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Volume 10, Issue 4
December 2023
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Volume 10, Issue 4
December 2023
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Journals article Case study

Compound Angiotrophic Biphasic Myeloid Sarcoma with JAK2 (V617F) and KRAS (G12C) mutations

Ibrahim Abukhiran1*, Nancy Rosenthal2, Sergei I. Syrbu3
https://doi.org/10.52645/MJHS.2023.4.10

Manuscript received: 25.06.2023

Accepted for publication: 29.10.2023

Published: 11.12.2023

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Ibrahim Abukhiran1*, Nancy Rosenthal2, Sergei I. Syrbu3 . Compound Angiotrophic Biphasic Myeloid Sarcoma with JAK2 (V617F) and KRAS (G12C) mutations. Mold J Health Sci. 2023;4(10):76-80.https://doi.org/10.52645/MJHS.2023.4.10

Abstract

Introduction

Myeloid sarcomas (MS) are extramedullary manifestations of myeloid neoplasms, associated with conditions like acute myeloid leukemia (AML), myelodysplastic syndromes (MDS), and myeloproliferative neoplasms (MPN). MS presents as tumor masses in various body sites, often expressing myeloid or monocytic markers. This case report details an unusual biphasic MS relapse with a significant "intravascular" component.

Materials and methods

A 59-year-old male with a history of JAK2-V617F positive MDS/MPN underwent allogeneic hematopoietic stem cell transplantation and presented with abdominal pain, skin lesions, and systemic symptoms. Biopsy of colonic masses was performed, and subsequent analysis was carried out.

Results

The biopsy revealed a neoplasm with solid and intravascular components. The solid part was mainly composed of monocytic lineage cells expressing specific markers, with a small population of myeloid blasts. In contrast, the "intravascular" component was mainly myeloid blasts expressing different markers. Genetic analysis uncovered JAK2 (V617F) and KRAS (G12C) mutations. Despite treatment, the disease progressed, and the patient eventually passed away.

Conclusions

Myeloid sarcomas are challenging to diagnose, often being mistaken for large cell lymphomas. They can manifest as isolated extramedullary relapses, with a unique molecular profile. This case stands out due to its biphasic nature, featuring distinct components with differing characteristics, which has not been documented previously in English literature. It underscores the intricate and diverse nature of myeloid sarcomas, emphasizing the need for further research to comprehend their biology and behavior effectively.

Key Messages

What is not yet known on the issue addressed in the submitted manuscript

The submitted manuscript introduces a unique case of biphasic myeloid sarcoma with an extensive "intravascular" component, a phenomenon not previously reported in English literature. The distinct spatial, morphological, and immunophenotypic differences between these components represent an unexplored aspect of myeloid sarcomas.

The research hypothesis

The manuscript does not explicitly state a research hypothesis, as it primarily focuses on reporting a rare and novel case of myeloid sarcoma rather than presenting a specific research hypothesis.

The novelty added by manuscript to the already published scientific literature

This manuscript contributes novelty to the existing scientific literature by presenting a previously undocumented case of biphasic myeloid sarcoma with a unique "intravascular" component. The distinct characteristics and spatial separation of these components are unprecedented in the English literature on myeloid sarcomas, highlighting the complex and heterogeneous nature of these neoplasms. This case underscores the need for further research to better understand the biology and behavior of myeloid sarcomas, especially in cases with atypical presentations and features.

Introduction

Myeloid sarcomas (MS), formerly known as chloromas or granulocytic sarcomas, are extramedullary manifestations of myeloid neoplasms including acute myeloid leukemia (AML) and to a lesser extent myelodysplastic syndromes (MDS), and myeloproliferative neoplasms (MPN) [1]. By the World Health Organization’s classification definition, MS’s are composed of myeloid blasts with or without maturation and must present as a tumor mass that infiltrates and effaces the architecture of the extramedullary tissue [2]. MS can occur at any site, with different sites having different prognoses [3, 4]. The most commonly reported organs are lymph nodes, bones, soft tissues, and central nervous system [5, 6]. Atypical sites such as eyes, gall bladder, testis, and gastrointestinal system have also been reported [3, 7-11]. The majority of MS’s typically express myeloid (CD13, CD33, CD34, CD117, PU.1, Myeloperoxidase) or monocytic markers (CD11B, CD14, CD13, CD33, CD64, CD68, CD163, PU.1, Lysozyme) and lack expression of B/T cell markers (CD3, CD5, CD7, CD20, Pax-5) [2, 12]. Here we report an unusual biphasic MS relapse after Allo-SCT with an extensive “intravascular” component previously unreported in literature.

