Skip to main content
Top
Published in: Annals of Hematology 12/2017

01-12-2017 | Original Article

Clinicopathological features of primary splenic follicular lymphoma

Authors: Joji Shimono, Hiroaki Miyoshi, Tomohiko Kamimura, Tetsuya Eto, Takuto Miyagishima, Yuya Sasaki, Daisuke Kurita, Keisuke Kawamoto, Koji Nagafuji, Masao Seto, Takanori Teshima, Koichi Ohshima

Published in: Annals of Hematology | Issue 12/2017

Login to get access

Abstract

Follicular lymphoma (FL) is a low-grade lymphoma that is usually characterized by generalized lymphadenopathy. Extranodal invasion by FL generally involves the bone marrow, skin, and duodenum; splenic infiltration often occurs in the advanced stages. However, primary splenic FL is very rare. Hence, few studies have been performed on splenic FL, and its clinicopathological features have not been established. This study aimed to investigate the clinicopathological features of primary splenic FL, as compared to nodal FL. We analyzed 17 patients diagnosed with primary splenic FL and 153 control patients with systemic FL. Hepatitis C virus (HCV)-positive status was significantly more common in patients with splenic FL than in the control patients (p = 0.02). Ann Arbor stage III or IV (p = 0.0003) and high-risk FLIPI (Follicular Lymphoma International Prognostic Index) (p = 0.03) were significantly less common in patients with splenic FL than in the control patients; however, the overall and progression-free survival curves were not significantly different between the groups. Among the 17 patients with splenic FL, the progression-free survival was significantly worse in patients who underwent splenectomy without receiving postoperative chemotherapy than in those who did (p = 0.03). These results suggest that primary splenic FL should be considered different from systemic FL; accordingly, its management should also be conducted differently.
Appendix
Available only for authorised users
Literature
1.
go back to reference Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (2009) World Health Organization classification of tumours: pathology and genetics of tumours of haematopoietic and lymphoid tissues, 4th edn. IARC Press, Lyon Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (2009) World Health Organization classification of tumours: pathology and genetics of tumours of haematopoietic and lymphoid tissues, 4th edn. IARC Press, Lyon
2.
go back to reference Nakamura S, Ichimura K, Sato Y, Nakamura S, Nakamine H, Inagaki H, Sadahira Y, Ohshima K, Sakugawa S, Kondo E, Yanai H, Ohara N, Yoshino T (2006) Follicular lymphoma frequently originates in the salivary gland. Pathol Int 56:576–583CrossRefPubMed Nakamura S, Ichimura K, Sato Y, Nakamura S, Nakamine H, Inagaki H, Sadahira Y, Ohshima K, Sakugawa S, Kondo E, Yanai H, Ohara N, Yoshino T (2006) Follicular lymphoma frequently originates in the salivary gland. Pathol Int 56:576–583CrossRefPubMed
3.
go back to reference Bacon CM, Ye H, Diss TC, McNamara C, Kueck B, Hasserjian RP, Rohatiner AZ, Ferry J, Du MQ, Dogan A (2007) Primary follicular lymphoma of testis and epididymis in adults. Am J Surg Pathol 31:1050–1058CrossRefPubMed Bacon CM, Ye H, Diss TC, McNamara C, Kueck B, Hasserjian RP, Rohatiner AZ, Ferry J, Du MQ, Dogan A (2007) Primary follicular lymphoma of testis and epididymis in adults. Am J Surg Pathol 31:1050–1058CrossRefPubMed
4.
go back to reference Grange F, Bekkenk MW, Wechsler J, Meijer CJ, Cerroni L, Bernengo M, Bosq J, Hedelin G, Fink Puches R, van Vloten WA, Joly P, Bagot M, Willemze R (2001) Prognostic factors in primary cutaneous large B-cell lymphomas: a European multicenter study. J Clin Oncol 19:3602–3610CrossRefPubMed Grange F, Bekkenk MW, Wechsler J, Meijer CJ, Cerroni L, Bernengo M, Bosq J, Hedelin G, Fink Puches R, van Vloten WA, Joly P, Bagot M, Willemze R (2001) Prognostic factors in primary cutaneous large B-cell lymphomas: a European multicenter study. J Clin Oncol 19:3602–3610CrossRefPubMed
5.
