Characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in France

Abstract: Malignant histiocytoses (MH) are rare and poorly understood cancers, with no established therapeutic guidelines. We conducted a national retrospective study of MH diagnosed in France between 2000 and 2023. All cases underwent centralized histological review, and several malignant tumors wi...

Full description

Saved in:
Bibliographic Details
Main Authors: Camille Bigenwald, Damien Roos-Weil, Arnaud Pagès, Zofia Hélias-Rodzewicz, Christiane Copie-Bergman, Marzieh Nashvi, Pierre Khneisser, Marie Parrens, Alexandra Traverse-Glehen, Isabelle Ray-Coquard, Loïc Ysebaert, Tony Marchand, Jérôme Razanamahery, Frédéric Charlotte, Antoine Neel, Gandhi Damaj, Jérémie Dion, Eve-Marie Nazal-Traissac, Stéphanie Tardy, Géraldine Salmeron, Hélène Monjanel, Ahmed Idbaih, Sébastien Héritier, Julien Haroche, Jean Donadieu, Jean-François Emile
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Blood Advances
Online Access:http://www.sciencedirect.com/science/article/pii/S2473952925001314
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849714622089658368
author Camille Bigenwald
Damien Roos-Weil
Arnaud Pagès
Zofia Hélias-Rodzewicz
Christiane Copie-Bergman
Marzieh Nashvi
Pierre Khneisser
Marie Parrens
Alexandra Traverse-Glehen
Isabelle Ray-Coquard
Loïc Ysebaert
Tony Marchand
Jérôme Razanamahery
Frédéric Charlotte
Antoine Neel
Gandhi Damaj
Jérémie Dion
Eve-Marie Nazal-Traissac
Stéphanie Tardy
Géraldine Salmeron
Hélène Monjanel
Ahmed Idbaih
Sébastien Héritier
Julien Haroche
Jean Donadieu
Jean-François Emile
author_facet Camille Bigenwald
Damien Roos-Weil
Arnaud Pagès
Zofia Hélias-Rodzewicz
Christiane Copie-Bergman
Marzieh Nashvi
Pierre Khneisser
Marie Parrens
Alexandra Traverse-Glehen
Isabelle Ray-Coquard
Loïc Ysebaert
Tony Marchand
Jérôme Razanamahery
Frédéric Charlotte
Antoine Neel
Gandhi Damaj
Jérémie Dion
Eve-Marie Nazal-Traissac
Stéphanie Tardy
Géraldine Salmeron
Hélène Monjanel
Ahmed Idbaih
Sébastien Héritier
Julien Haroche
Jean Donadieu
Jean-François Emile
author_sort Camille Bigenwald
collection DOAJ
description Abstract: Malignant histiocytoses (MH) are rare and poorly understood cancers, with no established therapeutic guidelines. We conducted a national retrospective study of MH diagnosed in France between 2000 and 2023. All cases underwent centralized histological review, and several malignant tumors with a stroma highly enriched in histiocytes were excluded. In total, 141 patients were included, with a median age of 62 years (range, 1-87). The cases comprised either primary MH (64%) or MH associated with other hematologic malignancies (36%). Phenotypes corresponded to histiocytic (43%), interdigitating dendritic cell (37%) or Langerhans cell (12%) sarcomas, or high-grade indeterminate dendritic cell tumors (10%), as per the World Health Organization classification. Tumor cells were almost universally positive for CSF1R and PU.1, and 85% showed phosphorylated extracellular signal–regulated kinase positivity. Next-generation sequencing was performed in 75 cases. Mutations in the MAPK pathway were more frequent in secondary compared with primary MH (90% vs 55%; P = .0012). PTPN11 mutations were exclusively observed in primary MH (P = .0035). Mutations in genes related to DNA methylation mechanisms (TET2, ASXL1, DNMT3A) and TP53 were present in 20% and 14% of cases, respectively. Although therapeutic regimens varied considerably, our results demonstrate that surgical resection in localized cases, and the use of BRAF or MEK inhibitors achieved the highest complete response rates, at 63% and 21%, respectively. The prognosis remains poor, with a 5-year overall survival rate of 31%, which is comparable to that of T/natural killer cell lymphomas. Prospective follow-up and a standardized treatment approach in specialized reference centers are crucial to improving patient survival. This trial was registered at www.clinicaltrials.gov as #NCT04437381.
