Helicobacter pylori and its role in the pathogenesis of follicular gastritis: an overview

Yeison Carlosama-Rosero; Gonzalo Latorre; Arnoldo Riquelme; José Darío Portillo-Miño

doi:10.47892/rgp.2024.444.1791

Authors

Yeison Carlosama-Rosero Interdisciplinary Health-Disease Research Group (GIISE), Universidad Cooperativa de Colombia. Campus Pasto. Nariño. Colombia; Department of Pathology, Universidad Cooperativa de Colombia, Campus Pasto. Nariño. Colombia; Health Sciences Doctoral Program, Universidad Autónoma de Manizales, Manizales. Colombia. https://orcid.org/0000-0002-6529-9758
Gonzalo Latorre Department of Gastroenterology, Faculty of Medicine, Pontificia Universidad Catolica de Chile, Santiago. Chile. https://orcid.org/0009-0000-2311-8747
Arnoldo Riquelme Department of Gastroenterology, Faculty of Medicine, Pontificia Universidad Catolica de Chile, Santiago. Chile; Centro para la Prevencion y Control del Cancer (CECAN), Santiago. Chile. https://orcid.org/0000-0002-8259-8960
José Darío Portillo-Miño Grupo de Investigación en Infecciosas y Cancer (GINFYCA), Fundacion Hospital San Pedro. Pasto. Nariño. Colombia; Centro de Investigaciones Clínicas, Fundación Hospital San Pedro. Pasto. Nariño. Colombia. https://orcid.org/0000-0003-4858-9400

DOI:

https://doi.org/10.47892/rgp.2024.444.1791

Keywords:

Helicobacter pylori, Pseudolymphoma, Hyperplasia, Lymphoma, Follicular

Abstract

The role of Helicobacter pylori in the pathogenesis of peptic ulcers and gastric adenocarcinoma is widely known; however, it is not entirely understood how bacterial infection is closely related to the genesis of follicular gastritis and some types of gastric lymphoma. Diagnosing and pathogenic mechanisms follicular gastritis remain challenging. Therefore, this article aims to examine the role of H. pylori in the development of follicular gastritis. In addition, it emphasizes the clinical and histopathological fundamentals. A broader overview of follicular gastritis is presented, and implementing preventive strategies, such as H. pylori eradication remains the standard treatment.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Malfertheiner P, Camargo MC, El-Omar E, Liou JM, Peek R, Schulz C, et al. Helicobacter pylori infection. Nat Rev Dis Primers. 2023;9(1):19. doi: 10.1038/s41572-023-00431-8.

Malfertheiner P, Link A, Selgrad M. Helicobacter pylori: perspectives and time trends. Nat Rev Gastroenterol Hepatol. 2014;11:628-638. doi: 10.1038/nrgastro.2014.99.

Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017;153:420-429.

Tang Y, Tang G, Pan L, Zhu H, Zhou S, Wei Z. Clinical factors associated with initial Helicobacter pylori eradication therapy: a retrospective study in China. Scientific Reports. 2020;10:15403. doi: 10.1038/s41598-020-72400-0.

Eusebi LH, Zagari RM, Bazzoli F. Epidemiology of Helicobacter pylori infection. Helicobacter. 2014;19(Suppl 1):1-5.

Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015;64:1353-1367.

Yamaoka, Y. How to eliminate gastric cancer-related death worldwide? Nat Rev Clin Oncol. 2018;15:407-408.

Tshibangu-Kabamba E, Yamaoka Y. Helicobacter pylori infection and antibiotic resistance — from biology to clinical implications. Nat Rev Gastroenterol Hepatol. 2021;18:613-629. doi: 10.1038/s41575-021-00449-x.

Humans IWGotEoCRt. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Red Meat and Processed Meat. Lyon (FR): International Agency for Research on Cancer; 2018.

IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994. Schistosomes, liver flukes and Helicobacter pylori. IARC Monogr Eval Carcinog Risks Hum. 1994;61:1-241.

World Health Organization. ICD-11 Revision [Internet]. Ginebra: WHO; 2019. Disponible en: http://www.who.int/classifications/icd/revision/en/

Malfertheiner P, Megraud F, Rokkas T, Gisbert JP, Liou JM, Schulz C, et al. Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report. Gut. 2022;gutjnl-2022-327745.

Mejia CR, Vera CA, Huiza-Espinoza L. Association between follicular gastritis and Helicobacter pylori in children seen at a public hospital in Peru. Rev Gastroenterol Mex. 2016;81(2):80-5.

Ma Z-Q TT, Nihei Z, Sugihara K, Nakamura K. Follicular gastritis associated with Helicobacter pylori. J Med Dent Sci. 2001;1: 39-47.

Miyamoto M, Haruma K, Hiyama T, Kamada T, Masuda H, Shimamoto F, et al. High incidence of B-cell monoclonality in follicular gastritis: a possible association between follicular gastritis and MALT lymphoma. Virchows Arch. 2002;440(4):376-80.

