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Primary esophageal non-Hodgkin’s lymphoma: demographics, clinical characteristics, histopathologic types, and survival in 179 patients from the SEER program and systematic review of the literature

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Abstract

Background

The most frequent site for the extranodal appearance of primary non-Hodgkin’s lymphomas (NHL) is the gastrointestinal (G.I.) tract. However, primary esophageal lymphoma is extremely rare. The purpose of the present study was to describe and analyze the demographics, clinical characteristics, histopathologic types, and long-term survival of patients with primary esophageal NHL registered in the surveillance, epidemiology, and end results (SEER) database.

Methods

Retrospective cohort study. Individuals with primary esophageal lymphoma (PEL) were identified using the international classification of disease for oncology, third edition histology codes. Patients were excluded if there was no microscopic confirmation of the neoplasm or if the diagnosis was made by autopsy or death certificate. Data on demographics, clinical characteristics, histopathology and survival were analyzed using the Kaplan–Meier method, life table, and cox proportional hazard models.

Results

179 patients were included (68% males, median age 66 years [IQR 46–79]). The overall survival at 1, 5 and 10 years was 65% (95% CI 57.9–72.3%), 49% (95% CI 42.1–57.3%), and 31% (95% CI 24.5–38.6%), respectively. On univariate analyses, individuals with extranodal marginal zone lymphoma (MZL) had a significantly higher overall survival when compared to patients with diffuse large B cell lymphoma (HR 0.29; 95% CI 0.11–0.73. p = 0.008). Furthermore, patients whose cancer was diagnosed after 1997 showed an improved overall survival (HR 0.40; 95% CI 0.26–0.61. p < 0.001) when compared to those diagnosed before 1997.

Conclusions

In this large population-based series, diagnosis after 1997 (year of rituximab approval by the FDA) and MZL subtype were associated with improved survival outcomes in patients with PEL.

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References

  1. Ghai S, Pattison J, Ghai S, O’Malley ME, Khalili K, Stephens M. Primary gastrointestinal lymphoma: spectrum of imaging findings with pathologic correlation. Radiographics. 2007;27(5):1371–88.

    Article  PubMed  Google Scholar 

  2. Malik AO, Baig Z, Ahmed A, Qureshi N, Malik FN. Extremely rare case of primary esophageal mucous associated lymphoid tissue lymphoma. World J Gastrointest Endosc. 2013;5(9):446–9.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Berman MD, Falchuk KR, Trey C, Gramm HF. Primary histiocytic lymphoma of the esophagus. Dig Dis Sci. 1979;24(11):883–6.

    Article  CAS  PubMed  Google Scholar 

  4. Inayat F, Munir A, Wahab A, Younus F, Zafar F, Ullah W. Primary esophageal diffuse large B-Cell lymphoma: a comparative review of 15 cases. J Investig Med High Impact Case Rep [Internet]. 25 de diciembre de 2018 [citado 25 de abril de 2020]; 6. Disponible en: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6305950/

  5. Bernal A, del Junco GW. Endoscopic and pathologic features of esophageal lymphoma: a report of four cases in patients with acquired immune deficiency syndrome. Gastrointest Endosc. 1986;32(2):96–9.

    Article  CAS  PubMed  Google Scholar 

  6. Pasqualucci L, Dalla-Favera R. Genetics of diffuse large B-cell lymphoma. Blood. 2018;131(21):2307–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Weeratunge CN, Bolivar HH, Anstead GM, Lu DH. Primary esophageal lymphoma: a diagnostic challenge in acquired immunodeficiency syndrome–two case reports and review. South Med J. 2004;97(4):383–7.

    Article  PubMed  Google Scholar 

  8. Gupta NM, Goenka MK, Jindal A, Behera A, Vaiphei K. Primary lymphoma of the esophagus. J Clin Gastroenterol. 1996;23(3):203–6.

    Article  CAS  PubMed  Google Scholar 

  9. Muka T, Glisic M, Milic J, Verhoog S, Bohlius J, Bramer W, et al. A 24-step guide on how to design, conduct, and successfully publish a systematic review and meta-analysis in medical research. Eur J Epidemiol. 2020;35(1):49–60.

