Splenic marginal zone lymphoma pathophysiology: Difference between revisions

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==Overview==
==Overview==
Genes involved in the pathogenesis of splenic marginal zone lymphoma include [[immunoglobulin]] genes and CDK6 gene. On microscopic histopathological analysis, [[B-cells]],  villous lymphocytes, and [[sinus]] invasion are characteristic findings of splenic marginal zone lymphoma.
Genes involved in the pathogenesis of splenic marginal zone lymphoma include [[immunoglobulin]] genes and CDK6 gene. On microscopic histopathological analysis, [[B-cells]],  villous lymphocytes, and [[sinus]] invasion are characteristic findings of splenic marginal zone lymphoma.
__NOTOC__
__NOTOC__
__NOTOC__
==Pathophysiology==
==Pathophysiology==
===Pathogenesis===  
===Pathogenesis===  
===Genetics===
===Genetics===
* Clonal rearrangements of the [[immunoglobulin]] genes (heavy and light chains) <ref name="dun1">[http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=9635678&query_hl=24&itool=pubmed_ExternalLink]
* [[Clonal rearrangements]] of the [[immunoglobulin]] genes (heavy and light chains) <ref name="dun1">[http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=9635678&query_hl=24&itool=pubmed_ExternalLink]
Dunn-Walters DK, Boursier L, Spencer J, Isaacson PG. "Analysis of immunoglobulin genes in splenic marginal zone lymphoma suggests ongoing mutation." '''Hum Pathol'''. 1998 Jun;29(6):585-93. PMID: 9635678</ref>  
Dunn-Walters DK, Boursier L, Spencer J, Isaacson PG. "Analysis of immunoglobulin genes in splenic marginal zone lymphoma suggests ongoing mutation." '''Hum Pathol'''. 1998 Jun;29(6):585-93. PMID: 9635678</ref>  
* Most common chromosomal abnormality seen in splenic marginal zone lymphoma is the deletion of 7q region.<ref name="pmid14681321">{{cite journal |vauthors=Boonstra R, Bosga-Bouwer A, van Imhoff GW, Krause V, Palmer M, Coupland RW, Dabbagh L, van den Berg E, van den Berg A, Poppema S |title=Splenic marginal zone lymphomas presenting with splenomegaly and typical immunophenotype are characterized by allelic loss in 7q31-32 |journal=Mod. Pathol. |volume=16 |issue=12 |pages=1210–7 |date=December 2003 |pmid=14681321 |doi=10.1097/01.MP.0000095895.19756.77 |url=}}</ref>
* Most common [[chromosomal]] abnormality seen in [[splenic marginal zone lymphoma]] is the deletion of 7q region.<ref name="pmid14681321">{{cite journal |vauthors=Boonstra R, Bosga-Bouwer A, van Imhoff GW, Krause V, Palmer M, Coupland RW, Dabbagh L, van den Berg E, van den Berg A, Poppema S |title=Splenic marginal zone lymphomas presenting with splenomegaly and typical immunophenotype are characterized by allelic loss in 7q31-32 |journal=Mod. Pathol. |volume=16 |issue=12 |pages=1210–7 |date=December 2003 |pmid=14681321 |doi=10.1097/01.MP.0000095895.19756.77 |url=}}</ref>
*Other abnormalities such as gain of function mutation in 3q, 4q, 5q, 9q, 12q, 20q and loss of function mutations in 7q and 17p have also been found.<ref name="pmid11337382">{{cite journal |vauthors=Hernández JM, García JL, Gutiérrez NC, Mollejo M, Martínez-Climent JA, Flores T, González MB, Piris MA, San Miguel JF |title=Novel genomic imbalances in B-cell splenic marginal zone lymphomas revealed by comparative genomic hybridization and cytogenetics |journal=Am. J. Pathol. |volume=158 |issue=5 |pages=1843–50 |date=May 2001 |pmid=11337382 |pmc=1891967 |doi=10.1016/S0002-9440(10)64140-5 |url=}}</ref><ref name="pmid15642391">{{cite journal |vauthors=Andersen CL, Gruszka-Westwood A, Atkinson S, Matutes E, Catovsky D, Pedersen RK, Pedersen BB, Pulczynski S, Hokland P, Jacobsen E, Koch J |title=Recurrent genomic imbalances in B-cell splenic marginal-zone lymphoma revealed by comparative genomic hybridization |journal=Cancer Genet. Cytogenet. |volume=156 |issue=2 |pages=122–8 |date=January 2005 |pmid=15642391 |doi=10.1016/j.cancergencyto.2004.04.026 |url=}}</ref><ref name="pmid20479288">{{cite journal |vauthors=Salido M, Baró C, Oscier D, Stamatopoulos K, Dierlamm J, Matutes E, Traverse-Glehen A, Berger F, Felman P, Thieblemont C, Gesk S, Athanasiadou A, Davis Z, Gardiner A, Milla F, Ferrer A, Mollejo M, Calasanz MJ, Florensa L, Espinet B, Luño E, Wlodarska I, Verhoef G, García-Granero M, Salar A, Papadaki T, Serrano S, Piris MA, Solé F |title=Cytogenetic aberrations and their prognostic value in a series of 330 splenic marginal zone B-cell lymphomas: a multicenter study of the Splenic B-Cell Lymphoma Group |journal=Blood |volume=116 |issue=9 |pages=1479–88 |date=September 2010 |pmid=20479288 |doi=10.1182/blood-2010-02-267476 |url=}}</ref>
*Other abnormalities such as gain of function [[mutation]] in 3q, 4q, 5q, 9q, 12q, 20q and loss of function mutations in 7q and 17p have also been found.<ref name="pmid11337382">{{cite journal |vauthors=Hernández JM, García JL, Gutiérrez NC, Mollejo M, Martínez-Climent JA, Flores T, González MB, Piris MA, San Miguel JF |title=Novel genomic imbalances in B-cell splenic marginal zone lymphomas revealed by comparative genomic hybridization and cytogenetics |journal=Am. J. Pathol. |volume=158 |issue=5 |pages=1843–50 |date=May 2001 |pmid=11337382 |pmc=1891967 |doi=10.1016/S0002-9440(10)64140-5 |url=}}</ref><ref name="pmid15642391">{{cite journal |vauthors=Andersen CL, Gruszka-Westwood A, Atkinson S, Matutes E, Catovsky D, Pedersen RK, Pedersen BB, Pulczynski S, Hokland P, Jacobsen E, Koch J |title=Recurrent genomic imbalances in B-cell splenic marginal-zone lymphoma revealed by comparative genomic hybridization |journal=Cancer Genet. Cytogenet. |volume=156 |issue=2 |pages=122–8 |date=January 2005 |pmid=15642391 |doi=10.1016/j.cancergencyto.2004.04.026 |url=}}</ref><ref name="pmid20479288">{{cite journal |vauthors=Salido M, Baró C, Oscier D, Stamatopoulos K, Dierlamm J, Matutes E, Traverse-Glehen A, Berger F, Felman P, Thieblemont C, Gesk S, Athanasiadou A, Davis Z, Gardiner A, Milla F, Ferrer A, Mollejo M, Calasanz MJ, Florensa L, Espinet B, Luño E, Wlodarska I, Verhoef G, García-Granero M, Salar A, Papadaki T, Serrano S, Piris MA, Solé F |title=Cytogenetic aberrations and their prognostic value in a series of 330 splenic marginal zone B-cell lymphomas: a multicenter study of the Splenic B-Cell Lymphoma Group |journal=Blood |volume=116 |issue=9 |pages=1479–88 |date=September 2010 |pmid=20479288 |doi=10.1182/blood-2010-02-267476 |url=}}</ref>
