Distinct Cytologic Features of Spindle Cell Lipoma
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1 CANCER CYTOPATHOLOGY 381 Distinct Cytologic Features of Spindle Cell Lipoma A Cytologic-Histologic Study with Clinical, Radiologic, Electron Microscopic, and Cytogenetic Correlations Henryk A. Domanski, M.D. 1 Birgitta Carlén, Ph.D. 1 Kjell Jonsson, M.D., Ph.D. 2 Fredrik Mertens, M.D., Ph.D. 3 Måns Åkerman, M.D., Ph.D. 1 1 Department of Pathology and Cytology, Lund University Hospital, Lund, Sweden. 2 Department of Radiology, Lund University Hospital, Lund, Sweden. 3 Department of Clinical Genetics, Lund University Hospital, Lund, Sweden. BACKGROUND. Spindle cell lipoma (SCL) is a relatively uncommon, benign tumor that usually presents in the subcutaneous fat of adult men. Although some studies have addressed the histologic findings of SCL, only a few descriptions of aspiration cytology findings have been published. The cytologic features are poorly defined, and aspirates from SCL may cause diagnostic problems, because SCL shares some features with other fatty/spindle cell or myxoid lesions, benign as well as malignant. METHODS. Twelve patients underwent fine-needle aspiration (FNA) cytology as the primary diagnostic modality before surgery. FNA findings were evaluated and correlated with histologic features. In addition, radiologic, electron microscopic, and cytogenetic findings were analyzed. The objective of this study was to determine cytologic criteria of SCL by reviewing cytologic specimens in 12 patients with SCL who underwent FNA cytology. RESULTS. All of the tumors arose in adults, and 10 tumors developed in the subcutaneous tissue of the neck, back, or shoulder girdle. Two patients presented with tumors in atypical locations; one in the tongue and one in the cheek. Cytologically, all 12 tumors were characterized by a mixture of mature adipocytes, uniform spindle cells, and collagen bundles and/or fibers in varying proportions. The presence of a myxoid matrix and of mast cells was less specific and occurred in six aspirates. CONCLUSIONS. SCL has a characteristic cytologic appearance that, together with clinical data, helps to exclude low-grade liposarcoma as well as other spindle cell and myxoid lesions. Cancer (Cancer Cytopathol) 2001;93: American Cancer Society. KEYWORDS: spindle cell lipoma, fine-needle aspiration, cytology, histology, electron microscopy, radiology. Supported by grants from the Hanna Frideborg Soderbergs Foundation for Cancer Research, H and J Forssmans Foundation for Medical Research, and the Swedish Cancer Society. Address for reprints: Henryk A. Domanski, M.D., Department of Pathology and Cytology, Lund University Hospital, S Lund, Sweden; Fax: ; henryk.domanski@pat.lu.se. Received April 6, 2001; revision received June 27, 2001; accepted July 20, Although fine-needle aspiration (FNA) cytology is a widely accepted technique for the diagnosis of tumors in different locations, experience in the aspiration of soft tissue tumors remains limited, and histology is regarded as the gold standard for the evaluation of patients with soft tissue tumors. However, centers from various parts of the world increasingly use FNA cytology as either a substitute for or a complement to surgical biopsy in the evaluation of patients with primary and recurrent and/or metastatic soft tissue tumors. 1 5 Despite the facts that lipomatous tumors are the most common soft tissue tumors and that liposarcomas are one of the most common types of soft tissue sarcoma, 6 only a few reports dealing with the FNA findings from rare benign adipose tissue tumors exist. Spindle cell lipoma (SCL) is a slowly growing, benign, solitary tumor usually arising in men ages years. This subcutaneous 2001 American Cancer Society DOI /cncr.10142
2 382 CANCER (CANCER CYTOPATHOLOGY) December 25, 2001 / Volume 93 / Number 6 tumor is located most frequently in the upper back and neck and clinically resembles ordinary lipoma. The clinical and histologic features of SCL have been described previously There are also a few reports that included electron microscopic and cytogenetic findings of SCL. 8,11 13 The cytologic features of SCL, however, are poorly defined, with only three patients described in the literature In addition, there are two series of FNA in patients with soft tissue lesions that mention SCLs, but without providing any further descriptions of their cytology. 