go back to reference Yoshino T, Miyake K, Ichimura K, Mannami T, Ohara N, Hamazaki S, Akagi T (2000) Increased incidence of follicular lymphoma in the duodenum. Am J Surg Pathol 24:688–693CrossRefPubMed Yoshino T, Miyake K, Ichimura K, Mannami T, Ohara N, Hamazaki S, Akagi T (2000) Increased incidence of follicular lymphoma in the duodenum. Am J Surg Pathol 24:688–693CrossRefPubMed
6.
go back to reference Bende RJ, Smit LA, van Noesel CJ (2007) Molecular pathways in follicular lymphoma. Leukemia 21:18–29CrossRefPubMed Bende RJ, Smit LA, van Noesel CJ (2007) Molecular pathways in follicular lymphoma. Leukemia 21:18–29CrossRefPubMed
7.
go back to reference Kimura Y, Sato K, Arakawa F, Karube K, Nomura Y, Shimizu K, Aoki R, Hashikawa K, Yoshida S, Kiyasu J, Takeuchi M, Nino D, Sugita Y, Morito T, Yoshino T, Nakamura S, Kikuchi M, Ohshima K (2010) Mantle cell lymphoma shows three morphological evolutions of classical, intermediate, and aggressive forms, which occur in parallel with increased labeling index of cyclin D1 and Ki-67. Cancer Sci 101:806–814CrossRefPubMed Kimura Y, Sato K, Arakawa F, Karube K, Nomura Y, Shimizu K, Aoki R, Hashikawa K, Yoshida S, Kiyasu J, Takeuchi M, Nino D, Sugita Y, Morito T, Yoshino T, Nakamura S, Kikuchi M, Ohshima K (2010) Mantle cell lymphoma shows three morphological evolutions of classical, intermediate, and aggressive forms, which occur in parallel with increased labeling index of cyclin D1 and Ki-67. Cancer Sci 101:806–814CrossRefPubMed
8.
go back to reference Iannito E, Tripodo C (2011) How I diagnose and treat splenic lymphomas. Blood 117:2585–2595CrossRef Iannito E, Tripodo C (2011) How I diagnose and treat splenic lymphomas. Blood 117:2585–2595CrossRef
9.
go back to reference Shimizu-Kohno K, Kimura Y, Kiyasu J, Miyoshi H, Yoshida M, Ichikawa R, Niino D, Ohshima K (2012) Malignant lymphoma of the spleen in Japan: a clinicopathological analysis of 115 cases. Pathol Int 62:577–582CrossRefPubMed Shimizu-Kohno K, Kimura Y, Kiyasu J, Miyoshi H, Yoshida M, Ichikawa R, Niino D, Ohshima K (2012) Malignant lymphoma of the spleen in Japan: a clinicopathological analysis of 115 cases. Pathol Int 62:577–582CrossRefPubMed
10.
go back to reference Howard MT, Dufresne S, Swerdlow SH, Cook JR (2009) Follicular lymphoma of the spleen: multiparameter analysis of 16 cases. Am J Clin Pathol 131:656–662CrossRefPubMed Howard MT, Dufresne S, Swerdlow SH, Cook JR (2009) Follicular lymphoma of the spleen: multiparameter analysis of 16 cases. Am J Clin Pathol 131:656–662CrossRefPubMed
11.
go back to reference Mollejo M, Rodríguez-Pinilla MS, Montes-Moreno S, Algara P, Dogan A, Cigudosa JC, Juarez R, Flores T, Forteza J, Arribas A, Piris MA (2009) Splenic follicular lymphoma: clinicopathologic characteristics of a series of 32 cases. Am J Surg Pathol 33:730–738CrossRefPubMed Mollejo M, Rodríguez-Pinilla MS, Montes-Moreno S, Algara P, Dogan A, Cigudosa JC, Juarez R, Flores T, Forteza J, Arribas A, Piris MA (2009) Splenic follicular lymphoma: clinicopathologic characteristics of a series of 32 cases. Am J Surg Pathol 33:730–738CrossRefPubMed
12.
