International Journal of Hematology

, Volume 110, Issue 3, pp 375–380 | Cite as

Transformation of follicular lymphoma to double-hit lymphoma during adjuvant chemotherapy for concurrent ovarian carcinoma

  • Taisuke Narazaki
  • Yasuhiro Nakashima
  • Yasuhiro Tsukamoto
  • Mariko Tsuda
  • Toru Masuda
  • Daisaku Kimura
  • Akiko Takamatsu
  • Koichi Ohshima
  • Motoaki ShiratsuchiEmail author
  • Yoshihiro Ogawa
Case Report


The frequency of multiple primary malignant neoplasms (MPMN) is increasing due to population aging. Since consensus guidelines for the treatment of MPMN are lacking, treatment strategies are determined by disease status on a per-patient basis. In this report, we describe a case of MPMN with follicular lymphoma (FL) grade 1 that transformed to double-hit lymphoma during adjuvant chemotherapy for concurrent ovarian carcinoma. A 64-year-old woman was diagnosed with MPMN of FL and endometrioid carcinoma by staging laparotomy and lymph node biopsy. She received four cycles of adjuvant chemotherapy (carboplatin and paclitaxel) for endometrioid carcinoma, but during chemotherapy, the FL grade 1 transformed to double-hit lymphoma. We speculate that adjuvant chemotherapy for endometrioid carcinoma may have triggered the transformation of FL in the present case.


Follicular lymphoma Transformation Double-hit lymphoma Multiple primary malignant neoplasms 


Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Demandante CG, Troyer DA, Miles TP. Multiple primary malignant neoplasms: case report and a comprehensive review of the literature. Am J Clin Oncol. 2003;26:79–83.CrossRefPubMedGoogle Scholar
  2. 2.
    Tamura M, Shinagawa M, Funaki Y. Synchronous triple early cancers occurring in the stomach, colon and gallbladder. Asian J Surg. 2003;26:46–8.CrossRefPubMedGoogle Scholar
  3. 3.
    Van Dalen R, Church J, McGannon E, Fay S, Burke C, Clark B. Patterns of surgery in patients belonging to amsterdam-positive families. Dis Colon Rectum. 2003;46:617–20.CrossRefPubMedGoogle Scholar
  4. 4.
    Mozessohn L, Cheung MC, Crump M, Buckstein R, Berinstein N, Imrie K, et al. Chemoimmunotherapy resistant follicular lymphoma: predictors of resistance, association with transformation and prognosis. Leuk Lymphoma. 2014;55:2502–7.CrossRefPubMedGoogle Scholar
  5. 5.
    Prat J, FIGO Committee on Gynecologic Oncology. Staging classification for cancer of the ovary, fallopian tube, and peritoneum. Int J Gynaecol Obstet. 2014;124:1–5.CrossRefPubMedGoogle Scholar
  6. 6.
    Solal-Céligny P, Roy P, Colombat P, White J, Armitage JO, Arranz-Saez R, et al. Follicular lymphoma international prognostic index. Blood. 2004;104:1258–65.CrossRefPubMedGoogle Scholar
  7. 7.
    Warren S, Gates O. Multiple primary malignant tumors: a survey of the literature and a statistical study. Am J Cancer. 1932;16:1358–414.Google Scholar
  8. 8.
    Brice P, Bastion Y, Lepage E, Brousse N, Haïoun C, Moreau P, et al. Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: a randomized study from the Groupe d’Etude des Lymphomes Folliculaires Groupe d’Etude des Lymphomes de l’Adulte. J Clin Oncol. 1997;15:1110–7.CrossRefPubMedGoogle Scholar
  9. 9.
    Ardeshna KM, Qian W, Smith P, Braganca N, Lowry L, Patrick P, et al. Rituximab versus a watch-and-wait approach in patients with advanced-stage, asymptomatic, non-bulky follicular lymphoma: an open-label randomized phase 3 trial. Lancet Oncol. 2014;15:424–35.CrossRefPubMedGoogle Scholar
  10. 10.
    Xu X, Zhang L, Wang Y, Zhang Q, Zhang L, Sun B, et al. Double-hit and triple-hit lymphomas arising from follicular lymphoma following acquisition of MYC: report of two cases and literature review. Int J Clin Exp Pathol. 2013;6:788–94.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Pedersen MØ, Gang AO, Poulsen TS, Knudsen H, Lauritzen AF, Nielsen SL, et al. Double-hit BCL2/MYC translocations in a consecutive cohort of patients with large B-cell lymphoma—a single centre’s experience. Eur J Haematol. 2012;89:63–71.CrossRefPubMedGoogle Scholar
  12. 12.
    Bischin AM, Dorer R, Aboulafia DM. Transformation of follicular lymphoma to a high-grade B-cell lymphoma with MYC and BCL2 Translocations and Overlapping Features of Burkitt lymphoma and acute lymphoblastic leukemia: a case report and literature review. Clin Med Insights Blood Disord. 2017;10:1–8.CrossRefGoogle Scholar
  13. 13.
    Casulo C, Burack WR, Friedberg JW. Transformed follicular non-Hodgkin lymphoma. Blood. 2015;125:40–7.CrossRefPubMedGoogle Scholar
  14. 14.
    Kridel R, Sehn LH, Gascoyne RD. Can histologic transformation of follicular lymphoma be predicted and prevented? Blood. 2017;130:258–66.CrossRefPubMedGoogle Scholar
  15. 15.
    Kridel R, Chan FC, Mottok A, Boyle M, Farinha P, Tan K, et al. Histological transformation and progression in follicular lymphoma: a clonal evolution study. PLoS Med. 2016;13:e1002197.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Okosun J, Bödör C, Wang J, Araf S, Yang CY, Pan C, et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat Genet. 2014;46:176–81.CrossRefPubMedGoogle Scholar
  17. 17.
    Pasqualucci L, Khiabanian H, Fangazio M, Vasishtha M, Messina M, Holmes AB, et al. Genetics of follicular lymphoma transformation. Cell Rep. 2014;6:130–40.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med. 2004;351:2159–69.CrossRefPubMedGoogle Scholar
  19. 19.
    Andrews PA, Howell SB. Cellular pharmacology of cisplatin: perspectives on mechanisms of acquired resistance. Cancer Cells. 1990;2:35–43.PubMedGoogle Scholar
  20. 20.
    Travis LB, Andersson M, Gospodarowicz M, van Leeuwen FE, Bergfeldt K, Lynch CF, et al. Treatment-associated leukemia following testicular cancer. J Natl Cancer Inst. 2000;92:1165–71.CrossRefPubMedGoogle Scholar
  21. 21.
    Danesi CC, Bellagamba BC, Dihl RR, de Andrade HH, Cunha KS, Lehmann M. Evaluation of the genotoxicity of cisplatin, paclitaxel and 5-fluorouracil combined treatment in the Drosophila wing-spot test. Food Chem Toxicol. 2010;48:3120–4.CrossRefPubMedGoogle Scholar
  22. 22.
    Dertinger SD, Avlasevich SL, Torous DK, Bemis JC, Phonethepswath S, Labash C, et al. Persistence of cisplatin-induced mutagenicity in hematopoietic stem cells: implications for secondary cancer risk following chemotherapy. Toxicol Sci. 2014;140:307–14.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Takagi M. DNA damage response and hematological malignancy. Int J Hematol. 2017;106:345–56.CrossRefPubMedGoogle Scholar
  24. 24.
    Walker TL, White JD, Esdale WJ, Burton MA, DeCruz EE. Tumour cells surviving in vivo cisplatin chemotherapy display elevated c-myc expression. Br J Cancer. 1996;73:610–4.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Ikeguchi M, Nakamura S, Kaibara N. Quantitative analysis of expression levels of bax, bcl-2, and survivin in cancer cells during cisplatin treatment. Oncol Rep. 2002;9:1121–6.PubMedGoogle Scholar
  26. 26.
    Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med. 2004;18(351):2159–69.CrossRefGoogle Scholar

Copyright information

© Japanese Society of Hematology 2019

Authors and Affiliations

  • Taisuke Narazaki
    • 1
  • Yasuhiro Nakashima
    • 1
  • Yasuhiro Tsukamoto
    • 1
  • Mariko Tsuda
    • 1
  • Toru Masuda
    • 1
  • Daisaku Kimura
    • 1
  • Akiko Takamatsu
    • 1
  • Koichi Ohshima
    • 2
  • Motoaki Shiratsuchi
    • 1
    Email author
  • Yoshihiro Ogawa
    • 1
  1. 1.Department of Medicine and Bioregulatory Science, Graduate School of Medical SciencesKyushu UniversityFukuokaJapan
  2. 2.Department of PathologyKurume University School of MedicineKurumeJapan

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