Case Report

A 59-year-old male presented to our institution with abdominal and bilateral lower limb pain in addition to systemic symptoms including fatigue, decreased appetite, and weight loss. The patient had a history of JAK2-V617F positive myelodysplastic syndrome/myeloproliferative neoplasm (MDS/MPN) and underwent allogeneic hematopoietic stem cell transplantation three years before his presentation. Physical examination showed multiple inguinal and bilateral lower limb skin lesions.

Material and methods

Complete blood count and peripheral blood smear were unremarkable except for normocytic anemia. A computerized tomography scan showed partial small and large bowel obstruction due to multiple colonic masses involving the transverse and descending colon, in addition to enlarged mesenteric and inguinal lymph nodes. Laparotomy revealed multiple masses involving all parts of the colon invading into the adjacent organs. Biopsy of the largest mass (7 cm) in the transverse colon was performed. Due to extensive disease, no tumor debulking was done.

Results

Histopathologic examination of the biopsy revealed a neoplasm consisting of both solid and intravascular components which were immunophenotypically and morphologically different (Fig. 1 and 2). The solid component (Fig. 1) was mainly composed of large cells of monocytic lineage which strongly expressed Lysozyme, CD163, CD45, CD68, and PU.1. Myeloid blasts (CD34, CD117) were only focally increased and comprised 3-5% of total cells. In contrast, the “intravascular” component (Fig. 2) was mainly composed of myeloid blasts with high nuclear: cytoplasmic ratios (NC) which strongly expressed CD10, CD34, CD45, partial/heterogeneous CD117, and PU.1, but were negative for CD3, CD20, Pax-5, Lysozyme, myeloperoxidase, and TdT.  Next-generation sequencing (NGS) of DNA from the tissue biopsy revealed JAK2 (V617F) and KRAS (G12C) mutations. Fluorescence in situ hybridization (FISH) for MLL [11q23], PML/RARA [15q22/17q21.1], CBFB [16q22], and RUNX1/RUNX1T1 [21q22/8q22] exhibited normal signal patterns. Fine needle aspiration of an inguinal lymph node revealed a population of myeloid blasts that expressed CD45, CD13, CD33, CD34, CD38, CD71 (dim), CD117, and HLA-DR, and lacked expression of CD14 and CD64. Bone marrow aspiration and biopsy revealed markedly hypocellular marrow with decreased trilineage hematopoiesis and no increase in blasts. The patient was treated with FLAG (fludarabine, cytarabine, and filgrastim) followed by cytarabine and daunorubicin chemotherapy protocols. Despite the therapy, there was disease progression. Therefore, he was referred to hospice and died two months after surgery. 

 

Discussion

MS occurs at an incidence of 2–9% in newly diagnosed AML patients [13, 14]. The prognosis of AML with concurrent MS carries an overall poor prognosis with a 5-year survival rate ranging between 20% and 30% [3]. It can be present upon the initial diagnosis of leukemia, or as a manifestation of relapsed disease after chemotherapy or hematopoietic cell transplantation [15, 16]. MS can be the first manifestation of disease relapse before relapse occurs within the marrow space, as seen in our case. In addition, isolated extramedullary relapse of AML more commonly occurs post allogeneic hematopoietic stem cell transplantation than post chemotherapy [16, 17]. The absence of concurrent leukemia makes the diagnosis of isolated MS a challenging one.  MS’s are frequently misdiagnosed as large cell lymphomas with a high rate of misdiagnosis that can be up to 75% of cases [18]. 

