Inflammatory leiomyosarcoma shows frequent co-expression of smooth and skeletal muscle markers supporting a primitive myogenic phenotype: a report of 9 cases with a proposal for reclassification as low-grade inflammatory myogenic tumor.


Journal

Virchows Archiv : an international journal of pathology
ISSN: 1432-2307
Titre abrégé: Virchows Arch
Pays: Germany
ID NLM: 9423843

Informations de publication

Date de publication:
Aug 2020
Historique:
received: 12 11 2019
accepted: 10 02 2020
revised: 04 02 2020
pubmed: 23 2 2020
medline: 30 7 2020
entrez: 21 2 2020
Statut: ppublish

Résumé

Inflammatory leiomyosarcoma (ILMS) is a very rare soft tissue tumor that usually follows an indolent clinical course, but long-term follow-up studies are lacking. Recent publications primarily focused on its genetic profile characterized by a near haploid genome. One study also showed these tumors to have upregulation of genes known to be crucial for skeletal muscle differentiation. Nevertheless, immunohistochemical expression of skeletal muscle markers, as well as markers that would help to distinguish ILMS from a long list of relevant differential diagnostic entities, has not been extensively studied. Nine cases of ILMS were collected and stained by a broad IHC panel which, besides others, contained MyoD1, myogenin, and PAX-7. A subset of cases was also analyzed by 2 different NGS assays and by MDM2 fluorescence in situ hybridization. Five male and 4 female patients ranged in age from 25 to 54 years (mean, 36 years). The tumors showed a predilection for intramuscular sites of the lower limbs (n = 4) and back (n = 2), whereas the remaining 3 cases affected an unspecified skeletal muscle, lung, and omentum. Follow-up with an average length of 10.6 years (range 0.5-22) was available for 8 patients. The omental tumor spread locally within the abdominal cavity, but the patient has been free of disease 7 years after treatment. None of the 5 patients with somatic soft tissue tumors (and follow-up longer than 1.5 years) had either recurrence or metastasis. Immunohistochemical studies revealed a substantial expression of skeletal muscle markers in almost all cases. This phenotype coupled with a highly characteristic genotype and significantly more indolent clinical behavior as compared with conventional leiomyosarcoma of deep soft tissue offers a strong rationale to change the current nomenclature. Based on the clinicopathological features and gene expression profile, we propose the name low-grade inflammatory myogenic tumor.

Identifiants

pubmed: 32078043
doi: 10.1007/s00428-020-02774-z
pii: 10.1007/s00428-020-02774-z
doi:

Substances chimiques

Biomarkers, Tumor 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

219-230

Subventions

Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : SVV-2019 No. 260 391
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LO1503

