoral (F) and meniscotibial (T) extensions are part of deep MCL. Also note posterior oblique (O) portion of MCL. TALE 1 In one specimen, the medial aspect of the knee was dissected and the MCL bursa was opened. The other six specimens were refrozen and sectioned with a band saw (NSV; Modena, Italy) into slices 3 4 mm thick that correlated with MR images. Three specimens were sectioned along the coronal plane and three others along the transverse plane. The region of the MCL bursa was examined by consensus of an anatomist and a musculoskeletal radiologist. This assessment included evaluation of separate Fig. 2. Line drawing represents axial section of medial side of knee. Note three distinct layers (I, II, and III). Layer I corresponds to crural fascia, layer II contains superficial portion of medial collateral ligament (MCL), and layer III contains deep portion of MCL. MCL bursa (black area, ) is located between superficial and deep portion of MCL. Also note split in layer II along anterior margin of superficial MCL (arrowheads). Anteriorly, layer I is fused with layer II (curved arrow), whereas posteriorly, layer II joins layer III (short arrows). Sartorius tendon is embedded in layer I (S). femoral and tibial components of the MCL bursa, measurement of the size of these compartments, and evaluation of the distribution of injected dye. Microscopic examination of the MCL bursa was performed in a randomly selected tissue sample that included the superficial and deep portions of the MCL. Histologic staining included H and E staining and immunological staining with epithelial membrane antigen (Dako A/S; Glostrup, Denmark). The microscopic slides were examined by a senior pathologist who was unaware of the results of gross anatomy and MR imaging. Clinical Study The reports of all MR examinations of the knee performed in 1998 and 1999 at our institution (n = 2454) were retrospectively reviewed. The details of typical MR imaging protocols are shown in Table 1. The initial reports had been made by one of two senior musculoskeletal radiologists. oth radiologists used consistent criteria for diagnosing fluid in the MCL bursa, based on previously published data in the literature [2]. These criteria included presence of a collection with high signal intensity on short tau inversion recovery weighted MR images, or signal intensity higher than that of fat on T2-weighted MR images, located deep in relation to the superficial portion of the MCL is distinguishable from intraarticular joint fluid by the interposition of the deep layer of the MCL. The records of all patients with a fluid collection confined to the MCL bursa were selected. Patients with MR imaging signs of MCL tears were not included. MR imaging signs of MCL tears included visualization of a tear, nonvisualization of a portion of the MCL, edema in the substance of the MCL or periligamentous edema, and characteristic bone contusions. In addition, 20 patients with a meniscal tear on MR images or at arthroscopy were not included in the further analysis. The imaging studies and clinical charts of six patients (three men, three women) with fluid confined to the MCL bursa were reviewed by consensus of two musculoskeletal radiologists. This evaluation in- MR Imaging Protocols in Medial Collateral Ligament ursa Studies of Cadaveric Specimens and Patients Study Type T Sequence Imaging Plane Section (mm) TR/TE (msec) Signals Averaged Matrix (pixels) Field of View (cm) Cadaveric T1, SE Coronal 3 680/15 2 170 256 150 200 Cadaveric PD, FSE Coronal 3 3000/15 2 252 512 150 240 Cadaveric T2, SE Coronal, axial 3 2400/80 1 170 256 150 240 Cadaveric with bursal injection T1, SE, FS Coronal, axial 3 740/14 2 256 256 130 130 Clinical 1 PD, T2, SE Sagittal 3 2400/20, 70 a 1 192 256 200 200 Clinical 1 PD, T2, FSE Coronal, axial 3 4700/19, 93 a 1 192 256 200 200 Clinical 1.5 PD, T2, SE Sagittal 3 2000/20, 80 a 1 170 256 200 200 Clinical 1.5 PD, T2, FSE Coronal, axial 3 4700/19, 98 a 2 150 256 150 200 Clinical 1.5 PD, FSE Coronal 3 2900/15 2 252 512 150 240 Clinical 1.5 STIR (120 b ) Coronal 3 5920/60 2 160 256 150 200 Note. T1= T1-weighted, T2= T2-weighted, PD = proton density weighted, SE = spin echo, FSE = fast spin echo, FS = fat saturation, STIR = short tau inversion recovery weighted. a TR/first-echo TE, second-echo TE. b Inversion time (msec). 912 AJR:177, October 2001