Sagaert X, Van Cutsem E, De Hertogh G, Geboes K, Tousseyn T. Gastric MALT lymphoma: a model of chronic inflammation induced tumor development. Nat Rev Gastroenterol Hepatol. 2010;7(6):336-346. doi: 10.1038/nrgastro.2010.58

Bujanover Y, Konikoff F, Baratz M. Nodular gastritis and Helicobacter pylori. J Pediatr Gastroenterol Nutr. 1990;11:41-44.

Bahú Mda G, da Silveira TR, Maguilnick I, Ulbrich-Kulczynski J. Endoscopic nodular gastritis: an endoscopic indicator of high-grade bacterial colonization and severe gastritis in children with Helicobacter pylori. J Pediatr Gastroenterol Nutr. 2003;36(2):217-222.

Carlson SJ, Yokoo H, Vanagunas A. Progression of gastritis to monoclonal B-cell lymphoma with resolution and recurrence following eradication of Helicobacter pylori. JAMA. 1996;275(12):937-9.

Asano N, Iijima K, Koike T, Imatani A, Shimosegawa T. Helicobacter pylori-negative gastric mucosa-associated lymphoid tissue lymphomas: A review. World J Gastroenterol. 2015;21(26):8014-20.

De Giacomo FR, Villani L, Lisato L, Diegoli N, Donnadini A, et al. Helicobacter pylori infection and chronic gastritis: clinical, serological and histologic correlations in childrens treated with amoxicillin and colloidal bismuto subcitrate. J Pediatr Gastroenterol Nutr. 1991;11: 310-316.

Raymond J; Bergeret M BP, Mensah K, Dupont C. A 2-year study of Helicobacter pylori in children. J Clini Microbiol. 1994;32:461-3.

Romero-Flores JL, Fernandez-Rivero JA, Marroquín-Fabian E, Téllez-Ávila FI, Sánchez-Jiménez BA, Juárez-Hernández E, et al. Diagnostic accuracy of nodular gastritis for H. pylori infection. Ther Clin Risk Manag. 2017;13:9-14.

Kalali B, Formichella L, Gerhard M. Diagnosis of Helicobacter pylori: Changes towards the Future. Diseases. 2015;3(3):122-35.

Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017;112(2):212-39.

Lo WY LJ, Chan YK, Lai LS, Yeung YW, Lo ST, Tsui WM, Ng CS. Inestability of clonality in gastric lymphoid infiltrates: a study with emphasis on serial biopsies. Am J Surg Pathol. 2005;29:1582-92.

Hong K, Tae Wong N, Seuong -Yon B. Nodular Gastritis A Pathologic Findings In Children And Young Adults With Helicobacter Pylori Infection. Yonsei Med J. 2007;48(2):240-246.

Wyatt JI, Rathbone BJ. Immune response of the gastric mucosa to Campylobacter pylori. Scand J Gastroenterol. 1988;142:44-9.

Eidt S, Stolte M. Prevalence of lymphoid follicles and aggregates in Helicobacter pylori gastritis in antral and body mucosa. J Clin Pathol. 1993;46:832-5.

Genta RM, Hammer HW. The significance of lymphoid follicles in the interpretation of gastric biopsy specimens. Arch Pathol Lab Med. 1994;118:740-3.

Chen XY, Liu WZ, Shi Y, Zhang DZ, Xiao SD, Tytgat GN. Helicobacter pylori associated gastric diseases and lymphoid tissue hyperplasia in gastric antral mucosa. J Clin Pathol. 2002;55(2):133-7. doi: 10.1136/jcp.55.2.133

Chen MJ, Wang TE, Chang WH, Liao TC, Lin CC, Shih SC. Nodular gastritis: an endoscopic indicator of Helicobacter Pylori infection. Dig Dis Sci. 2007;52(10):2662-6.

Shimatani T, Inoue M, Iwamoto K, Hyogo H, Yokozaki M, Saeki T, et al. Gastric acidity in patients with follicular gastritis is significantly reduced, but can be normalized after eradication for Helicobacter pylori. Helicobacter. 2005;10(3):256-65.

Choi HJ, Lee SY, Lee JH, Seol DC, Kim SY, Choi HJ, et al. Two Atypical Cases of Nodular Gastritis: A Poorly Differentiated Gastric Adenocarcinoma and a Pseudo-Low Grade Gastric MALT Lymphoma. Gastroenterology Res. 2010;3(1):41-5.

Martínez-Marín JD, Henao-Riveros SC. Hiperplasia linfoide folicular gástrica e infección por Helicobacter pylori en adultos colombianos. Rev Col Gastroenterol. 2009;24(2): 148-156.

Melo-Peñaloza MA, Mendoza-Rodriguez A. Frequency of morphological changes in gastric biopsies associated with Helicobacter pylori infection. Acta Med Colomb. 2021;46(3):25-31. doi: 10.36104/amc.2021.1987.