* Most common genetic mutation is of [[NOTCH2]] [[gene]].<ref name="pmid22891273">{{cite journal |vauthors=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 |title=The coding genome of splenic marginal zone lymphoma: activation of NOTCH2 and other pathways regulating marginal zone development |journal=J. Exp. Med. |volume=209 |issue=9 |pages=1537–51 |date=August 2012 |pmid=22891273 |doi=10.1084/jem.20120904 |url=}}</ref><ref name="pmid18508802">{{cite journal |vauthors=Trøen G, Wlodarska I, Warsame A, Hernández Llodrà S, De Wolf-Peeters C, Delabie J |title=NOTCH2 mutations in marginal zone lymphoma |journal=Haematologica |volume=93 |issue=7 |pages=1107–9 |date=July 2008 |pmid=18508802 |doi=10.3324/haematol.11635 |url=}}</ref>
* Most common [[genetic]] [[mutation]] is of [[NOTCH2]] [[gene]].<ref name="pmid22891273">{{cite journal |vauthors=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 |title=The coding genome of splenic marginal zone lymphoma: activation of NOTCH2 and other pathways regulating marginal zone development |journal=J. Exp. Med. |volume=209 |issue=9 |pages=1537–51 |date=August 2012 |pmid=22891273 |doi=10.1084/jem.20120904 |url=}}</ref><ref name="pmid18508802">{{cite journal |vauthors=Trøen G, Wlodarska I, Warsame A, Hernández Llodrà S, De Wolf-Peeters C, Delabie J |title=NOTCH2 mutations in marginal zone lymphoma |journal=Haematologica |volume=93 |issue=7 |pages=1107–9 |date=July 2008 |pmid=18508802 |doi=10.3324/haematol.11635 |url=}}</ref>
* Other genes involved with decreasing frequency are [[KLF2]], CARD1, [[TRAF3]], [[MYD88]],[[TP53]].<ref name="pmid25283840">{{cite journal |vauthors=Piva R, Deaglio S, Famà R, Buonincontri R, Scarfò I, Bruscaggin A, Mereu E, Serra S, Spina V, Brusa D, Garaffo G, Monti S, Dal Bo M, Marasca R, Arcaini L, Neri A, Gattei V, Paulli M, Tiacci E, Bertoni F, Pileri SA, Foà R, Inghirami G, Gaidano G, Rossi D |title=The Krüppel-like factor 2 transcription factor gene is recurrently mutated in splenic marginal zone lymphoma |journal=Leukemia |volume=29 |issue=2 |pages=503–7 |date=February 2015 |pmid=25283840 |doi=10.1038/leu.2014.294 |url=}}</ref><ref name="pmid21881048">{{cite journal |vauthors=Rossi D, Deaglio S, Dominguez-Sola D, Rasi S, Vaisitti T, Agostinelli C, Spina V, Bruscaggin A, Monti S, Cerri M, Cresta S, Fangazio M, Arcaini L, Lucioni M, Marasca R, Thieblemont C, Capello D, Facchetti F, Kwee I, Pileri SA, Foà R, Bertoni F, Dalla-Favera R, Pasqualucci L, Gaidano G |title=Alteration of BIRC3 and multiple other NF-κB pathway genes in splenic marginal zone lymphoma |journal=Blood |volume=118 |issue=18 |pages=4930–4 |date=November 2011 |pmid=21881048 |doi=10.1182/blood-2011-06-359166 |url=}}</ref><ref name="pmid27503810">{{cite journal |vauthors=Spina V, Rossi D |title=NF-κB deregulation in splenic marginal zone lymphoma |journal=Semin. Cancer Biol. |volume=39 |issue= |pages=61–7 |date=August 2016 |pmid=27503810 |doi=10.1016/j.semcancer.2016.08.002 |url=}}</ref><ref name="pmid8018922">{{cite journal |vauthors=Baldini L, Fracchiolla NS, Cro LM, Trecca D, Romitti L, Polli E, Maiolo AT, Neri A |title=Frequent p53 gene involvement in splenic B-cell leukemia/lymphomas of possible marginal zone origin |journal=Blood |volume=84 |issue=1 |pages=270–8 |date=July 1994 |pmid=8018922 |doi= |url=}}</ref><ref name="pmid11369650">{{cite journal |vauthors=Gruszka-Westwood AM, Hamoudi RA, Matutes E, Tuset E, Catovsky D |title=p53 abnormalities in splenic lymphoma with villous lymphocytes |journal=Blood |volume=97 |issue=11 |pages=3552–8 |date=June 2001 |pmid=11369650 |doi= |url=}}</ref>
* Other genes involved with decreasing frequency are [[KLF2]], CARD1, [[TRAF3]], [[MYD88]],[[TP53]].<ref name="pmid25283840">{{cite journal |vauthors=Piva R, Deaglio S, Famà R, Buonincontri R, Scarfò I, Bruscaggin A, Mereu E, Serra S, Spina V, Brusa D, Garaffo G, Monti S, Dal Bo M, Marasca R, Arcaini L, Neri A, Gattei V, Paulli M, Tiacci E, Bertoni F, Pileri SA, Foà R, Inghirami G, Gaidano G, Rossi D |title=The Krüppel-like factor 2 transcription factor gene is recurrently mutated in splenic marginal zone lymphoma |journal=Leukemia |volume=29 |issue=2 |pages=503–7 |date=February 2015 |pmid=25283840 |doi=10.1038/leu.2014.294 |url=}}</ref><ref name="pmid21881048">{{cite journal |vauthors=Rossi D, Deaglio S, Dominguez-Sola D, Rasi S, Vaisitti T, Agostinelli C, Spina V, Bruscaggin A, Monti S, Cerri M, Cresta S, Fangazio M, Arcaini L, Lucioni M, Marasca R, Thieblemont C, Capello D, Facchetti F, Kwee I, Pileri SA, Foà R, Bertoni F, Dalla-Favera R, Pasqualucci L, Gaidano G |title=Alteration of BIRC3 and multiple other NF-κB pathway genes in splenic marginal zone lymphoma |journal=Blood |volume=118 |issue=18 |pages=4930–4 |date=November 2011 |pmid=21881048 |doi=10.1182/blood-2011-06-359166 |url=}}</ref><ref name="pmid27503810">{{cite journal |vauthors=Spina V, Rossi D |title=NF-κB deregulation in splenic marginal zone lymphoma |journal=Semin. Cancer Biol. |volume=39 |issue= |pages=61–7 |date=August 2016 |pmid=27503810 |doi=10.1016/j.semcancer.2016.08.002 |url=}}</ref><ref name="pmid8018922">{{cite journal |vauthors=Baldini L, Fracchiolla NS, Cro LM, Trecca D, Romitti L, Polli E, Maiolo AT, Neri A |title=Frequent p53 gene involvement in splenic B-cell leukemia/lymphomas of possible marginal zone origin |journal=Blood |volume=84 |issue=1 |pages=270–8 |date=July 1994 |pmid=8018922 |doi= |url=}}</ref><ref name="pmid11369650">{{cite journal |vauthors=Gruszka-Westwood AM, Hamoudi RA, Matutes E, Tuset E, Catovsky D |title=p53 abnormalities in splenic lymphoma with villous lymphocytes |journal=Blood |volume=97 |issue=11 |pages=3552–8 |date=June 2001 |pmid=11369650 |doi= |url=}}</ref>
* Translocations of the CDK6 gene  located at 7q21 have also been reported<ref name="cor1">
* Translocations of the [[CDK6]] gene  located at 7q21 have also been reported<ref name="cor1">
[http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=10597225&query_hl=28&itool=pubmed_ExternalLink]
[http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=pubmed&cmd=Retrieve&dopt=AbstractPlus&list_uids=10597225&query_hl=28&itool=pubmed_ExternalLink]
Corcoran MM, Mould SJ, Orchard JA, Ibbotson RE, Chapman RM, Boright AP, Platt C, Tsui LC, Scherer SW, Oscier DG. "Dysregulation of cyclin dependent kinase 6 expression in splenic marginal zone lymphoma through chromosome 7q translocations." '''Oncogene'''. 1999 Nov 4;18(46):6271-7. PMID: 10597225</ref>
Corcoran MM, Mould SJ, Orchard JA, Ibbotson RE, Chapman RM, Boright AP, Platt C, Tsui LC, Scherer SW, Oscier DG. "Dysregulation of cyclin dependent kinase 6 expression in [[splenic marginal zone lymphoma]] through chromosome 7q translocations." '''Oncogene'''. 1999 Nov 4;18(46):6271-7. PMID: 10597225</ref>