MR Imaging of the Medial Collateral Ligament ursa Fig. 3. Cadaveric study. A, Coronal proton density weighted MR image (TR/TE, 2900/15) reveals superficial medial collateral ligament (MCL, short arrows), as well as meniscofemoral and meniscotibial portions of deep MCL (curved arrows). MCL bursa is not seen., Corresponding anatomic slice also shows superficial MCL (short arrows), and deep portion of MCL (curved arrows). MCL bursa is seen between superficial and deep MCLs. cluded an assessment of the size and location of the MCL bursa, as well as presence of other MR imaging findings (ligament tear, osteoarthritis, edema, and others). Criteria used for diagnosis of osteoarthritis included joint space narrowing, signal changes and ulcerations of cartilage, osteophytes, meniscal subluxation, and subchondral bone changes. The length and thickness of the MCL bursa were measured on the coronal MR image best showing the superficial portion of the MCL. On the axial MR image, the anteroposterior dimensions of the femoral and tibial compartments were measured. Results Cadaveric Study The MCL bursa was not apparent on MR images obtained from the cadaveric specimens without intrabursal contrast injection (Fig. 3). In one specimen, the tibial portion of the MCL bursa could be outlined on MR images after intrabursal injection of contrast medium. The intrabursal location of dye was shown on the anatomic slices. In another specimen, the injection was unsuccessful but the MCL bursa was shown to be present at macroscopic inspection. At macroscopic inspection of the specimens, the MCL bursa corresponded to a vertically elongated compartment located between the superficial and the deep portions of the MCL. The MCL bursa was located at the level of the middle third of the medial side of the knee (Figs. 3 and 4). A femoral component of the MCL bursa was found in five (71%) of seven specimens, whereas a tibial component was observed in all specimens. The dimensions of the MCL bursa, measured on anatomic sections, are listed in Table 2. The mediolateral dimension was not recorded in specimens because this measurement depends on the amount of fluid injected. At microscopic inspection, a thin layer of flattened mesothelial cells was seen lining both sides of the cavity between the superficial and deep MCLs (Figs. 5 and 6). Staining with epithelial membrane antigen showed uptake in this cell layer. TALE 2 A Clinical Study The patients ranged in age from 16 to 58 years (mean age, 41 years). The right knee was involved in two patients and the left knee was affected in four patients. Five patients had medial knee pain. One patient, a 33-year-old man, was asymptomatic; he was found to have an effusion in the MCL bursa in his asymptomatic knee (Fig. 7). In our institution, the contralateral knee is examined in patients undergoing MR assessment of joint injuries in the setting of lawsuits. On MR images, a femoral component of the MCL bursa was observed in four of six patients (Figs. 8 and 9), whereas a tibial component was observed in two of six patients. In one patient, both the femoral and tibial portions of the MCL bursa contained fluid. One patient had no separation between femoral and tibial compartments, and the MCL bursa in that patient spanned the joint Dimensions of the Medial Collateral Ligament ursa in Cadaveric Specimens and in Patients Cadaveric Studies No. Mean Dimensions H W (cm) Note. H = craniocaudal dimension, W = anteroposterior dimension, = mediolateral dimension. Range H W (cm) Femoral component of bursa 5 1.4 0.7 0.6 2.0 0.6 0.9 Tibial component of bursa 7 1.3 0.9 0.8 2.2 0.6 1.2 Clinical Studies No. Mean Dimensions H W (cm) Range H W (cm) Femoral component of bursa 4 1.7 1.2 0.25 1.5 2 0.6 1.8 0.2 0.3 Tibial component of bursa 2 1.7 1.4 0.2 1.5 1.8 0.6 2.1 0.2 ursa spanning the joint line 1 2.2 2.2 0.2 AJR:177, October 2001 913

