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ORIGINAL ARTICLE Table of Contents  
Ahead of print publication
Categorizing malignant small round cell tumors in aspiration cytology: An institutional experience

 Department of Pathology, Institute of Medical Sciences and SUM Hospital, Bhubaneswar, Odisha, India

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Date of Submission10-Jul-2021
Date of Decision30-Dec-2021
Date of Acceptance21-Jan-2022
Date of Web Publication05-Jan-2023


Aim and Objectives: The study aims to categorize malignant small round cell tumors (MSRCTs) originating in various sites of the body with the objective of utilization of cytomorphological features and ancillary techniques. Study Design: It is a cross-sectional study conducted over a time span of 3 years (2017–2020). 33 cases of tumors with round cell morphology were evaluated by fine needle aspiration cytology (FNAC). Materials and Methods: The application of cell block preparation supported by immunohistochemistry aided in the categorization of 23 cases with definite diagnosis and the rest were reported as MSRCTs. Results: Among the categorized 23/33 cases, the most common diagnosis was Ewing's sarcoma (7/23) followed by 6 cases of lymphoma. There were 2 cases each of rhabdomyosarcoma and Langerhans cell histiocytosis (LCH) and 1 case each of neuroblastoma, desmoplastic small round cell tumor (DSRCT), myeloid sarcoma, neuroendocrine tumor of pancreas, plasmacytoma, and small cell carcinoma. Histopathology confirmation was available in 24/33 cases. Among the categorized tumors (23/33), biopsy correlation was available in 19 cases, of which concordant result was seen in 17 cases (89.47%), which were 6 cases of lymphoma, 5 cases of Ewing's sarcoma (EWS), 2 of rhabdomyosarcoma, and 1 each of neuroblastoma, small cell carcinoma, DSRCT, and LCH. Discordant result was seen in one case of rhabdomyosarcoma and a case of synovial sarcoma reported as extraskeletal EWS in cytology. Out of the uncategorized cases reported as MSRTCs, histopathology was available in 5 cases which were diagnosed as rhabdomyosarcoma (1 cases), lymphoma (1 case), amelanotic melanoma (1 case), and extraskeletal EWS (2 cases). Conclusion: Categorization of MSRCTs should be done to implement appropriate therapeutic protocol. FNAC provides a rapid diagnosis contributing immensely for the timely management of the patient. Detailed cytomorphological evaluation serves as a guide for further evaluation by ancillary techniques leading to definitive diagnosis.

Keywords: Cell block, Ewing's sarcoma, immunocytochemistry, lymphoma, round cell tumor

How to cite this URL:
Sahoo N, Ghosh U, Mohapatra D, Dehuri P. Categorizing malignant small round cell tumors in aspiration cytology: An institutional experience. J Microsc Ultrastruct [Epub ahead of print] [cited 2023 Feb 8]. Available from: https://www.jmau.org/preprintarticle.asp?id=362493

  Introduction Top

Malignant small round cell tumors (MSRCTs) are a heterogenous group of morphologically similar neoplasms with variable histogenesis and biological behavior. These tumors are comprised of small, round, relatively undifferentiated cells having size slightly larger than or double the size of RBCs in air-dried smears or measure <10 μm in diameter in alcohol fixed smears and have scanty cytoplasm.[1] The tumors that are included in this category are Ewing's Sarcoma/primitive neuroectodermal tumor (EWS/PNET), neuroblastoma, non Hodgkin lymphoma (NHL), small cell osteosarcoma, mesenchymal chondrosarcoma, poorly differentiated (round cell) synovial sarcoma, desmoplastic small round cell tumor (DSRCT), Langerhans cell histiocytosis (LCH), myeloid sarcoma, and carcinomas like small cell and neuroendocrine tumors.[2],[3] Fine needle aspiration cytology (FNAC) is a safe and cost-effective technique for diagnosing these tumors depending on the cellularity, morphology, arrangement of cells, and the background.[4],[5],[6] However, it plays a diagnostic challenge to the cytopathologists for proper categorization of these tumors, especially with limited aspirate or in cases of poorly/undifferentiated morphology. To implement appropriate therapeutic protocol, an accurate diagnosis is required for these tumors and imprecise diagnosis such as MSRCT should be strongly discouraged.

Hence, the aim of our study is to categorize MSRCTs. The objective is to analyze the cytomorphological features of various subtypes of MSRCTs and categorize them depending on the morphology and results of ancillary techniques like special stain, immunocytochemistry (ICC), cell block, and immunohistochemistry (IHC).