1,17 Needle aspirates from SCL share some cytologic features with fatty/spindle cell or myxoid lesions of other origins, benign as well malignant. The differential diagnoses, thus, include benign spindle cell lesions, such as schwannomas and solitary fibrous tumors. Malignant fatty/spindle cell or myxoid tumors also occasionally may appear similar to SCL in FNA smears. The current study, to our knowledge, is the first FNA series on SCL. Our objective was to delineate the characteristic cytologic features of SCL, which may permit a confident diagnosis in smears. MATERIALS AND METHODS Records for 12 patients with SCL who underwent FNA cytology examination were obtained from the files of the Department of Pathology and Cytology, University Hospital, Lund (9 patients) and the Department of Pathology and Cytology, Central Hospital, Kristianstad (3 patients). The aspirations were performed using a syringe holder (Cameco, Täby, Sweden) with a 10-mL (Lund) or 20-mL (Kristianstad) disposable plastic syringe and needles with an outer diameter of mm. Aspirates were prepared as air-dried smears (all 12 patients) or fixed in 95% ethanol (7 patients), and May Grünwald Giemsa or hematoxylin and eosin (H & E) stains were applied, respectively. Histologic sections for routine evaluation were stained with H & E. Immunostains for CD34, S-100, and bcl-2 were performed on all histologic material. One patient was examined preoperatively by magnetic resonance imaging (MRI), including examination after intravenous injection of Gadodiamide. Material for electron microscopy (EM) was obtained by FNA in two patients and from excised fresh tumor tissue in two patients. The aspirates and fresh tumor tissues were fixed immediately in 2% glutaraldehyde, postfixed in 1% osmium tetroxide, dehydrated in graded ethanol, and embedded in Agar 100 resin. Ultrathin sections were stained with uranyl acetate and lead citrate and examined in a Philips CM 10 electron microscope at 60 kv. Fresh tumor biopsies were obtained from excised tumors for cytogenetic analysis from seven patients. Short-term cell culturing and preparation and analysis of metaphase chromosome spreads were performed as described previously. 13 Karyotypes were described according to the International System for Human Cytogenetic Nomenclature (1995). 18 Cytologic specimens were compared with the histology of the excised specimen in all patients. Twelve microscopic features of SCL were evaluated in smears and related to the histologic findings of SCL described in previous reports. Clinical information was obtained from the medical records or referring clinicians. RESULTS Clinical Data The patients included 10 men and 2 women ranging in age from 27 years to 75 years. The tumor locations were the neck in eight patients, the back in one patient, the shoulder girdle in one patient, the cheek in one patient, and the tongue in one patient. The greatest dimension of the lesions ranged from 1.5 cm to 4.5 cm. MRI examination performed preoperatively with and without intravenous contrast injection on one patient (Patient 11) disclosed a relatively well-defined lesion measuring 29 mm 10 mm 20 mm located in the subcutaneous fat in the midline of the lower thoracic spine. The lesion had MRI characteristics of a nonfatty tumor (Fig. 1). The composition of the FNA smears, together with the typical tumor location, allowed a diagnosis of SCL in seven patients. Two of these patients were referred to us for a second opinion before surgery and originally were diagnosed with myxoid liposarcoma and suspected myxoid liposarcoma, respectively. In three patients, the cytologic diagnoses were benign soft tissue lesion/tumor, whereas, in two patients, the FNA diagnoses were fibrolipoma and low-grade myxofibrosarcoma (MFS) versus myxoid SCL, respectively. Histologic sections of excised tumors had been diagnosed as SCL in 10 patients before review. One tumor labeled as a spindle cell/pleomorphic lipoma appeared histologically as a classic SCL with focal occurrence of floret cells. One patient who was referred to us for a second opinion was diagnosed originally as suspicious of myxoid liposarcoma, and one patient had an extremely myxoid SCL that was diagnosed in our institution was labeled as a low-grade or benign myxoid tumor of uncertain biologic potential. Follow-up information was available for all patients. Follow-up was between 8 months and 15 years. No recurrences were seen. The clinical data and primary cytologic diagnoses are summarized in Table 1.
