Granulocytic Sarcoma of the Spine: MRI and Clinical Review
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1 Musculoskeletal Imaging Original Research Seok et al. MRI of Granulocytic Sarcoma of the Spine Musculoskeletal Imaging Original Research Jee Hyun Seok 1 Jeongmi Park 1 Sun Ki Kim 2 Jung Eun Choi 3 Choon-Choo Kim 4 Seok JH, Park J, Kim SK, Choi JE, Kim CC Keywords: granulocytic sarcoma, leukemia, spine DOI: /JR Received May 24, 2009; accepted after revision ugust 4, Presented at the 2009 annual meeting of the merican Roentgen Ray Society, oston, M. 1 Department of Radiology, St. Mary s Hospital, The Catholic University of Korea, 62 Youido-dong, Yongdungpo-gu, Seoul , South Korea. ddress correspondence to J. Park (jmpark@catholic.ac.kr). 2 Department of Radiology, Seoul St. Mary s Hospital, The Catholic University of Korea, Seoul, Korea. 3 Department of Radiology, St. Paul s Hospital, The Catholic University of Korea, Seoul, Korea. 4 Division of Hematology, Department of Internal Medicine, St. Mary s Hospital, The Catholic University of Korea, Seoul, Korea. JR 2010; 194: X/10/ merican Roentgen Ray Society Granulocytic Sarcoma of the Spine: MRI and Clinical Review OJECTIVE. Granulocytic sarcoma is a tumor formed by myeloid precursors at an extramedullary site. The purpose of this study was to evaluate the MRI findings and clinical manifestations in 32 cases of granulocytic sarcoma of the spine. MTERILS ND METHODS. Thirty-two patients (21 males, 11 females; mean age, 32 years) with myeloid leukemia and spinal granulocytic sarcoma were included in this study. ll of the patients underwent radiotherapy with chemotherapy, and four patients underwent surgical decompression or excisional biopsy. ll 32 patients underwent MRI of the spine; 21 patients underwent follow-up MRI. RESULTS. Nine patients had spinal granulocytic sarcoma in the initial manifestation of leukemia. The other 23 diagnoses were made during a remission or relapse period. The lumbosacral and thoracic portions of the spine were commonly involved. Twenty-seven patients had multiple or contiguous multilevel involvement. ccording to location, spinal granulocytic sarcoma was classified as epidural in the central spinal canal, epidural along the nerve course, thickening of the nerve root itself, or prevertebral. Lesions were seen as isointense on T1-weighted images and had intermediate signal intensity with homogeneous enhancement on T2-weighted images. Nine patients had complete reduction of the tumor volume, and 12 patients had partial reduction. The median survival period was 9 months, and the 1-year survival rate was 41%. CONCLUSION. Knowledge of the imaging findings of spinal granulocytic sarcoma, which consists of multiple extramedullary masses with diffuse leukemic bone marrow infiltration, can lead to early diagnosis and appropriate treatment to reduce neurologic symptoms. G ranulocytic sarcoma is a localized tumor formed by primitive myeloid cells at an extramedullary site. It is associated with myeloid leukemia and is known by other names, such as chloroma, myeloid sarcoma, and extramedullary myeloid tumor [1, 2]. The tumor was first described by urns [3] in 1811 and then called chloroma by King in 1853 because of a greenish appearance, which is caused by the presence of myeloperoxidase granules in the malignant myeloid cells. Rappaport [4] first used the term granulocytic sarcoma in Granulocytic sarcoma can involve any organ system. Commonly affected areas include the skin, bone, soft tissue of the head and neck, and lymph nodes; rarely affected areas are the heart and small intestine. Spinal epidural granulocytic sarcoma is not common, and spinal cord compression caused by a granulocytic sarcoma is even rarer [2, 5, 6]. This tumor, how- ever, is an important cause of morbidity among patients with leukemia. We describe the MRI findings and clinical manifestations of 32 cases of spinal granulocytic sarcoma. Materials and Methods Patients The ethics committees at our institution did not require informed patient consent for this study. We performed a retrospective clinical and imaging review of the cases of 32 patients (21 males, 11 females; mean age, 32 years; range, years) with spinal granulocytic sarcoma among 3,359 patients with myeloid leukemia (2,292 with acute myeloid leukemia, 1,067 chronic myeloid leukemia) at our institution from January 1998 through February The cumulative prevalence of spinal granulocytic sarcoma was 1.0% among the patients with myeloid leukemia at our hospital. Granulocytic sarcoma can develop during relapse or remission of leukemia or as the initial manifestation of a previously undiagnosed case of leu- JR:194, February
