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Clinicopathological features of in situ follicular neoplasm and relations with follicular lymphoma in Japan

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Abstract

This study aims to investigate the clinicopathological features of in situ follicular neoplasm (ISFN) in Japan. ISFN is a rare condition formerly considered as an early precursor of follicular lymphoma (FL). This is a first original report of ISFN from Asian country. We reviewed 19 biopsy samples of ISFN. ISFNs were categorized into two groups: (1) ISFN, consisting of ISFN with strong positivity for BCL-2 immunohistochemical staining (IHC), and obvious translocation of BCL-2; and (2) ISFN-like FL, featuring cases without obvious translocation but having morphological features and characteristic IHC findings of ISFN. As control, we adopted obvious FL. For some cases showing coexisting ISFN and FL lesions in the same lymph node, we could conduct further clonality analysis for each lesion. Nine of the 19 cases of ISFN coexisted with FL or had a history of overt B- or T-cell lymphoma including FL. Statistical comparison among ISFN-like FL and FL showed no significant differences in pathological features. Molecular analysis suggested that ISFN lesion and FL lesion in the same lymph node each have a different clonality. ISFN coexists or associates with other overt lymphomas frequently.

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References

  1. Jaffe ES, Harris NL, Swerdlow SH et al (2017) Follicular lymphoma. In: Swerdlow SH, Campo E, Harris NL (eds) WHO classification of tumours of haematopoietic and lymphoid tissues. Revised, 4th edn. International Agency for Research on Cancer, Lyon, pp 266–277

    Google Scholar 

  2. Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R, Advani R, Ghielmini M, Salles GA, Zelenetz AD, Jaffe ES (2016) The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood 127:2375–2390

    Article  CAS  Google Scholar 

  3. Bermudez G, Gonzalez de Villambrosia S, Martinez-Lopez A et al (2016) Incidental and isolated follicular lymphoma in situ and mantle cell lymphoma in situ lack clinical significance. Am J Surg Pathol 40:943–949

    Article  Google Scholar 

  4. Henopp T, Quintanilla-Martinez L (2011) Prevalence of follicular lymphoma in situ in consecutively analysed reactive lymph nodes. Histopathology 59:139–142

    Article  Google Scholar 

  5. Carvajal-Cuenca A, Sua LF, Silva NM, Pittaluga S, Royo C, Song JY, Sargent RL, Espinet B, Climent F, Jacobs SA, Delabie J, Naresh KN, Bagg A, Brousset P, Warnke RA, Serrano S, Harris NL, Swerdlow SH, Jaffe ES, Campo E (2012) In situ mantle cell lymphoma: clinical implications of an incidental finding with indolent clinical behavior. Haematologica 97:270–278

    Article  Google Scholar 

  6. Scheler F, Hirt C (2003) Chromosomal translocation t(14;18) in healthy individuals. Semin Cancer Biol 13:203–209

    Article  Google Scholar 

  7. Ohshima K, Kikuchi M (1993) Amplified bcl-2/JH rearrangements in reactive lymphadenopathy. Virchows Arch B Cell Pathol Incl Mol Pathol 63:197–198

    Article  CAS  Google Scholar 

  8. Levy D, Bertoldi ERM (2017) Presence of t(14;18) translocation in healthy individuals varies according to ethnic background in the Brazilian population. Braz J Med Biol Res 50:e6172

    Article  CAS  Google Scholar 

  9. Yasukawa M, Bando S, Dolken G et al (2001) Low frequency of BCL-2/J(H) translocation in peripheral blood lymphocytes of healthy Japanese individuals. Blood 98:486–488

    Article  CAS  Google Scholar 

  10. Roulland S, Kelly RS, Morgado E et al (2014) t(14;18) translocation: a predictive blood biomarker for follicular lymphoma. J Clin Oncol 32:1347–1355

    Article  Google Scholar 

  11. Cheung MC, Bailey D, Pennell N, Imrie KR, Berinstein NL, Amato D, Ghorab Z (2009) In situ localization of follicular lymphoma: evidence for subclinical systemic disease with detection of an identical BCL-2/IGH fusion gene in blood and lymph node. Leukemia 23:1176–1179

