Musculoskeletal Imaging Original Research hun et al. MRI of Skeletal Muscle Lymphoma Musculoskeletal Imaging Original Research hang Woo hun 1 Won-Hee Jee 1 Hye Jung Park 1 Yeo Joo Kim 1 Jeong-Mi Park 1 Sang-Hoon Lee 2 Sung-Hwan Park 3 hun W, Jee WH, Park HJ, et al. Keywords:, MRI, muscle, primary DOI:10.2214/JR.09.3904 Received November 1, 2009; accepted after revision January 11, 2010. 1 Department of Radiology, Seoul St. Mary s Hospital School of Medicine, The atholic University of Korea, 505 anpo-dong, Seocho-gu, Seoul 137-701, South Korea. ddress correspondence to W. H. Jee (whjee@catholic.ac.kr). 2 Department of Radiology, san Medical enter, Seoul, Korea. 3 Department of Internal Medicine, The atholic University of Korea, Seoul, Korea. JR 2010; 195:1355 1360 0361 803X/10/1956 1355 merican Roentgen Ray Society MRI Features of Skeletal Muscle Lymphoma OJETIVE. The purpose of this study was to assess the MRI findings of skeletal muscle. MTERILS ND METHODS. MR images of pathologically proven of skeletal muscle in 20 patients were retrospectively reviewed for the presence or absence of individual imaging findings. Nine patients had primary muscle, and 11 patients had muscle metastasis from systemic. RESULTS. The initial manifestation of skeletal muscle was a muscle mass in 15 patients (75%) and abnormal muscle signal in five patients (25%). Muscle enlargement was found in all cases. Long segmental involvement with orientation of the tumor along muscle fascicles was found in 15 patients (75%). Seventeen patients (85%) had traversing vessels within involved muscles. ll of the tumors had equal to slightly increased signal compared with normal muscle on T1-weighted images and intermediate signal compared with fat on T2-weighted images. mong the 19 patients who underwent contrast-enhanced imaging, skeletal muscle exhibited diffuse homogeneous enhancement in 13 patients (68%), predominantly peripheral thick bandlike enhancement in four patients (21%), and marginal septal enhancement in two patients (11%). Thick irregular enhancement of both deep and superficial fascia was found in 16 patients (84%), and one patient (5%) had deep enhancement only. Subcutaneous stranding was found in 16 patients (80%) and skin thickening in four patients (20%). ONLUSION. Skeletal muscle has distinctive MRI features that help differentiate it from other soft-tissue tumors and tumorlike lesions. L ymphoma is a heterogeneous disease representing approximately 4% of new cases of cancer in the United States; almost all extranodal types of tissue are involved [1]. Involvement of skeletal muscle, however, is rare. Inclusion of in the differential diagnosis of soft-tissue tumors is important in relevant cases because the pathologic diagnosis can be influenced by the use of special staining procedures [2]. Unlike other malignant soft-tissue tumors, skeletal muscle responds well to chemotherapy with or without radiation therapy [3, 4]. To avoid unnecessary surgery, the correct diagnosis is required. Differentiation of skeletal muscle from various neoplastic and inflammatory diseases, however, often is difficult on the basis of clinical and imaging findings alone [5, 6]. Therefore, specific MRI findings of skeletal would be of value in differential diagnosis. Except for case reports, there have been few studies of the MRI findings of skeletal muscle [4, 7]. The purpose of our study was to assess the MRI findings of this tumor. Materials and Methods Patients This study was approved by our institutional review board and complied with HIP guidelines. The requirement for informed consent was waived for this retrospective study. search for cases of pathologically proven skeletal muscle identified 26 distinct cases from October 1995 through September 2009. ll records were reviewed for clinical, imaging, and pathologic findings. Six patients with apparent direct extension from primary of the bone were excluded because the study criteria specified tumor originating from muscle and not extension from an adjacent origin. ases of concurrent nodal or systemic disease were categorized as nonprimary muscle. JR:195, December 2010 1355