Références

Merchant W, Calonje E, Fletcher CD (1995) Inflammatory leiomyosarcoma: a morphological subgroup within the heterogeneous family of so-called inflammatory malignant fibrous histiocytoma. Histopathology 27:525–532
doi: 10.1111/j.1365-2559.1995.tb00323.x
Dal Cin P, Sciot R, Fletcher CD, Samson I, De Vos R, Mandahl N et al (1998) Inflammatory leiomyosarcoma may be characterized by specific near-haploid chromosome changes. J Pathol 185:112–115
doi: 10.1002/(SICI)1096-9896(199805)185:1<112::AID-PATH54>3.0.CO;2-U
Nord KH, Paulsson K, Veerla S, Wejde J, Brosjo O, Mandahl N et al (2012) Retained heterodisomy is associated with high gene expression in hyperhaploid inflammatory leiomyosarcoma. Neoplasia 14:807–812
doi: 10.1593/neo.12930
Chang A, Schuetze SM, Conrad EU 3rd, Swisshelm KL, Norwood TH, Rubin BP (2005) So-called “inflammatory leiomyosarcoma”: a series of 3 cases providing additional insights into a rare entity. Int J Surg Pathol 13:185–195
doi: 10.1177/106689690501300210
Arbajian E, Koster J, Vult von Steyern F, Mertens F (2018) Inflammatory leiomyosarcoma is a distinct tumor characterized by near-haploidization, few somatic mutations, and a primitive myogenic gene expression signature. Mod Pathol 31:93–100
doi: 10.1038/modpathol.2017.113
Michal M, Agaimy A, Contreras AL, Svajdler M, Kazakov DV, Steiner P, Grossmann P, Martinek P, Hadravsky L, Michalova K, Svajdler P, Szep Z, Michal M, Fetsch JF (2018) Dysplastic lipoma: a distinctive atypical lipomatous neoplasm with anisocytosis, focal nuclear atypia, p53 overexpression, and a lack of MDM2 gene amplification by FISH; a report of 66 cases demonstrating occasional multifocality and a rare association with retinoblastoma. Am J Surg Pathol 42:1530–1540
doi: 10.1097/PAS.0000000000001129
Svajdler M, Michal M, Martinek P, Ptakova N, Kinkor Z, Szepe P et al (2019) Fibro-osseous pseudotumor of digits and myositis ossificans show consistent COL1A1-USP6 rearrangement: a clinicopathological and genetic study of 27 cases. Hum Pathol 88:39–47
doi: 10.1016/j.humpath.2019.02.009
Donati M, Kastnerova L, Martinek P, Grossmann P, Sticova E, Hadravsky L et al (2019) Spitz tumors with ROS1 fusions: A clinicopathological study of 6 cases, including FISH for chromosomal copy number alterations and mutation analysis using next-generation sequencing. Am J Dermatopathol. https://doi.org/10.1097/DAD.0000000000001499
Aspberg F, Mertens F, Bauer HC, Lindholm J, Mitelman F, Mandahl N (1995) Near-haploidy in two malignant fibrous histiocytomas. Cancer Genet Cytogenet 79:119–122
doi: 10.1016/0165-4608(94)00124-T
de Saint Aubain Somerhausen N, Gengler C, Reginster M, Christophe J, Ronsse G, Gebhart M (2003) Inflammatory leiomyosarcoma: a case report. Ann Pathol 23:336–339
pubmed: 14597897
Morovic A, Delcore R, Damjanov I (2003) Inflammatory leiomyosarcoma of the retroperitoneum. Pathol Res Pract 199:41–43 discussion 5-6
doi: 10.1078/0344-0338-00351
Efstathopoulos N, Lazarettos J, Nikolaou V, Chronopoulos E (2006) Inflammatory leiomyosarcoma of the ankle: a case report and review of the literature. J Foot Ankle Surg 45:127–130
doi: 10.1053/j.jfas.2005.12.010
Morita I, Isoda R, Hirabayashi Y, Naomoto Y (2016) A long-living case of carotid aneurysm caused by inflammatory leiomyosarcoma. Asian Cardiovasc Thorac Ann 24:801–804
doi: 10.1177/0218492316659975
Martinez AP, Fritchie KJ, Weiss SW, Agaimy A, Haller F, Huang HY et al (2019) Histiocyte-rich rhabdomyoblastic tumor: rhabdomyosarcoma, rhabdomyoma, or rhabdomyoblastic tumor of uncertain malignant potential? A histologically distinctive rhabdomyoblastic tumor in search of a place in the classification of skeletal muscle neoplasms. Mod Pathol 32:446–457
doi: 10.1038/s41379-018-0145-0
Salzano RP Jr, Tomkiewicz Z, Africano WA (1991) Dedifferentiated liposarcoma with features of rhabdomyosarcoma. Conn Med 55:200–202
pubmed: 2070605
Tallini G, Erlandson RA, Brennan MF, Woodruff JM (1993) Divergent myosarcomatous differentiation in retroperitoneal liposarcoma. Am J Surg Pathol 17:546–556
doi: 10.1097/00000478-199306000-00002
Henricks WH, Chu YC, Goldblum JR, Weiss SW (1997) Dedifferentiated liposarcoma: a clinicopathological analysis of 155 cases with a proposal for an expanded definition of dedifferentiation. Am J Surg Pathol 21:271–281
doi: 10.1097/00000478-199703000-00002
Binh MB, Guillou L, Hostein I, Chateau MC, Collin F, Aurias A et al (2007) Dedifferentiated liposarcomas with divergent myosarcomatous differentiation developed in the internal trunk: a study of 27 cases and comparison to conventional dedifferentiated liposarcomas and leiomyosarcomas. Am J Surg Pathol 31:1557–1566
doi: 10.1097/PAS.0b013e31804b4109
Weiss SW (2002) Smooth muscle tumors of soft tissue. Adv Anat Pathol 9:351–359
doi: 10.1097/00125480-200211000-00004
Marino-Enriquez A, Wang WL, Roy A, Lopez-Terrada D, Lazar AJ, Fletcher CD et al (2011) Epithelioid inflammatory myofibroblastic sarcoma: an aggressive intra-abdominal variant of inflammatory myofibroblastic tumor with nuclear membrane or perinuclear ALK. Am J Surg Pathol 35:135–144
doi: 10.1097/PAS.0b013e318200cfd5
Antonescu CR, Suurmeijer AJ, Zhang L, Sung YS, Jungbluth AA, Travis WD, al-Ahmadie H, Fletcher CD, Alaggio R (2015) Molecular characterization of inflammatory myofibroblastic tumors with frequent ALK and ROS1 gene fusions and rare novel RET rearrangement. Am J Surg Pathol 39:957–967
doi: 10.1097/PAS.0000000000000404
Agaimy A, Michal M, Hadravsky L, Michal M (2016) Follicular dendritic cell sarcoma: clinicopathologic study of 15 cases with emphasis on novel expression of MDM2, somatostatin receptor 2A, and PD-L1. Ann Diagn Pathol 23:21–28
doi: 10.1016/j.anndiagpath.2016.05.003
Alaggio R, Zhang L, Sung YS, Huang SC, Chen CL, Bisogno G, Zin A, Agaram NP, LaQuaglia M, Wexler LH, Antonescu CR (2016) A molecular study of pediatric spindle and sclerosing rhabdomyosarcoma: identification of novel and recurrent VGLL2-related fusions in infantile cases. Am J Surg Pathol 40:224–235
pubmed: 26501226 pmcid: 4712098
Le Loarer F, Cleven AHG, Bouvier C, Castex MP, Romagosa C, Moreau A et al (2019) A subset of epithelioid and spindle cell rhabdomyosarcomas is associated with TFCP2 fusions and common ALK upregulation. Mod Pathol. https://doi.org/10.1038/s41379-019-0323-8

