Systematic Reviews Open Access
Copyright ©The Author(s) 2023. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Apr 14, 2023; 29(14): 2202-2221
Published online Apr 14, 2023. doi: 10.3748/wjg.v29.i14.2202
Effectiveness of Helicobacter pylori eradication in the treatment of early-stage gastric mucosa-associated lymphoid tissue lymphoma: An up-to-date meta-analysis
Fabian Fellipe Bueno Lemos, Mariana Santos Calmon, Marcel Silva Luz, Samuel Luca Rocha Pinheiro, Clara Faria Souza Mendes dos Santos, Gabriel Lima Correa Santos, Henrique Affonso Delgado, Cláudio Lima Souza, Márcio Vasconcelos Oliveira, Fabrício Freire de Melo, Instituto Multidisciplinar em Saúde, Universidade Federal da Bahia, Vitória da Conquista 45029094, Bahia, Brazil
Caroline Tianeze de Castro, Instituto de Saúde Coletiva, Universidade Federal da Bahia, Salvador 40110040, Bahia, Brazil
Hanna Santos Marques, Campus Vitória da Conquista, Universidade Estadual do Sudoeste da Bahia, Vitória da Conquista 45029094, Bahia, Brazil
Kádima Nayara Teixeira, Campus Toledo, Universidade Federal do Paraná, Toledo 85919899, Paraná, Brazil
ORCID number: Fabian Fellipe Bueno Lemos (0000-0002-4686-7086); Caroline Tianeze de Castro (0000-0002-9445-8842); Mariana Santos Calmon (0000-0002-3871-7408); Marcel Silva Luz (0000-0003-1650-5807); Samuel Luca Rocha Pinheiro (0000-0002-8877-892X); Clara Faria Souza Mendes dos Santos (0000-0003-2424-7780); Gabriel Lima Correa Santos (0000-0003-3673-9889); Hanna Santos Marques (0000-0001-5741-1570); Henrique Affonso Delgado (0000-0002-8847-7078); Kádima Nayara Teixeira (0000-0002-2928-9181); Cláudio Lima Souza (0000-0002-8094-8357); Márcio Vasconcelos Oliveira (0000-0002-8959-0478); Fabrício Freire de Melo (0000-0002-5680-2753).
Author contributions: Lemos FFB, Castro CT, Teixeira KN, Souza CL, Oliveira MV, and Freire de Melo F contributed to the conceptualization of the manuscript; Lemos FFB, Castro CT, Teixeira KN, Souza CL, Oliveira MV, and Freire de Melo F designed the study methodology; Lemos FFB, Castro CT, Calmon MS, Silva Luz M, Pinheiro SLR, Faria Souza Mendes dos Santos C, Santos GLC, Marques HS and Delgado HA were responsible for manuscript visualization; Lemos FFB, Calmon MS, Silva Luz M, Pinheiro SLR, Faria Souza Mendes dos Santos C, Santos GLC, Marques HS, Delgado HA, Teixeira KN, Souza CL, Oliveira MV, and Freire de Melo F contributed to the investigation; Lemos FFB, Calmon MS, Silva Luz M, Pinheiro SLR, Faria Souza Mendes dos Santos C, Santos GLC, Marques HS, Delgado HA performed formal analysis; Lemos FFB wrote the original draft; Castro CT and Silva Luz M were responsible for manuscript editing; Castro CT, Silva Luz M, Teixeira KN, Souza CL, and Oliveira MV were responsible for manuscript writing and review; and Freire de Melo F supervised the writing of the original draft.
Supported by the Scientific Initiation Scholarship Programme (PIBIC) of the Bahia State Research Support Foundation, FAPESB, Brazil; the Doctorate Scholarship Program of the Coordination of Improvement of Higher Education Personnel, CAPES, Brazil; the Scientific Initiation Scholarship Programme (PIBIC) of the National Council for Scientific and Technological Development, CNPq, Brazil; and the CNPq Research Productivity Fellowship (PQ).
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
PRISMA 2009 Checklist statement: The authors have read the PRISMA 2009 Checklist, and the manuscript was prepared and revised according to the PRISMA 2009 Checklist.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Fabrício Freire de Melo, PhD, Professor, Instituto Multidisciplinar em Saúde, Universidade Federal da Bahia, Estrada do Bem Querer, 3293-3391 - Candeias, Vitória da Conquista 45029094, Bahia, Brazil. freiremeloufba@gmail.com
Received: November 19, 2022
Peer-review started: November 19, 2022
First decision: November 30, 2022
Revised: December 10, 2022
Accepted: March 14, 2023
Article in press: March 14, 2023
Published online: April 14, 2023