go back to reference Skarin AT, Davey FR, Moloney WC (1971) Lymphosarcoma of the spleen. Results of diagnostic splenectomy in 11 patients. Arch Intern Med 127:259–265CrossRefPubMed Skarin AT, Davey FR, Moloney WC (1971) Lymphosarcoma of the spleen. Results of diagnostic splenectomy in 11 patients. Arch Intern Med 127:259–265CrossRefPubMed
13.
go back to reference Kehoe J, Straus DJ (1988) Primary lymphoma of the spleen. Clinical features and outcome after splenectomy. Cancer 62:1433–1438CrossRefPubMed Kehoe J, Straus DJ (1988) Primary lymphoma of the spleen. Clinical features and outcome after splenectomy. Cancer 62:1433–1438CrossRefPubMed
14.
go back to reference Miyoshi H, Sato K, Yoshida M, Kimura Y, Kiyasu J, Ichikawa A, Ishibashi Y, Arakawa F, Nakamura Y, Nakashima S, Niino D, Sugita Y, Ohshima K (2014) CD5-positive follicular lymphoma characterized by CD25, MUM1, low frequency of t(14;18) and poor prognosis. Pathol Int 64:95–103CrossRefPubMed Miyoshi H, Sato K, Yoshida M, Kimura Y, Kiyasu J, Ichikawa A, Ishibashi Y, Arakawa F, Nakamura Y, Nakashima S, Niino D, Sugita Y, Ohshima K (2014) CD5-positive follicular lymphoma characterized by CD25, MUM1, low frequency of t(14;18) and poor prognosis. Pathol Int 64:95–103CrossRefPubMed
15.
go back to reference Yoshida M, Ichikawa A, Miyoshi H, Takeuchi M, Kimura Y, Nino D, Ohshima K (2012) High frequency of t(14;18) in Hodgkin’s lymphoma associated with follicular lymphoma. Pathol Int 62:518–524CrossRefPubMed Yoshida M, Ichikawa A, Miyoshi H, Takeuchi M, Kimura Y, Nino D, Ohshima K (2012) High frequency of t(14;18) in Hodgkin’s lymphoma associated with follicular lymphoma. Pathol Int 62:518–524CrossRefPubMed
16.
go back to reference Karube K, Martínez D, Royo C, Navarro A, Pinyol M, Cazorla M, Castillo P, Valera A, Carrió A, Costa D, Colomer D, Rosenwald A, Ott G, Esteban D, Giné E, López-Guillermo A, Campo E (2014) Recurrent mutations of NOTCH genes in follicular lymphoma identify a distinctive subset of tumors. J Pathol 234:423–430CrossRefPubMed Karube K, Martínez D, Royo C, Navarro A, Pinyol M, Cazorla M, Castillo P, Valera A, Carrió A, Costa D, Colomer D, Rosenwald A, Ott G, Esteban D, Giné E, López-Guillermo A, Campo E (2014) Recurrent mutations of NOTCH genes in follicular lymphoma identify a distinctive subset of tumors. J Pathol 234:423–430CrossRefPubMed
17.
go back to reference Yoshida N, Miyoshi H, Kato T, Sakata-Yanagimoto M, Niino D, Taniguchi H, Moriuchi Y, Miyahara M, Kurita D, Sasaki Y, Shimono J, Kawamoto K, Utsunomiya A, Imaizumi Y, Seto M, Ohshima K (2016) CCR4 frameshift mutation identifies a distinct group of adult T cell leukemia/lymphoma with poor prognosis. J Pathol 238:621–626CrossRefPubMed Yoshida N, Miyoshi H, Kato T, Sakata-Yanagimoto M, Niino D, Taniguchi H, Moriuchi Y, Miyahara M, Kurita D, Sasaki Y, Shimono J, Kawamoto K, Utsunomiya A, Imaizumi Y, Seto M, Ohshima K (2016) CCR4 frameshift mutation identifies a distinct group of adult T cell leukemia/lymphoma with poor prognosis. J Pathol 238:621–626CrossRefPubMed
18.
