Skip to main content

Advertisement

Log in

Indolent lymphomas in the pediatric population: follicular lymphoma, IRF4/MUM1+ lymphoma, nodal marginal zone lymphoma and chronic lymphocytic leukemia

  • Review and Perspectives
  • Published:
Virchows Archiv Aims and scope Submit manuscript

Abstract

Indolent lymphomas in the pediatric population were discussed during the 2014 European Association for Haematopathology/Society of Hematopathology workshop in Istanbul, Turkey. This session was focused on pediatric-type follicular lymphoma (FL), and its differential diagnosis with the newly recognized entity of IRF4/MUM1+ lymphomas mainly involving Waldeyer’s ring. The differential diagnosis between t(14;18) negative FL grade 1/2 and pediatric-type FL in adults was highlighted. The overlapping pathological and clinical features between FL and nodal marginal zone lymphoma (NMZL) in children and young adults were recognized and morphologic and immunophenotypical criteria helpful for the differential diagnosis were presented. Both pediatric-type FL and NMZL are indolent processes that should be distinguished from atypical lymphoid hyperplasia of the tonsils and lymph nodes. The demonstration of a B cell monoclonal population by molecular studies is strongly recommended for the diagnosis. Recognition of these indolent variants to avoid overtreatment was emphasized. Whereas most indolent lymphomas in the pediatric population show characteristic clinical, pathologic, and genetic features that differ from the adult counterpart, other rare indolent lymphoid tumors such as chronic lymphocytic leukemia (CLL) have similar characteristics. In this report, novel findings, areas of special interest, and diagnostic challenges emerging from the cases submitted to the workshop will be discussed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Burkhardt B, Oschlies I, Klapper W, Zimmermann M, Woessmann W, Meinhardt A, Landmann E, Attarbaschi A, Niggli F, Schrappe M, Reiter A (2011) Non-Hodgkin’s lymphoma in adolescents: experiences in 378 adolescent NHL patients treated according to pediatric NHL-BFM protocols. Leukemia 25:153–160. doi:10.1038/leu.2010.245

    Article  CAS  PubMed  Google Scholar 

  2. Oschlies I, Klapper W (2014) Malignant lymphomas in children and adolescents. Practical knowledge for diagnosis. Pathologe 35:383–395. doi:10.1007/s00292-014-1891-5, quiz 396–387

    Article  CAS  PubMed  Google Scholar 

  3. Harris NL, Swerdlow SH, Jaffe ES (2008) Follicular lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (eds) WHO classification of tumours of haematopoietic and lymphoid tissues. International Agency for Research on Cancer, Lyon, pp 220–226

    Google Scholar 

  4. Frizzera G, Murphy SB (1979) Follicular (nodular) lymphoma in childhood: a rare clinical-pathological entity. Report of eight cases from four cancer centers. Cancer 44:2218–2235

    Article  CAS  PubMed  Google Scholar 

  5. Winberg CD, Nathwani BN, Bearman RM, Rappaport H (1981) Follicular (nodular) lymphoma during the first two decades of life: a clinicopathologic study of 12 patients. Cancer 48:2223–2235

    Article  CAS  PubMed  Google Scholar 

  6. Oschlies I, Salaverria I, Mahn F, Meinhardt A, Zimmermann M, Woessmann W, Burkhardt B, Gesk S, Krams M, Reiter A, Siebert R, Klapper W (2010) Pediatric follicular lymphoma—a clinico-pathological study of a population-based series of patients treated within the non-Hodgkin’s lymphoma--Berlin-Frankfurt-Munster (NHL-BFM) multicenter trials. Haematologica 95:253–259. doi:10.3324/haematol.2009.013177

    Article  PubMed  PubMed Central  Google Scholar 

  7. Liu Q, Salaverria I, Pittaluga S, Jegalian AG, Xi L, Siebert R, Raffeld M, Hewitt SM, Jaffe ES (2013) Follicular lymphomas in children and young adults: a comparison of the pediatric variant with usual follicular lymphoma. Am J Surg Pathol 37:333–343. doi:10.1097/PAS.0b013e31826b9b57