    Article  PubMed  Google Scholar 

  10. Moher D, Liberati A, Tetzlaff J, Altman DG, Group TP. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLOS Med. 2009;6(7):e1000097.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kobayashi S, Iwamuro M, Nishida K, Tanaka T, Kawano S, Kawahara Y, et al. Primary localized esophageal mucosa-associated lymphoid tissue lymphoma treated by endoscopic submucosal dissection. Intern Med Tokyo Jpn. 2018;57(16):2347–52.

    Article  Google Scholar 

  12. Yaakup H, Sagap I, Fadilah SA. Primary oesophageal Ki (CD30)-positive ALK+ anaplastic large cell lymphoma of T-cell phenotype. Singapore Med J. 2008;49(10):e289-292.

    CAS  PubMed  Google Scholar 

  13. Shim CS, Lee JS, Kim JO, Cho JY, Lee MS, Jin SY, et al. A case of primary esophageal B-cell lymphoma of MALT type, presenting as a submucosal tumor. J Korean Med Sci. 2003;18(1):120–4.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Ximenes M, Piauilino MA, Oliveira HA, Vaz Neto JP. Primary esophageal lymphoma. Rev Col Bras Cir. 2012;39(3):243–6.

    Article  PubMed  Google Scholar 

  15. Baek DH, Kim GH, Song GA, Ryu KD, Cho EJ, Shin MJ, et al. Primary esophageal mucosa-associated lymphoid tissue lymphoma treated with endoscopic resection. Gastrointest Endosc. 2012;75(6):1282–3.

    Article  PubMed  Google Scholar 

  16. Basseri RJ, Cole J, Jamil LH. Primary esophageal B-cell lymphoma. Clin Gastroenterol Hepatol. 2011;9(3):e23-24.

    Article  PubMed  Google Scholar 

  17. Chadha KS, Hernandez-Ilizaliturri FJ, Javle M. Primary esophageal lymphoma: case series and review of the literature. Dig Dis Sci. 2006;51(1):77–83.

    Article  PubMed  Google Scholar 

  18. Golioto M, Mcgrath K. Primary lymphoma of the esophagus in a chronically immunosuppressed patient with hepatitis C infection: case report and review of the literature. Am J Med Sci. 2001;321(3):203–5.

    Article  CAS  PubMed  Google Scholar 

  19. Hosaka S, Nakamura N, Akamatsu T, Fujisawa T, Ogiwara Y, Kiyosawa K, et al. A case of primary low grade mucosa associated lymphoid tissue (MALT) lymphoma of the oesophagus. Gut. 2002;51(2):281–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gaskin CM, Low VH, Ho LM. Isolated primary non-hodgkin’s lymphoma of the esophagus. Am J Roentgenol. 2001;176(2):551–2.

    Article  CAS  Google Scholar 

  21. Kim JH, Lee JH, Lee J, Oh S-O, Chang DK, Rhee P-L, et al. Primary NK-/T-cell lymphoma of the gastrointestinal tract: clinical characteristics and endoscopic findings. Endoscopy. 2007;39(2):156–60.

    Article  CAS  PubMed  Google Scholar 

  22. Kitamoto Y, Hasegawa M, Ishikawa H, Saito J, Yamakawa M, Kojima M, et al. Mucosa-associated lymphoid tissue lymphoma of the esophagus: a case report. J Clin Gastroenterol. 2003;36(5):414–6.

    Article  PubMed  Google Scholar 

  23. Byun SJ, Kang HW, Cha JK, Ryoo SR, Lee JH, Kim DY, et al. Primary mucosa-associated lymphoid tissue lymphoma metachronously involving esophagus and stomach. Korean J Gastroenterol Taehan Sohwagi Hakhoe Chi. 2016;67(5):257–61.

    Article  PubMed  Google Scholar 

  24. Kudo K, Ota M, Narumiya K, Shirai Y, Ohki T, Yamamoto M. Primary esophageal mucosa-associated lymphoid tissue lymphoma treated by endoscopic submucosal dissection. Dig Endosc. 2014;26(3):478–81.