3 FNA of Spindle Cell Lipoma/Domanski et al. 383 FIGURE 1. Spindle cell lipoma (SCL) has the magnetic resonance imaging characteristics of a nonfatty tumor. (A) A T1-weighted sequence reveals a lesion with low signal intensity in contrast to the subcutaneous fat. (B) With a sagittal short time inversion recovery (STIR) sequence, the lesion has higher signal intensity than the subcutaneous fat. (C) Axial view after intravenous injection of Gadodiamide. There is increased signal intensity with thin streaks of nonenhancing material. Cytologic Features The cytologic findings are summarized in Table 2. In FNA smears, all 12 tumors were characterized by a mixture of mature adipocytes, uniform spindle cells, and collagen fibers in varying proportions. The cytologic specimens from 10 patients showed spindle cells in cohesive groups as well as scattered single cells. In two patients with a sparse spindle cell component, only scattered spindle cells were observed. The spindle cells had pale and poorly defined cytoplasm. The nuclei were fusiform or ovoid and basophilic with a mild anisokaryosis and occasionally somewhat irregular borders, nuclear grooves, and inconspicuous nucleoli. In Patient 11, however, some spindle cells with irregular, moderately pleomorphic nuclei without hyperchromasia, coarse chromatin, or mitoses were observed in both FNA smears and histologic sections (Fig. 2). In Patient 12, in addition to spindle cells, cells with enlarged nuclei occasionally of floret type were seen. No mitotic activity was seen in any of the patients. Mature fat cells and collagen bundles/fibers were seen in all aspirates. Although the wavy collagen bundles in histologic sections usually were short and stubby, the collagen occurred also as small, long, and brightly eosinophilic (H & E-stained) fibers in the cytologic smears (Fig. 3). Mast cells were found in six aspirates. The occurrence of mast cells in cytologic smears corresponded strongly with myxoid changes observed in the aspirates (Fig. 4). In four aspirates, small or middle-sized capillaries were observed, usually together with fragments of tumor tissue containing a mixture of adipocytes, spindle cells, and collagen. In Patient 11, aspiration smears appeared with multiple cohesive fragments of spindle cells with wavy/spindle nuclei and faint nuclear palisading resembling neurogenic tumors (Fig. 2). The presence of fat and collagen fibers helped to exclude neurilemmoma in this patient. Histologic Features In general, the histologic findings in SCL correlated well with these found in the cytologic smears. In particular, the proportions of spindle cells, adipocytes, and collagen fibers in the FNA smears corresponded well with those seen in the histologic sections in most of the patients (Figs. 2, 3, 5). The absence of nuclear pleomorphism, lipoblasts, and mitoses in spindle cells and fatty components corresponded well with histology in 10 patients. Moderately pleomorphic spindle cells, as described above, were seen occasionally in
4 384 CANCER (CANCER CYTOPATHOLOGY) December 25, 2001 / Volume 93 / Number 6 TABLE 1 Clinical Data and Fine-Needle Aspiration Diagnosis in 12 Patients with Spindle Cell Lipoma Patient Age (yrs) Gender Location Size (cm) Clinical data Clinical diagnosis FNA diagnosis 1 73 F Cheek 3.0 Submucosal, polyp-like tumor, 2 months duration Salivary gland tumor Benign soft tissue tumor 2 71 F Tongue a 1.0 Submucosal tumor, 1 yr duration Fibroma? Inflammatory tumor? Benign soft tissue tumor 3 33 M Neck 2,0 Subcutaneous, hard, mobile tumor, 2 yrs duration No clinical diagnosis SCL 4 51 M Neck 1,5 Subcutaneous hard, elastic tumor with long duration No clinical diagnosis SCL b 5 63 M Neck 3.0 Subcutaneous, hard, tender tumor, some yrs Lymphadenitis Benign soft tissue tumor duration 6 74 M Neck 2.0 Subcutaneous tumor, several yrs duration Epidermoid cyst? Schwannoma? Benign lesion, fibrolipoma? 7 53 M Neck 4.0 Subcutaneous, elastic, mobile tumor, 1 yr duration No clinical diagnosis SCL 8 52 M Back 2.0 Subcutaneous, soft tumor, some months duration No clinical diagnosis Low-grade MFS vs. myxoid SCL 9 27 M Shoulder 4.0 Subcutaneous, soft tumor, 1 yr duration No clinical diagnosis SCL M Neck 1.5 Subcutaneous, soft tumor Lipoma? Lymph node? SCL? b M Neck 3.0 Subcutaneous, soft tumor, 2 yrs duration Lipoma SCL M Neck 4.5 Subcutaneous, elastic tumor, several yrs duration Lipoma SCL vs. pleomorphic lipoma FNA: fine-needle aspiration; F: female; M: male; SCL: spindle cell lipoma; MFS: myxofibrosarcoma. a Previously reported by Domanski and Åkerman. 