    Article  PubMed  PubMed Central  Google Scholar 

  8. Swerdlow SH (2004) Pediatric follicular lymphomas, marginal zone lymphomas, and marginal zone hyperplasia. Am J Clin Pathol 122(Suppl):S98–S109

    PubMed  Google Scholar 

  9. Lorsbach RB, Shay-Seymore D, Moore J, Banks PM, Hasserjian RP, Sandlund JT, Behm FG (2002) Clinicopathologic analysis of follicular lymphoma occurring in children. Blood 99:1959–1964

    Article  CAS  PubMed  Google Scholar 

  10. Kussick SJ, Kalnoski M, Braziel RM, Wood BL (2004) Prominent clonal B-cell populations identified by flow cytometry in histologically reactive lymphoid proliferations. Am J Clin Pathol 121:464–472. doi:10.1309/4EJ8-T3R2-ERKQ-61WH

    Article  PubMed  Google Scholar 

  11. Salaverria I, Philipp C, Oschlies I, Kohler CW, Kreuz M, Szczepanowski M, Burkhardt B, Trautmann H, Gesk S, Andrusiewicz M, Berger H, Fey M, Harder L, Hasenclever D, Hummel M, Loeffler M, Mahn F, Martin-Guerrero I, Pellissery S, Pott C, Pfreundschuh M, Reiter A, Richter J, Rosolowski M, Schwaenen C, Stein H, Trumper L, Wessendorf S, Spang R, Kuppers R, Klapper W, Siebert R (2011) Translocations activating IRF4 identify a subtype of germinal center-derived B-cell lymphoma affecting predominantly children and young adults. Blood 118:139–147. doi:10.1182/blood-2011-01-330795

    Article  CAS  PubMed  Google Scholar 

  12. Taddesse-Heath L, Pittaluga S, Sorbara L, Bussey M, Raffeld M, Jaffe ES (2003) Marginal zone B-cell lymphoma in children and young adults. Am J Surg Pathol 27:522–531

    Article  PubMed  Google Scholar 

  13. Rizzo KA, Streubel B, Pittaluga S, Chott A, Xi L, Raffeld M, Jaffe ES (2010) Marginal zone lymphomas in children and the young adult population; characterization of genetic aberrations by FISH and RT-PCR. Mod Pathol 23:866–873. doi:10.1038/modpathol.2010.63

    Article  CAS  PubMed  Google Scholar 

  14. Louissaint A Jr, Ackerman AM, Dias-Santagata D, Ferry JA, Hochberg EP, Huang MS, Iafrate AJ, Lara DO, Pinkus GS, Salaverria I, Siddiquee Z, Siebert R, Weinstein HJ, Zukerberg LR, Harris NL, Hasserjian RP (2012) Pediatric-type nodal follicular lymphoma: an indolent clonal proliferation in children and adults with high proliferation index and no BCL2 rearrangement. Blood 120:2395–2404. doi:10.1182/blood-2012-05-429514

    Article  CAS  PubMed  Google Scholar 

  15. Gitelson E, Al-Saleem T, Robu V, Millenson MM, Smith MR (2010) Pediatric nodal marginal zone lymphoma may develop in the adult population. Leuk Lymphoma 51:89–94. doi:10.3109/10428190903349670

    Article  PubMed  PubMed Central  Google Scholar 

  16. Pinto A, Hutchison RE, Grant LH, Trevenen CL, Berard CW (1990) Follicular lymphomas in pediatric patients. Mod Pathol 3:308–313

    CAS  PubMed  Google Scholar 

  17. Moertel CL, Watterson J, McCormick SR, Simonton SC (1995) Follicular large cell lymphoma of the testis in a child. Cancer 75:1182–1186

    Article  CAS  PubMed  Google Scholar 

  18. Finn LS, Viswanatha DS, Belasco JB, Snyder H, Huebner D, Sorbara L, Raffeld M, Jaffe ES, Salhany KE (1999) Primary follicular lymphoma of the testis in childhood. Cancer 85:1626–1635. doi:10.1002/(SICI)1097-0142(19990401)85:7<1626::AID-CNCR27>3.0.CO;2-0