    Article  PubMed  Google Scholar 

  25. Lee DS, Ahn YC, Eom DW, Lee SJ. Primary esophageal mucosa-associated lymphoid tissue lymphoma diagnosed by using stacked forceps biopsy. Dis Esophagus. 2016;29(7):887–90.

    Article  CAS  PubMed  Google Scholar 

  26. Ma Q, Zhang C, Fang S, Zhong P, Zhu X, Lin L, et al. Primary esophageal mucosa-associated lymphoid tissue lymphoma: a case report and review of literature. Medicine (Baltimore). 2017;96(13):e6478.

    Article  Google Scholar 

  27. Madabhavi I, Patel A, Revannasiddaiah S, Choudhary M, Anand A, Das P, et al. Primary esophageal Burkitt’s lymphoma: a rare case report and review of literature. Gastroenterol Hepatol Bed Bench. 2014;7(4):230–7.

    PubMed  PubMed Central  Google Scholar 

  28. Bardisi ES, Alghanmi N, Merdad AA. Primary mucosa-associated lymphoid tissue lymphoma of the esophagus masquerading as a benign tumor. Ann Med Surg. 2014;3(2):39–42.

    Article  Google Scholar 

  29. Moriya K, Tamura H, Nakamura K, Hosone M, Inokuchi K. A primary esophageal MALT lymphoma patient with Helicobacter pylori infection achieved complete remission after H. Pylori eradication without anti-lymphoma treatment. Leuk Res Rep. 2017;7:2–5.

    PubMed  Google Scholar 

  30. Ye X-T, Luo Y-L, Xia S-C, Sun Q-F, Ding J-G, Zhou Y, et al. Clinical efficacy of lopinavir/ritonavir in the treatment of Coronavirus disease 2019. Eur Rev Med Pharmacol Sci. 2020;24(6):3390–6.

    PubMed  Google Scholar 

  31. Musquer N, Zidane-Marinnes M, Dib M. Primary mucosa-associated lymphoid tissue lymphoma of the entire esophagus. Gastrointest Endosc. 2017;86(3):560–1.

    Article  PubMed  Google Scholar 

  32. Neshatian L, Katzka DA. A hidden cause of dysphagia. Prim Esophageal Lymphoma Gastroenterol. 2015;149(3):549–50.

    Google Scholar 

  33. Liang P, Ren X-C, Gao J-B. Radiological and clinical features of primary NK/T-cell lymphoma involving the whole length of the esophagus: a case report. Oncol Lett. 2017;14(2):2147–52.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Park S, Jeen YT, Kwon YD, Keum B, Seo YS, Kim YS, et al. Successfully cured primary esophageal lymphoma in a patient with acquired immune deficiency syndrome (AIDS). Endoscopy. 2009;41(Suppl 2):E148-149.

    Article  PubMed  Google Scholar 

  35. Ruiz-Carazo E, Lacasa Pérez N, Salmerón Ruiz A, Molina Nuevo JD. MALT-type primary lymphoma of the esophagus: imaging findings. Radiologia. 2008;50(4):327–30.

    Article  CAS  PubMed  Google Scholar 

  36. Sabljak P, Stojakov D, Bjelovic M, Mihaljevic B, Velickovic D, Ebrahimi K, et al. Primary esophageal diffuse large B-cell lymphoma: report of a case. Surg Today. 2008;38(7):647–50.

    Article  PubMed  Google Scholar 

  37. Soon M-S, Yen H-H, Soon A, Lin OS. Primary esophageal B-cell lymphoma: evaluation by EUS. Gastrointest Endosc. 2005;61(7):901–3.

    Article  PubMed  Google Scholar 

  38. Wagner PL, Tam W, Lau PY, Port JL, Paul S, Altorki NK, et al. Primary esophageal large T-cell lymphoma mimicking esophageal carcinoma: a case report and literature review. J Thorac Cardiovasc Surg. 2008;135(4):957-8 el.

    Article  PubMed  Google Scholar 

  39. Kalogeropoulos IV, Chalazonitis AN, Tsolaki S, Laspas F, Ptohis N, Neofytou I, et al. A case of primary isolated non-Hodgkin’s lymphoma of the esophagus in an immunocompetent patient. World J Gastroenterol. 2009;15(15):1901–3.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Teerakanok J, Dewitt JP, Juarez E, Thein KZ, Warraich I. Primary esophageal diffuse large B-cell lymphoma presenting with tracheoesophageal fistula: a rare case and review. World J Gastrointest Oncol. 2018;9(10):431–5.