* There are several pathways involved in the normal functioning of the cells. Genetic dysregulation may affect these pathways resulting in abnormal function.
* There are several pathways involved in the normal functioning of the cells. [[Genetic]] dysregulation may affect these pathways resulting in abnormal function.
* Common genetic abnormalities and their affected pathways in splenic marginal zone lymphoma are summarized under:
* Common [[genetic]] abnormalities and their affected pathways in [[splenic marginal zone lymphoma]] are summarized under:
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===Associated conditions===
===Associated conditions===
* [[Hepatitis C]] infection
* [[Hepatitis C]] infection
** A strong association between [[splenic marginal zone lymphoma]] ([[SMZL]]) and [[hepatitis C]] infection has been observed in several studies indicating that viral antigen may be involved in the pathogenesis of the lymphoma.<ref name="pmid20530156">{{cite journal |vauthors=Chuang SS, Liao YL, Chang ST, Hsieh YC, Kuo SY, Lu CL, Hwang WS, Lin IH, Tsao CJ, Huang WT |title=Hepatitis C virus infection is significantly associated with malignant lymphoma in Taiwan, particularly with nodal and splenic marginal zone lymphomas |journal=J. Clin. Pathol. |volume=63 |issue=7 |pages=595–8 |date=July 2010 |pmid=20530156 |doi=10.1136/jcp.2010.076810 |url=}}</ref><ref name="pmid17852855">{{cite journal |vauthors=Gurvits GE, Mahtani R, Halperin I |title=Hepatitis C virus and splenic marginal zone lymphoma with villous lymphocytes: away from conventional therapy |journal=Scand. J. Gastroenterol. |volume=42 |issue=11 |pages=1392–3 |date=November 2007 |pmid=17852855 |doi=10.1080/00365520701420800 |url=}}</ref>
** A strong association between [[splenic marginal zone lymphoma]] ([[SMZL]]) and [[hepatitis C]] infection has been observed in several studies indicating that [[viral antigen]] may be involved in the pathogenesis of the lymphoma.<ref name="pmid20530156">{{cite journal |vauthors=Chuang SS, Liao YL, Chang ST, Hsieh YC, Kuo SY, Lu CL, Hwang WS, Lin IH, Tsao CJ, Huang WT |title=Hepatitis C virus infection is significantly associated with malignant lymphoma in Taiwan, particularly with nodal and splenic marginal zone lymphomas |journal=J. Clin. Pathol. |volume=63 |issue=7 |pages=595–8 |date=July 2010 |pmid=20530156 |doi=10.1136/jcp.2010.076810 |url=}}</ref><ref name="pmid17852855">{{cite journal |vauthors=Gurvits GE, Mahtani R, Halperin I |title=Hepatitis C virus and splenic marginal zone lymphoma with villous lymphocytes: away from conventional therapy |journal=Scand. J. Gastroenterol. |volume=42 |issue=11 |pages=1392–3 |date=November 2007 |pmid=17852855 |doi=10.1080/00365520701420800 |url=}}</ref>
** It is assumed that may be the HCV antigen stimulate the monoclonal B-cell proliferation through their specific receptor on the cell surface.<ref name="pmid12916862">{{cite journal |vauthors=Weng WK, Levy S |title=Hepatitis C virus (HCV) and lymphomagenesis |journal=Leuk. Lymphoma |volume=44 |issue=7 |pages=1113–20 |date=July 2003 |pmid=12916862 |doi=10.1080/1042819031000076972 |url=}}</ref><ref name="pmid11739181">{{cite journal |vauthors=Quinn ER, Chan CH, Hadlock KG, Foung SK, Flint M, Levy S |title=The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis |journal=Blood |volume=98 |issue=13 |pages=3745–9 |date=December 2001 |pmid=11739181 |doi= |url=}}</ref>
** It is assumed that may be the [[HCV]] [[antigen]] stimulate the [[monoclonal]] [[B-cell proliferation]] through their specific receptor on the cell surface.<ref name="pmid12916862">{{cite journal |vauthors=Weng WK, Levy S |title=Hepatitis C virus (HCV) and lymphomagenesis |journal=Leuk. Lymphoma |volume=44 |issue=7 |pages=1113–20 |date=July 2003 |pmid=12916862 |doi=10.1080/1042819031000076972 |url=}}</ref><ref name="pmid11739181">{{cite journal |vauthors=Quinn ER, Chan CH, Hadlock KG, Foung SK, Flint M, Levy S |title=The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis |journal=Blood |volume=98 |issue=13 |pages=3745–9 |date=December 2001 |pmid=11739181 |doi= |url=}}</ref>
** Regression of the lymphoma was seen in patients after treatment with anti viral therapy again suggesting the role of viral antigen in its pathogenesis.<ref name="pmid12110736">{{cite journal |vauthors=Hermine O, Lefrère F, Bronowicki JP, Mariette X, Jondeau K, Eclache-Saudreau V, Delmas B, Valensi F, Cacoub P, Brechot C, Varet B, Troussard X |title=Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection |journal=N. Engl. J. Med. |volume=347 |issue=2 |pages=89–94 |date=July 2002 |pmid=12110736 |doi=10.1056/NEJMoa013376 |url=}}</ref>
** [[Regression]] of the lymphoma was seen in patients after treatment with [[anti viral]] therapy again suggesting the role of [[viral]] [[antigen]] in its pathogenesis.<ref name="pmid12110736">{{cite journal |vauthors=Hermine O, Lefrère F, Bronowicki JP, Mariette X, Jondeau K, Eclache-Saudreau V, Delmas B, Valensi F, Cacoub P, Brechot C, Varet B, Troussard X |title=Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection |journal=N. Engl. J. Med. |volume=347 |issue=2 |pages=89–94 |date=July 2002 |pmid=12110736 |doi=10.1056/NEJMoa013376 |url=}}</ref>
===Microscopic Pathology===