    Article  CAS  PubMed  Google Scholar 

  19. Pileri SA, Sabattini E, Rosito P, Zinzani PL, Ascani S, Fraternali-Orcioni G, Gamberi B, Piccioli M, Vivenza D, Falini B, Gaidano G (2002) Primary follicular lymphoma of the testis in childhood: an entity with peculiar clinical and molecular characteristics. J Clin Pathol 55:684–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lu D, Medeiros LJ, Eskenazi AE, Abruzzo LV (2001) Primary follicular large cell lymphoma of the testis in a child. Arch Pathol Lab Med 125:551–554. doi:10.1043/0003-9985(2001)125<0551:PFLCLO>2.0.CO;2

    CAS  PubMed  Google Scholar 

  21. Kridel R, Sehn LH, Gascoyne RD (2012) Pathogenesis of follicular lymphoma. J Clin Invest 122:3424–3431. doi:10.1172/JCI63186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Launay E, Pangault C, Bertrand P, Jardin F, Lamy T, Tilly H, Tarte K, Bastard C, Fest T (2012) High rate of TNFRSF14 gene alterations related to 1p36 region in de novo follicular lymphoma and impact on prognosis. Leukemia 26:559–562. doi:10.1038/leu.2011.266

    Article  CAS  PubMed  Google Scholar 

  23. Cheung KJ, Johnson NA, Affleck JG, Severson T, Steidl C, Ben-Neriah S, Schein J, Morin RD, Moore R, Shah SP, Qian H, Paul JE, Telenius A, Relander T, Lam W, Savage K, Connors JM, Brown C, Marra MA, Gascoyne RD, Horsman DE (2010) Acquired TNFRSF14 mutations in follicular lymphoma are associated with worse prognosis. Cancer Res 70:9166–9174. doi:10.1158/0008-5472.CAN-10-2460

    Article  CAS  PubMed  Google Scholar 

  24. Morin RD, Mendez-Lago M, Mungall AJ, Goya R, Mungall KL, Corbett RD, Johnson NA, Severson TM, Chiu R, Field M, Jackman S, Krzywinski M, Scott DW, Trinh DL, Tamura-Wells J, Li S, Firme MR, Rogic S, Griffith M, Chan S, Yakovenko O, Meyer IM, Zhao EY, Smailus D, Moksa M, Chittaranjan S, Rimsza L, Brooks-Wilson A, Spinelli JJ, Ben-Neriah S, Meissner B, Woolcock B, Boyle M, McDonald H, Tam A, Zhao Y, Delaney A, Zeng T, Tse K, Butterfield Y, Birol I, Holt R, Schein J, Horsman DE, Moore R, Jones SJ, Connors JM, Hirst M, Gascoyne RD, Marra MA (2011) Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 476:298–303. doi:10.1038/nature10351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R, Paul JE, Boyle M, Woolcock BW, Kuchenbauer F, Yap D, Humphries RK, Griffith OL, Shah S, Zhu H, Kimbara M, Shashkin P, Charlot JF, Tcherpakov M, Corbett R, Tam A, Varhol R, Smailus D, Moksa M, Zhao Y, Delaney A, Qian H, Birol I, Schein J, Moore R, Holt R, Horsman DE, Connors JM, Jones S, Aparicio S, Hirst M, Gascoyne RD, Marra MA (2010) Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet 42:181–185. doi:10.1038/ng.518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pasqualucci L, Dominguez-Sola D, Chiarenza A, Fabbri G, Grunn A, Trifonov V, Kasper LH, Lerach S, Tang H, Ma J, Rossi D, Chadburn A, Murty VV, Mullighan CG, Gaidano G, Rabadan R, Brindle PK, Dalla-Favera R (2011) Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature 471:189–195. doi:10.1038/nature09730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Martin-Guerrero I, Salaverria I, Burkhardt B, Szczepanowski M, Baudis M, Bens S, de Leval L, Garcia-Orad A, Horn H, Lisfeld J, Pellissery S, Klapper W, Oschlies I, Siebert R (2013) Recurrent loss of heterozygosity in 1p36 associated with TNFRSF14 mutations in IRF4 translocation negative pediatric follicular lymphomas. Haematologica 98:1237–1241. doi:10.3324/haematol.2012.073916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ryan RJ, Nitta M, Borger D, Zukerberg LR, Ferry JA, Harris NL, Iafrate AJ, Bernstein BE, Sohani AR, Le LP (2011) EZH2 codon 641 mutations are common in BCL2-rearranged germinal center B cell lymphomas. PLoS One 6:e28585. doi:10.1371/journal.pone.0028585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Oschlies I, Klapper W, Zimmermann M, Krams M, Wacker HH, Burkhardt B, Harder L, Siebert R, Reiter A, Parwaresch R (2006) Diffuse large B-cell lymphoma in pediatric patients belongs predominantly to the germinal-center type B-cell lymphomas: a clinicopathologic analysis of cases included in the German BFM (Berlin-Frankfurt-Munster) Multicenter Trial. Blood 107:4047–4052. doi:10.1182/blood-2005-10-4213