go back to reference Kalpadakis C, Pangalis GA, Vassilakopoulous TP, Sachanas S, Angelopoulou MK (2014) Treatment of splenic marginal zone lymphoma: should splenectomy be abandoned? Leuk Lymphoma 55:1463–1470CrossRefPubMed Kalpadakis C, Pangalis GA, Vassilakopoulous TP, Sachanas S, Angelopoulou MK (2014) Treatment of splenic marginal zone lymphoma: should splenectomy be abandoned? Leuk Lymphoma 55:1463–1470CrossRefPubMed
19.
go back to reference Xing KH, Kahlon A, Skinnider BF, Connors JM, Gascoyne RD, Sehn LH, Savage KJ, Slack GW, Shenkier TN, Klasa R, Gerrie AS, Villa D (2015) Outcomes in splenic marginal zone lymphoma: analysis of 107 patients treated in British Columbia. Br J Haematol 169:520–527CrossRefPubMed Xing KH, Kahlon A, Skinnider BF, Connors JM, Gascoyne RD, Sehn LH, Savage KJ, Slack GW, Shenkier TN, Klasa R, Gerrie AS, Villa D (2015) Outcomes in splenic marginal zone lymphoma: analysis of 107 patients treated in British Columbia. Br J Haematol 169:520–527CrossRefPubMed
20.
go back to reference Troussard X, Valensi F, Duchayne E, Garand R, Felman P, Tulliez M, Henry-Amar M, Bryon PA, Flandrin G (1996) Splenic lymphoma with villous lymphocytes: clinical presentation, biology and prognostic factors in a series of 100 patients. Groups Francais d’Hématologie Cellulaire (GFHC). Br J Haematol 93:731–736CrossRefPubMed Troussard X, Valensi F, Duchayne E, Garand R, Felman P, Tulliez M, Henry-Amar M, Bryon PA, Flandrin G (1996) Splenic lymphoma with villous lymphocytes: clinical presentation, biology and prognostic factors in a series of 100 patients. Groups Francais d’Hématologie Cellulaire (GFHC). Br J Haematol 93:731–736CrossRefPubMed
21.
go back to reference Lenglet J, Traullé C, Mounier N, Benet C, Munoz-Bongrand N, Amorin S, Noguera ME, Traverse-Glehen A, Ffrench M, Baseggio L, Felman P, Callet-Bauchu E, Brice P, Berger F, Salles G, Brière J, Coiffier B, Thieblemont C (2014) Long-term follow-up analysis of 100 patients with splenic marginal zone lymphoma treated with splenectomy as first-line treatment. Leuk Lymphoma 55:1854–1860CrossRefPubMed Lenglet J, Traullé C, Mounier N, Benet C, Munoz-Bongrand N, Amorin S, Noguera ME, Traverse-Glehen A, Ffrench M, Baseggio L, Felman P, Callet-Bauchu E, Brice P, Berger F, Salles G, Brière J, Coiffier B, Thieblemont C (2014) Long-term follow-up analysis of 100 patients with splenic marginal zone lymphoma treated with splenectomy as first-line treatment. Leuk Lymphoma 55:1854–1860CrossRefPubMed
22.
go back to reference Rossi D, Trifonov V, Fangazio M, Bruscaggin A, Rasi S, Spina V, Monti S, Vaisitti T, Arruga F, Famà R, Ciardullo C, Greco M, Cresta S, Piranda D, Holmes A, Fabbri G, Messina M, Rinaldi A, Wang J, Agostinelli C, Piccaluga PP, Lucioni M, Tabbò F, Serra R, Franceschetti S, Deambrogi C, Daniele G, Gattei V, Marasca R, Facchetti F, Arcaini L, Inghirami G, Bertoni F, Pileri SA, Deaglio S, Foà R, Dalla-Favera R, Pasqualucci L, Rabadan R, Gaidano G (2012) The coding genome of splenic marginal zone lymphoma: activation of NOTCH2 and other pathways regulating marginal zone development. J Exp Med 209:1537–1551CrossRefPubMedPubMedCentral Rossi D, Trifonov V, Fangazio M, Bruscaggin A, Rasi S, Spina V, Monti S, Vaisitti T, Arruga F, Famà R, Ciardullo C, Greco M, Cresta S, Piranda D, Holmes A, Fabbri G, Messina M, Rinaldi A, Wang J, Agostinelli C, Piccaluga PP, Lucioni M, Tabbò F, Serra R, Franceschetti S, Deambrogi C, Daniele G, Gattei V, Marasca R, Facchetti F, Arcaini L, Inghirami G, Bertoni F, Pileri SA, Deaglio S, Foà R, Dalla-Favera R, Pasqualucci L, Rabadan R, Gaidano G (2012) The coding genome of splenic marginal zone lymphoma: activation of NOTCH2 and other pathways regulating marginal zone development. J Exp Med 209:1537–1551CrossRefPubMedPubMedCentral
23.