  Materials and Methods Top

This is a hospital-based cross-sectional study including cases diagnosed as MSRCT in FNAC during the time period from July 2017 to July 2020. The clinical details such as age, sex, size, site, and prior treatment history were recorded from the hospital archival. After taking detailed history and obtaining informed consent from the patient or patient's kin, FNAC was performed by nonaspiration and aspiration technique using 22-gauze needles. The nonaspiration technique or needling was preferred in the pediatric age group as it was performed without the aspirator and negative pressure, thus causing minimum pain and discomfort to the patient. For deep seated lesions or where direct aspiration did not yield diagnostic material, image-guided aspiration was done. Smears were stained by Diff-Quik, hematoxylin and eosin (HE), and Papanicolaou stain. Additional samples were obtained, wherever possible, for ICC or to make cell block. Cell blocks were prepared using plasma–thrombin method. The cytology slides were examined, and wherever available, its corresponding histopathology slides/cell block sections and blocks were also retrieved.

For ICC, the wet-fixed smears or alcohol-fixed stained slides after decolorization were used. For decolorization, the slides were put on 1% acid alcohol solution. ICC was performed by manual method by standard horse radish peroxidase technique and the antibodies used were CD99 (MIC2Geneproduct, RTU; DAKO), desmin (EP15, RTU; PathnSitu), MyoD1 (EP212, RTU; PathnSitu), leukocyte common antigen (LCA) (2B11 + PD7/26, RTU; PathnSitu), and NSE (ENO2/1462, RTU; PathnSitu).

For cell block preparation, the aspirated material was taken in normal saline and centrifuged at 2500 rpm for 15 min. After discarding the supernatant, the cell pellet was mixed with 2 drops of thromboplastin and 2 drops of pooled plasma. After clot formation, the pellet was fixed in 10% neutral buffered formalin and taken for routine histopathological processing and staining. Special stains such as periodic acid–Schiff (PAS), PAS with diastase, and myeloperoxidase (MPO) were done wherever necessary. Histopathology slides were examined in cases where biopsy was done. According to the clinical, cytological, and histological features, immunohistochemical panels were decided. The antibodies used were Pan cytokeratin (CK), CD99, vimentin, epithelial membrane antigen, LCA, desmin, MyoD1, S100, CD68, CD1a, Langerin, synaptophysin, chromogranin, and Ki 67.

Ethical clearance was obtained for the study from the institutional ethical committee. IRB Board name – Institutional Ethical Committee,Institute of Medical sciences and SUM Hospital, Siksha ' O 'Anusandhan University. Date of approval – 9.7.21.

  Results Top

A total of 33 cases of MSRCTs were diagnosed during this period, out of which 25 were male and 8 were female, with a male-to-female sex ratio of approximately 3:1. The age group ranged from 3 to 72 years. The lower extremity was most commonly aspirated with thigh being the most common site. While presentation of 7/33 cases was metastatic/recurrent, the rest 26/33 cases were primary.

Out of 33 cases, exact subtyping of the tumors could be done in 23 cases. Among the 23 cases, 15 cases could be categorized on the basis of cytomorphology with history and cytochemical stains and 7 more cases were categorized using ICC. One more case was categorized with cell block technique and IHC [Table 1]. Out of the 23 cases, the most common diagnosis was EWS (both skeletal and extraskeletal) (7/23), followed by 6 cases of lymphoma, 2 cases of rhabdomyosarcoma, 2 cases of LCH, and 1 case each of neuroblastoma, DSRCT, myeloid sarcoma, neuroendocrine tumor of pancreas, and small cell carcinoma. Furthermore, one case of plasmacytoma was diagnosed, showing a monotonous population of discretely lying plasmacytoid cells with unevenly clumped chromatin and few cells with binucleation. Ten cases that could not be subcategorized in cytology were reported as MSRCT [Table 2].
Table 1: Distribution of cases

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Table 2: Cytomorphological evaluation of categorized cases (n=23)

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Histopathology confirmation was available in 24/33 cases. Among the categorized tumors (23/33), histopathology was available in 19 cases, of which concordant result was seen in 17 cases (89.47%). The concordant cases were 6 cases of lymphoma, 5 cases of EWS, 2 cases of rhabdomyosarcoma, one case of neuroblastoma, one case of small cell carcinoma, one case of DSRCT, and one case of LCH. Discordant result was seen in 2 cases and one each of rhabdomyosarcoma and of synovial sarcoma reported as extraskeletal EWS in cytology [Table 3]. Out of the uncategorized cases reported as MSRTCs, histopathology was available in 5 cases, reported as rhabdomyosarcoma (1 cases), lymphoma (1 case), amelanotic melanoma (1 case), and extraskeletal EWS (2 cases).
Table 3: Cases with fine needle aspiration cytology and histopathological diagnosis (n=24)