    Article  CAS  PubMed  Google Scholar 

  30. Attarbaschi A, Beishuizen A, Mann G, Rosolen A, Mori T, Uyttebroeck A, Niggli F, Csoka M, Krenova Z, Mellgren K, Kabickova E, Chiang AK, Reiter A, Williams D, Burkhardt B (2013) Children and adolescents with follicular lymphoma have an excellent prognosis with either limited chemotherapy or with a “watch and wait” strategy after complete resection. Ann Hematol 92:1537–1541. doi:10.1007/s00277-013-1785-2

    Article  CAS  PubMed  Google Scholar 

  31. Adam P, Baumann R, Schmidt J, Bettio S, Weisel K, Bonzheim I, Fend F, Quintanilla-Martinez L (2013) The BCL2 E17 and SP66 antibodies discriminate 2 immunophenotypically and genetically distinct subgroups of conventionally BCL2-“negative” grade 1/2 follicular lymphomas. Hum Pathol 44:1817–1826. doi:10.1016/j.humpath.2013.02.004

    Article  CAS  PubMed  Google Scholar 

  32. Leich E, Salaverria I, Bea S, Zettl A, Wright G, Moreno V, Gascoyne RD, Chan WC, Braziel RM, Rimsza LM, Weisenburger DD, Delabie J, Jaffe ES, Lister A, Fitzgibbon J, Staudt LM, Hartmann EM, Mueller-Hermelink HK, Campo E, Ott G, Rosenwald A (2009) Follicular lymphomas with and without translocation t(14;18) differ in gene expression profiles and genetic alterations. Blood 114:826–834. doi:10.1182/blood-2009-01-198580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Leich E, Zamo A, Horn H, Haralambieva E, Puppe B, Gascoyne RD, Chan WC, Braziel RM, Rimsza LM, Weisenburger DD, Delabie J, Jaffe ES, Fitzgibbon J, Staudt LM, Mueller-Hermelink HK, Calaminici M, Campo E, Ott G, Hernandez L, Rosenwald A (2011) MicroRNA profiles of t(14;18)-negative follicular lymphoma support a late germinal center B-cell phenotype. Blood 118:5550–5558. doi:10.1182/blood-2011-06-361972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wang SA, Wang L, Hochberg EP, Muzikansky A, Harris NL, Hasserjian RP (2005) Low histologic grade follicular lymphoma with high proliferation index: morphologic and clinical features. Am J Surg Pathol 29:1490–1496

    Article  PubMed  Google Scholar 

  35. Falini B, Fizzotti M, Pucciarini A, Bigerna B, Marafioti T, Gambacorta M, Pacini R, Alunni C, Natali-Tanci L, Ugolini B, Sebastiani C, Cattoretti G, Pileri S, Dalla-Favera R, Stein H (2000) A monoclonal antibody (MUM1p) detects expression of the MUM1/IRF4 protein in a subset of germinal center B cells, plasma cells, and activated T cells. Blood 95:2084–2092

    CAS  PubMed  Google Scholar 

  36. Campo E, Pileri S, Jaffe ES, Müller-Hermelink HK, Nathwani BN (2008) Nodal marginal zone lymphoma. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri S, Stein H, Thiele J, Vardiman JW (eds) WHO classification of tumours of haematopoietic and lymphoid tissues. IARC, Lyon, pp 218–219