29 b FNA smears from Patients 4 and 10 were sent to Lund University Hospital with suspected myxoid liposarcomas. TABLE 2 Cytologic Findings in 12 Patients with Spindle Cell Lipoma Patient Cellularity Spindle cells Adipocytes Mast cells Inflammatory cells Collagenous fibers Blood vessels Myxoid matrix 1 Sparse 2 Moderate 3 Rich 4 Rich 5 Sparse 6 Rich 7 Rich 8 Rich 9 Rich 10 Rich 11 Rich 12 Rich : Absent, present; : scanty; : moderate; : abundant. the smears of Patient 11 as well as in histologic sections (Fig. 2). Patient 12 showed focal floret cells in cytologic smears and in histologic sections. In addition to the usual features of SCL, some small areas mimicking pleomorphic lipoma were found. Rare mitotic figures were identified in these areas of histologic sections. Mast cells, which are another typical component of SCL, were observed in the histologic sections from all 12 patients. In smears, mast cells were found in only six patients: These patients also showed a myxoid matrix in the background. The myxoid changes in these patients were even more prominent in the histologic slides. Immunohistochemical examination of the resected specimens showed clearly positive CD34 staining in the spindle cell component in all patients. Positivity for bcl-2 in spindle cells also was observed in all patients. In some of patients, however, the bcl-2 immunostaining was positive only focally and with variable intensity and sometimes was very weak. EM and Cytogenetic Findings Four samples from three patients (Patients 7, 10, and 12) were examined in the electron microscope (Fig. 6). All four showed striking similarities with spindleshaped cells, some with cytoplasmic projections, set in
5 FNA of Spindle Cell Lipoma/Domanski et al. 385 FIGURE 2. Patient 11: (A) Fine-needle aspiration biopsy smears containing cohesive fragments of cells with spindle/wavy nuclei resembling those of neurilemmoma (hematoxylin and eosin [H & E] stain; original magnification, 25). (B) High-power view with some anisokaryosis and occasional inconspicuous nucleoli (H & E stain; original magnification, 200). (C) A corresponding histologic section (H & E stain; original magnification, 100). a stroma comprised of collagen and finely granular, mucoid material. The nuclei were elongated and often had a narrow, deep cleft. The nuclei had a thick, fibrous lamina adjacent to the inner membrane of the nuclear envelope. The cytoplasm was sparse to moderate and contained rough endoplasmatic reticulum, bundles of vimentin filaments, mitochondria, and a well-developed Golgi apparatus. Small, nonmembrane-bound lipid droplets were noticed in some of the spindle cells. Along the cell membrane, pinocytic vesicles were observed, and beneath were remnants of basement membrane. More often, however, flucculant material coated the cells. Mast cells were seen near the spindle cells. Cytogenetic analysis showed a normal karyotype in two patients. The remaining five investigated tumors had clonal chromosomal rearrangements, with all patients sharing loss of 13q material: Four patients displayed loss of the entire chromosome 13, and one patient had an interstitial deletion of bands 13q12 13 (Fig. 7). DISCUSSION Although lipomatous tumors are the most common soft tissue tumors and probably the most frequent tumors examined by FNA, experience in the aspiration of rare benign lipomatous tumors, such as SCL or pleomorphic lipoma and chondroid lipoma, remains limited. 14,15,19,20 The differentiation of rare benign lipomatous tumors from their malignant counterparts or from other soft tissue tumors may cause diagnostic dilemmas both in cytologic smears and in histologic sections. SCL is a relatively uncommon benign tumor, accounting for approximately 1.5% of all lipomatous tumors. 8 It frequently displays a distinct histologic and immunohistochemical pattern that, together with a typical clinical presentation, allows a correct diagnosis. Furthermore, cytogenetic analysis has shown that SCL cells have characteristic karyotypic aberrations, notably, loss of material from the long arms of chromosomes 13 and 16. Thus, at the chromosome level, SCL shares some features with pleomorphic lipoma but is distinct from other types of benign and malignant adipose tissue tumors. 13 The three major histologic components of SCL are mature adipocytes, uniform spindle cells, and bundles of collagen. These components also were observed in all smears of SCL in the current study. The main reason that SCL may be difficult to distinguish from cytologic smears is that, similar to histologic sections,