De Maeseneer et al. line. The dimensions of the MCL bursa, measured on MR images of patients, are shown in Table 1. Medial osteoarthritis was seen in three of six patients with fluid confined to the MCL bursa. In three of six patients, fluid confined to the MCL bursa was the only MR imaging finding. A Fig. 4. Cadaveric study. A, Coronal T1-weighted MR image (TR/TE, 740/14) with fat saturation technique obtained after injection of gadolinium-based contrast medium mixed with dye into medial collateral ligament (MCL) bursa reveals MCL bursa (arrows)., Axial MR image also shows MCL bursa (arrows). C, Corresponding coronal anatomic slice reveals MCL bursa (arrows) deep in relation to superficial portion of MCL. Discussion rantigan and Voshell [1], in 1943, showed by their anatomic dissections that a bursa was present deep in relation to the MCL in most patients. Our observations in anatomic specimens confirmed these findings, although some variations in the location and dimensions of the bursa occurred. Often separate femoral and tibial compartments were shown, a finding that was also reported by rantigan and Voshell. The femoral component is located adjacent to the femoral cortex, whereas the tibial component is located adjacent to the tibial cortex. Histologically, the MCL bursa was lined by a single layer of mesothelial cells. Results from immunologic staining showed that these cells had an epithelial origin. oth Fig. 5. Photograph of histologic section along coronal plane of cadaveric tissue sample from medial side of knee including superficial and deep medial collateral ligaments (MCLs) shows thin layer of cells (arrowheads) along wall of MCL bursa (). (H and E, 400) findings indicate that the MCL bursa is lined by epithelial cells. ecause these cells exhibit a flattened appearance, they resemble the type of cell usually seen in the wall of ganglion cysts. On the basis of these findings, it remains uncertain whether the MCL bursa corresponds to a primary bursa that was present at birth or to a secondary bursa formed as a result of chronic friction. oth types of bursa may be lined by epithelial cells [6]. Histologic and immunohistochemical examination of a fetal specimen would likely provide the definite answer. Reported clinical findings of MCL bursitis include pain along the medial side of the knee over the MCL and the presence of a palpable nodule along the anterior edge of the femoral portion of the MCL [3, 4]. The pain may be increased by applying valgus stress to the knee. Stuttle [3] reported that patients with MCL bursitis tend to respond favorably to injections of corticosteroids in the superficial soft tissues, but not to intraarticular injections. Our findings in patients suggest that fluid confined to the MCL bursa as the single finding is extremely uncommon in a patient population undergoing MR imaging of the knee. In only three (0.1%) of 2454 MR examinations, fluid in the MCL bursa was C 914 AJR:177, October 2001

MR Imaging of the Medial Collateral Ligament ursa Fig. 6. Immunologic staining (epithelial membrane antigen) of cadaveric specimen shows granular uptake in cytoplasm of marginal cell layer (arrows), indicating epithelial origin. ( 1000) reported as the single MR imaging finding. The first of these patients had severe genu valgus deformity, the second patient had gouty arthritis, and the third patient was asymptomatic. Genu valgus has been reported previously as a cause of MCL bursitis [3, 4]. Other conditions that have been implicated as causes of MCL bursitis Fig. 7. Axial T2-weighted MR image (TR/TE, 4700/93) in 33-year-old asymptomatic man undergoing imaging in medicolegal setting shows fluid confined to medial collateral ligament bursa in a perimeniscal location (arrows). No MR evidence of meniscal tear exists. include trauma, osteophytic spurs, rheumatoid disorders, and flatfoot deformity [2 4]. MCL bursitis may also be encountered in professional athletes involved in horseback riding and motorcycling, because of the friction applied to the medial aspect of the knee (Plenevaux P, unpublished data). In this study, medial joint osteoarthritis was present in three of six patients with fluid in the MCL bursa. The fluid in the MCL bursa in these patients may be caused by the osteoarthritis, and the contribution of the fluid to the clinical symptoms may be questionable. In osteoarthritis, marginal osteophytes may impinge on the MCL and lead to inflammation