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  Discussion Top

FNAC is a safe and cost-effective technique in diagnosing these tumors depending on the cellularity, morphology, arrangement of cells, and the background.[4],[5],[6] However, it poses a diagnostic challenge to the cytopathologists for proper categorization of these tumors, especially with limited aspirate or in cases of poorly/undifferentiated morphology. Histopathology is recognized as the gold standard method for the evaluation of all tumors, and open surgical or transcutaneous image-guided core needle biopsies have been used to obtain material from the primary or metastatic lesional site.[5],[7] Open surgical biopsy is a troublesome one and it usually delays chemotherapy. Although core needle biopsy is a safer method with high sensitivity (90%) and low morbidity (<5%), spread of tumor through the needle track is one of the disadvantages.[8] In the current era, the material obtained from FNAC can be used for further ancillary diagnostic tests. Needle aspiration is a successful diagnostic tool for documenting primary and recurrent MSRCTs, especially in inoperable cases when chemotherapy and/or radiotherapy are the only modality of treatment. Characteristic cytomorphology may be observed in 70%–80% cases of MRCTS, and further diagnosis of the remaining cases is aided by ancillary techniques.[9] A definite diagnosis based on clinical and cytomorphological criteria was possible in 57% to even 90% or greater in some series.[4],[5],[6],[9] In comparison, in our study, with only history and cytomorphology, 45.45% of tumors could be subcategorized, while with ancillary techniques, 69.7% of tumors were subcategorized. Out of the categorized cases, concordant result with histopathology was observed in 89.47% of cases.

EWS/PNET is a family of MSRCTs exhibiting neuroepithelial differentiation. Because of their similar histogenetic, cytogenetic, and immunohistochemical features, the term EWS family of tumors is used for typical and atypical EWS and PNET of bone and soft tissue.[10],[11] EWS is the most undifferentiated and primitive type, while PNET is intermediately differentiated, but both have a similar modality of treatment and prognosis.[12] The cytological features of EWS/PNET include malignant cells with a high N/C ratio, hyperchromatic nuclei without prominent nucleoli, distinctively smooth nuclear membrane contour, finely granular chromatin, one or two small nucleoli, and scant cytoplasm with perinuclear clearing, suggesting epithelial differentiation. Few subtle differentiating points in favor of PNET are coarse nuclear chromatin, absence of cytoplasmic clear vacuoles, nuclear molding, unipolar cytoplasmic tags, and Homer–Wright rosettes.[12] In our study, we got 7 cases reported as EWS/PNET, while 2 cases were uncategorized as RCTs which were later confirmed as EWS/PNET in histopathological study. 5 cases showed two population of cells larger chief cells and smaller dark cells [Figure 1]a. Cytoplasmic vacuolations were observed in in 5 cases which were positive for PAS stain [Figure 1]b and [Figure 1]c.. Rosette and molding of nuclei were noted in 4 cases [Figure 1]d. One case also displayed perivascular rosettes [Figure 1]e. 6 cases showed CD 99 positivity by immunocytochemistry [Figure 1]f. Basement membrane like matrix material was seen in 3 cases. Along with clusters, discretely lying cells were present in all cases, except one case which demonstrated exclusively singly lying cells.
Figure 1: (Cases of Ewing's sarcoma/primitive neuroectodermal tumor): Two type of cell populations (a) (Diff Quik, ×400), Cytoplasmic vacuolation (b) (Diff Quik, ×400), PAS positive (c) (×200), Rosettes with nuclear molding (d) (Diff Quik, ×400), Perivascular rosettes (e) (Diff Quik, ×400), CD99 positive (f) (DAB, ×200)

