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Gama, J.M.; Almeida, R.; Oliveira, R.C.; Casanova, J. Inferior Vena Cava Leiomyosarcoma. Encyclopedia. Available online: https://encyclopedia.pub/entry/54030 (accessed on 19 May 2024).
Gama JM, Almeida R, Oliveira RC, Casanova J. Inferior Vena Cava Leiomyosarcoma. Encyclopedia. Available at: https://encyclopedia.pub/entry/54030. Accessed May 19, 2024.
Gama, João Martins, Rui Almeida, Rui Caetano Oliveira, José Casanova. "Inferior Vena Cava Leiomyosarcoma" Encyclopedia, https://encyclopedia.pub/entry/54030 (accessed May 19, 2024).
Gama, J.M., Almeida, R., Oliveira, R.C., & Casanova, J. (2024, January 18). Inferior Vena Cava Leiomyosarcoma. In Encyclopedia. https://encyclopedia.pub/entry/54030
Gama, João Martins, et al. "Inferior Vena Cava Leiomyosarcoma." Encyclopedia. Web. 18 January, 2024.
Inferior Vena Cava Leiomyosarcoma
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This entry is adapted from the peer-reviewed paper 10.3390/jvd3010003

Leiomyosarcomas (LMSs) are malignant neoplasms of soft muscle differentiation that can be classified into five distinct groups according to site-related origin: intra-abdominal, subcutaneous or deep soft tissue of the limbs, cutaneous, external genitalia, and vascular.

leiomyosarcoma inferior vena cava leiomyosarcoma vascular

1. Introduction

Leiomyosarcoma (LMS) is a malignant neoplasm of soft muscle differentiation [1]. Although uncommon, it is one of the most common sarcomas. LMSs of the soft tissue can be grouped into five distinctive categories according to site-related origin: intra-abdominal, subcutaneous or deep soft tissue of the limbs, cutaneous, external genitalia, and vascular. The distinction is important since there are clinical differences between these subgroups [2]. Intra-abdominal and deep soft tissue are the most common subgroups, and the least common is the vascular LMS group. Although rare, LMS is the most common malignant tumor involving the vascular system [3]. Vascular LMS originates in the walls of medium-sized or large blood vessels, usually from the inferior vena cava. This distinction is fundamental since it reflects distinct biological origins, molecular changes, and prognoses.
Inferior vena cava LMS was first described by Leopold Perl and Rudolph Virchow in 1871 [4]. Since then, many discoveries have been made and a clearer image of this interesting entity has emerged.

2. Epidemiology

It is estimated that LMS of the soft tissue represents up to 15% of all soft tissue sarcomas [5]. LMS of vascular origin is rare, and most of the knowledge gathered so far comes from isolated case reports or small series.
It is estimated that vascular LMS represents 5% of soft tissue LMS, and half arise from the inferior vena cava or veins of the lower limbs. Leiomyosarcomas are five times more common in veins than arteries [6]. Autopsy-based studies estimated an incidence of 1/7000-34,000 autopsies [7]. Currently, less than 400 cases are described in the literature.
Older adults are usually the most affected, with a median age at diagnosis of 56 years (range: 34–75) [8], but interestingly, more than three-quarters of all vena cava leiomyosarcomas occur in women [8][9]. The hormonal influence on growth and proliferation of smooth muscle tissue might explain this. LMS is the most common malignancy in the vascular system in adults, and albeit rare, some cases have been reported in the pediatric age [10].
The distribution of vascular leiomyosarcomas is grossly inversely proportional to the pressure in the vascular bed [7][11]. Vascular leiomyosarcomas are more common in large veins, where the pressure is lower [12]; the most common location is in the inferior vena cava, followed by other large veins. Less commonly, vascular LMSs can arise in the pulmonary artery and in large systemic arteries [6][11]. In 1973, Kevorkian and Cento [11] conducted an extensive review of all of the cases of vascular leiomyosarcomas published in the literature, and out of a total of 86 patients, 33 were found in the inferior vena cava, 35 in other large veins, 10 in the pulmonary artery, and 8 cases in large systemic arteries. LMS arising in an arteriovenous fistula has also been reported [13].