and distension of the MCL bursa [3]. Our observations in cadaveric specimens indicate that the MCL bursa is not identifiable at MR imaging in the absence of a fluid effusion. When distended by fluid, however, the MCL bursa can be depicted as a vertically elongated compartment exhibiting high signal intensity on T2-weighted MR images and low signal intensity on T1-weighted MR images. On anatomic slices and MR images, the MCL bursa was shown to be located between the superficial and deep portions of the MCL. On axial anatomic slices and MR images, the anterior margin of the MCL bursa is located adjacent to the anterior edge of the superficial portion of the MCL (Fig. 2). The posterior margin of the MCL bursa is outlined by the junction between the superficial and deep portions of the MCL (Fig. 2). Our results show the compartmentlike distribution of fluid confined to the MCL bursa. These findings may be helpful in differentiating fluid in the MCL bursa from other cystic lesions located along the medial aspect of the knee. As a basic rule, a fluid collection that is located superficially, anteriorly or posteriorly with regard to the anterior superficial portion of the MCL, is unlikely to correspond to fluid in the MCL bursa (Fig. 2). The pes anserinus bursa is located inferiorly with respect to the tibial component of the MCL bursa. Ganglion cysts often show a septate and lobulated appearance and may occur in various periarticular locations; they are unlikely to be confined to the normal location of the MCL bursa [7]. Peripheral meniscal tears and meniscocapsular separation may lead to high signal intensity on T2-weighted MR images in the meniscal periphery or perimeniscal tissues [8]. However, high signal intensity in these conditions tends to be ill defined and is located in or adjacent to the meniscus. Fluid in the MCL bursa, in contradistinction, tends to be well defined and extends adjacent to the femoral and tibial cortexes. In addition, meniscal tears and meniscocapsular separation predominantly involve the posterior horn of the medial meniscus and thus are located posteriorly with respect to the normal location of the MCL bursa. Meniscal cysts represent the most realistic differential diagnostic consideration of fluid in the MCL bursa [9, 10]. Our review of imaging reports yielded 20 patients with fluid collections confined to the normal boundaries of the MCL bursa, but with an adjacent meniscal tear (Fig. 10). The differentiation of bursal fluid from a meniscal cyst remains difficult. Neither type of fluid collection is visualized at arthroscopy because of their extraarticular location. In addition, only the large meniscal cysts are surgically removed; therefore, histologic proof is seldom obtained. Meniscal cysts tend to occur in a posteromedial location, and thus posteriorly with respect to the MCL bursa, although this is not a general rule. In the case of meniscal cysts, a direct communication with a meniscal tear or area of intrameniscal degeneration may be present. Some limitations of our investigation should be considered. First, the number of specimens examined was limited and this small sample may not take into account normal anatomic variation. It might be argued that, in our investigation, injections of dye and the freezing and thawing of specimens may have created an artificial cleavage plane between the superficial and deep MCLs [11]. However, macroscopic and histologic observa- AJR:177, October 2001 915

De Maeseneer et al. tions were consistent with a preexisting compartment. Our retrospective selection of cases also represents a limitation of our study. Nevertheless, the radiologists who made the initial reports were familiar with previously described MR signs of fluid in the MCL bursa [2] and used consistent criteria. ecause our analysis was retrospective, patients with MCL Fig. 8. Coronal short tau inversion recovery weighted MR image (TR/TE, 5920/60; inversion time, 120 msec) in overweight 52-year-old man with medial knee pain and osteoarthritis shows fluid collection in femoral portion of medial collateral ligament (MCL) bursa (short arrows) located between superficial MCL (s) and meniscofemoral extension of deep MCL (d). Also note