    Google Scholar 

  37. Miranda RN, Cousar JB, Hammer RD, Collins RD, Vnencak-Jones CL (1999) Somatic mutation analysis of IgH variable regions reveals that tumor cells of most parafollicular (monocytoid) B-cell lymphoma, splenic marginal zone B-cell lymphoma, and some hairy cell leukemia are composed of memory B lymphocytes. Hum Pathol 30:306–312

    Article  CAS  PubMed  Google Scholar 

  38. Elenitoba-Johnson KS, Kumar S, Lim MS, Kingma DW, Raffeld M, Jaffe ES (1997) Marginal zone B-cell lymphoma with monocytoid B-cell lymphocytes in pediatric patients without immunodeficiency. A report of two cases. Am J Clin Pathol 107:92–98

    CAS  PubMed  Google Scholar 

  39. Naresh KN (2008) Nodal marginal zone B-cell lymphoma with prominent follicular colonization—difficulties in diagnosis: a study of 15 cases. Histopathology 52:331–339. doi:10.1111/j.1365-2559.2007.02951.x

    Article  CAS  PubMed  Google Scholar 

  40. Wang E, West D, Kulbacki E (2010) An unusual nodal marginal zone lymphoma with bright CD10 expression: a potential diagnostic pitfall. Am J Hematol 85:546–548. doi:10.1002/ajh.21729

    Article  PubMed  Google Scholar 

  41. Katzenberger T, Kalla J, Leich E, Stocklein H, Hartmann E, Barnickel S, Wessendorf S, Ott MM, Muller-Hermelink HK, Rosenwald A, Ott G (2009) A distinctive subtype of t(14;18)-negative nodal follicular non-Hodgkin lymphoma characterized by a predominantly diffuse growth pattern and deletions in the chromosomal region 1p36. Blood 113:1053–1061. doi:10.1182/blood-2008-07-168682

    Article  CAS  PubMed  Google Scholar 

  42. Karube K, Ohshima K, Tsuchiya T, Yamaguchi T, Kawano R, Suzumiya J, Harada M, Kikuchi M (2005) A “floral” variant of nodal marginal zone lymphoma. Hum Pathol 36:202–206. doi:10.1016/j.humpath.2004.12.010

    Article  PubMed  Google Scholar 

  43. Attygalle AD, Liu H, Shirali S, Diss TC, Loddenkemper C, Stein H, Dogan A, Du MQ, Isaacson PG (2004) Atypical marginal zone hyperplasia of mucosa-associated lymphoid tissue: a reactive condition of childhood showing immunoglobulin lambda light-chain restriction. Blood 104:3343–3348. doi:10.1182/blood-2004-01-03852004-01-0385

    Article  CAS  PubMed  Google Scholar 

  44. Kluin PM, Langerak AW, Beverdam-Vincent J, Geurts-Giele WR, Visser L, Rutgers B, Schuuring E, Van Baarlen J, Lam KH, Seldenrijk K, Kibbelaar RE, de Wit P, Diepstra A, Rosati S, van Noesel MM, Zwaan CM, Hunting JC, Hoogendoorn M, van der Gaag EJ, van Esser JW, de Bont E, Kluin-Nelemans HC, Winter RH, Lo Ten Foe JR, van der Zanden AG (2015) Paediatric nodal marginal zone B-cell lymphadenopathy of the neck: a Haemophilus influenzae-driven immune disorder? J Pathol 236:302–314. doi:10.1002/path.4524

    Article  CAS  PubMed  Google Scholar 

  45. Dores GM, Anderson WF, Curtis RE, Landgren O, Ostroumova E, Bluhm EC, Rabkin CS, Devesa SS, Linet MS (2007) Chronic lymphocytic leukaemia and small lymphocytic lymphoma: overview of the descriptive epidemiology. Br J Haematol 139:809–819. doi:10.1111/j.1365-2141.2007.06856.x

    Article  PubMed  Google Scholar 

  46. Mauro FR, Foa R, Giannarelli D, Cordone I, Crescenzi S, Pescarmona E, Sala R, Cerretti R, Mandelli F (1999) Clinical characteristics and outcome of young chronic lymphocytic leukemia patients: a single institution study of 204 cases. Blood 94:448–454