6 386 CANCER (CANCER CYTOPATHOLOGY) December 25, 2001 / Volume 93 / Number 6 FIGURE 4. Patient 8: Mast cells were easy to find in air-dried and May Grünwald Giemsa (MGG)-stained smears of myxoid spindle cell lipoma (MGG stain; original magnification, 200). FIGURE 3. Patient 9: (A) Wavy collagen fibers are appreciated better in wet fixed smears (hematoxylin and eosin [H & E] stain; original magnification, 100). (B) A corresponding histologic section (H & E stain; original magnification, 50). they may show considerable variation in the proportion of each of these three components. In addition, a prominent myxoid matrix is seen occasionally that makes it difficult to differentiate SCL from other myxoid lesions (Fig. 8). FNA of SCL with a predominance of spindle cells may closely resemble the aspirate appearance of neurilemmoma. One previous study described two SCLs that were examined by FNA and diagnosed cytologically as benign neurogenic tumors. 1 FNA of neurilemmoma often shows a distinct cytologic pattern of cohesive sheets and dissociated spindle cells with a metachromatic and fibrillar background matrix. Absence of fat and immunostaining negative for CD34 and positive for S-100 helps to differentiate this lesion from SCL. Other spindle cell lesions, such as dermatofibrosarcoma protuberans (DFSP) or solitary fibrous tumor (SFT), with their relatively uniform spindle cells and an immunopositivity for CD34, 21 also should be included as differential diagnoses in predominantly spindle cell smears. Lack of fatty and collagenous components as well as rare mitoses in cytologic smears of DFSP help to differentiate this tumor from SCL. Cytologic features of extrapleural SFT are poorly defined. In our experience, FNA of SFT shows cellular smears with mostly cohesive sheets and clusters or dissociated spindle cells with absent or moderate nuclear atypia and occasional mitoses. The cell clusters show a collagenous matrix, and the smears do not contain fat cells or fragments of fat tissue. SCL with marked myxoid changes sometimes may be confused with myxoid liposarcoma as well as MFS. Myxoid liposarcoma, however, usually is deep-seated and shows delicate, branching blood vessels that, together with lipoblasts, help to make a correct diagnosis. 22 In our series of aspirates, for one patient, we had difficulties in both FNA and histologic sections differentiating myxoid SCL from low-grade MFS. FNA smears of MFS may be difficult to distinguish from SCL due to myxoid matrix and absence of prominent atypia in the spindle cell component. Benign fat from outside the tumor can be aspirated inadvertently. Thus, the presence of fat cells in SCL is not always helpful in the exclusion of low-grade MFS. 23 The presence of collagen bundles as well as ancillary studies, mainly immunocytochemical studies with CD-34, bcl-2, 21,24 and EM examination of aspirated material, also can be helpful in the differentiation of SCL from MFS and other myxoid lesions. Occasional anisokaryosis among spindle cells (Patients 11 and 12 in our study), together with a cellular fatty component, may cause difficulties in excluding atypical lipoma or low-grade sclerosing/lipoma-like liposarcoma in FNA
7 FNA of Spindle Cell Lipoma/Domanski et al. 387 FIGURE 5. Examples of myxoid change in spindle cell lipoma (SCL; Patient 7). Low-power view (A) and high-power view (B) of smears from an SCL with myxoid matrix, scanty adipocytic component, and relatively uniform spindle cells (May Grünwald Giemsa stain; original magnification, 50 in A and 200 in B). (C) A corresponding histologic section (hematoxylin and eosin stain; original magnification, 50). FIGURE 6. Patient 7: (A) Ultrastructural studies revealed spindle cells, some with cytoplasmic projections, and mast cells in a myxoid stroma (original magnification, 1450). (B) Photomicrograph showing a nonmembrane-bound lipid droplet (original magnification, 21,000). (C) Photomicrograph showing foci of basement membrane and surface pinocytotic vesicles (original magnification, 28,500).