3. Clinical Presentation

The clinical symptoms are diverse, non-specific, dependent on the location of the tumor, the growth rate, and the development of collateral blood flow [6]. When leiomyosarcomas develop in the superior vena cava segment, symptoms manifest as Budd–Chiari syndrome with hepatomegaly, jaundice, ascites, and nausea. In the middle segment, the symptoms are associated with abdominal discomfort and sometimes related to vascular compromise (e.g., edema of the lower limbs) [14]. In the inferior segment, the symptoms appear relatively late (e.g., edema, nausea, and back pain) [15][16]. Rarer presenting symptoms are recurrent pulmonary embolisms and metastases. LMSs may remain asymptomatic and are often incidentally diagnosed [11].

4. Etiology and Pathogenesis

Not much is known about the predisposing factors and etiology of vascular LMS, and the experience gathered from leiomyosarcomas from other sites is not always directly applicable to the soft tissue and vascular counterpart [7].
Leiomyosarcomas have a complex karyotype with complex numeric and structural anomalies, and multiple genes have been implicated in its pathogenesis [17], with significant mutational heterogeneity and frequent copy number variations with no characteristic chromosomal rearrangements [18]. In a study by Chudasama et al., chromothripsis was reported in 35% of LMSs. Losses of chromosome regions encoding for tumor suppressor genes such as TP53, PTEN, CDH1, and MYOCD have been reported [18][19], as well as genes involved in DNA homologous recombination repair (BRCA2 and ATM are a frequent target of deletions). Other recurrently mutated genes are chromatin modifiers (RBL2, DNMT3A, and KAT6B), cytokine receptors (ALK, FGFR2, FLT3, and LIFR), and transcriptional regulators (PAX3, FOXO1, CDX2, and SUFU) [18].
Alternative telomere lengthening, with alterations in telomere maintenance genes such as ATRX, RBL2, and SP100, were identified in 78% of leiomyosarcomas [18]. In the same study, anomalies in the Retinoblastoma–cyclin D1 pathway and TP53 were found in almost every single case of LMS.

5. Imaging Diagnosis

Radiology is essential for the diagnosis, and since the symptoms are rather unspecific, the clinical differential diagnosis is broad, encompassing entities such as liposarcomas and lymphomas [20]. Invariably, the clinician will order an imaging exam such as ultrasonography (US), computerized tomography (CT), magnetic resonance imaging (MRI), or positron emission tomography (PET). US is rather unspecific [21], so CT is usually the method of choice for the first approach, enabling imaging-guided biopsy [22][23].
MRI has no specific signal; it is usually hypointense in T1 and intermediate in T2 but may be helpful in assessing necrosis [24]. MRI has a higher soft tissue resolution, allowing for a better definition of the vascular structures involved, and does not expose the patients to radiation [25]. MRI can also be combined with angiography for better local tumor evaluation. Contrast-enhanced cavography MRI can be used to differentiate an intraluminal mass from a thrombus and will also allow for the determination of the degree of obstruction and the development of collateral circulation [26].
PET has been proposed as a valuable indicator of tumor grade. A study by Punt et al. has demonstrated a correlation between a higher standard uptake value (SUVmax) and higher histological grade and tumor size [27]. In addition, it is a useful tool for assessing distant metastases [25]. Therefore, PET is valuable for a pre-operative decision.
Despite the value of radiology, pathology is fundamental and the gold standard in assessing LMS [28].

