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Okay M, et al: Splenic Marginal Zone Lymphoma in TurkeyTurk J Hematol 2020;37:84-90HBV and SMZL in a considerably large SMZL cohort. Some otherstudies reported on only a few patients with SMZL associatedwith HBV [19,20,21,22,23]. Recently, Fetica et al. [24] fromRomania found HBV infection in 3 patients out of 34 SMZLpatients in the same time period as our early report. A morerecent study from China reported HBsAg positivity in 25/160(16%) and resolved HBV infection (HBsAg negative, anti-HBcpositive) in 54/160 (34%) patients [25]. A summary of the datain the literature on HBV and HCV seropositivity is shown in Table3 [19,20,21,22,23,24,25,26,27,28,29].Chronic antigenic stimulation is frequently blamed in thepathogenesis of extranodal marginal zone lymphomas. Theassociation between gastric mucosa-associated lymphoid tissuelymphoma and chronic Helicobacter pylori infection is theclassical example for this relationship. An association betweenHCV and SMZL has been previously reported in some geographicregions, mostly in South Europe [2,5,29]. Now we can suggestthat the association between SMZL and chronic viral hepatitisis not specific for HCV. HBV may also be involved in SMZLlymphomagenesis.Splenectomy and rituximab-based chemoimmunotherapieswere the most frequently used treatments in our cohort. Thisis in concordance with current treatment strategies for SMZL.Responses (most commonly hematological improvement aftersplenectomy as expected) were very frequent (94.9%) in ourcohort. The median follow-up duration (21.2 months) in ourpatients was relatively short for this indolent lymphoma.Estimated 10-year survival was 68.6%. We found manyparameters (lower albumin, splenectomy, thrombocytopenia,elevated LDH, higher b 2-microglobulin, and HBsAg positivity)to be associated with overall survival, but albumin was theonly parameter to retain marginal significance in multivariateanalysis (Figure 2). HBsAg positivity was an adverse prognosticfactor in univariate analysis, but not in the multivariate test. Itis possible that HBV may indirectly affect survival by loweringserum albumin levels due to liver impairment. This suggestionshould be investigated in further studies.Arcaini et al. [2] reported 10-year OS as 65% in SMZL. In thatstudy, the authors proposed a prognostic model includinghemoglobin of <12 g/dL, elevated LDH, and albumin level of <3.5Table 3. Summary of the data in the literature about hepatitis B and C.ReferenceType[19] Case report 1[20] Letter to the editor 1[22] Case report 1[26] Case report 1[23] Research article 129[24] Research article 34Number ofpatientsImportant clinical features56-year-old Lebanese male patient with B symptoms and elevated liverenzymes was diagnosed with HBV infection; after 6 months, SMZL wasdiagnosed due to persistent splenomegaly38-year-old male Greek patient with a history of chronic HBV infection wasdiagnosed with SMZL with developing B symptoms and splenomegaly64-year-old Chinese man with cirrhosis (HBV-positive) was diagnosed withhepatocellular cancer and SMZL (mass in liver and spleen)42-year-old Caucasian male patient with a history of chronic HCV infectionwas diagnosed with SMZL with increased lymphocyte count and mildsplenomegaly129 adult patients were consecutively diagnosed with SMZL in Italianhematological centers; HCV seropositivity was 16/129 (16%)731 lymphoma cases from Romania with Hodgkin lymphoma (160 cases),NHLs (571 cases), and SMZL (34 cases); results of tests for viral hepatitisinfection were available for 17 cases (17/34); 2/17 (11.7%) patients werepositive for HCV and 3/17 (17.7%) patients were positive for HBV[27] Research article 1401052 MZL cases with EMZL (633 cases), NMZL (157 cases), and SMZL (140cases) and 13766 controls from 12 case-control studies; HCV seropositivitywas 3.2%, OR was 3.04 (95% CI: 1.65-5.60)[28] Research article 100[25] Research article 160[29] Research article 15Study was based on real-life data from Italy; HCV positivity was 3.1% in 100SMZL patientsStudy was conducted with 160 SMZL patients from China; 25 patients (16%)were HBsAg-positive and 54 (34%) patients had resolved HBV infection; IGHgene was analyzed in 39 patients; patients with HBV infection presentedbiased IGHV-D-J rearrangements and mutational status9 SMZL patients with HCV infection from France who received IFN alpha hadremission; in contrast, none of the six HCV-negative patients had a responseto IFN therapyHBV: Hepatitis B infection, HCV: hepatitis C infection, MZL: marginal zone lymphoma, EMZL: extranodal marginal zone lymphoma, NMZL: nodal marginal zone lymphoma,OR: odds ratio, CI: confidence interval, IFN alpha: interferon alpha.88
