Skip to main content
SpringerLink
Log in

Transformation risk and associated survival outcome of marginal zone lymphoma: A nationwide study

  • Research
  • Published:
Annals of Hematology Aims and scope Submit manuscript

Abstract

Histological transformation into an aggressive B-cell lymphoma indicates a poor survival outcome for patients with indolent marginal zone lymphoma (MZL), which has been less studied. Large-scale data with long-term follow-up to investigate MZL transformation is limited. Here, by reporting a US-Nationwide cohort of 30,619 MZL patients diagnosed between 2000 and 2019, we found that transformation occurred in 2.08% (N = 624) of MZL cases, with the transformation incidence of 3.1 per 1,000 person-years. Advanced Ann Arbor stage, nodal MZL (NMZL) and splenic MZL (SMZL) were associated with an elevated risk of transformation. Certain subtype-specific characteristics, such as non-gastric extra-nodal MZL (vs. gastric, HR, 1.51, 95%CI 1.13–2.04; p = 0.006), and receiving splenectomy for SMZL (HR, 2.04, 95%CI 1.28–3.26; p = 0.003), also indicated a higher risk of transformation. Besides, transformation independently increased the overall mortality risk (HR, 1.38, 95%CI 1.24–1.53, p < 0.001), especially the higher lymphoma-caused mortality risk (HR, 3.21, 95%CI 2.81–3.67, p < 0.001). Transformation was also associated with a higher percentage of lymphoma-caused deaths. The post-transformation prognostic analyses demonstrated that female gender and age ≥ 65 years independently affected patients’ mortalities. These findings, based on the largest cohort to date, contribute to a better understanding of transformed MZL, and provide valuable reference points for guidelines and patient counseling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

No datasets were generated or analysed during the current study.

References

  1. Cerhan JR, Habermann TM (2021) Epidemiology of Marginal Zone Lymphoma. Ann Lymphoma ; 5. e-pub ahead of print 2021/04/09; https://doi.org/10.21037/aol-20-28

  2. Sriskandarajah P, Dearden CE (2017) Epidemiology and environmental aspects of marginal zone lymphomas. Best Pract Res Clin Haematol ; 30(1–2): 84–91. e-pub ahead of print 2017/03/16; https://doi.org/10.1016/j.beha.2016.07.002

  3. Alaggio R, Amador C, Anagnostopoulos I, Attygalle AD, Araujo IBO, Berti E, of the World Health Organization Classification of Haematolymphoid Tumours (2022) The 5th edition: Lymphoid Neoplasms. Leukemia ; 36(7): 1720–1748. e-pub ahead of print 2022/06/23; https://doi.org/10.1038/s41375-022-01620-2

  4. Campo E, Jaffe ES, Cook JR, Quintanilla-Martinez L, Swerdlow SH, Anderson KC et al (2022) The International Consensus classification of mature lymphoid neoplasms: a report from the Clinical Advisory Committee. Blood 140(11):1229–1253 e-pub ahead of print 2022/06/03. https://doi.org/10.1182/blood.2022015851

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Cheah CY, Seymour JF (2023) Marginal zone lymphoma: 2023 update on diagnosis and management. Am J Hematol 98(10):1645–1657 e-pub ahead of print 2023/08/22. https://doi.org/10.1002/ajh.27058

    Article  PubMed  Google Scholar 

  6. Amaador K, Thieblemont C, Trotman J, Minnema MC (2023) Recent updates in the indolent lymphomas: update on marginal zone lymphoma and Waldenström’s macroglobulinemia. Hematol Oncol. e-pub ahead of print 2023/07/17 https://doi.org/10.1002/hon.3210

    Article  PubMed  Google Scholar 

  7. Bult JAA, Huisman F, Zhong Y, Veltmaat N, Kluiver J, Tonino SH et al (2023) A population-based study of transformed marginal zone lymphoma: identifying outcome-related characteristics. Blood Cancer J 13(1):130 e-pub ahead of print 2023/09/02. https://doi.org/10.1038/s41408-023-00903-w