Zaitoun AM. The prevalence of lymphoid follicles in Helicobacter pylori associated gastritis in patients with ulcers and non-ulcer dyspepsia. J Clin Pathol. 1995;48:325-9.

Zerbib F, Vialette G, Cayla R, Rudelli A, Sauvet P, Bechade D, Seurat PL, Lamouliatte H. Follicular gastritis in adults. Relations with Helicobacter pylori, histological and endoscopic aspects. Gastroenterol Clin Biol. 1993;17(8-9):529-34.

Bedoya A, Arcos M, Sansón F, del Castillo G. Helicobacter pylori y cambios histológicos de la mucosa gástrica en menores de diez años. Pasto, 1999. Rev Colomb Gastroenterol. 2002;17: 36-42.

Martínez JD, Henao SC, Granados C. La Gastritis crónica atrófica y la edad. Rev Colomb Gastroenterol. 2007;22: 17-22.

Ladas SD, Rokkas T, Georgopoulos S, Kitsanta P, Liatsos C, Eustathiadou P, et al. Predictive factors and prevalence of follicular gastritis in adults with peptic ulcer and nonulcer dyspepsia. Dig Dis Sci. 1999;44(6):1156-60.

Rafeey M, Jafari Rouhi AH, Gassemi BA, Rouhi AJ. Relationship between endoscopic nodular gastritis and Helicobacter pylori infection in children. Indian J Gastroenterol. 2004;23(4):138-139.

Mansilla-Vivar R, Serrano CA, Palma C, Vera M, Hernandez C, Pizarro M, et al. High Helicobacter pylori Bacterial Load and Low Cytokine Expression Levels Are Associated with Nodular Gastropathy. Dig Dis Sci. 2020;65(2):565-75.

Marcelis L, Tousseyn T, Sagaert X. MALT Lymphoma as a Model of Chronic Inflammation-Induced Gastric Tumor Development. Curr Top Microbiol Immunol. 2019;421:77-106. doi: 10.1007/978-3-030-15138-6_4

Isaacson PG. Update on MALT lymphomas. Best Pract Res Clin Haematol [Internet]. 2005;18(1):57-68. doi: 10.1016/j.beha.2004.08.003.

Bardhan PK. Epidemiological features of Helicobacter pylori infection in developing countries. Clin Infect Dis. 1997;25(5):973-978. doi: 10.1086/516067.

Asenjo LM, Gisbert JP. [Prevalence of Helicobacter pylori infection in gastric MALT lymphoma: a systematic review]. Rev Esp Enferm Dig. 2007;99(7):398-404.

Garhart C, Czinn S. Helicobacter pylori infection: Review of pathogenesis and immunity. Int Semin Paediatr Gastroenterol Nutr. 2004;12:3-7.

Bergman MP, D’Elios MM. Cytotoxic T cells in H. pylori-related gastric autoimmunity and gastric lymphoma. J Biomed Biotechnol. 2010;2010:104918. doi: 10.1155/2010/104918.

Yamaoka Y. Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol. 2010;7:629-641. doi: 10.1038/nrgastro.2010.154.

Malfertheiner P, Megraud F, O’Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut. 2017;71:1724-1762. doi: 10.1136/gutjnl-2016-312288.

Araújo GRL, Marques HS, Santos MLC, da Silva FAF, da Brito BB, Correa Santos GL, et al. Helicobacter pylori infection: How does age influence the inflammatory pattern? World J Gastroenterol. 2022;28(4):402-11.

Onal IK, Gokcan H, Benzer E, Bilir G, Oztas E. What is the impact of Helicobacter pylori density on the success of eradication therapy: a clinico-histopathological study. Clin Res Hepatol Gastroenterol. 2013;37(6):642-6.

Elitsur Y, Lawrence Z, Triest WE. Distribution of Helicobacter pylori organisms in the stomachs of children with H. pylori infection. Hum Pathol. 2002;33(11):1133-5.

Camorlinga-Ponce M, Aviles-Jimenez F, Cabrera L, Hernández-Pando R, Muñoz O, Soza J, et al. Intensity of inflammation, density of colonization and interleukin-8 response in the gastric mucosa of children infected with Helicobacter pylori. Helicobacter. 2003;8(5):554-60.

Xu XQ, Wang ZH, Liao JX, Chen XY, Liu WZ, Xiao SD, et al. Predictive value of neutrophil infiltration as a marker of Helicobacter pylori infection. World J Gastroenterol. 2012;18(36):5101-5.

Hatakeyama M, Higashi H. Helicobacter pylori CagA: a new paradigm for bacterial carcinogenesis. Cancer Sci. 2005;96(12):835-843. doi: 10.1111/j.1349-7006.2005.00130.x.

