Advertisement
Position Paper| Volume 50, ISSUE 2, P124-131, February 2018

Gastrointestinal lymphomas: French Intergroup clinical practice recommendations for diagnosis, treatment and follow-up (SNFGE, FFCD, GERCOR, UNICANCER, SFCD, SFED, SFRO, SFH)

Published:December 18, 2017DOI:https://doi.org/10.1016/j.dld.2017.12.006

      Abstract

      Introduction

      This document is a summary of the French Intergroup guidelines on the management of gastro-intestinal lymphomas, available on the web-site of the French Society of Gastroenterology, SNFGE (www.tncd.org), updated in September 2017.

      Methods

      This collaborative work was realised under the auspices of several French medical societies and involved clinicians with specific expertise in the field of gastrointestinal lymphomas, including gastroenterologists, haematologists, pathologists, and radiation oncologist, representing the major French or European clinical trial groups. It summarises their consensus on the management of gastrointestinal lymphomas, based on the recent literature data, previous published guidelines and the expert opinions.

      Results

      The clinical management, and especially the therapeutic strategies of the gastro-intestinal lymphomas are specific to their histological subtypes and to their locations in the digestive tract, with the particularity of gastric MALT lymphomas which are the most frequent and usually related to gastritis induced by Helicobacter pylori.