format Article
id doaj-art-1767d8a40c2c4d14a705332734d0ac09
institution DOAJ
issn 2473-9529
language English
publishDate 2025-05-01
publisher Elsevier
record_format Article
series Blood Advances
spelling doaj-art-1767d8a40c2c4d14a705332734d0ac092025-08-20T03:13:39ZengElsevierBlood Advances2473-95292025-05-019102530254110.1182/bloodadvances.2024015208Characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in FranceCamille Bigenwald0Damien Roos-Weil1Arnaud Pagès2Zofia Hélias-Rodzewicz3Christiane Copie-Bergman4Marzieh Nashvi5Pierre Khneisser6Marie Parrens7Alexandra Traverse-Glehen8Isabelle Ray-Coquard9Loïc Ysebaert10Tony Marchand11Jérôme Razanamahery12Frédéric Charlotte13Antoine Neel14Gandhi Damaj15Jérémie Dion16Eve-Marie Nazal-Traissac17Stéphanie Tardy18Géraldine Salmeron19Hélène Monjanel20Ahmed Idbaih21Sébastien Héritier22Julien Haroche23Jean Donadieu24Jean-François Emile25Département d’Hématologie, Gustave Roussy, Villejuif, France; INSERM U1015, Gustave Roussy, Villejuif, France; Correspondence: Camille Bigenwald, Département d’Hématologie, Gustave Roussy, 114 Rue Edouard Vaillant, 94810 Villejuif, France;Sorbonne Université, Hematology Unit, Centre Hospitalier Universitaire Pitié-Salpêtrière, Assistance Publique Hôpitaux de Paris, Paris, FranceBureau de Biostatistique et d'Epidémiologie, Gustave Roussy et Centre de Recherche en Epidémiologie et Santé des Populations U1018, Oncostat, labellisé Ligue Contre le Cancer, INSERM, Villejuif, FranceParis-Saclay University, Versailles Saint Quentin en Yvelynes University, EA4340-Biomarqueurs et Essais Cliniques en Cancérologie et Onco-Hématologie, Assistance Publique Hôpitaux de Paris, Ambroise-Paré Hospital, Smart Imaging, Service de Pathologie, Boulogne, FranceParis-Est Créteil University, INSERM, Institut Mondor de Recherche Biomédicale, Pathology Department, Assistance Publique des Hôpitaux de Paris, Centre Hospitalier Universitaire Henri Mondor, Créteil, FranceINSERM U1015, Gustave Roussy, Villejuif, FranceDepartment of Pathology, Gustave Roussy Cancer Campus, Villejuif, FrancePathology Department, University of Bordeaux, Haut-Lévêque Hospital, Pessac, FranceUnité de Formation et de Recherche Claude Bernard Lyon 1, Hospices Civils de Lyon, Institut de Pathologie Multisite, Hôpital Lyon Sud, Lyon, FranceUniversité Claude Bernard Lyon 1, Hesper Laboratory, Department of Medical Oncology, Centre Leon Berard, Lyon, FranceHematology Department, Institut Universitaire du Cancer de Toulouse Oncopole, Toulouse, FranceService d'Hématologie Clinique, Centre Hospitalier Universitaire de Rennes, Universitéde Rennes, Unité Mixte de Recherche 1236, INSERM, Établissement Français du Sang Bretagne, Rennes, FranceDepartment of internal medicine and clinical immunology, Dijon University Hospital, Dijon, FrancePathology Department, Pitié Salpêtrière, Assistance Publique Hôpitaux de Paris, Paris, FranceService de Médecine Interne, Centre Hospitalier Universitaire de Nantes, Nantes, FranceInstitut d’Hématologie, Centre Hospitalier Universitaire de Caen, Université de Caen-Normandie, Caen, FranceInternal Medicine and Immunopathology Department, University Hospital Center of Toulouse Oncopole, Toulouse, FranceService de Médecine Interne, Centre Hospitalier Agen-Nérac, Agen, FranceDepartement d'Hématologie, Centre Hospitalier Annecy Genevois, Annecy, FranceDépartement d’Hématologie, Centre Hospitalier Intercommunal de Poissy, Saint Germain en Laye, FranceService de Médecine Interne, Centre Hospitalier Henri Mondor d'Aurillac, Aurillac, FranceSorbonne Université, INSERM, Centre National de la Recherche Scientifique, Unité Mixte de Recherche S 1127, Institut du Cerveau et de la Moelle Épinière, Institut du Cerveau et de la Moelle, Assistance Publique Hôpitaux de Paris, Hôpitaux Universitaires La Pitié Salpêtrière Charles Foix, Service de Neurologie 2-Mazarin, Paris, FranceFrench Reference Center for Histiocytosis, Department of Pediatric Hematology and Oncology, Trousseau Hospital, Assistance Publique Hôpitaux de Paris, Sorbonne Université, Paris, FranceSorbonne University, Internal Medicine Department 2, Institut E3M, French Reference Centre for Histiocytosis, Pitié-Salpȇtrière Hospital, Centre d'Immunologie et des Maladie Infectieuses INSERM-UMRS 1135, Assistance Publique Hôpitaux de Paris, Paris, FranceFrench Reference Center for Histiocytosis, Department of Pediatric Hematology and Oncology, Trousseau Hospital, Assistance Publique Hôpitaux de Paris, Sorbonne Université, Paris, FranceParis-Saclay University, Versailles Saint Quentin en Yvelynes University, EA4340-Biomarqueurs et Essais Cliniques en Cancérologie et Onco-Hématologie, Assistance Publique Hôpitaux de Paris, Ambroise-Paré Hospital, Smart Imaging, Service de Pathologie, Boulogne, France; Jean-François Emile, Département de Pathologie, Hôpital Ambroise Paré, 9 Ave Charles de Gaulle, 92104 Boulogne, France;Abstract: Malignant histiocytoses (MH) are rare and poorly understood cancers, with no established therapeutic guidelines. We conducted a