===Microscopic Pathology===
* '''Splenic marginal zone lymphoma''' (SMZL) tends to involve different organs such as spleen, bone marrow, blood and lymph nodes.<ref name="pmid23233614">{{cite journal |vauthors=Zinzani PL |title=The many faces of marginal zone lymphoma |journal=Hematology Am Soc Hematol Educ Program |volume=2012 |issue= |pages=426–32 |date=2012 |pmid=23233614 |doi=10.1182/asheducation-2012.1.426 |url=}}</ref>.<ref name="pmid26989207">{{cite journal |vauthors=Arcaini L, Rossi D, Paulli M |title=Splenic marginal zone lymphoma: from genetics to management |journal=Blood |volume=127 |issue=17 |pages=2072–81 |date=April 2016 |pmid=26989207 |doi=10.1182/blood-2015-11-624312 |url=}}</ref>
* '''Splenic marginal zone lymphoma''' (SMZL) tends to involve different organs such as [[spleen]], [[bone marrow]], [[blood]] and [[lymph nodes]].<ref name="pmid23233614">{{cite journal |vauthors=Zinzani PL |title=The many faces of marginal zone lymphoma |journal=Hematology Am Soc Hematol Educ Program |volume=2012 |issue= |pages=426–32 |date=2012 |pmid=23233614 |doi=10.1182/asheducation-2012.1.426 |url=}}</ref>.<ref name="pmid26989207">{{cite journal |vauthors=Arcaini L, Rossi D, Paulli M |title=Splenic marginal zone lymphoma: from genetics to management |journal=Blood |volume=127 |issue=17 |pages=2072–81 |date=April 2016 |pmid=26989207 |doi=10.1182/blood-2015-11-624312 |url=}}</ref>
* The microscopic features of these organs are described below:
* The microscopic features of these organs are described below:
* '''Spleen'''
* '''Spleen'''
**  Micronodular pattern of lymphocytic infiltration of the white pulp involving both mantle and marginal zone component.<ref name="pmid17325486">{{cite journal |vauthors=Papadaki T, Stamatopoulos K, Belessi C, Pouliou E, Parasi A, Douka V, Laoutaris N, Fassas A, Anagnostopoulos A, Anagnostou D |title=Splenic marginal-zone lymphoma: one or more entities? A histologic, immunohistochemical, and molecular study of 42 cases |journal=Am. J. Surg. Pathol. |volume=31 |issue=3 |pages=438–46 |date=March 2007 |pmid=17325486 |doi=10.1097/01.pas.0000213419.08009.b0 |url=}}</ref>
**  Micronodular pattern of [[lymphocytic]] infiltration of the [[white pulp]] involving both mantle and marginal zone component.<ref name="pmid17325486">{{cite journal |vauthors=Papadaki T, Stamatopoulos K, Belessi C, Pouliou E, Parasi A, Douka V, Laoutaris N, Fassas A, Anagnostopoulos A, Anagnostou D |title=Splenic marginal-zone lymphoma: one or more entities? A histologic, immunohistochemical, and molecular study of 42 cases |journal=Am. J. Surg. Pathol. |volume=31 |issue=3 |pages=438–46 |date=March 2007 |pmid=17325486 |doi=10.1097/01.pas.0000213419.08009.b0 |url=}}</ref>
** Biphasic distribution of  neoplastic B-cell in the follicles i.e small cells having dense chromatin and scant cytoplasm surrounded by intermediate size cells of marginal zone having variable nuclear contour and relatively abudnant cytoplasm with interspersed large B-cells.
** [[Biphasic]] distribution of  neoplastic B-cell in the follicles i.e small cells having dense chromatin and scant [[cytoplasm]] surrounded by intermediate size cells of marginal zone having variable nuclear contour and relatively abundant [[cytoplasm]] with interspersed large B-cells.
** Red pulp may also be involved either sparingly or diffusely penetrating the sinuses and cords.<ref name="pmid11903595">{{cite journal |vauthors=Mollejo M, Algara P, Mateo MS, Sánchez-Beato M, Lloret E, Medina MT, Piris MA |title=Splenic small B-cell lymphoma with predominant red pulp involvement: a diffuse variant of splenic marginal zone lymphoma? |journal=Histopathology |volume=40 |issue=1 |pages=22–30 |date=January 2002 |pmid=11903595 |doi= |url=}}</ref>
** [[Red pulp]] may also be involved either sparingly or diffusely penetrating the sinuses and cords.<ref name="pmid11903595">{{cite journal |vauthors=Mollejo M, Algara P, Mateo MS, Sánchez-Beato M, Lloret E, Medina MT, Piris MA |title=Splenic small B-cell lymphoma with predominant red pulp involvement: a diffuse variant of splenic marginal zone lymphoma? |journal=Histopathology |volume=40 |issue=1 |pages=22–30 |date=January 2002 |pmid=11903595 |doi= |url=}}</ref>
* '''Bone Marrow''':
* '''Bone Marrow''':