Li SP, Chen XJ, Sun AH, Zhao JF, Yan J. CagA(+) H. pylori induces Akt1 phosphorylation and inhibits transcription of p21(WAF1/CIP1) and p27(KIP1) via PI3K/Akt1 pathway. Biomed Environ Sci. 2010;23(4):273-278. doi: 10.1016/S0895-3988(10)60063-3.

Keikha M, Sahebkar A, Yamaoka Y, Karbalaei M. Helicobacter pylori cagA status and gastric mucosa-associated lymphoid tissue lymphoma: a systematic review and meta-analysis. J Health Popul Nutr. 2022;41:2.

Yong X, Tang B, Li BS, Xie R, Hu CJ, Luo G, et al. Helicobacter pylori virulence factor CagA promotes tumorigenesis of gastric cancer via multiple signaling pathways. Cell Commun Signal. 2015;13:30.

Machado AMD, Figueiredo C, Touati E, Máximo V, Sousa S, Michel V, et al. Helicobacter pylori infection induces genetic instability of nuclear and mitochondrial DNA in gastric cells. Clin Cancer Res. 2009;15(9):2995-3002.

Fox JG, Wang TC. Inflammation, atrophy, and gastric cancer. J Clin Invest. 2007;117(1):60-9.

Jaffe ES, Harris NL, Stein H, Isaacson PG. Classification of lymphoid neoplasms: the microscope as a tool for disease discovery. Blood. 2008;112(12):4384-99.

Lim KH, Yang Y, Staudt LM. Pathogenetic importance and therapeutic implications of NF-κB in lymphoid malignancies. Immunol Rev. 2012;246(1):359-78.

Lin WC, Tsai HF, Kuo SH, Wu MS, Lin CW, Hsu PI, et al. Translocation of Helicobacter pylori CagA into Human B lymphocytes, the origin of mucosa-associated lymphoid tissue lymphoma. Cancer Res. 2010;70(14):5740-8.

Umehara S, Higashi H, Ohnishi N, Asaka M, Hatakeyama M. Effects of Helicobacter pylori CagA protein on the growth and survival of B lymphocytes, the origin of MALT lymphoma. Oncogene. 2003;22(51):8337-42.

Krisch LM, Posselt G, Hammerl P, Wessler S. CagA Phosphorylation in Helicobacter pylori-Infected B Cells Is Mediated by the Nonreceptor Tyrosine Kinases of the Src and Abl Families. Infect Immun. 2016;84(9):2671-80.

Bagheri V, Memar B, Momtazi AA, Sahebkar A, Gholamin M, Abbaszadegan MR. Cytokine networks and their association with Helicobacter pylori infection in gastric carcinoma. J Cell Physiol. 2018;233(4):2791-803.

Touati E, Michel V, Thiberge JM, Wuscher N, Huerre M, Labigne A. Chronic Helicobacter pylori infections induce gastric mutations in mice. Gastroenterology. 2003;124(5):1408-19.

Traci L, Testerman JM. Beyond the stomach: An updated view of Helicobacter pylori pathogenesis, diagnosis, and treatment. World J Gastroenterol. 2014;28(36):12781-808.

Backert S, Clyne M. Pathogenesis of Helicobacter pylori infection. Helicobacter. 2011;16 Suppl 1:19-25.

Bagheri N, Salimzadeh L, Shirzad H. The role of T helper 1-cell response in Helicobacter pylori-infection. Microb Pathog. 2018;123:1-8.

Imlay JA. Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem. 2008;77:755-76.

Spiro S, D’Autréaux B. Non-heme iron sensors of reactive oxygen and nitrogen species. Antioxid Redox Signal. 2012;17(9):1264-76.

Vázquez-Torres A. Redox active thiol sensors of oxidative and nitrosative stress. Antioxid Redox Signal. 2012;17(9):1201-14.

Iseki K, Tatsuta M, Iishi H, Baba M, Mikuni T, Hirasawa R, et al. Attenuation by methionine of monochloramine-enhanced gastric carcinogenesis induced by N-methyl-N’-nitro-N-nitrosoguanidine in Wistar rats. Int J Cancer. 1998;76(1):73-6.

Iishi H, Tatsuta M, Baba M, Mikuni T, Yamamoto R, Iseki K, et al. Enhancement by monochloramine of the development of gastric cancers in rats: A possible mechanism ofHelicobacter pylori-associated gastric carcinogenesis. J Gastroenterol. 1997;32:435-441. doi: 10.1007/BF02934080.

Romagnani S, Parronchi P, D’Elios MM, Romagnani P, Annunziato F, Piccinni MP, et al. An update on human Th1 and Th2 cells. Int Arch Allergy Immunol. 1997;113:153-156.

Craig VJ, Cogliatti SB, Arnold I, Gerke C, Balandat JE, Wündisch T, et al. B-cell receptor signaling and CD40 ligand-independent T cell help cooperate in Helicobacter-induced MALT lymphomagenesis. Leukemia. 2010;24(6):1186-96.