Abstract
BACKGROUND

Gastric mucosa-associated lymphoid tissue (MALT) lymphoma (GML) is usually a low-grade B-cell neoplasia strongly associated with Helicobacter pylori (H. pylori)-induced chronic gastritis. Clinical practice guidelines currently recommend H. pylori eradication as the preferred initial treatment for early-stage GML. To determine the practical effect of bacterial eradication as the sole initial therapy for early-stage GML, an updated analysis and review of available evidence is imperative.

AIM

To perform a meta-analysis to assess the rate of complete remission (CR) of H. pylori-positive early-stage GML following bacterial eradication.

METHODS

We performed independent, computer-assisted literature searches using the PubMed/MEDLINE, Embase, and Cochrane Central databases through September 2022. Prospective and retrospective observational studies evaluating the CR of early-stage GML following bacterial eradication in H. pylori-positive patients. The risk of bias was assessed using Joanna Briggs Institute (JBI) Critical Appraisal Tools. The pooled estimate of the complete histopathological remission rate and respective confidence intervals (95%CI) were calculated following the random-effects model. Heterogeneity and inconsistency were assessed using Cochran’s Q test and I2 statistic, and heterogeneity was defined as P < 0.01 and > 50%, respectively. Subgroup and meta-regression analyses were conducted to explore potential sources of heterogeneity.

RESULTS

The titles and abstracts of 1576 studies were screened; 96 articles were retrieved and selected for full-text reading. Finally, 61 studies were included in the proportional meta-analysis (P-MA). Forty-six were prospective and fifteen were retrospective uncontrolled, single-arm, observational studies. The overall risk of bias was low to moderate in all but a single report, with an average critical appraisal score across all studies of 79.02%. A total of 2936 H. pylori-positive early-stage GML patients, in whom H. pylori was successfully eradicated, were included in the analysis. The pooled CR of H. pylori-positive early-stage GML after bacterial eradication was 75.18% (95%CI: 70.45%-79.91%). P-MA indicated the substantial heterogeneity in CR reported across studies (I2 = 92%; P < 0.01). Meta-regression analysis identified statistically significant effect modifiers, including the proportion of patients with t(11;18)(q21;q21)-positive GML and the risk of bias in each study.

CONCLUSION

Comprehensive synthesis of available evidence suggests that H. pylori eradication is effective as the sole initial therapy for early-stage GML. Although the substantial heterogeneity observed across studies limits the interpretation of the pooled overall CR, the present study is a relevant to informing clinical practice.

Key Words: Lymphoma, B-cell, Marginal zone, Gastric mucosa-associated lymphoid tissue lymphoma, Stomach lymphoma, Helicobacter pylori, Therapeutics, Eradication therapy

Core Tip: Gastric mucosa-associated lymphoid tissue (MALT) lymphoma (GML) is usually a low-grade B-cell neoplasia strongly associated with Helicobacter pylori (H. pylori)-induced chronic gastritis. Clinical practice guidelines currently recommend H. pylori eradication as the preferred initial treatment for early-stage GML. Despite advances in determining the practical effect of bacterial eradication as sole initial therapy for early-stage GML, an updated meta-analysis of available evidence is imperative. We performed a systematic review with proportional meta-analysis to assess the complete remission rate of H. pylori-positive early-stage GML after eradication therapy.


  • Citation: Lemos FFB, Castro CT, Calmon MS, Silva Luz M, Pinheiro SLR, Faria Souza Mendes dos Santos C, Correa Santos GL, Marques HS, Delgado HA, Teixeira KN, Souza CL, Oliveira MV, Freire de Melo F. Effectiveness of Helicobacter pylori eradication in the treatment of early-stage gastric mucosa-associated lymphoid tissue lymphoma: An up-to-date meta-analysis. World J Gastroenterol 2023; 29(14): 2202-2221
  • URL: https://www.wjgnet.com/1007-9327/full/v29/i14/2202.htm
  • DOI: https://dx.doi.org/10.3748/wjg.v29.i14.2202

INTRODUCTION

Marginal zone lymphomas (MZLs) are the third most common type of non-Hodgkin B-cell lymphoma following diffuse large B-cell lymphoma and follicular lymphoma[1]. The 5th edition of the World Health Organization Classification of Hematolymphoid Tumors - Lymphoid Neoplasms subdivides MZL into 4 subtypes: Extranodal MZL of mucosa-associated lymphoid tissue (MALT), primary cutaneous MZL, nodal MZL, and pediatric MZL[2].