Auteurs

Michael Michal (M)

Department of Pathology, Charles University, Faculty of Medicine in Plzen, Plzen, Czech Republic. michael.michal@biopticka.cz.
Biomedical Center, Charles University, Faculty of Medicine in Plzen, Plzen, Czech Republic. michael.michal@biopticka.cz.
Bioptical Laboratory, Ltd., Plzen, Czech Republic. michael.michal@biopticka.cz.

Brian P Rubin (BP)

Department of Pathology, Cleveland Clinic, Cleveland, OH, USA.

Dmitry V Kazakov (DV)

Department of Pathology, Charles University, Faculty of Medicine in Plzen, Plzen, Czech Republic.
Bioptical Laboratory, Ltd., Plzen, Czech Republic.

Květoslava Michalová (K)

Department of Pathology, Charles University, Faculty of Medicine in Plzen, Plzen, Czech Republic.
Bioptical Laboratory, Ltd., Plzen, Czech Republic.

Petr Šteiner (P)

Bioptical Laboratory, Ltd., Plzen, Czech Republic.

Petr Grossmann (P)

Bioptical Laboratory, Ltd., Plzen, Czech Republic.

Veronika Hájková (V)

Bioptical Laboratory, Ltd., Plzen, Czech Republic.

Petr Martínek (P)

Bioptical Laboratory, Ltd., Plzen, Czech Republic.

Marian Švajdler (M)

Department of Pathology, Charles University, Faculty of Medicine in Plzen, Plzen, Czech Republic.
Bioptical Laboratory, Ltd., Plzen, Czech Republic.

Abbas Agaimy (A)

Institute of Pathology, University Hospital, Friedrich-Alexander University Erlangen-Nürnberg, Erlangen, Germany.

Ladislav Hadravský (L)

Department of Pathology, First Faculty of Medicine, Charles University in Prague, Prague, Czech Republic.

Antonina V Kalmykova (AV)

CSD Health Care, Ltd., Kyiv, Ukraine.

Eiichi Konishi (E)

Department of Pathology, Kyoto Prefectural University of Medicine, Kyoto, Japan.

Filip Heidenreich (F)

Department of Radiology, Charles University, Faculty of Medicine in Plzen, Plzen, Czech Republic.

Michal Michal (M)

Department of Pathology, Charles University, Faculty of Medicine in Plzen, Plzen, Czech Republic.
Bioptical Laboratory, Ltd., Plzen, Czech Republic.

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