hun et al. Recurrence of previously treated was included in this category. The selected study group consisted of 20 patients (14 male patients, six female patients; mean age, 49 years; range, 5 90 years). Eleven patients with nonprimary and nine with primary of muscle were enrolled in this study. MRI MRI was performed with various 1.5-T (n = 17) and 3-T (n = 3) systems. ppropriate coils and fields of view were selected for the expected area of involvement. Fast spin-echo T2-weighted (TR/ TE, 3,000 4,900/63 112) and T1-weighted (450 1,002/10 21) images were obtained in the axial plane. Fat-suppressed fast spin-echo T2-weighted images (3,000 5,900/63 112) were obtained in at least one orthogonal plane for 13 patients. For all but one of the patients, axial and longitudinal fatsuppressed T1-weighted spin-echo images (450 1,002/10 21) were obtained after administration of 0.1 mmol/kg body weight gadopentetate dimeglumine (Magnevist, ayer Healthare). The matrix size was 192 256 512, and the number of signals averaged was 1 or 2. Evaluation of MR Images MR images of pathologically proven s of skeletal muscle were retrospectively analyzed for patterns of muscle involvement and contrast enhancement, muscle enlargement, presence of intramuscular traversing vessels, relative preservation of intramuscular fat planes, fascial involvement TLE 1: linical Information, MRI Findings, and Pathology in 20 Patients with Skeletal Muscle Lymphoma Patient No. ge (y) Sex Location Type Pattern T2-Weighted Images T1-Weighted Images T2-Weighted Fast Spin-Echo Images ontrast-enhanced T1-Weighted Images Pathologic Finding 1 60 M Thigh Primary Mass Intermediate High Hyperintense Diffuse Diffuse large -cell 2 44 M ack Primary Mass Intermediate Intermediate N/ N/ Diffuse large -cell 3 28 M ack Nonprimary Mass Intermediate Intermediate Intermediate Marginal septal naplastic large cell 4 71 M Trunk Primary Mass Intermediate Intermediate Intermediate Diffuse urkitt 5 74 F Forearm Primary bnormal signal 6 57 M Forearm Primary bnormal signal Intermediate Intermediate Hyperintense Peripheral band Natural killer T-cell, nasal type Intermediate Intermediate Hyperintense Peripheral band Natural killer T-cell, nasal type 7 53 M uttock Nonprimary Mass Intermediate Intermediate N/ Diffuse Diffuse large -cell 8 70 F Hand Primary Mass Intermediate Hyperintense N/ Diffuse Peripheral T-cell 9 55 F Forearm Nonprimary bnormal signal Intermediate Intermediate Intermediate Diffuse Mantle cell 10 70 M alf Primary Mass Intermediate Hyperintense Intermediate Peripheral band Peripheral T-cell 11 37 F Foot Primary bnormal signal Intermediate Intermediate N/ Diffuse Peripheral T-cell 12 57 M Thigh Nonprimary Mass Intermediate Hyperintense Hyperintense Marginal septal Diffuse large -cell 13 25 F Thigh Nonprimary bnormal signal Intermediate Hyperintense N/ Peripheral band Peripheral T-cell 14 80 M Thigh Nonprimary Mass Intermediate Hyperintense Intermediate Diffuse Diffuse large -cell 15 9 M ack Nonprimary Mass Intermediate Hyperintense N/ Diffuse naplastic large cell 16 5 M Thigh Nonprimary Mass Intermediate Hyperintense Hyperintense Diffuse naplastic large cell 17 90 F rm Nonprimary Mass Intermediate Intermediate Intermediate Diffuse Diffuse large -cell 18 32 M Shoulder Nonprimary Mass Intermediate Intermediate Intermediate Diffuse Diffuse large -cell 19 29 M Shoulder Primary Mass Intermediate Hyperintense Intermediate Diffuse Diffuse large -cell 20 35 M Thigh, leg Nonprimary Mass Intermediate Intermediate N/ Diffuse Diffuse large -cell Note N/ = not available. 1356 JR:195, December 2010
MRI of Skeletal Muscle Lymphoma (abnormal signal or enhancement), adjacent bone marrow involvement, and subcutaneous or cutaneous abnormalities. On T1-weighted images the reference was normal adjacent muscle with resulting hypo (signal less than that of muscle), intermediate signal (similar to that of muscle), and hyper (signal greater than that of muscle). On T2-weighted images, tumor was compared with normal fat as hypointense, of intermediate signal, and hyperintense. The images were reviewed and independently scored by two reviewers; discrepancies were resolved by consensus. Results Skeletal muscle was most commonly located in the thigh (n = 