      Conclusion

      Lymphomas are much less common than epithelial tumours of gastro-intestinal digestive tract. Their different histological subtypes determine their management and prognosis. Each individual case should be discussed within the expert multidisciplinary team.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Digestive and Liver Disease
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Isaacson P.G.
        Update on MALT lymphomas.
        Best Pract Res Clin Haematol. 2005; 18: 57-68
        • Andrews C.N.
        • John Gill M.
        • Urbanski S.J.
        • Stewart D.
        • Perini R.
        • Beck P.
        Changing epidemiology and risk factors for gastrointestinal non-Hodgkin’s lymphoma in a North American population: population-based study.
        Am J Gastroenterol. 2008; 103: 1762-1769
        • Lepage C.
        • Bouvier A.M.
        • Manfredi S.
        • Dancourt V.
        • Faivre J.
        Incidence and management of primary malignant small bowel cancers: a well-defined French population study.
        Am J Gastroenterol. 2006; 101: 2826-2832
        • Ruskone-Fourmestraux A.
        • Aegerter P.
        • Delmer A.
        • Brousse N.
        • Galian A.
        • Rambaud J.C.
        Primary digestive tract lymphoma: a prospective multicentric study of 91 patients. Groupe d'Etude des Lymphomes Digestifs.
        Gastroenterology. 1993; 105: 1662-1671
        • Fischbach W.
        • Dragosics B.
        • Kolve-Goebeler M.E.
        • Ohmann C.
        • Greiner A.
        • Yang Q.
        • et al.
        Primary gastric B-cell lymphoma: results of a prospective multicenter study: The German–Austrian Gastrointestinal Lymphoma Study Group.
        Gastroenterology. 2000; 119: 1191-1202
        • Koch P.
        • del Valle F.
        • Berdel W.E.
        • Willich N.A.
        • Reers B.
        • Hiddemann W.
        • et al.
        Primary gastrointestinal non-Hodgkin’s lymphoma: I. Anatomic and histologic distribution, clinical features, and survival data of 371 patients registered in the German Multicenter Study GIT NHL 01/92.
        J Clin Oncol. 2001; 19: 3861-3873
        • Ruskone-Fourmestraux A.
        • Fischbach W.
        • Aleman B.M.
        • Boot H.
        • Du M.Q.
        • Megraud F.
        • et al.
        EGILS consensus report: gastric extranodal marginal zone B-cell lymphoma of MALT.
        Gut. 2011; 60: 747-758
        • Zucca E.
        • Copie-Bergman C.
        • Ricardi U.
        • Thieblemont C.
        • Raderer M.
        • Ladetto M.
        Gastric marginal zone lymphoma of MALT type: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up.
        Ann Oncol. 2013; 24: vi144-vi148
        • Dreyling M.
        • Thieblemont C.
        • Gallamini A.
        • Arcaini L.
        • Campo E.
        • Hermine O.
        • et al.
        ESMO consensus conferences: guidelines on malignant lymphoma. Part 2: marginal zone lymphoma, mantle cell lymphoma, peripheral T-cell lymphoma.
        Ann Oncol. 2013; 24: 857-877
        • Matysiak-Budnik T.
        • Jamet P.
        • Fabiani B.
        • Nion-Larmurier I.
        • Marjanovic Z.
        • Ruskone-Fourmestraux A.
        Primary intestinal B-cell lymphoma: a prospective multicentre clinical study of 91 cases.
        Dig Liver Dis. 2013; 45: 947-952
        • Franco M.
        • Rugge M.
        • D'Andrea E.
        • Mescoli C.
        • Menin C.
        • Farinati F.
        Gastric mucosa-associated lymphoid tissue lymphoma and Helicobacter pylori: scratch and win.
        Scand J Gastroenterol. 2005; 40: 115-119
        • Lehours P.
        • Ruskone-Fourmestraux A.
        • Lavergne A.
        • Cantet F.
        • Megraud F.
        Which test to use to detect Helicobacter pylori infection in patients with low-grade gastric mucosa-associated lymphoid tissue lymphoma?.
        Am J Gastroenterol. 2003; 98: 291-295
        • Malfertheiner P.
        • Megraud F.
        • O'Morain C.A.
        • Gisbert J.P.
        • Kuipers E.J.
        • Axon A.T.
        • et al.
        Management of Helicobacter pylori infection—the Maastricht V/Florence Consensus Report.
        Gut. 2017; 66: 6-30
        • Swerdlow S.H.
        • Campo E.
        • Pileri S.A.
        • Harris N.L.
        • Stein H.
        • Siebert R.
        • et al.
        The 2016 revision of the World Health Organization classification of lymphoid neoplasms.
        Blood. 2016; 127: 2375-2390
        • Copie-Bergman C.
        • Wotherspoon A.C.
        • Capella C.
        • Motta T.
        • Pedrinis E.
        • Pileri S.A.