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kalashnikov I, Tanskanen T, Viisanen L, Malila N, Jyrkkiö S, Leppä S (2023) Transformation and survival in marginal zone lymphoma: a Finnish nationwide population-based study. Blood Cancer J ; 13(1): 62. e-pub ahead of print 2023/05/15; https://doi.org/10.1038/s41408-023-00831-9

  9. Olszewski AJ, Castillo JJ (2013) Survival of patients with marginal zone lymphoma: analysis of the Surveillance, Epidemiology, and end results database. Cancer 119(3):629–638 e-pub ahead of print 2012/08/16. https://doi.org/10.1002/cncr.27773

    Article  PubMed  Google Scholar 

  10. Montoto S, Fitzgibbon J (2011) Transformation of indolent B-cell lymphomas. J Clin Oncol 29(14):1827–1834

    Article  PubMed  Google Scholar 

  11. Godfrey J, Leukam MJ, Smith SM (2018) An update in treating transformed lymphoma. Best Pract Res Clin Haematol 31(3):251–261

    Article  PubMed  Google Scholar 

  12. Maeshima AM, Taniguchi H, Toyoda K, Yamauchi N, Makita S, Fukuhara S et al (2016) Clinicopathological features of histological transformation from extranodal marginal zone B-cell lymphoma of mucosa‐associated lymphoid tissue to diffuse large B‐cell lymphoma: an analysis of 467 patients. Br J Haematol 174(6):923–931

    Article  PubMed  CAS  Google Scholar 

  13. Bastidas-Mora G, Beà S, Navarro A, Gine E, Costa D, Delgado J et al (2022) Clinico‐biological features and outcome of patients with splenic marginal zone lymphoma with histological transformation. Br J Haematol 196(1):146–155

    Article  PubMed  CAS  Google Scholar 

  14. Fine JP, Gray RJ (1999) A proportional hazards model for the subdistribution of a competing risk. Publications Am Stat Association 94(446):496–509

    Article  MathSciNet  Google Scholar 

  15. Alderuccio JP, Zhao W, Desai A, Gallastegui N, Ramdial J, Kimble E et al Risk Factors for Transformation to Higher-Grade Lymphoma and Its Impact on Survival in a Large Cohort of Patients With Marginal Zone Lymphoma From a Single Institution. J Clin Oncol 2018: Jco1800138. e-pub ahead of print 2018/10/13; https://doi.org/10.1200/jco.18.00138

  16. Bastidas-Mora G, Beà S, Navarro A, Gine E, Costa D, Delgado J et al (2022) Clinico-biological features and outcome of patients with splenic marginal zone lymphoma with histological transformation. Br J Haematol 196(1):146–155 e-pub ahead of print 2021/09/15. https://doi.org/10.1111/bjh.17815

    Article  PubMed  CAS  Google Scholar 

  17. Conconi A, Franceschetti S, von Aprile K, Margiotta-Casaluci G, Stathis A, Moccia AA et al (2015) Histologic transformation in marginal zone lymphomas†. Ann Oncol 26(11):2329–2335 e-pub ahead of print 2015/09/25. https://doi.org/10.1093/annonc/mdv368

    Article  PubMed  CAS  Google Scholar 

  18. Maeshima AM, Taniguchi H, Toyoda K, Yamauchi N, Makita S, Fukuhara S et al (2016) Clinicopathological features of histological transformation from extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue to diffuse large B-cell lymphoma: an analysis of 467 patients. Br J Haematol 174(6):923–931 e-pub ahead of print 2016/07/28. https://doi.org/10.1111/bjh.14153

    Article  PubMed  CAS  Google Scholar 

  19. Meyer AH, Stroux A, Lerch K, Eucker J, Eitle J, Hohloch K et al (2014) Transformation and additional malignancies are leading risk factors for an adverse course of disease in marginal zone lymphoma. Ann Oncol 25(1):210–215 e-pub ahead of print 2013/12/21. https://doi.org/10.1093/annonc/mdt507