García M, Bellosillo B, Sánchez-González B, García-Payarols F, Seoane A, Ferrer AM, et al. Study of regulatory T-cells in patients with gastric malt lymphoma: influence on treatment response and outcome. PLoS One. 2012;7(12):e51681.

Uhl B, Prochazka KT, Fechter K, Pansy K, Greinix HT, Neumeister P, et al. Impact of the microenvironment on the pathogenesis of mucosa-associated lymphoid tissue lymphomas. World

J Gastrointest Oncol. 2022;14(1):153-62.

D’Elios MM, Manghetti M, Almerigogna F, Amedei A, Costa F, Burroni D, et al. Different cytokine profile and antigen-specificity repertoire in Helicobacter pylori-specific T cell clones from the antrum of chronic gastritis patients with or without peptic ulcer. Eur J Immunol. 1997;27:1751-1755.

Rosebeck S, Madden L, Jin X, Gu S, Apel IJ, Appert A, et al. Cleavage of NIK by the API2-MALT1 fusion oncoprotein leads to noncanonical NF-kappaB activation. Science. 2011;331(6016):468-72.

Jardin, F. NF-kB Pathway and Hodgkin Lymphoma. Biomedicines. 2022;10:2153. doi: 10.3390/ biomedicines10092153.

Bauer B, Moese S, Bartfeld S, Meyer TF, Selbach M. Analysis of cell type-specifïc responses mediated by the type IV secretion system of Helicobacter pylori. Infect Immun. 2005;73(8):4643-4652.

Nishikori M. Classical and alternative NF-kB activation pathways and their roles in lymphoid malignancies. J Clin Exp Hematopathol. 2005;45:15-24.

Ronchi A, Montella M, Panarese I, Costanzo RMA, Aquino G, De Chiara A, et al. MALT gastric lymphoma: An pathogenetic features. WCRJ. 2016;3(2):e715.

Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y, Noelle RJ. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev. 2009;229(1):152-72. doi: 10.1111/j.1600-065X.2009.00782.x.

Chan JK C, Ng CS, Isaacson PG . Relationship between high grade lymphoma and low-grade B-cell mucosa- associated lymphoid tissue lymphoma (MALToma) of the stomach. Am J Pathol. 1990;136:1153-1164.

Villuendas R, Piris MA , Orradre JL, Moll ejo M, Rodriguez, R, Morente M. Different bcl-2 protein expression in high-grade B-cell lymphomas derived from lymph node or mucosa-associated lymphoid tissue. Am J Pathol. 1991;139:989-993.

Blosse A, Peru S, Levy M, Marteyn B, Floch P, Sifré E, et al. APRIL-producing eosinophils are involved in gastric MALT lymphomagenesis induced by Helicobacter sp infection. Sci Rep. 2020;10(1):14858.

Yoon JH, Choi WS, Kim O, Park WS. The role of gastrokine 1 in gastric cancer. J Gastric Cancer. 2014;14:147-55.

Nardone G, Rippa E, Martin G, Rocco A, Siciliano RA, Fiengo, A, et al. Gastrokine 1 expression in patients with and without Helicobacter pylori infection. Dig Liver Dis. 2007;39:122-9.

Alarcón-Millán, J., Lorenzo-Nazario, S.I., Jiménez-Wences, H. et al. Women with chronic follicular gastritis positive for Helicobacter pylori express lower levels of GKN1. Gastric Cancer. 2020;23:754-759. doi: 10.1007/s10120-020-01049-5.

Cappell M. S., Garcia A. Gastric and duodenal ulcers during pregnancy. Gastroenterol Clin North Am. 1998;27:169-195.

Havard TJ, Sarsfield P, Wotherspoon AC, Steer HW. Increased gastric epithelial cell proliferation in Helicobacter pylori associated follicular gastritis. J Clin Pathol. 1996;49(1):68-71.

Blaser MJ. Helicobacter pylori and gastric diseases. BMJ. 1998;316(7143):1507-10.

Kuo SH, Chen LT, Lin CW, Wu MS, Hsu PN, Tsai HJ, et al. Detection of the Helicobacter pylori CagA protein in gastric mucosa-associated lymphoid tissue lymphoma cells: clinical and biological significance. Blood Cancer J. 2013;3(7):e125.

Carlosama-Rosero YH, Bolaños-Bravo H, Sierra-Tórres CH, Rosero EA. Association of the Helicobacter pylori cagA, vacA, and iceA genotypes with chronic follicular gastritis in a Colombian population at high risk for gastric cancer. Rev Gastroenterol Mex (Engl Ed). 2019;84(2):158-64.

Thorns C, Kuba J, Bernard V, Senft A, Szymczak S, Feller AC, et al. Deregulation of a distinct set of microRNAs is associated with transformation of gastritis into MALT lymphoma. Virchows Arch. 2012;460:371-377. doi: org/10.1007/s00428-012-1215-1.