Similar to AML, molecular events can also be identified in MS. Up to 55% of MS may contain cytogenetic abnormalities with the most  common being trisomy 8 and inv(16) [19]. Other events including mutations (such as the common NPM1 mutation), gene rearrangements (such as KMT2A), and copy number variations (such as CBFB gene amplification) have been also reported. The mutation pattern in our case is unique. The finding of the JAK2 V617F mutation in the MS was consistent with the primary malignancy (MDS/MPN) and is proof of the molecular linkage between the two tumors. Although mutations in the KRAS genes are mostly seen in solid malignancies, it can be found in about 4-6% of AML cases [20]. In our case, the presence of those two driver mutations can represent the aggressive clinical behavior that results from acquiring additional driver mutations with progressive neoplastic clonal evolution. 

The compound and complex nature of our case is also unique. The two components are distinct spatially, morphologically, and immunophenotypically. Spatially, each of the two components is localized to a particular compartment (solid tissue vs. vascular spaces). Morphologically, the intravascular component shows typical blast cytomorphology (fine/open chromatin with high N/C ratios) in contrast to the solid component, which shows a more differentiated cytomorphology (irregular nuclei with coarse chromatin and a relatively low N/C ratio). Immunophenotypically, the intravascular component expresses myeloid immature/blast markers (CD34 and CD117) with aberrant CD10 expression in contrast to the solid component, which lack those markers and instead express markers of monocytic lineage differentiation (Lysozyme/Muramidase, CD68, and CD163). Aberrant CD10 expression and other lymphoid-associated antigens have been reported to occur in AML in multiple studies [21-23]. Expression of aberrant lymphoid-associated antigens by AML has not been shown to alter the biologic behavior or response to therapy [24]. CD10 expression has been reported to occur with intravascular large B-cell lymphoma (ILBCL) and is usually associated with MUM-1 and BCL-6 expression, reflecting the germinal center origin of some cases [25-28]. In one study on 96 cases, CD10 expression was found in 13% of ILBCL cases [29].

ILBCL is an example of the isolated intravascular growth pattern of tumor cells [30-36]. In this phenomenon, there is a selective intraluminal proliferation of tumor cells in the small to medium-sized vessels due to a possible defect in adhesion molecules and homing receptor of malignant cells. Defects in molecules such as Intercellular Adhesion Molecule-1 and b1 integrin on the tumoral cells can impair the vascular transmigration of extracellular matrix required for tumor mass formation [37]. However, this phenomenon has not been reported to occur with MS. Although this report is limited for being a single case report, to the best of our knowledge, this is the first report in English literature of a compound biphasic myeloid sarcoma with an extensive “intravascular” component that is morphologically and immunophenotypically distinct. 

Conclusion

In conclusion, this case report sheds light on the remarkable complexity and diversity of myeloid sarcomas (MS), an area of study that continues to present unique challenges and intriguing phenomena. The presentation of a biphasic MS, featuring both solid and "intravascular" components with distinct characteristics, adds a significant layer of novelty to the existing scientific literature on myeloid neoplasms. This case underscores the ongoing need for in-depth research to better comprehend the biology and behavior of myeloid sarcomas, especially in cases with atypical features and presentations. As we unravel the intricacies of these rare extramedullary manifestations, we move closer to a more comprehensive understanding of their clinical significance and, potentially, improved approaches to diagnosis and treatment.

Competing interests

None declared.

Authors’ contribution

SS devised the main conceptual ideas of the project. IA drafted the manuscript. All authors reviewed the manuscript and approved the final version. 

Informed consent for publication

Written informed consent was not obtained from the patient for publication of this case report and any accompanying images, as it is not required by the regulations of our institution.

Funding 

None.

Authors’ ORCID IDs

Ibrahim Abukhiran – https://orcid.org/0000-0003-0948-8391

Nancy Rosenthal – https://orcid.org/0000-0001-8120-9049 

Sergei I. Syrbu – https://orcid.org/0000-0003-4620-7923

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