6), forearm (n = 3), and back (n = 3) (Table 1). Multicompartmental involvement was found in 14 patients (70%). The initial manifestation of skeletal muscle was a muscular mass in 15 patients (75%) (Figs. 1 and 2) and abnormal muscle signal in five patients (25%) (Figs. 3 and 4). The initial manifestation of nine of the 11 cases (82%) of systemic was a muscle mass rather than abnormal signal. Six of nine primary muscle s (67%) became evident as a muscle mass. Multiple muscle masses were found in 14 patients (70%). ll patients had enlargement of involved muscles. Long segmental involvement considered abnormal signal or contrast enhancement oriented in the direction of normal muscle fascicles was found in 15 patients (75%). Seventeen patients (85%) had intact traversing vessels within the involved muscle (Fig. 2D). Relative preservation of intramuscular fat planes was present in all patients. On T1-weighted images, all of the tumors had equal (n = 11) or slightly increased (n = 9) signal compared with normal muscle. On T2-weighted images, all lesions had intermediate signal. In 13 patients for whom fat-suppressed T2-weighted images were obtained, eight lesions (62%) had intermediate signal, and five (38%) had low signal. In the 19 patients who underwent contrast-enhanced MRI, skeletal muscle had homogeneous diffuse enhancement in 13 patients (68%) (Fig. 2), predominantly peripheral thick bandlike enhancement in four patients (21%) (Figs. 3 and 4), and marginal septal enhancement in two patients (11%) (Fig. 1). Thick irregular enhancement of both deep and superficial fascia was found in 16 patients (84%), and isolated enhancement of deep fascia was present in one patient (5%). Subcutaneous stranding was found in 16 patients (80%) and skin involvement in four patients (20%). No patient had adjacent bone marrow involvement. No discernible difference was found between 1.5-T and 3-T MRI systems with regard to signal and enhancement pattern, but only three patients underwent 3-T MRI. The results of open or needle biopsy confirmed the presence of different types of non- Hodgkin s in all patients. In our study the most common histologic variant was diffuse -cell, which is the most prevalent subtype of. No definite relation between imaging and pathologic features was noted, although two natural killer T-cell s exhibited peripheral bandlike abnormal signal rather than a mass, which may suggest the presence of an infiltrative process. Discussion Lymphoma involving skeletal muscle is rare, representing 1.5% of cases of non- Hodgkin s and 0.3% of Hodgkin s [8]. Involvement of muscle may be from systemic disease, be an extension of tous deposits in adjacent lymph nodes and bone, or, least commonly, be from a primary lesion [7, 9]. Muscle involvement most commonly is metastatic spread from adjacent lymph nodes or other primary sources, such as bone [9]. The least commonly encountered form of involving muscle is from an extranodal primary origin [2]. Soft-tissue s of various histologic types have been reported, including -cell, T-cell, and natural killer cell non-hodgkin s s and plasmacytomas. Hodgkin s is less likely to manifest a soft-tissue mass [10]. The usual clinical symptoms are local swelling and pain or systemic symptoms such as fever, sweating, and weight loss. The history can Fig. 1 28-year-old man with primary non-hodgkin s of left side of back. Images obtained with 1.5-T MRI system., xial T1-weighted MR image shows hypointense mass (arrows) in left latissimus dorsi muscle., oronal T2-weighted MR image reveals relatively homogeneous mass of intermediate signal (arrows)., oronal fat-suppressed contrast-enhanced T1-weighted MR image shows marginal septal enhancement (arrows). Long segmental involvement (arrowheads) is present along muscle fascicles. JR:195, December 2010 1357