2 Seok et al. kemia. ll of the patients underwent radiotherapy combined with chemotherapy, and four patients underwent surgical decompression or excisional biopsy. Four patients with acute spinal cord compression referred from other clinics underwent surgical decompression. MRI Technique MRI of the spine was performed with one of two 1.5-T superconducting MR units (Magnetom Vision Plus, Siemens Healthcare; Signa Excite, GE Healthcare). The imaging protocols varied according to the equipment and location at which the study was performed. Unenhanced spin-echo T1-weighted images (TR/TE, /10 17) and fast spin-echo T2-weighted images (3,000 4,700/94 124) in the sagittal and axial planes were available for all patients. Contrast-enhanced T1-weighted images with fat suppression were obtained for 32 patients after IV administration of a gadolinium contrast agent. Image nalysis ll patients with granulocytic sarcoma underwent MRI of the spine before treatment, and 21 patients underwent follow-up MRI after treatment. The MR images were analyzed on high-resolution monitors (2,048 2,560 matrix, 10-bit viewable gray scale) associated with a PCS. The MR images were retrospectively reviewed by consensus of two reviewers. The reviewers were aware of the clinical diagnosis of spinal granulocytic sarcoma with leukemia. The reviewers analyzed the images to designate the extramedullary location of the spinal granulocytic sarcoma as epidural in the central spinal canal, epidural along the nerve root course reflecting dural involvement, thickening of the nerve itself (Fig. 1), or a prevertebral lesion. Other imaging features, including the level, multiplicity, signal intensity, and enhancement pattern, also were evaluated. Statistical nalysis For clinical analysis, all data were evaluated with statistical analysis software (SPSS 12.0, SPSS). The survival rate was obtained with the Kaplan-Meier method. The log-rank test was used for univariate analysis. The overall survival rates were calculated from the date of diagnosis of spinal granulocytic sarcoma until the date of last contact or death. Results Clinical Characteristics The cases of 32 patients with spinal granulocytic sarcoma were identified over the 11-year 2-month period. There were 27 cases of acute myeloid leukemia and five cases of chronic myeloid leukemia. In nine cases, granulocytic sarcoma was the initial sign of myeloid leukemia; the other 23 diagnoses were made during a remission or relapse period. Patients with spinal granulocytic sarcoma had various symptoms, including back pain (n = 9), leg pain (n = 4), numbness (n = 5), weakness (n = 3), paraplegia (n = 2), flank pain (n = 2), hip pain (n = 2), shoulder pain (n = 2), arm pain (n = 1), amydriasis (n = 1), and neurogenic bladder (n = 1). spinal granulocytic sarcoma in one patient was detected incidentally during evaluation of another soft-tissue granulocytic sarcoma, which had become evident as a left flank mass. Fig. 1 Diagram shows extramedullary locations of spinal granulocytic sarcoma: epidural in central spinal canal, epidural along nerve root course, and thickening of nerve root itself. Prevertebral lesion is not shown. Sites of Granulocytic Sarcoma In this study, granulocytic sarcoma of the spine consisted of multiple or contiguous multilevel lesions in 27 cases and as isolated solitary lesions in five cases. ll levels of the spine were affected. Granulocytic sarcoma of the spine involved the lumbosacral level most frequently (23 cases). Thoracic involvement was found in 16 cases and cervical involvement in five cases. Thoracolumbar or cervicothoracic involvement also was found. MRI showed multiple extramedullary masses and obliteration of the spinal canal with parameningeal extension mainly through the neural foramina. The extramedullary locations of spinal granulocytic sarcoma were epidural in the central spinal canal in 16 cases (Fig. 2), the prevertebral region in 13 cases (Fig. 3), epidural along the nerve root course in nine cases (Fig. 4), and thickening of the nerve root itself in six cases (Fig. 5). In one case, the lesion originated from the conus medullaris (Table 1). Imaging Characteristics ll of the granulocytic sarcomas of the spine had similar signal intensity to muscle on T1-weighted images and intermediate signal intensity on T2-weighted images (Fig. 2). Contrast enhancement was used in imaging of 30 patients, and 26 of the granulocytic sarcomas had homogeneous enhancement. huge mass with a central necrotic portion was seen in one patient. Eight of