Belair C, Darfeuille F, Staedel C. Helicobacter pylori and gastric cancer: possible role of microRNAs in this intimate relationship. Clin Microbiol Infect. 2009;15:806-812. doi: 10.1111/j.1469-0691.2009.02960.x

Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, et al. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell. 2007;131:146-159. doi: 10.1016/j.cell.2007.07.021.

Roehle A, Hoefig KP, Repsilber D, Thorns C, Ziepert M, Wesche KO, et al. MicroRNA signatures characterize diffuse large B-cell lymphomas and follicular lymphomas. Br J Haematol. 2008;142:732-744. doi: 10. 1111/j.1365-2141.2008.07237.x.

Craig VJ, Cogliatti SB, Rehrauer H, Wündisch T, Müller A. Epigenetic silencing of microRNA-203 dysregulates ABL1 expression and drives Helicobacter-associated gastric lymphomagenesis. Cancer Res. 2011;71(10):3616-24.

Zipfel PA, Grove M, Blackburn K, Fujimoto M, Tedder TF, Pendergast AM. The c-Abl tyrosine kinase is regulated down-stream of the B cell antigen receptor and interacts with CD19. J Immunol. 2000;165: 6872-9.

Lin K, Glenn MA, Harris RJ, Duckworth AD, Dennett S, Cawley JC, et al. c-Abl expression in chronic lymphocytic leukemia cells: clinical and therapeutic implications. Cancer Res. 2006;66:7801-9.

Greeve J, Philipsen A, Krause K, Klapper W, Heidorn K, Castle BE, et al. Expression of activation-induced cytidine deaminase in human B-cell non-Hodgkin lymphomas. Blood. 2003;101(9):3574-80.

Pasqualucci L, Bhagat G, Jankovic M, Compagno M, Smith P, Muramatsu M, et al. AID is required for germinal center derived lymphomagenesis. Nat Genet. 2008;40(1):108-12.

Zhang J, Shi Y, Zhao M, Hu H, Huang H. Activation-induced cytidine deaminase overexpression in double-hit lymphoma: potential target for novel anticancer therapy. Sci Rep. 2020;10:14164. doi: 10.1038/s41598-020-71058-y.

Shikata H, Yakushijin Y, Matsushita N, Sakai A, Sugita A, Nakamura N, et al. Role of activation-induced cytidine deaminase in the progression of follicular lymphoma. Cancer Sci. 2012;103(3):415-21.

Matsumoto Y, Marusawa H, Kinoshita K, Endo Y, Kou T, Morisawa T, et al. Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nat Med. 2007;13(4):470-476. doi: 10.1038/nm1566.

Marusawa H, Chiba T. Helicobacter pylori-induced activation-induced cytidine deaminase expression and carcinogenesis. Curr Opin Immunol. 2010;22(4): 442-447.

Marusawa H. Aberrant AID expression and human cancer development. Int J Biochem Cell Biol. 2008;40(8):1399-402.

Deutsch AJA, Aigelsreiter A, Staber PB, Beham A, Linkesch W, Guelly C, et al. MALT lymphoma and extranodal diffuse large B-cell lymphoma are targeted by aberrant somatic hypermutation. Blood. 2007;109(8):3500-4.

Halldórsdótt ir AM , Frühwirth M, Deutsch A, Aigelsreiter, A, Beham-Schmid C, Agnarsson BA, et al. Quantifying the role of aberrant somatic hypermutation in transformation of follicular lymphoma. Leuk Res. 2008;32:1015-1021.

Gaidano G, Pasqualucci L, Capello D, Berra E, Deambrogi C, Rossi D, et al. Aberrant somatic hypermutation in multiple subtypes of AIDS-associated non-Hodgkin lymphoma. Blood. 2003;102:1833-1841.

Dijkman R, Tensen CP, Buettn er M, Niedobitek G, Willemze, R, Vermeer MH. Primary cutaneous follicle center lymphoma and primary cutaneous large B-cell lymphoma, leg type, are both targeted by aberrant somatic hypermutation but demonstrate differential expression of AID. Blood. 2006;107:4926-4929.

Bödör C, Bognár A, Reiniger L, Szepesi A, Tóth E, Kopper L, et al. Aberrant somatic hypermutation and expression of activation-induced cytidine deaminase mRNA in mediastinal large B-cell lymphoma. Br J Haematol. 2005;129:373-376.

Choi YJ, Kim N, Paik JH, Kim JM, Lee SH, Park YS, et al. Characteristics of Helicobacter pylori-positive and Helicobacter pylori-negative gastric mucosa-associated lymphoid tissue lymphoma and their influence on clinical outcome. Helicobacter. 2013;18(3):197-205.