        • et al.
        Gela histological scoring system for post-treatment biopsies of patients with gastric MALT lymphoma is feasible and reliable in routine practice.
        Br J Haematol. 2013; 160: 47-52
        • Liu H.
        • Ye H.
        • Ruskone-Fourmestraux A.
        • De Jong D.
        • Pileri S.
        • Thiede C.
        • et al.
        T(11;18) is a marker for all stage gastric MALT lymphomas that will not respond to H. pylori eradication.
        Gastroenterology. 2002; 122: 1286-1294
        • Levy M.
        • Copie-Bergman C.
        • Molinier-Frenkel V.
        • Riou A.
        • Haioun C.
        • Gaulard P.
        • et al.
        Treatment of t(11;18)-positive gastric mucosa-associated lymphoid tissue lymphoma with rituximab and chlorambucil: clinical, histological, and molecular follow-up.
        Leuk Lymphoma. 2010; 51: 284-290
        • Fischbach W.
        Gastric mucosa-associated lymphoid tissue lymphoma: a challenge for endoscopy.
        Gastrointest Endosc. 2008; 68: 632-634
        • Ruskone-Fourmestraux A.
        • Lavergne A.
        • Aegerter P.H.
        • Megraud F.
        • Palazzo L.
        • de Mascarel A.
        • et al.
        Predictive factors for regression of gastric MALT lymphoma after anti-Helicobacter pylori treatment.
        Gut. 2001; 48: 297-303
        • Flieger D.
        • Keller R.
        • May A.
        • Ell C.
        • Fischbach W.
        Capsule endoscopy in gastrointestinal lymphomas.
        Endoscopy. 2005; 37: 1174-1180
        • Cheson B.D.
        • Fisher R.I.
        • Barrington S.F.
        • Cavalli F.
        • Schwartz L.H.
        • Zucca E.
        • et al.
        Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification.
        J Clin Oncol. 2014; 32: 3059-3068
        • Song K.H.
        • Yun M.
        • Kim J.H.
        • Yang W.I.
        • Kang D.R.
        • Chung J.B.
        • et al.
        Role of F-FDG PET scans in patients with Helicobacter pylori-infected gastric low-grade MALT lymphoma.
        Gut Liver. 2011; 5: 308-314
        • Ruskone-Fourmestraux A.
        • Dragosics B.
        • Morgner A.
        • Wotherspoon A.
        • Dd Jong D.
        Paris staging system for primary gastrointestinal lymphomas.
        Gut. 2003; 52: 912-913
        • Park H.S.
        • Kim Y.J.
        • Yang W.I.
        • Suh C.O.
        • Lee Y.C.
        Treatment outcome of localized Helicobacter pylori-negative low-grade gastric MALT lymphoma.
        World J Gastroenterol. 2010; 16: 2158-2162
        • Raderer M.
        • Streubel B.
        • Wohrer S.
        • Hafner M.
        • Chott A.
        Successful antibiotic treatment of Helicobacter pylori negative gastric mucosa associated lymphoid tissue lymphomas.
        Gut. 2006; 55: 616-618
        • Janssen J.
        The impact of EUS in primary gastric lymphoma.
        Best Pract Res Clin Gastroenterol. 2009; 23: 671-678
        • Fischbach W.
        • Goebeler-Kolve M.E.
        • Greiner A.
        Diagnostic accuracy of EUS in the local staging of primary gastric lymphoma: results of a prospective, multicenter study comparing EUS with histopathologic stage.
        Gastrointest Endosc. 2002; 56: 696-700
        • Zullo A.
        • Hassan C.
        • Cristofari F.
        • Andriani A.
        • De Fansesco V.
        • Lerardi E.
        • et al.
        Effects of Helicobacter pylori eradication on early stage gastric mucosa-associated lymphoid tissue lymphoma.
        Clin Gastroenterol Hepatol. 2010; 8: 105-110
        • Liu H.
        • Ye H.
        • Dogan A.
        • Ranaldi R.
        • Hamoudi R.A.
        • Bearzi I.
        • et al.
        T(11;18)(q21;q21) is associated with advanced mucosa-associated lymphoid tissue lymphoma that expresses nuclear BCL10.
        Blood. 2001; 98: 1182-1187
        • Fischbach W.
        • Goebeler M.E.
        • Ruskone-Fourmestraux A.
        • Wundisch T.
        • Neubauer A.
        • Raderer M.
        • et al.
        Most patients with minimal histological residuals of gastric MALT lymphoma after successful eradication of Helicobacter pylori can be managed safely by a watch and wait strategy: experience from a large international series.
        Gut. 2007; 56: 1685-1687
        • Zullo A.
        • Hassan C.
        • Andriani A.
        • Cristofari F.
        • Bassanelli C.
        • Spinelli G.P.
        • et al.
        Treatment of low-grade gastric MALT-lymphoma unresponsive to Helicobacter pylori therapy: a pooled-data analysis.
        Med Oncol. 2010; 27: 291-295
        • Gobbi P.G.
        • Ghirardelli M.L.