** Various patterns of Lymphocytic infiltration such as intrasinusoidal, nodular, interstitial and intravascular have been observed.<ref name="pmid28892912">{{cite journal |vauthors=Mohanpuria A, Kumar V, Suteri P, Marwah S, Nigam AS |title=Important Diagnostic Clues for Diagnosing Splenic Marginal Zone Lymphoma in Absence of Splenic Histology |journal=J Clin Diagn Res |volume=11 |issue=7 |pages=ED15–ED17 |date=July 2017 |pmid=28892912 |pmc=5583942 |doi=10.7860/JCDR/2017/27149.10190 |url=}}</ref>
** Various patterns of [[Lymphocytic]] infiltration such as intrasinusoidal, [[nodular]], [[interstitial]] and [[intravascular]] have been observed.<ref name="pmid28892912">{{cite journal |vauthors=Mohanpuria A, Kumar V, Suteri P, Marwah S, Nigam AS |title=Important Diagnostic Clues for Diagnosing Splenic Marginal Zone Lymphoma in Absence of Splenic Histology |journal=J Clin Diagn Res |volume=11 |issue=7 |pages=ED15–ED17 |date=July 2017 |pmid=28892912 |pmc=5583942 |doi=10.7860/JCDR/2017/27149.10190 |url=}}</ref>
** Mixed pattern of lymphocytic infiltration with intrasinusoidal being predominant.<ref name="pmid15389479">{{cite journal |vauthors=Iannitto E, Ambrosetti A, Ammatuna E, Colosio M, Florena AM, Tripodo C, Minardi V, Calvaruso G, Mitra ME, Pizzolo G, Menestrina F, Franco V |title=Splenic marginal zone lymphoma with or without villous lymphocytes. Hematologic findings and outcomes in a series of 57 patients |journal=Cancer |volume=101 |issue=9 |pages=2050–7 |date=November 2004 |pmid=15389479 |doi=10.1002/cncr.20596 |url=}}</ref><ref name="pmid12090417">{{cite journal |vauthors=Kent SA, Variakojis D, Peterson LC |title=Comparative study of marginal zone lymphoma involving bone marrow |journal=Am. J. Clin. Pathol. |volume=117 |issue=5 |pages=698–708 |date=May 2002 |pmid=12090417 |doi=10.1309/MECJ-GLK1-WEBW-UEVE |url=}}</ref>  
** Mixed pattern of [[lymphocytic]] infiltration with intrasinusoidal being predominant.<ref name="pmid15389479">{{cite journal |vauthors=Iannitto E, Ambrosetti A, Ammatuna E, Colosio M, Florena AM, Tripodo C, Minardi V, Calvaruso G, Mitra ME, Pizzolo G, Menestrina F, Franco V |title=Splenic marginal zone lymphoma with or without villous lymphocytes. Hematologic findings and outcomes in a series of 57 patients |journal=Cancer |volume=101 |issue=9 |pages=2050–7 |date=November 2004 |pmid=15389479 |doi=10.1002/cncr.20596 |url=}}</ref><ref name="pmid12090417">{{cite journal |vauthors=Kent SA, Variakojis D, Peterson LC |title=Comparative study of marginal zone lymphoma involving bone marrow |journal=Am. J. Clin. Pathol. |volume=117 |issue=5 |pages=698–708 |date=May 2002 |pmid=12090417 |doi=10.1309/MECJ-GLK1-WEBW-UEVE |url=}}</ref>  
** Cell population consists of small, intermediate and large lymphoid cells but small cells having large nucleus with dense chromatin and scant cytoplasm are present in abundance.<ref name="pmid23073320">{{cite journal |vauthors=Ponzoni M, Kanellis G, Pouliou E, Baliakas P, Scarfò L, Ferreri AJ, Doglioni C, Bikos V, Dagklis A, Anagnostopoulos A, Ghia P, Stamatopoulos K, Papadaki T |title=Bone marrow histopathology in the diagnostic evaluation of splenic marginal-zone and splenic diffuse red pulp small B-cell lymphoma: a reliable substitute for spleen histopathology? |journal=Am. J. Surg. Pathol. |volume=36 |issue=11 |pages=1609–18 |date=November 2012 |pmid=23073320 |doi=10.1097/PAS.0b013e318271243d |url=}}</ref>
** Cell population consists of small, intermediate and large [[lymphoid]] cells but small cells having large [[nucleus]] with dense [[chromatin]] and scant [[cytoplasm]] are present in abundance.<ref name="pmid23073320">{{cite journal |vauthors=Ponzoni M, Kanellis G, Pouliou E, Baliakas P, Scarfò L, Ferreri AJ, Doglioni C, Bikos V, Dagklis A, Anagnostopoulos A, Ghia P, Stamatopoulos K, Papadaki T |title=Bone marrow histopathology in the diagnostic evaluation of splenic marginal-zone and splenic diffuse red pulp small B-cell lymphoma: a reliable substitute for spleen histopathology? |journal=Am. J. Surg. Pathol. |volume=36 |issue=11 |pages=1609–18 |date=November 2012 |pmid=23073320 |doi=10.1097/PAS.0b013e318271243d |url=}}</ref>
* '''Lymph nodes'''
* '''Lymph nodes'''
** Splenic hilar and peripheral lymph nodes may be involved but less frequently as compared to the other organs.
** Splenic [[hilar]] and [[peripheral]] [[lymph nodes]] may be involved but less frequently as compared to the other organs.
** Micronodular infiltration with no involvement of the sinuses.<ref name="pmid9236833">{{cite journal |vauthors=Mollejo M, Lloret E, Menárguez J, Piris MA, Isaacson PG |title=Lymph node involvement by splenic marginal zone lymphoma: morphological and immunohistochemical features |journal=Am. J. Surg. Pathol. |volume=21 |issue=7 |pages=772–80 |date=July 1997 |pmid=9236833 |doi= |url=}}</ref>
** Micronodular infiltration with no involvement of the [[sinuses]].<ref name="pmid9236833">{{cite journal |vauthors=Mollejo M, Lloret E, Menárguez J, Piris MA, Isaacson PG |title=Lymph node involvement by splenic marginal zone lymphoma: morphological and immunohistochemical features |journal=Am. J. Surg. Pathol. |volume=21 |issue=7 |pages=772–80 |date=July 1997 |pmid=9236833 |doi= |url=}}</ref>
* '''Blood'''
* '''Blood'''
** Unusual neoplastic lymphoid B-cells with irregular cytoplasmic processes.<ref name="pmid534161">{{cite journal |vauthors=Wolfe JM |title=The computer paper illusion |journal=Perception |volume=8 |issue=3 |pages=347–8 |date=1979 |pmid=534161 |doi=10.1068/p080347 |url=}}</ref>
** Unusual [[neoplastic]] [[lymphoid]] B-cells with irregular [[cytoplasmic]] processes.<ref name="pmid534161">{{cite journal |vauthors=Wolfe JM |title=The computer paper illusion |journal=Perception |volume=8 |issue=3 |pages=347–8 |date=1979 |pmid=534161 |doi=10.1068/p080347 |url=}}</ref>