Gastric MALT lymphoma (GML) is a low-grade B-cell neoplasia commonly associated with Helicobacter pylori (H. pylori)-induced chronic gastritis[3]. GML provides the best-characterized model of the antigen-induced transition from normal to malignant marginal-zone B-cells[4]. Despite the lack of lymphoid follicles in the normal gastric mucosa, MALT may appear as a result of inflammation. H. pylori chronic gastritis induces specific T helper cells and the subsequent expansion of polyclonal B cells, which can undergo malignant transformation[4,5]. Similar to that of gastric cancer, in advanced-stage GML, inflammatory signaling pathway and pro-oncogenic genetic changes allow a microenvironment-independent progression of the tumor, characterizing a “hit-and-run” mechanism[5,6]. The overwhelming evidence suggesting a causal relationship between H. pylori infection and GML is also supported by epidemiological data[7].

Although robust comparative studies such as randomized clinical trials have not been carried out, clinical practice guidelines currently recommend H. pylori eradication as the sole initial treatment for early-stage GML[8]. Triple-therapy, which comprises a proton pump inhibitor (PPI) for 4 wk and clarithromycin with either amoxicillin or metronidazole for 10-14 d, remains standard. However, given the increasing rate of bacterial clarithromycin resistance in many countries, international guidelines also recommend bismuth quadruple therapy (BQT) or concomitant non-BQT as possible alternatives[9-11]. Accordingly, a previous systematic review with pooled data analyses highlighted that, after a long-term follow-up period, lymphoma disappeared in more than 75% of low-grade, stage I or II1 gastric lymphoma patients treated with bacterial eradication[12]. This study also identified that when the neoplastic lesion is confined to the submucosa, the main lesion is localized in the distal stomach, and t(11;18)(q21;q21) translocation is absent, the effectiveness of H. pylori eradication is even greater.

Given the low incidence of GML and the small sample sizes and heterogeneity of available studies[12], there is a need for an updated statistical analysis of the current evidence regarding H. pylori eradication as the sole initial therapy. Here, we performed a systematic literature review with meta-analysis to assess the complete histopathologic remission rate of H. pylori-positive early-stage GML after bacterial eradication therapy.

MATERIALS AND METHODS

This study followed the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guideline, which consists of a 27-item checklist and a 3-phase flowchart. The checklist includes items considered critical to the transparent reporting of a systematic review[13].

Literature search

The search strategy was designed following the Joanna Briggs Institute (JBI) Manual for Evidence Synthesis (https://synthesismanual.jbi.global). We performed independent, computer-assisted searches of the PubMed/MEDLINE, Embase, and Cochrane Central databases for studies published before September 2022. Medical Subject Headings and Embase Subject Headings (Emtree) index terms and free-text words were combined. Search terms included “Lymphoma, B-Cell, Marginal Zone,” “Mucosa-Associated Lymphoid Tissue Lymphoma,” “Marginal Zone B-Cell Lymphoma,” “MALT lymphoma,” “Stomach lymphoma,” “Helicobacter pylori,” “Therapeutics,” and “Eradication therapy.” Boolean operators (AND, OR) were also used to narrow or broaden the search as required. All citations were exported to the Rayyan (https://www.rayyan.ai/) tool and all duplicates were removed.

Study selection

Two researchers independently assessed the articles according to predefined eligibility criteria. In the case of disagreement, a 3rd researcher was consulted. The titles and abstracts of the articles were analyzed and studies that did not fit the inclusion criteria were excluded. The full texts were then revised to select eligible studies for meta-analysis.

Studies that met the following criteria were included: (1) Prospective and retrospective observational studies (cohort, case-control, and case series) evaluating the complete remission (CR) rate of early-stage GML after bacterial eradication therapy in H. pylori-positive patients; and (2) Studies including H. pylori-positive patients exclusively treated with antibiotic eradication therapy. Also, only trials enrolling patients with either stage I or II1 GML according to Lugano classification were included[14].