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Neuroblastic tumors (NTs) are the most common extracranial solid nonlymphoreticular malignancy of childhood, originating from primordial neural crest cells that are related to the sympathetic nervous system.[13],[14] Depending on the degree of maturation, these tumors are divided into three types, i.e., neuroblastoma, ganglioneuroblastoma, and ganglioneuroma; of which, ganglioneuroma is benign, while the rest two are malignant with neuroblastic component.[15],[16] The immature neuroblastic component is composed of small round cells with high nucleocytoplasmic ratio, while large cells having abundant eosinophilic cytoplasm, large eccentric nuclei, and prominent nucleoli are mature ganglion cells. The poorly differentiated and undifferentiated neuroblastomas are sometime difficult to exclude from other small round blue cell tumors. These tumors are preferably diagnosed with imaging, biochemical investigations, and biopsy. Although fewer cases are referred for FNAC, it has characteristic cytomorphology of round cells with rosettoid clusters and a background of fibrillary neuropil material.[6],[17] The aspirate material can also be used for N-myc amplification by FISH or Southern blotting which predicts the tumor behavior and response to therapy.[18] Diagnostic accuracy was found to be very high in different studies reported in the literature.[14],[19],[20] In the current study, one case of metastatic neuroblastoma was diagnosed from aspirate of scalp nodule in a known case of neuroblastoma. The cells were prototypic immature neuroblastic with the presence of neuropil background and Homer–Wright rosettes [Figure 2]. High mitosis and karyorrhexis with focal streaking of cells forming chromatin threads were also observed.
Figure 2: (Case of Neuroblastoma): Homer wright rosette in a background of fibrillary neuropil material (Diff Quik, ×400)

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DSRCT is an intra-abdominal or pelvic small round cell tumor commonly seen in adolescent males, characterized by uniform round cells with scant cytoplasm having multilineage immunophenotype. In the present study, we encountered a rare case of metastatic deposit of DSRCT from a right cervical lymph node aspirate in a diagnosed case of DSRCT of retrovesicular mass confirmed by IHC markers. Cytologically, there was uniform population of round cells arranged in rosettoid clusters, discretely with irregular nuclear outline and clumped chromatin, inconspicuous nucleoli. Other features described in DSRCT like cytoplasmic vacuoles and metachromatic stroma were not observed in our case.

Rhabdomyosarcomas account for approximately 5% of the childhood tumors and its' distinction from other round cell tumors is important because of therapeutic implications, as neoadjuvant chemotherapy can be given in such cases before undergoing surgery.[1] It is characterized cytologically by the presence of two main cell types: a predominantly primitive, small round cell with scant cytoplasm and a large cell with abundant cytoplasm, sometimes presence of tadpole or ribbon shaped cells with striations. Binucleated and multinucleated cells are also seen with the presence of intracytoplasmic vacuoles.[21] Plasmacytoid cells with eccentric nucleus, moderate to abundant dense cytoplasm, and conspicuous nucleoli are clues to the diagnosis, which we observed in our cases [Figure 3]a. One case demonstrated intranuclear cytoplasmic inclusions [Figure 3]b. In one case of recurrent RMS, small cells were present in a rosettoid arrangement along with the presence of many tingible body macrophages [Figure 3]d and [Figure 3]e. We retrospectively analyzed one case of RMS, which was given a diagnosis of MSRCT with a possibility of PNET. The cells were predominantly arranged in diffuse sheets with many having pale vacuolated cytoplasm [Figure 3]f. All the suspected cases of RMS should be confirmed by ICC panel including myogenic markers such as desmin, myoglobin, muscle-specific actin, and more specific marker MyoD1.[22],[23] In our study, 2 cases displayed positivity for desmin and Myo D1 [Figure 3]c, while one case ICC was noncontributory.
Figure 3: (Cases of rhabdomyosarcoma): (a) Small round cells with few plasmacytoid cells having abundant dense cytoplasm (arrow) (Diff Quik, ×400), (b) Intranuclear cytoplasmic inclusion (arrow) (H and E, ×400), (c) Positive for Myo D1 (DAB, ×400), (d and e) Tingible body macrophages (arrow) (Diff Quik, ×200) and (H and E, ×200) respectively (f) Cells with cytoplasmic vacuolation (Diff Quik, ×400)

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Hematopoietic tumors included in small round cell tumor category are NHL, plasma cell dyscrasias, granulocytic sarcoma, and LCH.[24],[25],[26] Diffuse sheets of cells with the presence of lymphoglandular bodies are closely associated with a diagnosis of NHL.[6],[27] Infrequent lymphoglandular bodies may be noted in EWS and rhabdomyosarcoma.[28] All our six cases of cytologically diagnosed lymphoma were confirmed on histopathology, while a single case could not be categorized due to hemorrhagic aspirate and clustering of cells. Two cases of LCH were diagnosed, which revealed discretely lying histiocyte like round cell with many of them displaying nuclear grooves. Along with that, few eosinophils and lymphocytes were also present in the background. Confirmation was done with cell block and IHC (S-100, CD1a, and Langerin) [Figure 4]a and [Figure 4]b in one case, while the other by biopsy and IHC. A single case of myeloid sarcoma revealed various stages of myeloid precursors, which were confirmed by cytochemistry with MPO stain [Figure 4]c and [Figure 4]d.
Figure 4: (a) Case of LCH: Small histiocyte like cells with nuclear groove (arrow) (H and E, ×400), (b) Histology section and immunohistochemistry of CD1a (inset), (c and d) Case of myeloid sarcoma: Myeloid precursor cells (Leishman stain, ×1000), MPO stain highlighting the cytoplasmic granules (×1000) respectively