==References==
==References==

Revision as of 22:31, 5 January 2019

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [3]; Associate Editor(s)-in-Chief: Sowminya Arikapudi, M.B,B.S. [4]

Overview

Genes involved in the pathogenesis of splenic marginal zone lymphoma include immunoglobulin genes and CDK6 gene. On microscopic histopathological analysis, B-cells, villous lymphocytes, and sinus invasion are characteristic findings of splenic marginal zone lymphoma.


Pathophysiology

Pathogenesis

Genetics

  • There are several pathways involved in the normal functioning of the cells. Genetic dysregulation may affect these pathways resulting in abnormal function.
  • Common genetic abnormalities and their affected pathways in splenic marginal zone lymphoma are summarized under:
Pathways Gene mutations

NFkB[14][15][9]

Apoptosis[16][17]

Cell communication[18][19][20]

Cell cycle control[5][17][20]

Lymphocyte development and regulation[18][15][20]

Chromosomal and transcriptional regulation[15][21]

Associated conditions

Microscopic Pathology

  • Splenic marginal zone lymphoma (SMZL) tends to involve different organs such as spleen, bone marrow, blood and lymph nodes.[27].[28]
  • The microscopic features of these organs are described below:
  • Spleen
    • Micronodular pattern of lymphocytic infiltration of the white pulp involving both mantle and marginal zone component.[29]
    • Biphasic distribution of neoplastic B-cell in the follicles i.e small cells having dense chromatin and scant cytoplasm surrounded by intermediate size cells of marginal zone having variable nuclear contour and relatively abundant cytoplasm with interspersed large B-cells.
    • Red pulp may also be involved either sparingly or diffusely penetrating the sinuses and cords.[30]
  • Bone Marrow:
  • Lymph nodes
  • Blood

