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Polish Journal of Pathology
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Case report

Primary cardiac atrial sarcomas. Report of two histologically different cases and review of the literature

Mirosława Püsküllüoglu
1
,
Anna Kruczak
2
,
Katarzyna Mularz
2
,
Magdalena Rozmus
2
,
Agnieszka Harazin-Lechowska
2
,
Agnieszka Pietruszka
3
,
Justyna Jaworska
1
,
Marek Ziobro
1
,
Aleksandra Grela-Wojewoda
1
,
Janusz Ryś
2

1.
Department of Clinical Oncology, Maria Sklodowska-Curie National Research Institute of Oncology, Cracow Branch, Krakow, Poland
2.
Department of Tumor Pathology, Maria Sklodowska-Curie National Research Institute of Oncology, Cracow Branch, Krakow, Poland
3.
1st Radiation and Clinical Oncology Department, Maria Sklodowska-Curie National Research Institute of Oncology, Gliwice Branch, Poland
Pol J Pathol 2021; 72 (3): 358-369
Online publish date: 2022/03/08
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Introduction

Primary cardiac tumors are extremely rare with an incidence of 0.001-0.03% based on the autopsy findings [1]. Metastases to the heart occur 20-40 times more frequently than primary neoplasms [2]. Approximately 75% of primary cardiac tumors are benign with 50% of those being myxomas. The remaining 25% of primary cardiac tumors are malignant with sarcomas accounting for 95% and lymphomas accounting for 5% of these tumors [1]. It was believed that angiosarcoma and undifferentiated pleomorphic sarcoma were the most frequently occurring cardiac sarcomas [3]. However, a retrospective analysis by Neuville et al, showed cardiac intimal sarcomas (InS) (42%) to be the most frequent primary cardiac sarcoma followed by angiosarcoma (26%), undifferentiated sarcoma (22%), synovial sarcomas (SS) (7%), leiomyosarcomas (2%) and peripheral neuroectodermal tumor (1%) [4].
What is more different sarcomas have predilection of developing in various parts of the heart and thus their initial manifestation can differ. In one analysis of 124 cases the most common location was right atrium (38%), and left atrium (36%), left and right ventricles (8% and 7% respectively) and pericardium (2.4%) were less common [5]. Other studies suggest left predilection [6].
Here, we present two histologically different cases of atrial sarcoma with particular attention to their differential diagnosis and the role of molecular studies.

Clinical data

Case 1
A 34-year-old female was admitted to the cardiac surgery clinic for an urgent procedure. Initially she presented with heart failure symptoms: New York Heart Association (NYHA) class II and weakness. An intraoperative transesophageal echocardiography (TEE) study revealed well circumscribed mass filling almost the entire left atrium of the heart. She underwent open heart surgery. Initial histopathology examination suggested high-grade sarcoma, re-consultation of the specimen in a reference center allowed to diagnose an intimal sarcoma.
Two months after the surgery she was diagnosed with malignancy localized in brainsteam and pons. At that time the patient was symptomatic with motor aphasia, dysarthria, dysphagia, left hemiparesis, asymmetric deep reflexes and positive Babinski symptom thus the biopsy of the lesion was not performed. The origin of the brain mass (sarcoma metastasis versus primary malignancy) remained unsure. Despite palliative radiochemotherapy (20 Gy in 5 fractions for pons and surrounding area and one cycle of doxorubicin) patient’s condition gradually deteriorated with continuous deterioration in central nervous system (CNS) symptoms. Patient was discharged home and died soon after.

Case 2
A 30-year-old man complained of exercise dyspnea, heart arrhythmia and weakness. The diagnosis of right atrium tumor compressing right and left ventricle with pulmonary and pericardial effusion was set after obtaining magnetic resonance imaging (MRI) and positron emission tomography (PET). The patient underwent emergency surgery in December 2019, but the operation was not radical (R1). Histopathology report revealed biphasic synovial sarcoma.
The patient received 6 curses of adjuvant anthracycline monotherapy with no side effects. Three months later computed tomography (CT) revealed a mediastinal mass 82 × 39 × 25 mm invading right atrium, right ventricle and coronary sinus. The patient was offered a proton therapy, but refused. High-dose ifosfamid was administered as a first line of palliative treatment, but the progression in tumor mass with pericardial effusion after 3 cycles was noted. 4 cycles of gemcitabine with docetaxel were administered as a second line with further progression and an embolus in a heart. For the next 6 months pazopanib was continued till mildly symptomatic tamponade of the heart was seen on echocardiogram. The patient was hospitalized with surgical intervention. Additional imaging studies showed further progression. The patient started fourth line of palliative chemotherapy consisting of cisplatin and etoposide, but his performance status deteriorated soon after first cycle with clinical progression observed. He died 26 months after the heart surgery.
Histological, immunohistochemical and molecular characteristics of the atrial tumors