the nine cases of initial manifestation of granulocytic sarcoma exhibited diffuse leukemic bone marrow infiltration on MR images. Twelve of the 23 spinal granulocytic sarcomas found in the remission phase or relapse period of leukemia, however, exhibited no diffuse leukemic bone marrow infiltration on MR images. This finding can be explained as a regression of leukemic bone marrow abnormalities due to proper leukemia treatment such as chemotherapy (n = 3), allogenic bone marrow transplantation (n = 8), and unrelated peripheral blood stem cell transplantation (n = 1). Follow-Up During the follow-up period, 17 patients (53%) died of disease, and seven patients (22%) were alive. The other eight patients were lost to follow-up. The overall survival data on all 32 patients were a mean survival time of 42 months, median survival time of 9 months, range of months, and 1-year survival rate of 41%. The follow-up MRI examinations of 21 patients showed complete reduction of spinal granulocytic sarcoma volume in nine patients (43%) (Fig. 2). Partial reduction was found in 12 patients (57%) regardless of the follow-up bone marrow biopsy results or clinical outcome. The other 11 patients did not undergo follow-up MRI because of death or other reasons. 486 JR:194, February 2010
3 MRI of Granulocytic Sarcoma of the Spine Discussion Granulocytic sarcoma is a localized tumor composed of immature cells of the granulocytic series. s described by Novick et al. [7], granulocytic sarcoma of any organ is associated with % of cases of acute myeloid leukemia. t our institution, the prevalence of granulocytic sarcoma in any organ was 2.9% among all patients with acute and chronic myeloid leukemia. In addition, the prevalence of granulocytic sarcoma of the spine was 1.0% among all patients with acute and chronic myeloid leukemia. The association of granulocytic sarcoma with leukemia was first made by Dock [8] Fig year-old man with 16-month history of acute myeloid leukemia who reported general weakness. C, T1-weighted spin-echo (TR/TE, 616/14) (), T2-weighted fast spin-echo (4,050/94) (), and contrast-enhanced T1-weighted spin-echo (500/9) (C) axial MR images show trilobulated epidural mass in right L2 L3 neural foramen with extension into paraspinal area, right back muscle, and spinal canal, resulting in left anterior displacement of thecal sac. in 1893 and has been frequently found in patients with acute myeloid leukemia [1]. few authors, however, have reported that granulocytic sarcoma can occur with other myeloproliferative or myelodysplastic syndromes [9] and in rare instances even occurs with lymphocytic leukemia [10, 11]. t our institution, four cases of spinal granulocytic sarcoma occurred in patients with acute lymphocytic leukemia. We did not include these four cases in our series because doing so seemed debatable. Nevertheless, these four cases of spinal granulocytic sarcoma associated with acute lymphocytic leukemia had MRI manifestations similar to those associated with my eloid Fig year-old woman with initial occurrence of acute myeloid leukemia who reported flank pain., Sagittal T1- weighted spin-echo (TR/TE, 616/14) MR image shows epidural and prevertebral masses (arrows) with diffuse low signal intensity of spinal bone marrow., Follow-up sagittal T1-weighted spinecho MR image (616/14) obtained 2 months after shows no remaining mass and fatty reconversion of bone marrow due to radiation therapy. leukemia, such as multiple extramedullary masses with similar signal intensities and enhancement patterns and combined diffuse leukemic bone marrow infiltration. Granulocytic sarcoma in the absence of clinically detectable leukemia is extremely rare, and only a few granulocytic sarcomas in patients without leukemia have become evident as spinal involvement [5, 12]. ntic et al. [5] proposed that granulocytic sarcoma be treated as acute myelogenous leukemia, even in the absence of clinically detectable leukemia. In our study, all of the patients with spinal granulocytic sarcoma had leukemia. We found no case of granulocytic sarcoma in patients without leukemia. Spinal granulocytic sarcoma usually occurs outside the spinal cord or the medulla oblongata with signs of cord compression due to mass effect. However, a few cases of intramedullary or spinal cord involvement have been reported [13 15]. One patient in our study had a granulocytic sarcoma that originated from the conus medullaris. The other 31 patients had granulocytic sarcoma situated outside the spinal cord. The bone marrow is thought to be the origin of spinal granulocytic sarcoma, which migrates to extraosseous locations through the haversian canals [16, 17]. However, the site of initial deposition of leukemic masses is unclear. Some investigators believe that most deposits begin in the dura, but others consider the most probable origin the paravertebral lymph nodes. Paraspinal and intraspinal lesions also are thought to result from perivenous arachnoid spread of leukemic cells [18]. t surgery, cells are found adhering to the vertebral periosteum or the superficial layer of the dura, with rare involvement of the pia arachnoid [19]. n C JR:194, February