    Article  Google Scholar 

  41. Ghimire P, Wu G-Y, Zhu L. Primary esophageal lymphoma in immunocompetent patients: two case reports and literature review. World J Radiol. 2010;2(8):334–8.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Wu N, Pang L, Chen Z, Wang Y, Ma Q, Chen G, et al. Primary esophageal CD30-positive ALK-positive anaplastic large cell lymphoma: a case report and literature review. J Gastrointest Cancer. 2011;42(1):57–60.

    Article  PubMed  Google Scholar 

  43. Yano S, Usui N, Dobashi N, Yahagi Y, Takahara S, Sugiyama K, et al. A case of primary esophageal mucosa-associated lymphoid tissue lymphoma with a numerical abnormality of 18q21 detected by fluorescence in situ hybridization. Ann Hematol. 2009;88(7):703–4.

    Article  PubMed  Google Scholar 

  44. Chung J-J, Kim M-J, Kie J-H, Kim KW. Mucosa-associated lymphoid tissue lymphoma of the esophagus coexistent with bronchus-associated lymphoid tissue lymphoma of the lung. Yonsei Med J. 2005;46(4):562–6.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Zhu Q, Xu B, Xu K, Li J, Jin XL. Primary non-Hodgkin’s lymphoma in the esophagus. J Dig Dis. 2008;9(4):241–4.

    Article  PubMed  Google Scholar 

  46. Yu L, Chen K, Xu Y, Wang S, Liu Q, Ye Q, et al. The value of EUS in combination with cytological, flow cytometry, and gene rearrangement in the diagnosis of gastrointestinal lymphoma. Hematol Oncol. 2017;35(3):303–9.

    Article  CAS  PubMed  Google Scholar 

  47. Macqueen IT, Shannon EM, Dawes AJ, Ostrzega N, Russell MM, Maggard-Gibbons M. The Role of surgery in the clinical management of primary gastrointestinal non-Hodgkin’s lymphoma. Am Surg. 2015;81(10):988–94.

    Article  PubMed  Google Scholar 

  48. Aoki T, Yamada A, Takahashi M, Niikura R, Toyama K, Ushiku T, et al. Development and internal validation of a risk scoring system for gastrointestinal events requiring surgery in gastrointestinal lymphoma patients. J Gastroenterol Hepatol. 2019;34(4):693–9.

    Article  PubMed  Google Scholar 

  49. Huh J. Epidemiologic overview of malignant lymphoma. Korean J Hematol. 2012;47(2):92–104.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Howlader N, Morton LM, Feuer EJ, Besson C, Engels EA. Contributions of subtypes of non-Hodgkin lymphoma to mortality trends. Cancer Epidemiol Biomark. 2016;25(1):174–9.

    Article  Google Scholar 

  51. Cheson BD, Fisher RI, Barrington SF, Cavalli F, Schwartz LH, 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(27):3059–68.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Makita S, Maruyama D, Maeshima AM, Taniguchi H, Yuda S, Toyoda K, et al. A comparison of clinical staging using the Lugano versus Ann Arbor classifications in Japanese patients with Hodgkin lymphoma. Asia Pac J Clin Oncol. 2020;16(3):108–14.

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank the Universidad Industrial de Santander for its continuous support in formative research.

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Correspondence to Andrea Carolina Quiroga-Centeno.

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Ethical Statement

As our study was based on the SEER database, ethical approval was not required.

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Dr. Quiroga-Centeno, Dr. Bautista-Parada, Dr. Tapias and Dr. Gómez-Ochoa have no conflicts of interest or financial ties to disclose.

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Quiroga-Centeno, A.C., Bautista-Parada, I.R., Tapias, L.F. et al. Primary esophageal non-Hodgkin’s lymphoma: demographics, clinical characteristics, histopathologic types, and survival in 179 patients from the SEER program and systematic review of the literature. Esophagus 18, 734–742 (2021). https://doi.org/10.1007/s10388-021-00842-0

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