Exclusion criteria were as follows: (1) Studies that did not report the CR rate of H. pylori-positive early-stage GML after bacterial eradication; (2) Studies investigating high-grade or diffuse large B cell lymphomas, except for those where it is possible to extrapolate data from a subgroup with early-stage GML; (3) Studies that included patients with non-gastric sites of MALT lymphoma or ineligible study subjects, such as animals or children; (4) Full-text article not available or article not available in English; (5) Case reports, reviews, meta-analyses, systematic reviews, editorials, conference abstracts; and (6) Studies with insufficient data regarding treatment outcome.

Risk of bias assessment

Two researchers independently assessed the risk of bias using the JBI checklists for cohort, case-control, and case series studies[15]. In cases of disagreement, a 3rd researcher was consulted. These tools include multiple questions to assess the methodological quality of a study and determine the extent to which a study has addressed the possibility of bias in its design, conduct, and analysis. The bias percentage risk was calculated by the number of “yes” (Y) answers selected in the checklist. Questions with “not applicable” (N/A) answers were not considered in the calculation. The risk of bias was classified using the following categories: High (scores up to 49.0%), moderate (scores between 50.0% and 70.0%), and low (scores above 70.0%).

Data extraction

Two investigators extracted data from the selected studies using a predefined data extraction worksheet. Any discrepancies were resolved by a 3rd reviewer. The primary outcome was the complete histopathologic remission of the lymphoma after bacterial eradication in H. pylori-positive early-stage GML patients. Data were extracted with respect to the following: (1) Included study-related information (1st author, year of publication, country of origin, study design, and study size); (2) Clinical characteristics of the study population (disease stage, diagnostic methods for H. pylori infection, and eradication schemes); (3) Number of H. pylori-positive early-stage GML patients treated only with bacterial eradication; (4) Number of patients in whom H. pylori was successfully eradicated (either provided or calculated); and (5) Number of patients who finally achieved complete remission of the lymphoma (either provided or calculated). The stage of the lymphoma was assessed using the Lugano classification system[13].

Statistical analysis

The pooled estimate of the complete histopathological remission rate and respective confidence intervals (95%CI) were calculated following the random-effects model. Forest plots were used to summarize the results. Heterogeneity and inconsistency were assessed using Cochran’s Q test and I2 statistic[16]; heterogeneity was defined as P < 0.01 and > 50%, respectively. A subgroup analysis by study design (prospective; retrospective) was conducted to create more homogenous groups. Furthermore, a meta-regression analysis was conducted to explore potential sources of heterogeneity, such as publication year (≤ 2015; > 2015), geographic region of the study (Asian; Western), the prevalence of the translocation t(11;18)(q21; q21), and risk of bias (low; moderate; high). Analysis of publication bias was not performed as this measure is inappropriate for proportional meta-analysis (P-MA)[17]. All analyses were performed using R software version 4.2.1 (R: A Language and Environment for Statistical Computing, Vienna, Austria), using the ‘Meta’ package, version 5.2-0.

RESULTS
Literature search and study selection

Figure 1 depicts the flow of information through the different phases of the systematic review. Database searches identified 2375 reports, and duplicates were removed. The titles and abstracts of 1576 studies were screened and 96 articles were retrieved and selected for full-text reading. Finally, 61 studies were included in the meta-analysis. Reasons for exclusion were as follows: (1) 10 reports did not consider different stages in CR calculation; (2) 8 had insufficient data on H. pylori infection status; (3) 6 were conference abstracts; (4) 5 were publications of the same investigator or group; (5) 4 had insufficient data on the outcome; and (6) 2 included ineligible study subjects.