4 Seok et al. epidural mass in the central spinal canal or along the course of the nerve root can be explained as an initial deposition site in the dura or the pia arachnoid space. prevertebral lesion can be explained as being due to spread from a paravertebral lymph node or along the vertebral periosteum. Thickening of the nerve root itself can be explained as due to the initial deposition of the granulocytic sarcoma at the nerve fascicle itself. Discrimination between a mass along the nerve root and thickening of the nerve itself is difficult at MRI, especially in cases of large tumor volume. MRI allows some discrimination of features, however. separated or displaced normal nerve adjacent to a mass represents an epidural mass along the nerve course rather than thickening of the nerve itself (Fig. 4). Only an enlarged nerve without an epidural mass represents thickening of the nerve itself rather than an epidural mass along the nerve course (Fig. 5). Follow-up MRI can be used to determine whether a dominant remaining image Fig year-old man with 5-month history of acute myeloid leukemia who reported left thigh pain. and, T1-weighted spin-echo (TR/TE, 600/13) () and T2-weighted fast spin-echo (4,050/93) () axial MR images show tubular or ovoid mass (short arrow) with medially displaced left S2 nerve (long arrow) at left S2 S3 neural foramen level, suggesting presence of granulocytic sarcoma along nerve course adjacent to left S2 nerve. Fig year-old woman with 20-month history of acute myeloid leukemia who reported left thigh pain. and, T1-weighted spin-echo (TR/TE, 616/14) () and contrast-enhanced T1-weighted fast spin-echo (616/14) () axial MR images show only left S1 nerve thickening (arrow) without surrounding epidural lesion. feature is nerve enlargement or an epineural mass after tumor volume reduction due to treatment. In some cases of granulocytic sarcoma, however, the two locations cannot be clearly discriminated. The differential diagnosis of spinal granulocytic sarcoma includes lymphoma, metastasis, extramedullary hematopoiesis, and neurogenic tumor with extramedullary imaging features. The imaging finding of a multiple or contiguous multilevel extramedullary mass of the spine with diffuse abnormal bone marrow signal intensity helps in the initial diagnosis of granulocytic sarcoma of the spine in association with leukemia. When a solitary dumbbell-shaped mass in the intervertebral foramen with diffuse bone marrow infiltration is visualized on MR images, the presence of spinal granulocytic sarcoma can be considered. Unless evidence of diffuse bone marrow infiltration is seen on an MR image, the signal intensity of granulocytic sarcoma can be used to differentiate a granulocytic sarcoma from a neurogenic tumor. In this circumstance of mimicking a neurogenic tumor, the intermediate signal intensity (less high signal intensity) of granulocytic sarcoma on T2-weighted images is a helpful finding. Intermediate signal intensity on T2-weighted images and isointensity on T1-weighted images of spinal granulocytic sarcoma correspond with previous findings by Guermazi et al. [18] and Ooi et al. [20]. Extramedullary hematopoiesis, which refers to the location of hematopoietic elements in locations other than the bone marrow medullary space, is also a confusing MRI finding. Extramedullary hematopoiesis is seen in many conditions, including chronic anemia, blood dyscrasia such as leukemia, and as an incidental finding. limitation of this study was that there were only four pathologically proven cases; the other 28 cases were managed with radiation therapy without surgical decompression or excisional biopsy. The use of radiation therapy and adjuvant chemotherapy for extramedullary lesions relieved neurologic symptoms, but six patients died during or before therapy. The local effect of radiation therapy and chemotherapy on spinal granulocytic sarcoma is favorable as depicted on MR images after treatment. In our study, the tumor volume in all patients regressed completely or partially after local