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

Virchows Archiv

Volumn 468, Issue 2, 2016, Pages 141-157

  Quintanilla Martinez, Leticia ^a   Sander, Birgitta ^b   Chan, John K C ^c   Xerri, Luc ^d   Ott, German ^e   Campo, Elias ^f   Swerdlow, Steven H ^g  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c QUEEN ELIZABETH HOSPITAL   (Hong Kong)

^d INSTITUT PAOLI CALMETTES   (France)

^e DR MARGARETE FISCHER BOSCH INSTITUTE OF CLINICAL PHARMACOLOGY   (Germany)

^f UNIVERSITY OF BARCELONA   (Spain)

^g UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Indolent pediatric lymphomas; IRF4 MUM1+ lymphomas; Pediatric nodal marginal zone lymphoma; Pediatric type follicular lymphoma; Waldeyer s ring lymphomas

Indexed keywords

INTERFERON REGULATORY FACTOR 4;

ADOLESCENT; B LYMPHOCYTE; CANCER DIAGNOSIS; CHILD; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; CLINICAL FEATURE; DIFFERENTIAL DIAGNOSIS; FEMALE; FOLLICULAR LYMPHOMA; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOPHENOTYPING; LYMPHOID HYPERPLASIA; LYMPHOMA; MALE; NODAL MARGINAL ZONE LYMPHOMA; PRIORITY JOURNAL; REVIEW; ANIMAL; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPH NODE; LYMPHOMA, B-CELL, MARGINAL ZONE; LYMPHOMA, FOLLICULAR; PATHOLOGY;

ANIMALS; B-LYMPHOCYTES; DIAGNOSIS, DIFFERENTIAL; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPH NODES; LYMPHOMA, B-CELL, MARGINAL ZONE; LYMPHOMA, FOLLICULAR;

EID: 84959552933     PISSN: 09456317     EISSN: 14322307     Source Type: Journal    
DOI: 10.1007/s00428-015-1855-z     Document Type: Review

References (53)

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
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
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
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
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
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
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
8. Swerdlow SH (2004) Pediatric follicular lymphomas, marginal zone lymphomas, and marginal zone hyperplasia. Am J Clin Pathol 122(Suppl):S98–S109
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
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
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
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
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
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
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
16. Pinto A, Hutchison RE, Grant LH, Trevenen CL, Berard CW (1990) Follicular lymphomas in pediatric patients. Mod Pathol 3:308–313
17. Moertel CL, Watterson J, McCormick SR, Simonton SC (1995) Follicular large cell lymphoma of the testis in a child. Cancer 75:1182–1186
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
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
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
21. Kridel R, Sehn LH, Gascoyne RD (2012) Pathogenesis of follicular lymphoma. J Clin Invest 122:3424–3431. doi:10.1172/JCI63186
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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 (
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
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
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
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
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