8 388 CANCER (CANCER CYTOPATHOLOGY) December 25, 2001 / Volume 93 / Number 6 FIGURE 7. Karyogram from subclone of Patient 7: 46,X,tas(Y;21)(p11;p13),t(4; 6)(q25;p23),der(11)t(11;13)(p15;q14),del (13)(q12 13). FIGURE 8. Patient 12: Fine-needle aspiration (FNA) biopsy of a myxoid spindle cell lipoma mimics FNA biopsy of myxoid liposarcoma but lacks the characteristic branching capillary vessels (May Grünwald Giemsa stain; original magnification, 50). of SCL. Adequate clinical/radiologic data, therefore, are important, because the typical anatomic seating and superficial location of SCL help to exclude other lipomatous tumors. Only a few reports of MRI findings in patients with SCL are available, and these describe varying appearances. In one report, a lobulated, fatty mass with low signal septations between the lobules was seen. 25 In two patients, 26,27 the tumor was comprised mainly of septated fat, whereas central areas had a nonfatty appearance. In one of these patients, 26 there was a heterogeneous enhancement after intravenous contrast medium injection. A fourth patient 27 had a tumor in the orbit that was described as a noncalcified mass that did not enhance. That report was illustrated with an MRI (without mentioning the sequence; probably a T2-weighted image) that showed a mass in the right orbit with a lower signal intensity than the surrounding fat. The lesion in our patient had an entirely nonfatty appearance on the MRI examination. Thus, the MRI appearance of SCL can vary from completely nonfatty to heterogeneous and lipoma-like. Therefore, the MRI examination is good for localizing and evaluating the extent of the lesion but is of little help in establishing a specific diagnosis. Some attention has been paid to the origin of the spindle cells in SCL. In previous reports, it was believed that these cells arose from an early lipoblast lineage. 7,8 In EM examination of the tumors from our patients, spindle cells showed some features of fibroblasts, although some of these cells contained nonmembrane-bound lipid droplets, suggesting a prelipoblastic nature of spindle cells. This study represents the first analysis of a series of SCLs examined preoperatively by FNA. The most common elements in smears of SCL were benign adipocytes and benign uniform spindle cells, which were dissociated or arranged in fascicles. These two elements were mixed in variable proportions with collagenous fibers and occasionally also with myxoid material and mast cells. It is important to emphasize, however, that, although the collagenous bundles usually are short and blunt in histologic slides, in cytologic smears, they may be long and slender. Another interesting difference between the cytologic and histologic appearances of SCL was the occurrence of mast cells, which were found in all of 12 histologic
9 FNA of Spindle Cell Lipoma/Domanski et al. 389 sections but in only 6 of 12 smears. Only the aspirates that had a myxoid background contained mast cells. This study showed that the cytologic features of SCL can be as characteristic as the histologic and cytogenetic features. When these characteristics are present in smears from a patient with a subcutaneous lesion in a location typical for SCL, other fatty or spindle cell entities can be ruled out preoperatively with confidence. In patients with tumors in atypical locations, however, even aspirates that contain all of the characteristic elements may be difficult to diagnose as SCL. In such patients, the possibility of SCL can be raised or, at least, the diagnosis of malignant tumor can be excluded. REFERENCES 1. Maitra A, Ashfaq R, Saboorian MH, Lindberg G, Gokasian ST. The role of fine-needle aspiration biopsy in the primary diagnosis of mesenchymal lesions. A community hospitalbased experience. 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