Case 1
Histological examination showed a tumor mostly composed of spindle cells with fascicular growth (Fig. 1AB) that were diffusely positive for vimentin and presented focal SMA reactivity. Epithelioid component (Fig. 1C) showed positive reaction to vimentin, CD31 and EMA. There was no reaction to pancytokearatins, S100 protein, melan A, desmin, miogenin, ERG, SOX10, ALK1, CD30, and PLAP. No signs of deletion in protein products of H3K27me3 and INI1 were noted. In situ hybridization revealed MDM2 gene amplification in most of the cells
(Fig 1D). This relatively specific finding, along with the clinicopathologic features, supported the diagnosis of a high grade intimal sarcoma.

Case 2
At the histologic level, the major part of the tumour was consisted of relatively uniform spindle-shaped cells (Fig. 2A). Furthermore, these areas showed a high mitotic rate and focal necrosis. Numerous vascular spaces resembling hemangiopericytoma-like texture were present (Fig. 2B).
Several areas, showed a biphasic pattern, the spindle cells being mixed with a prominent malignant epithelial component. The epithelial cells had large round vesicular nuclei and abundant pale-staining cytoplasm, and formed nests or gland-like spaces (Fig. 2C).
Epithelial cells were strongly positive for cytokeratin (Fig. 2D) and epithelial membrane antigen. Scattered spindle cells were also reactive for cytokeratin and, more often, epithelial membrane antigen. The spindle cells also showed reactivity for vimentin intermediate filaments. All components of the tumour were negative for S-100 protein, desmin, smooth muscle actin (SMA) and CD31.
Final diagnosis was confirmed by fluorescence in situ hybridization (FISH) showing the rearrangement of SS18 gene in the numerous tumour cells.

Discussion

Depending on the location of the sarcoma: in left or right atrium the malignancy may present different initial symptoms. Generally these tumors are accompanied by a triad of symptoms: generalized /systemic symptoms; signs of embolization and heart/local symptoms [7]
Interestingly, different sarcomas are also characterized by predominance of one or the other site. Synovial sarcomas would be more commonly found in right atrium, while InS, other poorly-differentiated sarcomas and leiomyosarcomas localize in left atrium [4, 5].
Although cardiac sarcomas are rare in comparison to their soft tissue counterparts, they are the second most common type of primary cardiac neoplasm.
Of the few hundred cases reported, most has been based on autopsy series. A series of 27 cardiac sarcomas removed at surgery for curative and diagnostic intent were reviewed for clinicopathologic features with correlation to available postoperative follow-up data in 17 patients [6]. There were 6 angiosarcomas, 6 myxofibrosarcomas, 3 malignant peripheral nerve sheath tumors (MPNST), 3 leiomyosarcomas, 2 synovial sarcomas, 1 epithelioid hemangioendothelioma, 1 chondrosarcoma, 1 osteosarcoma, and 4 poorly differentiated sarcomas [6]. More recent analysis of 100 cases indicated InS as the most frequent primary cardiac sarcoma followed by angiosarcoma and undifferentiated sarcoma [4]. A retrospective study of 124 cases performed by French Sarcoma Group did not provide detailed data regarding histology showing all group of poorly differentiated sarcomas counting for 36.%; angiosarcoma 32.%, leiomyosarcoma 13% and all other histologies 18.6% [5].
As suggested by Koelsche and colleagues poorly differentiated sarcomas and InS can be interpreted as the same diagnosis [8], which would show consistency of the French Sarcoma Group results with Neuville et al data [4].