Turk J Hematol 2020;37:84-90Okay M, et al: Splenic Marginal Zone Lymphoma in TurkeyS.K., S.N., S.S., G.A.C., S.D., I.B., E.O., F.V., M.T., B.E., G.O., R.Y.,M.H.D., I.B., M.A.E., F.A., Y.B.; Analysis or Interpretation: M.O.,U.Y.M., Y.B.; Literature Search: M.O., U.Y.M., Y.B.; Writing: M.O.,U.Y.M., Y.B.Conflict of Interest: No conflict of interest was declared by theauthors.Financial Disclosure: This research did not receive any specificgrants from funding agencies in the public, commercial, or notfor-profitsectors.Figure 2. Overall survival according to serum albumin level atdiagnosis.g/dL as adverse prognostic factors. In another study, Montalbánet al. [5] developed a continuous model for estimatinglymphoma-specific survival including decreased hemoglobinlevel, lower platelet count, elevated LDH, and extrahilarlymphadenopathy as unfavorable prognostic indicators. In arecent Chinese study [25], the authors also suggested a newprognostic system. Decreased hemoglobin, HBsAg positivity, andcomplex karyotype were related to decreased survival in thatstudy. We did not intend to develop a prognostic scoring systemor to test previously suggested scoring systems in our study,but it is convincing to observe that many of the risk factors weidentified in univariate analyses have been previously reportedto have prognostic significance in SMZL.The major limitations of this study are its retrospective designand somewhat limited number of patients.ConclusionOur results in association with some recent literature dataindicate that HBV may be a possible risk factor for developmentof SMZL in some geographical regions, similar to HCV in someWestern countries. It may also be an indirect prognostic factor.Larger studies about this rare lymphoma would obviouslyprovide better data and firmer conclusions on this relationshipand the prognostic impact of HBV.EthicsEthics Committee Approval: Retrospective study.Informed Consent: Approval was obtained from the patientsduring their first hospitalization as most of them were beingtreated in the hospital.Authorship ContributionsConcept: M.O., H.G., Y.B.; Design: M.O., H.G., Y.B.; Data Collectionor Processing: M.O., T.O., E.O., E.G., A.U., N.A.A., E.Y., A.A., M.S.D.,Acknowledgments: The interim results of this study werepresented at the American Society of Hematology 2016 AnnualMeeting.Gülsüm Emel Pamuk, M.D., previously affiliated with TrakyaUniversity’s Faculty of Medicine, could not be contacted duringthe preparation and submission of this paper. We would like tothank her for her contributions.References1. Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R, Advani R,Ghielmini M, Salles GA, Zelenetz AD, Jaffe ES. The 2016 revision of theWorld Health Organization classification of lymphoid neoplasms. Blood2016;127:2375-2390.2. Arcaini L, Lazzarino M, Colombo N, Burcheri S, Boveri E, Paulli M, Morra E,Gambacorta M, Cortelazzo S, Tucci A, Ungari M, Ambrosetti A, MenestrinaF, Orsucci L, Novero D, Pulsoni A, Frezzato M, Gaidano G, Vallisa D, MinardiV, Tripodo C, Callea V, Baldini L, Merli F, Federico M, Franco V, Iannitto E;Integruppo Italiano Linfomi. Splenic marginal zone lymphoma: a prognosticmodel for clinical use. Blood 2006;107:4643-4649.3. Olszewski AJ, Castillo JJ. Survival of patients with marginal zone lymphoma:analysis of the Surveillance, Epidemiology, and End Results database. Cancer2013;119:629-638.4. Peveling-Oberhag J, Crisman G, Schmidt A, Döring C, Lucioni M, ArcainiL, Rattotti S, Hartmann S, Piiper A, Hofmann WP, Paulli M, Küppers R,Zeuzem S, Hansmann ML. Dysregulation of global microRNA expression insplenic marginal zone lymphoma and influence of chronic hepatitis C virusinfection. Leukemia 2012;26:1654-1662.5. Montalbán C, Abraira V, Arcaini L, Domingo-Domenech E, Guisado-Vasco P,Iannitto E, Mollejo M, Matutes E, Ferreri A, Salar A, Rattotti S, Carpaneto A,Pérez Fernández R, Bello JL, Hernández M, Caballero D, Carbonell F, Piris MA;Splenic Marginal Zone Lymphoma Study Group. Risk stratification for splenicmarginal zone lymphoma based on haemoglobin concentration, plateletcount, high lactate dehydrogenase level and extrahilar lymphadenopathy:development and validation on 593 cases. Br J Haematol 2012;159:164-171.6. Thieblemont C, Felman P, Berger F, Dumontet C, Arnaud P, Hequet O, ArcacheJ, Callet-Bauchu E, Salles G, Coiffier B. Treatment of splenic marginal zoneB-cell lymphoma: an analysis of 81 patients. Clin Lymphoma 2002;3:41-47.7. Troussard X, Valensi F, Duchayne E, Garand R, Felman P, Tulliez M, Henry-Amar M, Bryon PA, Flandrin G. Splenic lymphoma with villous lymphocytes:clinical presentation, biology and prognostic factors in a series of 100patients. Groupe Francais d’Hématologie Cellulaire (GFHC). Br J Haematol1996;93:731-736.8. Parry-Jones N, Matutes E, Gruszka-Westwood AM, Swansbury GJ,Wotherspoon AC, Catovsky D. Prognostic features of splenic lymphoma withvillous lymphocytes: a report on 129 patients. Br J Haematol 2003;120:759-764.89
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