        • Cavalli C.
        • Baldini L.
        • Broglia C.
        • Clo V.
        • et al.
        The role of surgery in the treatment of gastrointestinal lymphomas other than low-grade MALT lymphomas.
        Haematologica. 2000; 85 ([In Process Citation]): 372-380
        • Tomita N.
        • Kodaira T.
        • Tachibana H.
        • Nakamura T.
        • Mizoguchi N.
        • Takada A.
        Favorable outcomes of radiotherapy for early-stage mucosa-associated lymphoid tissue lymphoma.
        Radiother Oncol. 2009; 90: 231-235
        • Tsang R.W.
        • Gospodarowicz M.K.
        • Pintilie M.
        • Wells W.
        • Hodgson D.C.
        • Sun A.
        • et al.
        Localized mucosa-associated lymphoid tissue lymphoma treated with radiation therapy has excellent clinical outcome.
        J Clin Oncol. 2003; 21: 4157-4164
        • Vrieling C.
        • de Jong D.
        • Boot H.
        • de Boer J.P.
        • Wegman F.
        • Aleman B.M.
        Long-term results of stomach-conserving therapy in gastric MALT lymphoma.
        Radiother Oncol. 2008; 87: 405-411
        • Wirth A.
        • Gospodarowicz M.
        • Aleman B.M.
        • Bressel M.
        • Ng A.
        • Chao M.
        • et al.
        Long-term outcome for gastric marginal zone lymphoma treated with radiotherapy: a retrospective, multi-centre, International Extranodal Lymphoma Study Group study.
        Ann Oncol. 2013; 24: 1344-1351
        • Ruskone-Fourmestraux A.
        • Matysiak-Budnik T.
        • Fabiani B.
        • Cervera P.
        • Brixi H.
        • Le Malicot K.
        • et al.
        Exclusive moderate-dose radiotherapy in gastric marginal zone B-cell MALT lymphoma: results of a prospective study with a long term follow-up.
        Radiother Oncol. 2015; 117: 178-182
        • Nam T.K.
        • Ahn J.S.
        • Choi Y.D.
        • Jeong J.U.
        • Kim Y.H.
        • Yoon M.S.
        • et al.
        The role of radiotherapy in the treatment of gastric mucosa-associated lymphoid tissue lymphoma.
        Cancer Res Treat. 2014; 46: 33-40
        • Zucca E.
        • Conconi A.
        • Laszlo D.
        • Lopez-Guillermo A.
        • Bouabdallah R.
        • Coiffier B.
        • et al.
        Addition of rituximab to chlorambucil produces superior event-free survival in the treatment of patients with extranodal marginal-zone B-cell lymphoma: 5-year analysis of the IELSG-19 randomized study.
        J Clin Oncol. 2013; 31: 565-572
        • Salles G.
        • Seymour J.F.
        • Offner F.
        • Lopez-Guillermo A.
        • Belada D.
        • Xerri L.
        • et al.
        Rituximab maintenance for 2 years in patients with high tumour burden follicular lymphoma responding to rituximab plus chemotherapy (PRIMA): a phase 3, randomised controlled trial.
        Lancet. 2011; 377: 42-51
        • Sacchi S.
        • Marcheselli L.
        • Bari A.
        • Marcheselli R.
        • Pozzi S.
        • Luminari S.
        • et al.
        Secondary malignancies after treatment for indolent non-Hodgkin’s lymphoma: a 16-year follow-up study.
        Haematologica. 2008; 93: 398-404
        • Raderer M.
        • Chott A.
        • Drach J.
        • Montalban C.
        • Dragosics B.
        • Jager U.
        • et al.
        Chemotherapy for management of localised high-grade gastric B-cell lymphoma: how much is necessary?.
        Ann Oncol. 2002; 13: 1094-1098
        • Fischbach W.
        Helicobacter pylori eradication therapy in primary high-grade gastric MALT lymphoma.
        Gastroenterology. 2002; 123: 393
        • Kim S.J.
        • Choi C.W.
        • Mun Y.C.
        • Oh S.Y.
        • Kang H.J.
        • Lee S.I.
        • et al.
        Multicenter retrospective analysis of 581 patients with primary intestinal non-hodgkin lymphoma from the Consortium for Improving Survival of Lymphoma (CISL).
        BMC Cancer. 2011; 11: 321
        • Ruskone-Fourmestraux A.
        • Audouin J.
        Primary gastrointestinal tract mantle cell lymphoma as multiple lymphomatous polyposis.
        Best Pract Res Clin Gastroenterol. 2010; 24: 35-42
        • Ruskone-Fourmestraux A.
        • Delmer A.
        • Lavergne A.
        • Molina T.
        • Brousse N.
        • Audouin J.
        • et al.
        Multiple lymphomatous polyposis of the gastrointestinal tract: prospective clinicopathologic study of 31 cases. Groupe D'etude des Lymphomes Digestifs.
        Gastroenterology. 1997; 112: 7-16
        • Kluin-Nelemans H.C.
        • Doorduijn J.K.
        Treatment of elderly patients with mantle cell lymphoma.