    CAS  PubMed  Google Scholar 

  47. Montserrat E, Gomis F, Vallespi T, Rios A, Romero A, Soler J, Alcala A, Morey M, Ferran C, Diaz-Mediavilla J et al (1991) Presenting features and prognosis of chronic lymphocytic leukemia in younger adults. Blood 78:1545–1551

    CAS  PubMed  Google Scholar 

  48. Parikh SA, Rabe KG, Kay NE, Call TG, Ding W, Schwager SM, Bowen DA, Conte M, Jelinek DF, Slager SL, Shanafelt TD (2014) Chronic lymphocytic leukemia in young (</= 55 years) patients: a comprehensive analysis of prognostic factors and outcomes. Haematologica 99:140–147. doi:10.3324/haematol.2013.086066

    Article  PubMed  PubMed Central  Google Scholar 

  49. Luskin M, Wertheim G, Morrissette J, Daber R, Biegel J, Wilmoth D, Kersun L, King R, Paessler M, Simon C, Aplenc R, Loren A (2014) CLL/SLL diagnosed in an adolescent. Pediatr Blood Cancer 61:1107–1110. doi:10.1002/pbc.24884

    Article  PubMed  Google Scholar 

  50. Gradowski JF, Sargent RL, Craig FE, Cieply K, Fuhrer K, Sherer C, Swerdlow SH (2012) Chronic lymphocytic leukemia/small lymphocytic lymphoma with cyclin D1 positive proliferation centers do not have CCND1 translocations or gains and lack SOX11 expression. Am J Clin Pathol 138:132–139. doi:10.1309/AJCPIVKZRMPF93ET

    Article  PubMed  PubMed Central  Google Scholar 

  51. Gutierrez A Jr, Tschumper RC, Wu X, Shanafelt TD, Eckel-Passow J, Huddleston PM 3rd, Slager SL, Kay NE, Jelinek DF (2010) LEF-1 is a prosurvival factor in chronic lymphocytic leukemia and is expressed in the preleukemic state of monoclonal B-cell lymphocytosis. Blood 116:2975–2983. doi:10.1182/blood-2010-02-269878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Martinez-Trillos A, Pinyol M, Navarro A, Aymerich M, Jares P, Juan M, Rozman M, Colomer D, Delgado J, Gine E, Gonzalez-Diaz M, Hernandez-Rivas JM, Colado E, Rayon C, Payer AR, Terol MJ, Navarro B, Quesada V, Puente XS, Rozman C, Lopez-Otin C, Campo E, Lopez-Guillermo A, Villamor N (2014) Mutations in TLR/MYD88 pathway identify a subset of young chronic lymphocytic leukemia patients with favorable outcome. Blood 123:3790–3796. doi:10.1182/blood-2013-12-543306

    Article  CAS  PubMed  Google Scholar 

  53. Schmidt J, Federmann B, Schindler N, Steinhilber J, Bonzheim I, Fend F, Quintanilla-Martinez L (2015) MYD88 L265P and CXCR4 mutations in lymphoplasmacytic lymphoma identify cases with high disease activity. Br J Haematol 169:795–803. doi:10.1111/bjh.13361

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Irina Bonzheim and Janine Schmidt from the Institute of Pathology, University of Tübingen, Germany, for performing the molecular analysis of B-cell clonality and MYD88 L265P mutation in cases submitted to the workshop. The authors also thank Dr. Reiner Siebert from the Institute of Human Genetics, University, Campus Kiel, Germany, for performing the fluorescence in situ hybridization analysis using an IRF4/MUM1 break-apart probe in two cases. The authors also thank the workshop participants for their case submissions and for use of their images in this review.

Conflict of interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leticia Quintanilla-Martinez.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Quintanilla-Martinez, L., Sander, B., Chan, J.K.C. et al. Indolent lymphomas in the pediatric population: follicular lymphoma, IRF4/MUM1+ lymphoma, nodal marginal zone lymphoma and chronic lymphocytic leukemia. Virchows Arch 468, 141–157 (2016). https://doi.org/10.1007/s00428-015-1855-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00428-015-1855-z

Keywords

Navigation