Recurrent primary cutaneous marginal zone lymphoma: a comparative study of initial tumours, recurrences, and outcomes in 61 patients

Fanny Beltzung; Marie Beylot-Barry; Maxime Battistella; Caroline Ram-Wolff; Adèle de Masson; Jean-Michel Cayuela; Brigitte Balme; Marie Donzel; Stéphane Dalle; Florent Grange; Laurence Lamant; Serge Boulinguez; Marie-Hélène Lorton; Géraldine Jeudy; Nicolas Ortonne; Saskia Ingen-Housz-Oro; Agnès Carlotti; Nathalie Franck; Sophie Schneider; Anne Pham-Ledard; Audrey Bidet; Rémi Vergara; Pierre Dubus; Charline Caumont; Samuel Amintas; Béatrice Vergier

doi:10.1111/his.15377

Recurrent primary cutaneous marginal zone lymphoma: a comparative study of initial tumours, recurrences, and outcomes in 61 patients

Histopathology. 2024 Dec 4. doi: 10.1111/his.15377. Online ahead of print.

Authors

Fanny Beltzung^{1

2

3}, Marie Beylot-Barry^{2

3

4}, Maxime Battistella^{3

5

6}, Caroline Ram-Wolff^{3

7}, Adèle de Masson^{3

7}, Jean-Michel Cayuela⁸, Brigitte Balme^{3

9}, Marie Donzel^{3

9}, Stéphane Dalle^{3

10}, Florent Grange^{3

11}, Laurence Lamant^{3

12}, Serge Boulinguez^{3

13}, Marie-Hélène Lorton^{3

14}, Géraldine Jeudy^{3

15}, Nicolas Ortonne^{3

16}, Saskia Ingen-Housz-Oro^{3

17}, Agnès Carlotti^{3

18}, Nathalie Franck^{3

19}, Sophie Schneider⁴, Anne Pham-Ledard^{2

3

4}, Audrey Bidet²⁰, Rémi Vergara¹, Pierre Dubus^{2

21}, Charline Caumont²¹, Samuel Amintas^{2

21}, Béatrice Vergier^{1

2

3}

Affiliations

¹ Pathology Department, CHU de Bordeaux, Bordeaux, France.
² University of Bordeaux, Inserm, UMR1312, BRIC, Bordeaux Institute of Oncology, Bordeaux, France.
³ French Study Group of Cutaneous Lymphomas, France.
⁴ Dermatology Department, CHU de Bordeaux, Bordeaux, France.
⁵ Pathology Department, Hôpital Saint Louis, AP-HP. Université de Paris, Paris, France.
⁶ INSERM UMR-S976, Human Immunology, Pathophysiology and Immunotherapies, Paris, France.
⁷ Dermatology Department, Hôpital Saint Louis, AP-HP, Paris, France.
⁸ Hematobiology Department, Hôpital Saint Louis, AP-HP, Paris, France.
⁹ Pathology Department, Hospices civils de Lyon, Lyon, France.
¹⁰ Dermatology Department, Hospices civils de Lyon, Lyon, France.
¹¹ Dermatology Department, Centre Hospitalier de Valence, Valence, France.
¹² Pathology Department, CHU de Toulouse, Toulouse, France.
¹³ Dermatology Department, CHU de Toulouse, Toulouse, France.
¹⁴ Pathology Department, CHU de Dijon, Dijon, France.
¹⁵ Dermatology Department, CHU de Dijon, Dijon, France.
¹⁶ Pathology Department, CHU de Créteil, Paris, France.
¹⁷ Dermatology Department, CHU de Créteil, Paris, France.
¹⁸ Pathology Department, Hôpital Tarnier, AP-HP, Paris, France.
¹⁹ Dermatology Department, Hôpital Tarnier, AP-HP, Paris, France.
²⁰ Hematobiology Department, CHU de Bordeaux, Bordeaux, France.
²¹ Tumor Biology Department, CHU de Bordeaux, Bordeaux, France.

PMID: 39628350
DOI: 10.1111/his.15377

Abstract

Aims: Primary cutaneous marginal zone lymphoma (PCMZL) is considered a lymphoproliferative disorder (International Consensus Classification, ICC) or an overt lymphoma (WHO-HAEM5). Seeking evidence for a reactive process or true lymphoma, we retrieved recurrent PCMZLs from the French Study Group of Cutaneous Lymphoma (GFELC) database.

Methods: Histology, phenotype (light-chain restriction, immunoglobulin, and immune-receptor translocation-associated protein-1 [IRTA1] expression) and B-cell clonality at diagnosis and recurrence were compared according to recurrence site (local, locoregional, or distant) and outcomes.

Results: Initial lesions of the 61 patients (mean age 52) were mostly isolated on the trunk (48%) and classified T1 (70%). Times to first recurrence for local, locoregional, and distant recurrences, were 20, 29, and 37 months, respectively. Light-chain restriction type did not differ significantly between local/locoregional recurrences and distal recurrences (P = 0.06; n = 60). The same B-cell clones were identified for 23/42 local/locoregional recurrences, while 5/19 distant recurrences showed different clonal profiles (P = 0.0003). No tumour expressed IRTA1. Fifty-eight tumours were heavy-chain (IgG/IgG4) class-switched PCMZLs and 3 IgM+/IgD- PCMZLs. All IgM+ tumours underwent either transformation (skin or brain) into diffuse large B-cell lymphomas (DLBCLs) and extracutaneous spreading.

Conclusion: As suggested by WHO-HAEM5, immunoglobulin phenotype assessment (IgM alongside IgD) appears to be a possible valuable tool in the initial diagnosis of PCMZL to differentiate between the indolent class-switched PCMZL (IgM-negative) and IgM+ (IgD-) PCMZL, which has an uncertain prognosis. The variation in B-cell rearrangements and light chain restriction observed in distant recurrences of PCMZL may suggest different antigen-driven stimulation processes.

Keywords: heavy‐chain class‐switched; primary cutaneous marginal zone lymphoma; primary cutaneous marginal zone lymphoproliferative disorder; transformed marginal zone lymphoma.