References

  1. ↑ [1] Dunn-Walters DK, Boursier L, Spencer J, Isaacson PG. "Analysis of immunoglobulin genes in splenic marginal zone lymphoma suggests ongoing mutation." Hum Pathol. 1998 Jun;29(6):585-93. PMID: 9635678
  2. ↑ Boonstra R, Bosga-Bouwer A, van Imhoff GW, Krause V, Palmer M, Coupland RW, Dabbagh L, van den Berg E, van den Berg A, Poppema S (December 2003). "Splenic marginal zone lymphomas presenting with splenomegaly and typical immunophenotype are characterized by allelic loss in 7q31-32". Mod. Pathol. 16 (12): 1210–7. doi:10.1097/01.MP.0000095895.19756.77. PMID 14681321.
  3. ↑ Hernández JM, García JL, Gutiérrez NC, Mollejo M, Martínez-Climent JA, Flores T, González MB, Piris MA, San Miguel JF (May 2001). "Novel genomic imbalances in B-cell splenic marginal zone lymphomas revealed by comparative genomic hybridization and cytogenetics". Am. J. Pathol. 158 (5): 1843–50. doi:10.1016/S0002-9440(10)64140-5. PMC 1891967. PMID 11337382.
  4. ↑ Andersen CL, Gruszka-Westwood A, Atkinson S, Matutes E, Catovsky D, Pedersen RK, Pedersen BB, Pulczynski S, Hokland P, Jacobsen E, Koch J (January 2005). "Recurrent genomic imbalances in B-cell splenic marginal-zone lymphoma revealed by comparative genomic hybridization". Cancer Genet. Cytogenet. 156 (2): 122–8. doi:10.1016/j.cancergencyto.2004.04.026. PMID 15642391.
  5. ↑ 5.0 5.1 Salido M, Baró C, Oscier D, Stamatopoulos K, Dierlamm J, Matutes E, Traverse-Glehen A, Berger F, Felman P, Thieblemont C, Gesk S, Athanasiadou A, Davis Z, Gardiner A, Milla F, Ferrer A, Mollejo M, Calasanz MJ, Florensa L, Espinet B, Luño E, Wlodarska I, Verhoef G, García-Granero M, Salar A, Papadaki T, Serrano S, Piris MA, Solé F (September 2010). "Cytogenetic aberrations and their prognostic value in a series of 330 splenic marginal zone B-cell lymphomas: a multicenter study of the Splenic B-Cell Lymphoma Group". Blood. 116 (9): 1479–88. doi:10.1182/blood-2010-02-267476. PMID 20479288.
  6. ↑ 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 (August 2012). "The coding genome of splenic marginal zone lymphoma: activation of NOTCH2 and other pathways regulating marginal zone development". J. Exp. Med. 209 (9): 1537–51. doi:10.1084/jem.20120904. PMID 22891273.
  7. ↑ Trøen G, Wlodarska I, Warsame A, Hernández Llodrà S, De Wolf-Peeters C, Delabie J (July 2008). "NOTCH2 mutations in marginal zone lymphoma". Haematologica. 93 (7): 1107–9. doi:10.3324/haematol.11635. PMID 18508802.
  8. ↑ Piva R, Deaglio S, Famà R, Buonincontri R, Scarfò I, Bruscaggin A, Mereu E, Serra S, Spina V, Brusa D, Garaffo G, Monti S, Dal Bo M, Marasca R, Arcaini L, Neri A, Gattei V, Paulli M, Tiacci E, Bertoni F, Pileri SA, Foà R, Inghirami G, Gaidano G, Rossi D (February 2015). "The Krüppel-like factor 2 transcription factor gene is recurrently mutated in splenic marginal zone lymphoma". Leukemia. 29 (2): 503–7. doi:10.1038/leu.2014.294. PMID 25283840.
  9. ↑ 9.0 9.1 Rossi D, Deaglio S, Dominguez-Sola D, Rasi S, Vaisitti T, Agostinelli C, Spina V, Bruscaggin A, Monti S, Cerri M, Cresta S, Fangazio M, Arcaini L, Lucioni M, Marasca R, Thieblemont C, Capello D, Facchetti F, Kwee I, Pileri SA, Foà R, Bertoni F, Dalla-Favera R, Pasqualucci L, Gaidano G (November 2011). "Alteration of BIRC3 and multiple other NF-κB pathway genes in splenic marginal zone lymphoma". Blood. 118 (18): 4930–4. doi:10.1182/blood-2011-06-359166. PMID 21881048.
  10. ↑ Spina V, Rossi D (August 2016). "NF-κB deregulation in splenic marginal zone lymphoma". Semin. Cancer Biol. 39: 61–7. doi:10.1016/j.semcancer.2016.08.002. PMID 27503810.
  11. ↑ Baldini L, Fracchiolla NS, Cro LM, Trecca D, Romitti L, Polli E, Maiolo AT, Neri A (July 1994). "Frequent p53 gene involvement in splenic B-cell leukemia/lymphomas of possible marginal zone origin". Blood. 84 (1): 270–8. PMID 8018922.
  12. ↑ Gruszka-Westwood AM, Hamoudi RA, Matutes E, Tuset E, Catovsky D (June 2001). "p53 abnormalities in splenic lymphoma with villous lymphocytes". Blood. 97 (11): 3552–8. PMID 11369650.
  13. ↑ [2] Corcoran MM, Mould SJ, Orchard JA, Ibbotson RE, Chapman RM, Boright AP, Platt C, Tsui LC, Scherer SW, Oscier DG. "Dysregulation of cyclin dependent kinase 6 expression in splenic marginal zone lymphoma through chromosome 7q translocations." Oncogene. 1999 Nov 4;18(46):6271-7. PMID: 10597225
  14. ↑ Clipson A, Wang M, de Leval L, Ashton-Key M, Wotherspoon A, Vassiliou G, Bolli N, Grove C, Moody S, Escudero-Ibarz L, Gundem G, Brugger K, Xue X, Mi E, Bench A, Scott M, Liu H, Follows G, Robles EF, Martinez-Climent JA, Oscier D, Watkins AJ, Du MQ (May 2015). "KLF2 mutation is the most frequent somatic change in splenic marginal zone lymphoma and identifies a subset with distinct genotype". Leukemia. 29 (5): 1177–85. doi:10.1038/leu.2014.330. PMID 25428260.
  15. ↑ 15.0 15.1 15.2 Parry M, Rose-Zerilli MJ, Ljungström V, Gibson J, Wang J, Walewska R, Parker H, Parker A, Davis Z, Gardiner A, McIver-Brown N, Kalpadakis C, Xochelli A, Anagnostopoulos A, Fazi C, de Castro DG, Dearden C, Pratt G, Rosenquist R, Ashton-Key M, Forconi F, Collins A, Ghia P, Matutes E, Pangalis G, Stamatopoulos K, Oscier D, Strefford JC (September 2015). "Genetics and Prognostication in Splenic Marginal Zone Lymphoma: Revelations from Deep Sequencing". Clin. Cancer Res. 21 (18): 4174–4183. doi:10.1158/1078-0432.CCR-14-2759. PMC 4490180. PMID 25779943.
  16. ↑ Ruiz-Ballesteros E, Mollejo M, Rodriguez A, Camacho FI, Algara P, Martinez N, Pollán M, Sanchez-Aguilera A, Menarguez J, Campo E, Martinez P, Mateo M, Piris MA (September 2005). "Splenic marginal zone lymphoma: proposal of new diagnostic and prognostic markers identified after tissue and cDNA microarray analysis". Blood. 106 (5): 1831–8. doi:10.1182/blood-2004-10-3898. PMID 15914563.
  17. ↑ 17.0 17.1 Trøen G, Nygaard V, Jenssen TK, Ikonomou IM, Tierens A, Matutes E, Gruszka-Westwood A, Catovsky D, Myklebost O, Lauritzsen G, Hovig E, Delabie J (November 2004). "Constitutive expression of the AP-1 transcription factors c-jun, junD, junB, and c-fos and the marginal zone B-cell transcription factor Notch2 in splenic marginal zone lymphoma". J Mol Diagn. 6 (4): 297–307. doi:10.1016/S1525-1578(10)60525-9. PMC 1867488. PMID 15507668.