go back to reference De Renzo A, Perna F, Persico M, Notaro R, Mainolfi C, de Sio I, Ciancia G, Picardi M, Del Vecchio L, Pane F, Rotoli B (2008) Excellent prognosis and prevalence of HCV infection of primary hepatic and splenic non-Hodgkin’s lymphoma. Eur J Haematol 81:51–57CrossRefPubMed De Renzo A, Perna F, Persico M, Notaro R, Mainolfi C, de Sio I, Ciancia G, Picardi M, Del Vecchio L, Pane F, Rotoli B (2008) Excellent prognosis and prevalence of HCV infection of primary hepatic and splenic non-Hodgkin’s lymphoma. Eur J Haematol 81:51–57CrossRefPubMed
24.
go back to reference Takeshita M, Sakai H, Okamura S, Oshiro Y, Higaki K, Nakashima O, Uike N, Yamamoto I, Kinjo M, Matsubara F (2005) Splenic large B-cell lymphoma in patients with hepatitis C virus infection. Hum Pathol 36:878–885CrossRefPubMed Takeshita M, Sakai H, Okamura S, Oshiro Y, Higaki K, Nakashima O, Uike N, Yamamoto I, Kinjo M, Matsubara F (2005) Splenic large B-cell lymphoma in patients with hepatitis C virus infection. Hum Pathol 36:878–885CrossRefPubMed
25.
go back to reference Michot JM, Canioni D, Driss H, Alric L, Cacoub P, Suarez F, Sibon D, Thieblemont C, Dupuis J, Terrier B, Feray C, Tilly H, Pol S, Leblond V, Settegrana C, Rabiega P, Barthe Y, Hendel-Chavez H, Nguyen-Khac F, Merle-Béral H, Berger F, Molina T, Charlotte F, Carrat F, Davi F, Hermine O, Besson C, ANRS HC-13Lympho-C Study Group (2015) Antiviral therapy is associated with a better survival in patients with hepatitis C virus and B-cell non Hodgkin lymphomas, ANRS HC-13 lympho-C study. Am J Hematol 90:197–203CrossRefPubMed Michot JM, Canioni D, Driss H, Alric L, Cacoub P, Suarez F, Sibon D, Thieblemont C, Dupuis J, Terrier B, Feray C, Tilly H, Pol S, Leblond V, Settegrana C, Rabiega P, Barthe Y, Hendel-Chavez H, Nguyen-Khac F, Merle-Béral H, Berger F, Molina T, Charlotte F, Carrat F, Davi F, Hermine O, Besson C, ANRS HC-13Lympho-C Study Group (2015) Antiviral therapy is associated with a better survival in patients with hepatitis C virus and B-cell non Hodgkin lymphomas, ANRS HC-13 lympho-C study. Am J Hematol 90:197–203CrossRefPubMed
26.
go back to reference Arcaini L, Besson C, Frigeni M, Fontaine H, Goldaniga M, Casato M, Visentini M, Torres HA, Loustaud-Ratti V, Peveling-Oberhag J, Fabris P, Rossotti R, Zaja F, Rigacci L, Rattotti S, Bruno R, Merli M, Dorival C, Alric L, Jaccard A, Pol S, Carrat F, Ferretti VV, Visco C, Hermine O (2016) Interferon-free antiviral treatment in B-cell lymphoproliferative disorders associated with hepatitis C virus infection. Blood 128:2527–2532CrossRefPubMed Arcaini L, Besson C, Frigeni M, Fontaine H, Goldaniga M, Casato M, Visentini M, Torres HA, Loustaud-Ratti V, Peveling-Oberhag J, Fabris P, Rossotti R, Zaja F, Rigacci L, Rattotti S, Bruno R, Merli M, Dorival C, Alric L, Jaccard A, Pol S, Carrat F, Ferretti VV, Visco C, Hermine O (2016) Interferon-free antiviral treatment in B-cell lymphoproliferative disorders associated with hepatitis C virus infection. Blood 128:2527–2532CrossRefPubMed
27.