hun et al. span from indolent to rapidly progressive [5]. Lymphoma can involve any muscle, but the sites reported most often, in order of prevalence, are the thigh, trunk, upper extremity, and leg [6], as was found in our series. Long segmental involvement was found with orientation of the tumor along muscle fascicles in 15 of our patients (75%), consistent with the findings in all six patients in a previous study by Lee et al. [7]. Muscle enlargement consistent with previous reports [4, 11, 12] was found in all of our patients. Intact vessels along the involved muscle fascicles, represented by voids of low signal or enhancing tubular vessels, were seen in 85% of the patients in our study. This finding may be due to angiogenesis or to the presence of high-flow vessels [13]. In our study, multicompartmental involvement was found in 70% of the patients with skeletal muscle, a finding also reported by Lee et al. In previous studies [5, 7, 11, 12] the reported T2-weighted signal has been conflicting for several reasons. First, the reference for comparison has varied, some investigators using muscle and others fat [7]. nother reason contributing to the disparity is different reference sequences, some investigators using conventional spin-echo T2- weighted images [7] and others using fast D Fig. 2 55-year-old woman with systemic recurrence of non-hodgkin s. Images obtained with 1.5-T MRI system., Sagittal fat-suppressed T2-weighted MR image shows diffuse long segmental mass of intermediate signal (arrows) and muscle enlargement in gastrocnemius and soleus muscles of right leg., xial T2-weighted MR image reveals muscle enlargement of intermediate signal (arrows) in soleus, gastrocnemius, and peroneal muscles with extension to flexor digitorum muscle (asterisk). Subcutaneous stranding is present., xial T1-weighted MR image shows fat planes (arrowheads) in involved muscle. D, xial fat-suppressed contrast-enhanced T1- weighted MR image shows diffuse, relatively homogeneous contrast enhancement (arrows). lso present is irregular enhancement along superficial and deep fascia (asterisks). Traversing vessels (arrowheads) are present in lesion. Subcutaneous stranding and skin thickening also are present. spin-echo T2-weighted images [4]. Furthermore, in some studies, findings on T2-weighted fat-suppressed images are described [5]. In our study, all lesions exhibited intermediate signal on T2-weighted images, a finding most consistent with those of Suresh et al. [4]. In contrast, Lee et al. [7] found that all six of their patients had high T2-weighted signal in relation to normal fat. This finding may be explained by the use of conventional spin-echo T2-weighted imaging for most of the patients. Similarly, three of 24 tumors in the study by Suresh et al. had high T2-weighted signal compared with fat. The three hyperintense lesions were 1358 JR:195, December 2010
MRI of Skeletal Muscle Lymphoma Fig. 3 57-year-old man with primary non-hodgkin s. Images obtained with 1.5-T MRI system. and, oronal T1-weighted () and fat-suppressed contrast-enhanced T1-weighted () images show long segmental involvement (arrows) in muscles of anterior and posterior compartments of left forearm., xial fat-suppressed T2-weighted image shows area of thick peripheral bandlike high signal (arrows) in involved muscles. Subcutaneous stranding is present. D, xial fat-suppressed contrast-enhanced T1- weighted image reveals thick peripheral bandlike enhancement (arrows) in involved muscles. Deep fascial enhancement, subcutaneous stranding, and skin thickening are present. found with fat-suppressed fast spin-echo T2- weighted imaging instead of nonsuppressed fast spin-echo T2-weighted imaging. In this study, the most commonly encountered pattern of contrast enhancement was diffuse, as has been reported previously [4, 11]. However, predominantly peripheral thick bandlike enhancement and deep fascial enhancement were found in 21% and 89% of the patients, respectively, findings not previously reported, to our knowledge. We assume that the enhancement pattern may be related to the infiltrative multicompartmental involvement of. We found subcutaneous stranding with or without cutaneous involvement in most of our patients, a finding similar to those in previous reports [4, 5, 7]. This finding may be explained by tous infiltration or the edematous change caused by the malignant cells [4, 5]. Most malignant muscle tumors are not commonly associated with subcutaneous and cutaneous involvement. Lymphoma is more likely to exhibit confluent lymphadenopathy, which