Rosenstiel P, Hellmig S, Hampe J, Ott S, Till A, Fischbach W, et al. Influence of polymorphisms in the NOD1/CARD4 and NOD2/CARD15 genes on the clinical outcome of Helicobacter pylori infection. Cell Microbiol. 2006;8(7):1188–1198.

Zullo A, Hassan C, Cristofari F, Andriani A, De Francesco V, Ierardi E, et al. Effects of Helicobacter pylori Eradication on Early Stage Gastric Mucosa-Associated Lymphoid Tissue Lymphoma. Clin Gastroenterol Hepatol. 2010;8(2):105-110.

Kuo SH, Yeh KH, Chen LT, Lin CW, Hsu PN, Hsu C, et al. Helicobacter pylori-related diffuse large B-cell lymphoma of the stomach: A distinct entity with lower aggressiveness and higher chemosensitivity. Blood Cancer J. 2014;4(6):e220. doi: 10.1038/bcj.2014.40.

Mahdavi J, Sondén B, Hurtig M, Olfat FO, Forsberg L, Roche N, et al. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science. 2002;297(5581):573-8.

Yepes S, Torres MM, Saavedra C, Andrade R. Gastric mucosa associated lymphoid tissue lymphomas and Helicobacter pylori infection: A Colombian perspective. World J Gastroenterol. 2012;18(7):685-91.

Wundiisch T, Neubauer A, Stolte M, Ritter M, Thiede C. B-cell monoclonality is associated with lymphoid follicles in gastritis. Am J Surg Pathol. 2003;27:882-887.

Yeh KH, Kuo SH, Chen LT, Mao TL, Doong SL, Wu MS, et al. Nuclear expression of BCL10 or nuclear factor kappa B helps predict Helicobacter pylori-independent status of low-grade gastric mucosa-associated lymphoid tissue lymphomas with or without t(11;18)(q21;q21). Blood. 2005;106(3):1037-41.

Morales-Fuentes GA, Zarate-Osorno A, Quiñónez-Urrego EE, Antonio-Manrique M, Martínez-García CL, Figueroa-Barojas P, et al. p53 expression in the gastric mucosa of patients infected with Helicobacter pylori. Rev Gastroenterol Mex. 2013;78(1):12-20.

Strehl JD, Hoegel J, Hornicek I, Hartmann A, Riener MO. Immunohistochemical expression of IMP3 and p53 in inflammatory lesions and neoplastic lesions of the gastric mucosa. Int J Clin Exp Pathol. 2014;7(5):2091-101.

Ruland J, Duncan GS , Elia A, Del Barco Barrantes I, Nguyen L, Plyte S, et al. Bcl-10 is a positive regulator of antigen receptor-induced activation of NF-kappaB and neural tube closure. Cell. 2001;104: 33-42.

Miyamoto M, Haruma K, Yoshihara M, Hiyama T, Sumioka M, Nishisaka T, et al. Nodular gastritis in adults is caused by Helicobacter pylori infection. Dig Dis Sci. 2003;48(5):968-975.

Iwamuro M, Tanaka T, Nishida K, Kanzaki H, Kawano S, Kawahara Y, et al. Two cases of gastric mucosa-associated lymphoid tissue (MALT) lymphoma masquerading as follicular gastritis. Ecancermedicalscience. 2019;13:933.

ASGE Standards of Practice Committee, Evans JA, Chandrasekhara V, Chathadi KV, Decker GA, Early DS, et al. The role of endoscopy in the management of premalignant and malignant conditions of the stomach. Gastrointest Endosc. 2015;82(1):1-8.

Rosh JR, Kurfist LA, Benkov KJ, Toor AH, Bottone EJ, LeLeiko NS. Helicobacter pylori and gastric lymphonodular hyperplasia in children. Am J Gastroenterol. 1992;87(1):135-9.

Sbeih F, Abdullah A, Sullivan S, Merenkov Z. Antral nodularity, gastric lymphoid hyperplasia, and Helicobacter pylori in adults. J Clin Gastroenterol. 1996;22(3):227-30.

Sipponen P, Price AB. The Sydney System for classification of gastritis 20 years ago. J Gastroenterol Hepatol. 2011;26 Suppl 1:31-4.

Sugimoto M, Ban H, Ichikawa H, Sahara S, Otsuka T, Inatomi O, et al. Efficacy of the Kyoto Classification of Gastritis in Identifying Patients at High Risk for Gastric Cancer. Intern Med. 2017;56(6):579-86.

Kamada T, Haruma K, Inoue K, Shiotani A. [Helicobacter pylori infection and endoscopic gastritis -Kyoto classification of gastritis]. Nihon Shokakibyo Gakkai Zasshi. 2015;112(6):982-93.

Lee KS, Yang HR, and Ko JS, Seo JK, Lee HS. A case of gastric MALT lymphoma presenting as nodular gastritis in a child. Korean J Pediatr Gastroenterol Nutr. 2008;11(2):187-192.