    Article  CAS  Google Scholar 

  12. Jegalian AG, Eberle FC, Pack SD, Mirvis M, Raffeld M, Pittaluga S, Jaffe ES (2011) Follicular lymphoma in situ: clinical implications and comparisons with partial involvement by follicular lymphoma. Blood 118:2976–2984

    Article  CAS  Google Scholar 

  13. Pillai RK, Surti U (2013) Follicular lymphoma-like B cells of uncertain significance (in situ follicular lymphoma) may infrequently progress, but precedes follicular lymphoma, is associated with other overt lymphomas and mimics follicular lymphoma in flow cytometric studies. Haematologica 98:1571–1580

    Article  Google Scholar 

  14. Montes-Moreno S, Castro Y (2010) Intrafollicular neoplasia/in situ follicular lymphoma: review of a series of 13 cases. Histopathology 56:658–661

    Article  Google Scholar 

  15. Carbone A, Tibiletti MG, Canzonieri V et al (2012) In situ follicular lymphoma associated with nonlymphoid malignancies. Leuk Lymphoma 53(4):603–608

    Article  CAS  Google Scholar 

  16. Bonzheim I, Salaverria I, Haake A, Gastl G, Adam P, Siebert R, Fend F, Quintanilla-Martinez L (2011) A unique case of follicular lymphoma provides insights to the clonal evolution from follicular lymphoma in situ to manifest follicular lymphoma. Blood 118:3442–3444

    Article  CAS  Google Scholar 

  17. Carbone A, Della LD, Zannier L et al (2011) In situ follicular lymphoma associated with overt B- or T-cell lymphomas in the same lymph node. Am J Hematol 86:E66–E70

    Article  Google Scholar 

  18. Torlakovic E, Torlakovic G (2002) Follicular colonization by follicular lymphoma. Arch Pathol Lab Med 126:1136–1137

    PubMed  Google Scholar 

  19. Schmidt J, Salaverria I, Haake A, Bonzheim I, Adam P, Montes-Moreno S, Piris MA, Fend F, Siebert R, Quintanilla-Martinez L (2014) Increasing genomic and epigenomic complexity in the clonal evolution from in situ to manifest t(14;18)-positive follicular lymphoma. Leukemia 28:1103–1112

    Article  CAS  Google Scholar 

  20. Cong P, Raffeld M (2002) In situ localization of follicular lymphoma: description and analysis by laser capture microdissection. Blood. 99:3376–3383

    Article  CAS  Google Scholar 

  21. Masir N, Campbell LJ (2010) Pseudonegative BCL2 protein expression in a t(14;18) translocation positive lymphoma cell line: a need for an alternative BCL2 antibody. Pathology 42(3):212–216

    Article  CAS  Google Scholar 

  22. Carbone A, Gloghini A (2014) Emerging issues after the recognition of in situ follicular lymphoma. Leuk Lymphoma 55(3):482–490

    Article  Google Scholar 

  23. Oishi N, Montes-Moreno S (2018) In situ neoplasia in lymph node pathology. Semin Diagn Pathol 35:76–83

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Pathology, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka, Japan

    Satoko Ogata, Hiroaki Miyoshi, Fumiko Arakawa, Joji Shimono, Kyohei Yamada, Eriko Yanagida & Koichi Ohshima

  2. Department of Pathology, Fukuoka University Chikushi Hospital, Fukuoka, Japan

    Satoko Ogata, Akinori Iwashita & Seiji Haraoka

  3. Department of Medical Technology, Kumamoto Health Science University, Kumamoto, Japan

    Masami Nambu

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  1. Satoko Ogata
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  2. Hiroaki Miyoshi
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  3. Fumiko Arakawa
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  4. Joji Shimono
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  5. Kyohei Yamada
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  6. Eriko Yanagida
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  7. Masami Nambu
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  8. Akinori Iwashita
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  9. Seiji Haraoka
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  10. Koichi Ohshima
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Correspondence to Hiroaki Miyoshi.

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Ogata, S., Miyoshi, H., Arakawa, F. et al. Clinicopathological features of in situ follicular neoplasm and relations with follicular lymphoma in Japan. Ann Hematol 99, 241–253 (2020). https://doi.org/10.1007/s00277-019-03841-5

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  • DOI: https://doi.org/10.1007/s00277-019-03841-5

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