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Small cell carcinomas are aggressive tumors requiring prompt diagnosis in cytology and distinction from NHL can be challenging in some cases. Cohesive clusters of tumor cells with nuclear streaking, molding, finely dispersed chromatin, frequent mitosis, and necrosis are evidence against lymphoma. One of our cases was diagnosed as metastatic SCCa from a cervical node aspirate of an old male with history of hemoptysis. The cells were small, arranged in sheets and clusters with nuclear molding and marked streaking. The chromatin was salt and pepper like with brisk mitosis. Later on, biopsy and IHC confirmed small cell carcinoma from lung primary.

One case of neuroendocrine tumor was diagnosed from a pancreatic neck mass aspirate as round cell tumor in cytology. Cell block preparation showed organoid pattern of arrangement of small cells which were diffusely immunopositive for synaptophysin and chromogranin [Figure 5]. No increased mitosis or necrosis was noted. A diagnosis of neuroendocrine tumor was rendered and later confirmed on biopsy.
Figure 5: (a and b) Case of neuroendocrine tumor with round cell morphology in FNAC (H and E, ×200) and cell block (H and E, ×100), (c and d) Immunohistochemistry positive for synaptophysin and chromogranin respectively (DAB, ×100)

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Poorly differentiated synovial sarcoma with small cell morphology is a differential of MSRCTs.[29] In our study, one case of poorly differentiated SS was misdiagnosed as EWS/PNET group of tumor. Retrograde evaluation of cytology slides revealed many tissue fragments of tumor cells along with collagenous stroma with the presence of ovoid to fusiform tumor cells along with round cells [Figure 6]a and [Figure 6]b. Similarly, one case of amelanotic melanoma was diagnosed as MSRCT, but later, biopsy with IHC confirmed the diagnosis of melanoma [Figure 6]c and [Figure 6]d. Malignant melanoma usually displays predominant population of dissociated cells with intracytoplasmic brown black pigments, nuclear pleomorphism, prominent nucleoli, and increased mitotic activity. Due to the absence of pigments, amelanotic melanoma can mimic small cell tumors.[30],[31] Small cell melanoma is a rare variant of melanoma comprising small monomorphic cells with round to oval nuclei, inconspicuous nucleoli, and scant cytoplasm.[32] Retrospective evaluation of slides showed few cells with plasmacytoid morphology and occasional binucleate cells.
Figure 6: (a and b) Case of poorly differentiated synovial sarcoma with occasional spindloid cells (arrow) (Diff Quik, ×400) and corresponding histosection with immunohistochemistry (IHC) for TLE1 (Inset), (c and d) Case of amelanotic melanoma showing discretely lying round cells with few plasmacytoid morphology (H and E, ×200), Corresponding histosection and IHC of S-100 (Inset)

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  Conclusion Top

The present study emphasizes the pivotal role of aspiration cytology along with the use of ancillary techniques like cell block and IHC in the diagnosis of the small round cell tumors affecting various sites of the body. Despite the challenges encountered in morphological diagnoses, FNAC still has an edge as it can be utilized for segregating round cell tumors with the aid of ancillary diagnostic techniques like ICC, cell block with IHC, flowcytometric immunophenotyping, electron microscopy, cytogenetics, and molecular genetics. The tumors arising at inaccessible sites can be well targeted for diagnosis by the minimally invasive technique of needle aspiration.

It is very essential for the pathologist to pay due attention to the minute cytomorphological details to avoid a broad diagnosis of MSRCTs. Needless to say, the early and accurate diagnosis of such tumors contributes immensely in the timely and effective management of cases, especially the advanced ones with the institution of neoadjuvant chemotherapy.

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Correspondence Address:
Priyadarshini Dehuri,
Department of Pathology, Institute of Medical Sciences and SUM Hospital, Bhubaneswar, Odisha
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jmau.jmau_66_21


  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]

  [Table 1], [Table 2], [Table 3]


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