  18. ↑ 18.0 18.1 Parry M, Rose-Zerilli MJ, Gibson J, Ennis S, Walewska R, Forster J, Parker H, Davis Z, Gardiner A, Collins A, Oscier DG, Strefford JC (2013). "Whole exome sequencing identifies novel recurrently mutated genes in patients with splenic marginal zone lymphoma". PLoS ONE. 8 (12): e83244. doi:10.1371/journal.pone.0083244. PMC 3862727. PMID 24349473.
  19. ↑ Fresquet V, Robles EF, Parker A, Martinez-Useros J, Mena M, Malumbres R, Agirre X, Catarino S, Arteta D, Osaba L, Mollejo M, Hernandez-Rivas JM, Calasanz MJ, Daibata M, Dyer MJ, Prosper F, Vizcarra E, Piris MÁ, Oscier D, Martinez-Climent JA (September 2012). "High-throughput sequencing analysis of the chromosome 7q32 deletion reveals IRF5 as a potential tumour suppressor in splenic marginal-zone lymphoma". Br. J. Haematol. 158 (6): 712–26. doi:10.1111/j.1365-2141.2012.09226.x. PMID 22816737.
  20. ↑ 20.0 20.1 20.2 Martínez N, Almaraz C, Vaqué JP, Varela I, Derdak S, Beltran S, Mollejo M, Campos-Martin Y, Agueda L, Rinaldi A, Kwee I, Gut M, Blanc J, Oscier D, Strefford JC, Martinez-Lopez J, Salar A, Sole F, Rodriguez-Peralto JL, Diez-Tascón C, García JF, Fraga M, Sebastián E, Alvés J, Menárguez J, González-Carreró J, Casado LF, Bayes M, Bertoni F, Gut I, Piris MA (June 2014). "Whole-exome sequencing in splenic marginal zone lymphoma reveals mutations in genes involved in marginal zone differentiation". Leukemia. 28 (6): 1334–40. doi:10.1038/leu.2013.365. PMID 24296945.
  21. ↑ Rinaldi A, Forconi F, Arcaini L, Mian M, Sozzi E, Zibellini S, Baldini L, Franceschetti S, Gaidano G, Marasca R, Mollejo M, Piris MA, Tucci A, Facchetti F, Bhagat G, Favera RD, Rancoita PM, Zucca E, Kwee I, Bertoni F (December 2010). "Immunogenetics features and genomic lesions in splenic marginal zone lymphoma". Br. J. Haematol. 151 (5): 435–9. PMID 21113978.
  22. ↑ Chuang SS, Liao YL, Chang ST, Hsieh YC, Kuo SY, Lu CL, Hwang WS, Lin IH, Tsao CJ, Huang WT (July 2010). "Hepatitis C virus infection is significantly associated with malignant lymphoma in Taiwan, particularly with nodal and splenic marginal zone lymphomas". J. Clin. Pathol. 63 (7): 595–8. doi:10.1136/jcp.2010.076810. PMID 20530156.
  23. ↑ Gurvits GE, Mahtani R, Halperin I (November 2007). "Hepatitis C virus and splenic marginal zone lymphoma with villous lymphocytes: away from conventional therapy". Scand. J. Gastroenterol. 42 (11): 1392–3. doi:10.1080/00365520701420800. PMID 17852855.
  24. ↑ Weng WK, Levy S (July 2003). "Hepatitis C virus (HCV) and lymphomagenesis". Leuk. Lymphoma. 44 (7): 1113–20. doi:10.1080/1042819031000076972. PMID 12916862.
  25. ↑ Quinn ER, Chan CH, Hadlock KG, Foung SK, Flint M, Levy S (December 2001). "The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis". Blood. 98 (13): 3745–9. PMID 11739181.
  26. ↑ Hermine O, Lefrère F, Bronowicki JP, Mariette X, Jondeau K, Eclache-Saudreau V, Delmas B, Valensi F, Cacoub P, Brechot C, Varet B, Troussard X (July 2002). "Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection". N. Engl. J. Med. 347 (2): 89–94. doi:10.1056/NEJMoa013376. PMID 12110736.
  27. ↑ Zinzani PL (2012). "The many faces of marginal zone lymphoma". Hematology Am Soc Hematol Educ Program. 2012: 426–32. doi:10.1182/asheducation-2012.1.426. PMID 23233614.
  28. ↑ Arcaini L, Rossi D, Paulli M (April 2016). "Splenic marginal zone lymphoma: from genetics to management". Blood. 127 (17): 2072–81. doi:10.1182/blood-2015-11-624312. PMID 26989207.
  29. ↑ Papadaki T, Stamatopoulos K, Belessi C, Pouliou E, Parasi A, Douka V, Laoutaris N, Fassas A, Anagnostopoulos A, Anagnostou D (March 2007). "Splenic marginal-zone lymphoma: one or more entities? A histologic, immunohistochemical, and molecular study of 42 cases". Am. J. Surg. Pathol. 31 (3): 438–46. doi:10.1097/01.pas.0000213419.08009.b0. PMID 17325486.
  30. ↑ Mollejo M, Algara P, Mateo MS, Sánchez-Beato M, Lloret E, Medina MT, Piris MA (January 2002). "Splenic small B-cell lymphoma with predominant red pulp involvement: a diffuse variant of splenic marginal zone lymphoma?". Histopathology. 40 (1): 22–30. PMID 11903595.
  31. ↑ Mohanpuria A, Kumar V, Suteri P, Marwah S, Nigam AS (July 2017). "Important Diagnostic Clues for Diagnosing Splenic Marginal Zone Lymphoma in Absence of Splenic Histology". J Clin Diagn Res. 11 (7): ED15–ED17. doi:10.7860/JCDR/2017/27149.10190. PMC 5583942. PMID 28892912.
  32. ↑ Iannitto E, Ambrosetti A, Ammatuna E, Colosio M, Florena AM, Tripodo C, Minardi V, Calvaruso G, Mitra ME, Pizzolo G, Menestrina F, Franco V (November 2004). "Splenic marginal zone lymphoma with or without villous lymphocytes. Hematologic findings and outcomes in a series of 57 patients". Cancer. 101 (9): 2050–7. doi:10.1002/cncr.20596. PMID 15389479.
  33. ↑ Kent SA, Variakojis D, Peterson LC (May 2002). "Comparative study of marginal zone lymphoma involving bone marrow". Am. J. Clin. Pathol. 117 (5): 698–708. doi:10.1309/MECJ-GLK1-WEBW-UEVE. PMID 12090417.
  34. ↑ Ponzoni M, Kanellis G, Pouliou E, Baliakas P, Scarfò L, Ferreri AJ, Doglioni C, Bikos V, Dagklis A, Anagnostopoulos A, Ghia P, Stamatopoulos K, Papadaki T (November 2012). "Bone marrow histopathology in the diagnostic evaluation of splenic marginal-zone and splenic diffuse red pulp small B-cell lymphoma: a reliable substitute for spleen histopathology?". Am. J. Surg. Pathol. 36 (11): 1609–18. doi:10.1097/PAS.0b013e318271243d. PMID 23073320.
  35. ↑ Mollejo M, Lloret E, Menárguez J, Piris MA, Isaacson PG (July 1997). "Lymph node involvement by splenic marginal zone lymphoma: morphological and immunohistochemical features". Am. J. Surg. Pathol. 21 (7): 772–80. PMID 9236833.
  36. ↑ Wolfe JM (1979). "The computer paper illusion". Perception. 8 (3): 347–8. doi:10.1068/p080347. PMID 534161.

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