treatment. However, the 1-year overall survival rate was 41% (mean survival time, 42 months; median survival time, 9 months; range, months) despite good control of spinal granulocytic sarcoma. Therefore, the clinical outcome of spinal granulocytic sarcoma seems to depend on not local tumor response but on the patient s systemic condition or underlying hematologic disorder. n early and exact diagnosis of spinal granulocytic sarcoma with MRI evaluation facilitates appropriate treatment with radiation therapy or adjuvant chemotherapy to reduce neurologic symptoms without ineffective or unnecessary surgery. The exact location and extent of spinal granulocytic sarcoma as determined at MRI evaluation can help clinicians plan targeted radiation therapy. Increased awareness of the imaging findings of spinal granulocytic sarcomas, which are multiple extramedullary masses with diffuse leukemic bone marrow infiltration, can facilitate early diagnosis and proper treatment, minimize preventable neurologic sequelae, and improve quality of life despite a low survival rate. 488 JR:194, February 2010
5 MRI of Granulocytic Sarcoma of the Spine TLE 1: Summary of MRI Findings of Spinal Granulocytic Sarcoma Level a Finding References 1. Liu PI, Ishimaru T, McGregor DH, et al. utopsy study of granulocytic sarcoma (chloroma) in patients with myelogenous leukemia, Hiroshima Nagasaki Cancer 1973; 31: Neiman RS, arcos M, erad C, et al. Granulocytic sarcoma: a clinicopathologic study of 61 biopsied cases. Cancer 1981; 48: urns. Observations on the surgical anatomy of the head and neck, 2nd ed. Glasgow, Scotland: Wardlaw and Cunninghame, 1824: Initial Occurrence (n = 9) Remission or Relapse Period (n = 23) Cervical spine 1 4 Thoracic spine 7 9 Lumbar spine 2 6 Sacrum 3 12 Number Solitary 0 5 Multiple or contiguous multilevel 9 18 Location Epidural in central spinal canal 8 8 long the nerve root course 5 14 Nerve thickening itself 0 6 Prevertebral 4 9 Signal intensity compared with muscle Isointensity on T1-weighted images 9 23 Intermediate signal intensity on T2-weighted images 9 23 Homogeneous enhancement 7 19 Inhomogeneous enhancement 0 1 Little enhancement 0 2 Central necrosis 1 0 bnormal signal intensity in bone marrow 8 10 a Most patients had multilevel involvement, for example, lumbosacral, thoracolumbar, or cervicolumbosacral involvement. 4. Rappaport H. Tumors of the hematopoietic system. In: tlas of tumor pathology, section 3, fascicle 8. Washington, DC: rmed Forces Institute of Pathology, 1966: ntic D, Verstovsek S, Elezovic I, et al. Spinal epidural granulocytic sarcoma in non-leukemic patient. Int J Hematol 2009; 89: alleari E, Panarello S, Capello E, et al. Granulocytic sarcoma: an unusual cause of spinal cord compression. Int J Clin Oncol 2007; 12: Novick SL, Nicol TL, Fishman EK. Granulocytic sarcoma (chloroma) of the sacrum: initial manifestation of leukemia. Skeletal Radiol 1998; 27: Dock G. Chloroma and its relation to leukemia. m J Med Sci 1893; 106: Lee HS, Jeon JW, Kim JH, et al. case of granulocytic sarcoma of the brain in a patient with myelodysplastic syndrome. Korean J Intern Med 1995; 10: hn JY, Kwon SO, Shin MS, et al. Meningeal chloroma (granulocytic sarcoma) in acute lymphoblastic leukemia mimicking a falx meningioma. J Neurooncol 2002; 60: Lee SH, Park J, Hwang SK. Isolated recurrence of intracerebral granulocytic sarcoma in acute lymphoblastic leukemia: a case report. J Neurooncol 2006; 80: Shiozawa Y, Kiyokawa N, Saito M, et al. Granulocytic sarcoma of the spine in a child without bone marrow involvement: a case report and literature review. Eur J Pediatr 2005; 164: Kook H, Hwang TJ, Kang HK, et al. Spinal intramedullary granulocytic sarcoma: magnetic resonance imaging. Magn Reson Imaging 1993; 11: Sullivan MP. Leukemic infiltration of meninges and spinal nerve roots. Pediatrics 1963; 32: ng P, Virapongse C. Magnetic resonance imaging of spinal intradural granulocytic sarcoma. Magn Reson Imaging 1990; 8: Pui MH, Fletcher D, Langston JW. Granulocytic sarcoma in childhood leukemia: imaging features. Radiology 1994; 190: Fritz J, Vogel W, ares R, et al. Radiologic spectrum of extramedullary relapse of myelogenous leukemia in adults. JR 2007; 189: Guermazi, Feger C, Rousselot P, et al. Granulocytic sarcoma (chloroma): imaging findings in adults and children. JR 2002; 178: Mostafavi H, Lennarson PJ, Traynelis VC. Granulocytic sarcoma of the spine. Neurosurgery 2000; 46: Ooi GC, Chim CS, Khong PL, et al. Radiologic manifestations of granulocytic sarcoma in adult leukemia. JR 2001; 176: JR:194, February
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