Figure 1
Figure 1 Preferred Reporting Items for Systematic Reviews and Meta-analyses 2020 flow diagram. The flow chart describes the flow of information through the different stages of the systematic review and maps the number of records identified, included, and excluded, and the reasons for study exclusion. H. pylori: Helicobacter pylori.
Study characteristics

Table 1 summarizes the characteristics of the studies included in the P-MA. The included reports were prospective and retrospective observational studies published between 1993 and 2021. A sample of 3315 patients with early-stage GML was obtained, of which 3003 were H. pylori-positive. A total of 2936 patients in whom H. pylori was successfully eradicated were included in the analysis. Twenty-nine of the included studies were conducted in Asian countries and 32 in Western countries. Concerning study design, 46 were prospective and 15 were retrospective uncontrolled, single-arm, observational studies. The median number of H. pylori-eradicated early-stage GML patients was 38 (ranging from 6-193). Multiple diagnostic tests for H. pylori infection and eradication were used, including histologic examination, H. pylori culture, rapid urease testing, 13C- or 14C-urea breath testing, serology, and H. pylori antigen stool testing. In most studies, at least 2 diagnostic tools were used to determine H. pylori infection status. Also in most studies eradication therapy consisted of a combination of 2 antibiotics, such as amoxicillin and clarithromycin, with a PPI. However, dual and quadruple therapies (2 antibiotics + PPI + bismuth or 3 antibiotics + PPI, respectively) were also used. Treatment duration ranged from 7 d to 21 d (Table 2).