    Article  PubMed  CAS  Google Scholar 

  20. Rodrigues CD, Peixeiro RP, Viegas D, Chorão P, Couto ME, Gaspar CL et al (2021) Clinical Characteristics, Treatment and Evolution of Splenic and Nodal Marginal Zone Lymphomas-Retrospective and Multicentric Analysis of Portuguese Centers. Clin Lymphoma Myeloma Leuk ; 21(11): e839-e844. e-pub ahead of print 2021/07/31; https://doi.org/10.1016/j.clml.2021.06.013

  21. Alderuccio JP, Zhao W, Desai A, Ramdial J, Gallastegui N, Kimble E et al (2019) Short survival and frequent transformation in extranodal marginal zone lymphoma with multiple mucosal sites presentation. Am J Hematol 94(5):585–596 e-pub ahead of print 2019/02/21. https://doi.org/10.1002/ajh.25446

    Article  PubMed  Google Scholar 

  22. Conconi A, Ponzio C, Lobetti-Bodoni C, Motta M, Rancoita PM, Stathis A et al (2012) Incidence, risk factors and outcome of histological transformation in follicular lymphoma. Br J Haematol ; 157(2): 188–196. e-pub ahead of print 2012/02/22; https://doi.org/10.1111/j.1365-2141.2012.09054.x

  23. Yang Z, Liu L, Leng K, Shi G (2023) Time Trend Analysis of Splenectomy for splenic marginal zone lymphoma: declining surgery, promising survival. Ann Surg Oncol. e-pub ahead of print 2023/07/30 https://doi.org/10.1245/s10434-023-13968-5

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

All authors sincerely thank the staff of the SEER Program for the development of the database.

Funding

This work was supported by Postdoctoral Fellowship Program of CPSF (No. GZB20230481), National Natural Science Foundation of China (No. 82303773, No. 82303772, No. 82204490, No. 82303694), Natural Science Foundation of Sichuan Province (No. 2023NSFSC1885), Key Research and Development Program of Sichuan Province (No. 23ZDYF2836), the 2024 College Students’ Innovative Entrepreneurial Training Plan Program (No. C2024130171, No. 2024128798), 1·3·5 project for disciplines of excellence, West China Hospital, Sichuan University (No. ZYJC21007), and National Key Research and Development Program of China (No. 2022YFC2502600, 2022YFC2502603).

Author information

Author notes

  1. Xu Sun and He Li contributed equally to this work.

Authors and Affiliations

  1. Department of Hematology, West China Hospital, Sichuan University, Chengdu, Sichuan, 610041, China

    Xu Sun, He Li, Qinyu Liu, Li Wang, Ailin Zhao & Ting Niu

  2. Cancer Center, West China Hospital, Sichuan University, Chengdu, Sichuan, 610041, China

    Yijun Wu, Kai Kang & Ren Luo

  3. West China School of Medicine, Sichuan University, Chengdu, Sichuan, 610041, China

    Yuqi Yang

Authors
  1. Xu Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. He Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuqi Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yijun Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kai Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qinyu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ren Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Li Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ailin Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ting Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XS, HL, YY, TN, and AZ designed, created the study, and wrote the manuscript. XS, YW, RL, LW, and KK performed the data analyses. XS, TN, and AZ supervised the study. XS, QL, and HL critically reviewed the manuscript. All authors approved the final manuscript.

Corresponding authors

Correspondence to Ailin Zhao or Ting Niu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Human Ethics and Consent to participate

Human Ethics and Consent to Participate declarations: not applicable.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, X., Li, H., Yang, Y. et al. Transformation risk and associated survival outcome of marginal zone lymphoma: A nationwide study. Ann Hematol (2024). https://doi.org/10.1007/s00277-024-05688-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00277-024-05688-x

Keywords

Search

Navigation