facilitates the diagnosis [10] but was not present in our series. t MRI, the differential diagnosis of skeletal muscle encompasses a wide range of tumorous and nontumorous conditions. The features differentiating skeletal muscle from other malignant softtissue tumors are long segmental involvement of skeletal muscle, traversing vessels in the lesion, multicompartmental involvement, subcutaneous stranding, and skin thickening, which are rarely observed in other malignant tumors involving muscle. lthough two thirds of the patients had homogeneous diffuse enhancement, we found that predominantly peripheral thick bandlike enhancement or marginal septal enhancement can be observed in skeletal muscle. In particular cases with predominantly peripheral thick bandlike enhancement in the involved muscles and deep fascial enhancement, these findings can mimic necrotizing fasciitis requiring emergency surgery [14]. This study was limited by its retrospective nature and bias in that the reviewers of the MR images knew beforehand that all patients had pathologically confirmed skeletal muscle. This factor may have increased the sensitivity of detection of each MRI finding. nother limitation was that the number of cases of primary muscle was small owing to the rarity of the tumor. t MRI the involvement of skeletal muscle by can be suspected in cases of diffuse muscle enlargement with long segmental or multicompartmental involvement, deep fascial involvement, and the presence of traversing vessels in the lesion, subcutaneous stranding, and skin thickening. Skeletal muscle can exhibit peripheral thick bandlike enhancement or marginal septal enhancement in addition to the well-known finding of diffuse homogeneous contrast enhancement. D JR:195, December 2010 1359
hun et al. Fig. 4 74-year-old woman with systemic recurrence of non-hodgkin s. Images obtained with 1.5-T MRI system., oronal fat-suppressed T2-weighted image shows area of long segmental high signal (arrows) in muscles of anterior and posterior compartments of left forearm., xial fat-suppressed T2-weighted image shows area of thick peripheral bandlike high signal (arrows) in involved muscles. Subcutaneous stranding is present. and D, xial T1-weighted () and axial fat-suppressed contrast-enhanced T1-weighted (D) images reveal thick peripheral bandlike enhancement (arrows) in involved muscles. Deep fascial enhancement and skin thickening are present. D References 1. Rademaker J. Hodgkin s and non-hodgkin s s. Radiol lin North m 2007; 45:69 83 2. Metzler JP, Fleckenstein JL, Vuitch F, Frenkel EP. Skeletal muscle : MRI evaluation. Magn Reson Imaging 1992; 10:491 494 3. Hampson F, Shaw S. Response assessment in. lin Radiol 2008; 63:125 135 4. Suresh S, Saifuddin, O Donnell P. Lymphoma presenting as a musculoskeletal soft tissue mass: MRI findings in 24 cases. Eur Radiol 2008; 18:2628 2634 5. eggs I. Primary muscle. lin Radiol 1997; 52:203 212 6. Hwang S. Imaging of of the musculoskeletal system. Radiol lin North m 2008; 46:379 396 7. Lee VS, Martinez S, oleman RE. Primary muscle : clinical and imaging findings. Radiology 1997; 203:237 244 8. Komatsuda M, Nagao T, rimori S. n autopsy case of malignant associated with remarkable infiltration in skeletal muscles [in Japanese] Rinsho Ketsueki 1981; 22:891 895 9. Travis WD, anks PM, Reiman HM. Primary extranodal soft tissue of the extremities. m J Surg Pathol 1987; 11:359 366 10. O Neill JK, Devaraj V, Silver D, Sarsfield P, Stone. Extranodal s presenting as soft tissue sarcomas to a sarcoma service over a two-year period. J Plast Reconstr esthet Surg 2007; 60:646 654 11. Hosono M, Kobayashi H, Kotoura Y, Tsuboyama T, Tsutsui K, Konishi J. Involvement of muscle by malignant : MR and T appearances. J omput ssist Tomogr 1995; 19:455 459 12. Eustace S, Winalski S, McGowen, Lan H, Dorfman D. Skeletal muscle : observations at MR imaging. Skeletal Radiol 1996; 25:425 430 13. Hatem SF, Petersilge, Park JK. Musculoskeletal case of the day: of skeletal muscle. JR 1997; 169:284, 288 289 14. Seok JH, Jee WH, hun K, et al. Necrotizing fasciitis versus pyomyositis: discrimination with using MR imaging. Korean J Radiol 2009; 10:121 128 1360 JR:195, December 2010