        Semin Hematol. 2011; 48: 208-213
        • Damaj G.
        • Verkarre V.
        • Delmer A.
        • Solal-Celigny P.
        • Yakoub-Agha I.
        • Cellier C.
        • et al.
        Primary follicular lymphoma of the gastrointestinal tract: a study of 25 cases and a literature review.
        Ann Oncol. 2003; 14: 623-629
        • Huang W.T.
        • Hsu Y.H.
        • Yang S.F.
        • Chuang S.S.
        Primary gastrointestinal follicular lymphoma: a clinicopathologic study of 13 cases from Taiwan.
        J Clin Gastroenterol. 2008; 42: 997-1002
        • Kodama T.
        • Ohshima K.
        • Nomura K.
        • Taniwaki M.
        • Nakamura N.
        • Nakamura S.
        • et al.
        Lymphomatous polyposis of the gastrointestinal tract, including mantle cell lymphoma, follicular lymphoma and mucosa-associated lymphoid tissue lymphoma.
        Histopathology. 2005; 47: 467-478
        • Brice S.L.
        Clinical evaluation of the use of low-intensity ultrasound in the treatment of recurrent aphthous stomatitis.
        Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1997; 83: 14-20
        • Patte C.
        • Ribrag V.
        • Brugieres L.
        Non Hodgkin’s lymphoma in adolescents.
        Bull Cancer. 2007; 94: 339-348
        • Rambaud J.C.
        • Brouet J.C.
        • Seligmann M.
        Alpha chain disease and related lymphoproliferative disorders.
        in: Ogra Handbook of mucosal immunol. Academic Press, New York1994: 425-433
        • Lecuit M.
        • Abachin E.
        • Martin A.
        • Poyart C.
        • Pochart P.
        • Suarez F.
        • et al.
        Immunoproliferative small intestinal disease associated with Campylobacter jejuni.
        N Engl J Med. 2004; 350: 239-248
        • Malamut G.
        • Meresse B.
        • Kaltenbach S.
        • Derrieux C.
        • Verkarre V.
        • Macintyre E.
        • et al.
        Small intestinal CD4+ T-cell lymphoma is a heterogenous entity with common pathology features.
        Clin Gastroenterol Hepatol. 2014; 12 (e1): 599-608
        • Carbonnel F.
        • d'Almagne H.
        • Lavergne A.
        • Matuchansky C.
        • Brouet J.C.
        • Sigaux F.
        • et al.
        The clinicopathological features of extensive small intestinal CD4 T cell infiltration.
        Gut. 1999; 45: 662-667
        • Cellier C.
        • Delabesse E.
        • Helmer C.
        • Patey N.
        • Matuchansky C.
        • Jabri B.
        • et al.
        Refractory sprue, coeliac disease, and enteropathy-associated T-cell lymphoma: French Coeliac Disease Study Group.
        Lancet. 2000; 356: 203-208
        • Malamut G.
        • Cellier C.
        Refractory celiac disease: epidemiology and clinical manifestations.
        Dig Dis. 2015; 33: 221-226
        • Malamut G.
        • Verkarre V.
        • Callens C.
        • Colussi O.
        • Rahmi G.
        • MacIntyre E.
        • et al.
        Enteropathy-associated T-cell lymphoma complicating an autoimmune enteropathy.
        Gastroenterology. 2012; 142 (e3; quiz e13–4): 726-729
        • Askling J.
        • Linet M.
        • Gridley G.
        • Halstensen T.S.
        • Ekstrom K.
        • Ekbom A.
        Cancer incidence in a population-based cohort of individuals hospitalized with celiac disease or dermatitis herpetiformis.
        Gastroenterology. 2002; 123: 1428-1435
        • Malamut G.
        • Chandesris O.
        • Verkarre V.
        • Meresse B.
        • Callens C.
        • Macintyre E.
        • et al.
        Enteropathy associated T cell lymphoma in celiac disease: a large retrospective study.
        Dig Liver Dis. 2013; 45: 377-384
        • Wundisch T.
        • Thiede C.
        • Morgner A.
        • Dempfle A.
        • Gunther A.
        • Liu H.
        • et al.
        Long-term follow-up of gastric MALT lymphoma after Helicobacter pylori eradication.
        J Clin Oncol. 2005; 23: 8018-8024
        • Copie-Bergman C.
        • Locher C.
        • Levy M.
        • Chaumette M.T.
        • Haioun C.
        • Delfau-Larue M.H.
        • et al.
        Metachronous gastric MALT lymphoma and early gastric cancer: is residual lymphoma a risk factor for the development of gastric carcinoma?.
        Ann Oncol. 2005; 16: 1232-1236
        • Capelle L.G.
        • de Vries A.C.
        • Looman C.W.
        • Casparie M.K.
        • Boot H.
        • Meijer G.A.
        • et al.
        Gastric MALT lymphoma: epidemiology and high adenocarcinoma risk in a nation-wide study.
        Eur J Cancer. 2008; 44: 2470-2476