Cheng TI, Tsou MH, and Tsai MP. Early gastric MALT lymphoma. J Chin Med Assoc. 2004;67(3):145-148.

Wotherspoon Ac, Doglioni C, Isaacson PG. Low-grade gastric B-cell lymphoma of mucosa- associated lymphoid tissue(MALT). A multifocal disease. Histopathology. 1992;20:29-34.

Hummel M, Oeschger S, Barth TF, Loddenkemper C, Cogliatti SB, Marx A, et al. Wotherspoon criteria combined with B cell clonality analysis by advanced polymerase chain reaction technology discriminates covert gastric marginal zone lymphoma from chronic gastritis. Gut. 2006;55(6):782-787. doi: 10.1136/gut.2005.080523.

Doglioni C, Ponzoni M, Ferreri AJM, Savio A, Gruppo Italiano Patologi Apparato Digerente (GIPAD), Società Italiana di Anatomia Patologica e Citopatologia Diagnostica/International Academy of Pathology, Italian division (SIAPEC/IAP). Gastric lymphoma: the histology report. Dig Liver Dis. 2011;43 Suppl 4:S310-318.

Perez CA, Dorfman RF. Benign lymphoid hiperplasia of the stomach and duodenum. Radiology. 1966;87:505-510.

Hyjek E, Kelényi G. Pseudolymphoma of the stomach. A lesion caractyerized by progressively transformed germinal centers. Histopathology. 1982;6:61-68.

Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al. WHO classification of tumours of haematopoietic and lymphoid tissues. IARC Press; 2008.

Isaacson PG, Spencer J. Malignant lymphoma of mucosa-associated lymphoid tissue. Histopathology. 1987;11(5):445-62.

Chan J. K. Gastrointestinal lymphomas: an overview with emphasis on new findings and diagnostic problems. Semin Diagn Pathol. 1996;13(4):260-96.

Dierlamm J, Wlodarska I, Michaux L. Genetic abnormalities in marginal zone B-cell lymphoma. Hematol Oncol. 2000;18:1-13.

Deutsch AJA , Aigelsreiter A, Steinb auer E, Neumeister, P. Distinct signatures of B-cell homeostatic and activation dependent chemokine receptors in the development and progression of extragastric MALT lymphomas. J Pathol. 2008;215:431-444.

Blanco R, Lyda M, Davis B, Kraus M, Fenoglio C. Trisomy 3 in gastric lymphomas of extranodal marginal zone B- cell (mucosa –associated lymphoid tissue) origin demonstrated by FISH in intact paraffin tissue sections. Hum Pathol. 1990;30:706-711.

Baens M, Maes B, Steyls A, Geboes K, Marynen P, De Wolff-Peters C. The product of the t(11-18), an AP12-MLT fusion, marks nearly half of the gastric MALT type lymphomas with-out large cell proliferation. An J Pathol. 2000;156:1433-1439.

Pileri SA, Sabattini E. A rational approach to immunohistochemical analysis of malignant lymphomas on paraffin wax sections. J Clin Pathol. 1997;50(1):2-4.

Wotherspoon A, Chot A, Gascoyne RD, Muller-Hermelinck HK. Lymphoma of the stomach. In Hamilton SR, Aaltonen LA (eds): Pathology and genetics of tumours of the digestive system, World Health Organization classification of tumours. Lyon: IARC Press; 2000. p. 57-61.

Mehmet S, Ozdal E, Kamil O, Beşir K, Huseyin D, Nihat A, Cigdem EY, Nusret E. Eradication of Helicobacter pylori in follicular and nonfollicular gastritis. Hepatogastroenterology. 2009;56(91-92):930-4.

Ruskoné-Fourmestraux A, Fischbach W, Aleman BM, Boot H, Du MQ, Megraud F, et al. Gastric extranodal marginal zone B-cell lymphoma of MALT. Gut. 2011;60:747-758.

Raderer M, Kiesewetter B, Ferreri AJ. Clinicopathologic characteristics and treatment of marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma). CA Cancer J Clin. 2016;66:153-171.

Jung K, Kim DH, Seo HI, Gong EJ, Bang CS. Efficacy of eradication therapy in Helicobacter pylori-negative gastric mucosa-associated lymphoid tissue lymphoma: A meta-analysis. Helicobacter. 2021;26(2):e12774.

Paydas S. Helicobacter pylori eradication in gastric diffuse large B cell lymphoma. World J Gastroenterol. 2015;21(13):3773-6.

Kuo SH, Cheng AL. Helicobacter pylori and mucosa-associated lymphoid tissue: what’s new. Hematology Am Soc Hematol Educ Program. 2013;2013:109-17.

Dwivedi M, Misra SP, Misra V. Nodular gastritis in adults: clinical features, endoscopic appearance, histopathological features, and response to therapy. J Gastroenterol Hepatol. 2008;23(6):943-947.