go back to reference Zuckerman E, Zuckerman T, Sahar D, Streichman S, Attias D, Sabo E, Yeshurun D, Rowe JM (2001) The effect of antiviral therapy on t(14;18) translocation and immunoglobulin gene rearrangement in patients with chronic hepatitis C virus infection. Blood 97:1555–1559CrossRefPubMed Zuckerman E, Zuckerman T, Sahar D, Streichman S, Attias D, Sabo E, Yeshurun D, Rowe JM (2001) The effect of antiviral therapy on t(14;18) translocation and immunoglobulin gene rearrangement in patients with chronic hepatitis C virus infection. Blood 97:1555–1559CrossRefPubMed
28.
go back to reference Chan CH, Hadlock KG, Foung SK, Levy S (2001) V(H)1-69 gene is preferentially used by hepatitis C virus-associated B cell lymphomas and by normal B cells responding to the E2 viral antigen. Blood 97:1023–1026CrossRefPubMed Chan CH, Hadlock KG, Foung SK, Levy S (2001) V(H)1-69 gene is preferentially used by hepatitis C virus-associated B cell lymphomas and by normal B cells responding to the E2 viral antigen. Blood 97:1023–1026CrossRefPubMed
29.
go back to reference Zuckerman E, Zuckerman T, Sahar D, Streichman S, Attias D, Sabo E, Yeshurun D, Rowe J (2001) bcl-2 and immunoglobulin gene rearrangement in patients with hepatitis C virus infection. Br J Haematol 112:364–369CrossRefPubMed Zuckerman E, Zuckerman T, Sahar D, Streichman S, Attias D, Sabo E, Yeshurun D, Rowe J (2001) bcl-2 and immunoglobulin gene rearrangement in patients with hepatitis C virus infection. Br J Haematol 112:364–369CrossRefPubMed
30.
go back to reference Giannelli F, Moscarella S, Giannini C, Caini P, Monti M, Gragnani L, Romanelli RG, Solazzo V, Laffi G, La Villa G, Gentilini P, Zignego AL (2003) Effect of antiviral treatment in patients with chronic HCV infection and t(14;18) translocation. Blood 102:1196–1201CrossRefPubMed Giannelli F, Moscarella S, Giannini C, Caini P, Monti M, Gragnani L, Romanelli RG, Solazzo V, Laffi G, La Villa G, Gentilini P, Zignego AL (2003) Effect of antiviral treatment in patients with chronic HCV infection and t(14;18) translocation. Blood 102:1196–1201CrossRefPubMed
31.
go back to reference Poetsch M, Weber-Matthiesen K, Plendl HJ, Grote W, Schlegelberger B (1996) Detection of the t(14;18) chromosomal translocation by interphase cytogenetics with yeast-artificial-chromosome probes in follicular lymphoma and nonneoplastic lymphoproliferation. J Clin Oncol 14:963–969CrossRefPubMed Poetsch M, Weber-Matthiesen K, Plendl HJ, Grote W, Schlegelberger B (1996) Detection of the t(14;18) chromosomal translocation by interphase cytogenetics with yeast-artificial-chromosome probes in follicular lymphoma and nonneoplastic lymphoproliferation. J Clin Oncol 14:963–969CrossRefPubMed
Metadata
Title
Clinicopathological features of primary splenic follicular lymphoma
Authors
Joji Shimono
Hiroaki Miyoshi
Tomohiko Kamimura
Tetsuya Eto
Takuto Miyagishima
Yuya Sasaki
Daisuke Kurita
Keisuke Kawamoto
Koji Nagafuji
Masao Seto
Takanori Teshima
Koichi Ohshima
Publication date
01-12-2017
Publisher
Springer Berlin Heidelberg
Published in
Annals of Hematology / Issue 12/2017
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-017-3139-y

Other articles of this Issue 12/2017

Annals of Hematology 12/2017 Go to the issue