intraarticular joint fluid (long arrow). bursitis who might have been treated conservatively and not referred for MR imaging by clinicians would not have been included. In addition, clinicians may not have looked specifically for clinical signs suggestive of MCL bursitis in all patients. We did not include patients with tears of the MCL in our study, although we acknowledge that periligamentous high signal intensity may be observed on T2- weighted images in patients with proximal or distal MCL tears [12]. However, other signs of MCL tear are present in most patients and allow a correct diagnosis. In addition, patients with fluid collections confined to the typical site of the MCL bursa but with associated meniscal tears were not included in further analysis. Although several of these patients may have had MCL bursitis, we could not exclude the possibility that these collections represented meniscal cysts. A Fig. 9. 58-year-old woman with medial knee pain and osteoarthritis. A, Coronal MR image (TR/TE, 4700/93) shows fluid collection in femoral portion of medial collateral ligament (MCL) bursa (). Meniscofemoral portion of deep MCL is also seen (arrow)., Axial MR image shows MCL bursa between superficial (s) and deep (d) MCL. Note free anterior edge of MCL (e) and posterior junction (j) of superficial and deep MCL. = MCL bursa. 916 AJR:177, October 2001

MR Imaging of the Medial Collateral Ligament ursa Fig. 10. Coronal T2-weighted MR image (TR/TE, 4500/93) in 57-year-old woman with medial knee pain and medial meniscal tear (not shown) that was arthroscopically treated reveals fluid in medial collateral ligament bursa (arrows) spanning joint line. In summary, the MCL bursa is located along the middle third of the medial aspect of the knee between the superficial and deep portions of the MCL. Although commonly observed in anatomic specimens of elderly patients, MCL bursitis is infrequently found in a patient population undergoing MR imaging of the knee. Understanding the normal anatomic location of the MCL bursa on MR images may help to differentiate fluid in the MCL bursa from other conditions causing fluid collections on the medial side of the knee. Acknowledgments We thank E. roodtaerts for photographic work; K. Vanderdood for help in image interpretation; M. Pauwels for performing histologic preparations; F. Grignard and J. de Mey for assistance with injections; E. arbaix for anatomic research; and J. M. Annaert, P. Oger, and T. Scheerlinck for clinical correlations. References 1. rantigan OC, Voshell AF. The tibial collateral ligament: its function, its bursae, and its relation to the medial meniscus. J one Joint Surg Am 1943;25:121 131 2. Lee JK, Yao L. Tibial collateral ligament bursa: MR imaging. Radiology 1991;178:855 857 3. Stuttle FL. The no-name and no-fame bursa. Clin Orthop 1959;15:197 199 4. Kerlan RK, Glousman RE. Tibial collateral ligament bursitis. Am J Sports Med 1988;16:344 346 5. Warren LF, Marshall JL. The supporting structures and layers on the medial side of the knee: an anatomical analysis. J one Joint Surg Am 1979;61:56 62 6. De Haas WHD, Van Heerde P. Synovial nature of pathologic periarticular structures including subcutaneous nodules. Descent from embryonic arthrogenic fibroblasts: a hypothesis. Z Rheumatol 1979;38:318 329 7. ui-mansfield LT, Youngberg RA. Intraarticular ganglia of the knee: prevalence, presentation, etiology, and management. AJR 1997;168:123 127 8. Rubin DA, ritton CA, Towers JD, Harner CD. Are MR imaging signs of meniscocapsular separation valid? Radiology 1996;201:829 836 9. Tyson LL, Daughters TC Jr, Ryu RKN, Crues JV III. MRI appearance of meniscal cysts. Skeletal Radiol 1995;24:421 424 10. urk DL Jr, Dalinka MK, Kanal E, et al. Meniscal and ganglion cysts of the knee: MR evaluation. AJR 1988;150:331 336 11. Hodler J, Trudell D, Kang HS, Kjellin I, Resnick D. Inexpensive technique for performing magnetic resonance-pathologic correlation in cadavers. Invest Radiol 1992;27:323 325 12. Schweitzer ME, Tran D, Deely DM, Hume EL. Medial collateral ligament injuries: evaluation of multiple signs, prevalence and location of associated bone bruises, and assessment with MR imaging. Radiology 1995;194:825 829 AJR:177, October 2001 917