national retrospective study of MH diagnosed in France between 2000 and 2023. All cases underwent centralized histological review, and several malignant tumors with a stroma highly enriched in histiocytes were excluded. In total, 141 patients were included, with a median age of 62 years (range, 1-87). The cases comprised either primary MH (64%) or MH associated with other hematologic malignancies (36%). Phenotypes corresponded to histiocytic (43%), interdigitating dendritic cell (37%) or Langerhans cell (12%) sarcomas, or high-grade indeterminate dendritic cell tumors (10%), as per the World Health Organization classification. Tumor cells were almost universally positive for CSF1R and PU.1, and 85% showed phosphorylated extracellular signal–regulated kinase positivity. Next-generation sequencing was performed in 75 cases. Mutations in the MAPK pathway were more frequent in secondary compared with primary MH (90% vs 55%; P = .0012). PTPN11 mutations were exclusively observed in primary MH (P = .0035). Mutations in genes related to DNA methylation mechanisms (TET2, ASXL1, DNMT3A) and TP53 were present in 20% and 14% of cases, respectively. Although therapeutic regimens varied considerably, our results demonstrate that surgical resection in localized cases, and the use of BRAF or MEK inhibitors achieved the highest complete response rates, at 63% and 21%, respectively. The prognosis remains poor, with a 5-year overall survival rate of 31%, which is comparable to that of T/natural killer cell lymphomas. Prospective follow-up and a standardized treatment approach in specialized reference centers are crucial to improving patient survival. This trial was registered at www.clinicaltrials.gov as #NCT04437381.http://www.sciencedirect.com/science/article/pii/S2473952925001314
spellingShingle Camille Bigenwald
Damien Roos-Weil
Arnaud Pagès
Zofia Hélias-Rodzewicz
Christiane Copie-Bergman
Marzieh Nashvi
Pierre Khneisser
Marie Parrens
Alexandra Traverse-Glehen
Isabelle Ray-Coquard
Loïc Ysebaert
Tony Marchand
Jérôme Razanamahery
Frédéric Charlotte
Antoine Neel
Gandhi Damaj
Jérémie Dion
Eve-Marie Nazal-Traissac
Stéphanie Tardy
Géraldine Salmeron
Hélène Monjanel
Ahmed Idbaih
Sébastien Héritier
Julien Haroche
Jean Donadieu
Jean-François Emile
Characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in France
Blood Advances
title Characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in France
title_full Characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in France
title_fullStr Characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in France
title_full_unstemmed Characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in France
title_short Characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in France
title_sort characterization and treatment outcomes of malignant histiocytoses in a retrospective series of 141 cases in france
url http://www.sciencedirect.com/science/article/pii/S2473952925001314
work_keys_str_mv AT camillebigenwald characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT damienroosweil characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT arnaudpages characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT zofiaheliasrodzewicz characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT christianecopiebergman characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT marziehnashvi characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT pierrekhneisser characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT marieparrens characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT alexandratraverseglehen characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT isabelleraycoquard characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT loicysebaert characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT tonymarchand characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT jeromerazanamahery characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT fredericcharlotte characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT antoineneel characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT gandhidamaj characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT jeremiedion characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT evemarienazaltraissac characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT stephanietardy characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT geraldinesalmeron characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT helenemonjanel characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT ahmedidbaih characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT sebastienheritier characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT julienharoche characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT jeandonadieu characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance
AT jeanfrancoisemile characterizationandtreatmentoutcomesofmalignanthistiocytosesinaretrospectiveseriesof141casesinfrance