6. Gross and Histologic Features

On gross examination, the majority are extraluminal (76%), with minimal or even absent luminal growth. Tumor size can range from 2 to 30 cm [8][9].
Histologically, the cells are elongated in shape, with abundant and eosinophilic cytoplasm, centrally placed nuclei, and blunt-ended edges, sometimes called “cigar-shaped”. Architecturally, the cells are arranged in fascicles [1]. Cytoplasmatic and perinuclear haloes are frequently observed [29]. An example can be seen in Figure 1.
Figure 1. Leiomyosarcoma composed of cells with a fascicular architecture. The tumor cells are elongated with an eosinophilic cytoplasm. The cells, although atypical, resemble normal smooth cells, indicating mild atypia.
At higher magnification, longitudinally oriented myofibrils are a common characteristic. They can clump, giving a clotted appearance of the cytoplasm [7].
As leiomyosarcomas become less differentiated, they lose the resemblance to the normal counterpart. In well-differentiated tumors, the cells are arranged in fascicles, there is mild nuclear polymorphism, and nuclei are centrally located and have a low mitotic rate. In moderately differentiated tumors, the mitotic rate, nuclear polymorphism, and nuclear hyperchromasia are increased. In higher grade tumors, the nuclei often lose the central location, and a fascicular architecture and multinucleated cells are common [8].
This kind of cellular changes can be seen in Figure 2 and Figure 3.
Figure 2. In this leiomyosarcoma, there is a pronounced atypia with pseudoinclusions and pleomorphic, hyperchromatic, and bizarre nuclei. The preserved vascular lumen can be recognized in the central region of the photo (arrow).
Figure 3. In this tumor, the cells are markedly pleomorphic with multinucleation.
Morphologically, there seems to be no histologic difference between vascular LMS and other types of soft tissue LMS [29]. The intimal layer is usually intact, but protrusions into the lumen can also be seen [29].
Immunohistochemistry is helpful in diagnosing leiomyosarcoma and is based on demonstrating myoid differentiation with muscle markers. α-smooth muscle actin (α-SMA), desmin, heavy chain muscle actin, and h-caldesmon, which are myoid markers, are expressed in leiomyosarcomas [30]. α-SMA and muscle-specific actin are considered the most sensitive markers [31]. Desmin is expressed in around 70% of leiomyosarcomas [32][33][34]. It is important to take into consideration not only the expression but also the type of expression of these antibodies: diffuse expression of desmin is indicative of myoid differentiation, but the focal expression of actin or desmin can also be found in myofibroblasts [35][36]. An example of the immunostaining is represented in Figure 4.
Figure 4. Diffuse staining for α-SMA (left side) and desmin (right side). Abbreviations: α-SMA—α-smooth muscle actin.
There are interesting differences in the immunostaining characteristics of leiomyosarcomas arising from vascular smooth muscle compared to leiomyosarcomas from different locations. Vascular leiomyosarcomas are more often desmin negative and h-caldesmon positive than leiomyosarcomas arising from soft tissue [36][37].
The expression of keratins, which is usually regarded as evidence of epithelial differentiation, can be detected in leiomyosarcomas [37]. A cross-reaction with the antibodies used to detect cytokeratins was first suspected to be the cause of immunoreactivity, but it has been demonstrated that cytokeratins are present both in non-neoplastic smooth muscle and in smooth muscle tumors [38][39]. The expression of cytokeratins is limited to low molecular weight keratins [40]. Epithelial membrane antigen (EMA) immunoreactivity can occur in up to 45–60% of cases. When present, staining for cytokeratins is usually focal, but diffuse expression was seen in 11% of cytokeratins and 6% with EMA [37][40]. A dot-like pattern of cytokeratin expression has been described, and it is associated, at least focally, with a diffuse or a fibrillary pattern [37]. There is no correlation between the expression of cytokeratins and the location, sex, age, histological grade, and histological features of LMS, but EMA expression is more common in vascular LMS when compared to LMS of the soft tissue, skin, and uterus [37].
CD34 [41], S100 [42], and HMB45 [43] can also be expressed. Estrogen and progesterone receptors were previously suggested as adjunct (and helpful) markers to distinguish between retroperitoneal leiomyosarcomas and leiomiomas [44], but it was found that they can be expressed in both uterine and extrauterine LMS [45][46], therefore not being useful in this distinction.
Histologically, the differential diagnosis for leiomyosarcoma can be extensive, including other spindle cell lesions such as malignant peripheral nerve sheath tumors, synovial sarcomas, leiomyomas, schwannomas, benign cellular myofibroblastic tumors, gastrointestinal stromal tumor, synovial sarcoma, and inflammatory myofibroblastic tumors, as well as other high-grade malignancies, in poorly differentiated cases.

References

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Subjects: Pathology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
João Martins Gama
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Rui Almeida
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Rui Caetano Oliveira
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José Casanova
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