Intimal sarcoma
Clinical characteristics of disease based on 46 cases collected from the literature are depicted in Table I [1, 8-43].
InS is a mesenchymal tumor arising from intimal subendothelial cells and composed of poorly differentiated spindle, pleomorphic and epithelioid cells [8, 28, 32]. It localizes in the large blood vessels and in the left atrium [5, 28, 31, 32]. By definition, InS lack specific lineage differentiation, although myofibroblastic and smooth muscle differentiation may occur [8, 31].
Immunohistochemically, almost all intimal atrial sarcomas express vimentin and MDM2. 35-50% express SMA and/or desmin, while cytokeratins, EMA, S100, and CD117 are usually negative or only weak or focal and vary depending on tumor differentiation (Table II) [4, 44]. The reactions to CD31, CD34 and Factor VIII are also negative, but can be positive in areas with angiosarcomatous differentiation [9, 46].
All reported cardiac intimal sarcomas have been H-caldesmon negative (Table II) [4, 44].
As the InS immunophenotype is non-specific, the final diagnosis of this entity should be based on molecular studies. InS is strongly associated with MDM2 amplification, however, this genetic alteration can be also diagnosed in case of other sarcomas including: well differentiated and dedifferentiated liposarcoma (in up to 95% of cases), angiosarcoma (in one third of all cases) and other sarcomas (in 18% of all cases) like low-grade central osteosarcoma or parosteal osteosarcoma [8, 28, 44, 47]. In case of InS FISH can show a typical pattern of small grouping of signals not characteristic for dedifferentiated liposarcomas [28]. For diagnosis of MDM2 amplification both: FISH and dual in situ hybridization (DISH) can be used [44]. As shown by our case InS has been commonly diagnosed as undifferentiated sarcoma or high-grade sarcoma. Performing FISH with the assessment of MDM2 amplification is an important step in assessing the final diagnosis [8].
Molecular studies are of particular importance in the differential diagnosis between InS and undifferentiated pleomorphic sarcoma (UPS), however UPS of the heart have recently been suggested to represent the cardiac analog of InS due to morphological overlap and high prevalence of MDM2 amplifications in both neoplasms. What is more, DNA methylation profiling (t-SNE) revealed an overlap of InS and cardiac UPS, too. This InS methylation signature was distinct from potential histologic and molecular mimics, especially in cases lacking MDM2, MDM4 or CDK6 amplifications [8].
Currently, due to uncommon diagnosis there is no standard of care (SoC) for InS treatment. Histologically clear margins (R0) achieved during radical surgery followed by adjuvant radiotherapy and chemotherapy seem to prolong the survival with surgery being pointed out as the mainstay of treatment [17, 18, 28]. In case of palliative treatment the options are surgery that can alleviate the symptoms and chemotherapy [18]. The chemotherapy regiments used in case of heart InS does not differ to these applied for other sarcomas [17]. New options that are investigated in clinical trials are MDM2 inhibitor milademetan, PDGFR inhibitor e.g. dasatinib and CDK4/6 inhibitors [28, 48, 49].
It seems that sarcomas of the left atrium carry poor, but slightly better prognosis to their counterparts localized in the right atrium [28]. Nevertheless, the survival in case of InS of the heart is usually few months with frequent recurrences within first year of radical treatment. Metastatic disease is reported in lungs, lymph nodes, brain and other sites [28]. Histological factors that indicate worse prognosis are high mitotic rate and necrosis [17].

Synovial sarcoma
Cardiac SS is an extremely rare and aggressive malignancy accounting for 3-5% of heart tumors with a significant male predominance and right heart location [2, 50, 51, 52]. The most common cardiac location is pericardium with atrium being the second one [52]. Only 27 cases of atrial synovial sarcomas have been reported previously (Table III). Twenty eight cases reported in the literature including our case are consisted of 19 men, and 6 female (2 unknown sex) with a median age of 40.5 years (13 to 66 years). Most of the tumors occur in the right atrium (in 20 cases).
In case of SS, the differential diagnosis includes mesothelioma, fibrosarcoma, MPNST and myxoid sarcoma/myxoma [50, 72]. For biphasic SS it is challenging to differentiate with mesothelioma with histology and immunohistochemistry with the support of molecular testing might be necessary [50]. For SS monophasic variant differential diagnosis with fibrosarcoma should be considered [50].
The role of immunohistochemical studies in the differential diagnosis of synovial sarcoma is limited, so the detection of t(X;18)(p11.2;q11.2) translocation resulting in fusion of SYT with SSX1, 2 or 4 present in 90% of SS cases is a hallmark in diagnosis of this malignancy [50, 73]. The diagnosis is based on FISH, but this genetic abnormality can also be detected with reverse transcription polymerase chain reaction (RT-PCT) next generation sequencing (NGS) [20, 72].
Treatment options consist of surgery – a gold standard rarely possible as a radical treatment with adjuvant chemo- or/and radiotherapy [74]. Traditionally, the first line of treatment for SS composes of high-dose ifosfamide, but other regiments are also applied [75]. As per the results of PALETTE trial the therapy with a multikinase inhibitor pazopanib in patients progressing after chemotherapy can be an option [76].
The prognosis of SS is extremely unfavorable with majority of patients dying shortly after diagnosis and only few patients with an observation time close to a year [50]. That makes our case special among only few others as current observation since the initial surgery is more than two years [62]. The reason of such poor survival can also be assigned to low radical surgery frequency resulting from tumour location [50]. It is suggested that age < 30 years at diagnosis can result in better prognosis [52].
The authors declare no conflict of interest.

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