Table 1 Characteristics of the included studies.
Ref.CountryDesignStudy periodStudy population
Early-stage gastric MALT lymphoma, n
Lugano stage
Median follow-up in mo
H. pylori-positive early-stage GML, n
Diagnosis of H. pylori infection
Yang et al[18], 2021ChinaRetrospective2003-201570703052UBT; HE
Schmelz et al[19], 2019GermanyProspective2001-20101091091299HE
Sugizaki et al[20], 2018JapanProspective2010-2016979737.497HE; HpC; RUT; UBT; HpSA; S
Song et al[21], 2018ChinaProspective2000-20131221223847RUT; HE; UBT
Li et al[22], 2016ChinaRetrospective2001-2013757562.969HE; UBT
Kim et al[24], 2016KoreaRetrospective2001-201449495140HE; UBT; RUT
Moleiro et al[23], 2016KoreaRetrospective2005-201410310350.582RUT; UBT; HE
Park et al[25], 2016PortugalRetrospective1993-201310310310587HE; HpC; S; UBT
Grgov et al[26], 2015SerbiaProspective2002-20122020NR20RUT; HE
Nonaka et al[27], 2014JapanRetrospective2007-20121616NR12HE; S; UBT
Lima et al[28], 2014BrazilProspective2009-201088247RUT; HE; UBT
Wündisch et al[29], 2012GermanyProspective1993-1999120120122120HE
Choi et al[30], 2011KoreaRetrospective2003-2010353521.526HE; RUT; UBT
Ono et al[31], 2011JapanRetrospective2003-20092121113RUT; UBT; HpC; HE; S
Andriani et al[32], 2009ItalyRetrospective1993-200660606560HE
Sumida et al[33], 2009JapanProspective1997-200766664057HE; S; UBT
Stathis et al[34], 2009SwitzerlandRetrospective1990-200610510575.685HE; S; UBT
Terai et al[35], 2008JapanProspective1995-200674744670RUT; HE; S; UBT
Fischbach et al[36], 2007GermanyRetrospectiveNR10810842.2108HE; UBT
Kim et al[37], 2007KoreaProspective1996-200699994199HE; RUT
El-Zahabi et al[38], 2007LebanonRetrospective1999-200522221219HE; S
Hong et al[39], 2006KoreaProspective1996-200390904590HE; RUT; UBT
Wündisch et al[40], 2006GermanyRetrospective1993-200319619627196HE
Akamatsu et al[41], 2006JapanProspective1993-2006555537.338HpC; HE
Wündisch et al[42], 2005GermanyProspectiveNR12012075120HE
Montalban et al[43], 2005SpainProspective1993-200224246424HE; UBT
Chen et al[44], 2005TaiwanProspective1996-199934347031HE; RUT; S
Taji et al[45], 2005JapanProspective1995-2001131332.512HE; HpC; S; UBT; RUT
Takenaka et al[46], 2004JapanProspective1995-20023333533HpC; RUT
Fischbach et al[47], 2004GermanyProspectiveNR909044.680RUT; HE; UBT
Sheu et al[48], 2003TaiwanProspectiveNR1515NR15RUT; HE
Caletti et al[49], 2002ItalyProspective1997-199951512451HE; RUT; S
Nakamura et al[50], 2002JapanProspective1994-2001212114.517HpC; S
Liu et al[51], 2002France; Netherlands; Italy; Germany; EnglandRetrospectiveNR111111NR111HE; HpC
Bertoni et al[52], 2002England; Italy; SwitzerlandProspectiveNR62622462HE; S
Ohashi et al[53], 2002JapanProspectiveNR1313NR13RUT; HE; HpC
Kim et al[54], 2002KoreaProspectiveNR202018.320RUT; HE
Matsushima et al[55], 2002JapanProspective1995-1997141427.514RUT; HE; HpC; UBT
Kanda et al[56], 2001JapanProspective1994-19991313713HE
Raderer et al[57], 2001AustriaRetrospective1997-199922222522HE
Nakamura et al[58], 2001JapanProspective1994-1998414120.541HpC; S; HE
Ruskoné-Fourmestraux et al[59], 2001FranceProspective1995-199844443534HE; HpC; S; PCR
Thiede et al[60], 2001GermanyProspectiveNR979720.897NR
de Jong et al[61], 2001NetherlandsProspectiveNR23233723HE; HpC
Urakami et al[62], 2000JapanProspectiveNR47472047RUT; HE; HpC
Papa et al[63], 2000ItalyProspective1995-199977487HE; UBT
Yamashita et al[64], 2000JapanProspectiveNR2121NR21HE; RUT; HpC
Ohashi et al[65], 2000JapanProspectiveNR1111NR11RUT; HE; HpC
Nakamura et al[66], 2000JapanProspective1993-19983030NR26HpC
Savio et al[67], 2000ItalyProspective1991-19977676NR76HE
Weston et al[68], 1999United StatesProspectiveNR6868NR65HE
Steinbach et al[69], 1999United StatesProspectiveNR3434NR28HE; RUT; S
Nobre-Leitão et al[70], 1998PortugalProspectiveNR17171217HE; HpC
Thiede et al[71], 1997GermanyProspectiveNR8484NR84NR
Sackmann et al[72], 1997GermanyProspectiveNR22221022HE; HpC
Neubauer et al[73], 1997GermanyProspectiveNR50502450HE
Pinotti et al[74], 1997Italy; SwitzerlandProspective1986-1995868623.345HE; S
Savio et al[75], 1996Italy; EnglandProspective1991-19931313NR13HE
Bayerdörffer et al[76], 1995GermanyProspectiveNR333312.533HE
Roggero et al[77], 1995Switzerland; ItalyProspectiveNR26261226HE
Wotherspoon et al[78], 1993England; ItalyProspectiveNR66NR6HE
Table 2 Characteristics of studies reporting the complete remission rate of Helicobacter pylori-positive early-stage gastric mucosa-associated lymphoid tissue lymphoma after bacterial eradication.
Ref.
Region
H. pylori-positive early-stage gastric MALT lymphoma, n
H. pylori-eradicated gastric MALT lymphoma patients, n
CR, n
t(11;18)(q21;q21)-investigated gastric MALT lymphoma, n
t(11;18)(q21;q21)-positive gastric MALT lymphoma, n
Eradication regimen
Yang et al[18]Asian524838NRNR7-d-14-d triple therapy or 10-d quadruple therapy
Schmelz et al[19]Western9999666977-d triple therapy
Sugizaki et al[20]Asian9786847317-d triple therapy
Song et al[21]Asian474735NRNR14-d triple therapy
Li et al[22]Asian696954NRNRND-day quadruple therapy
Kim et al[24]Asian403535NRNR7-d-14-d triple therapy or 7-d-14-d bismuth quadruple therapy
Moleiro et al[23]Western828177NRNR7-d triple therapy or 7-d bismuth quadruple therapy
Park et al[25]Asian878173NRNR7-d-14-d triple therapy
Grgov et al[26]Western202017NRNR10-d triple therapy
Nonaka et al[27]Asian12129NRNR7-d triple therapy
Lima et al[28]Western775847-d triple therapy or 10-d triple therapy
Wündisch et al[29]Western12012096661014-d dual therapy or 10-d triple therapy
Choi et al[30]Asian262622NRNRND-day triple therapy or ND-day bismuth quadruple therapy
Ono et al[31]Asian131313NRNR7-d-triple therapy
Andriani et al[32]Western605342NRNR7-d-14-d triple therapy or 10-d bismuth quadruple therapy
Sumida et al[33]Asian5757476677-d triple therapy
Stathis et al[34]Western858566NRNRND-day triple therapy
Terai et al[35]Asian7070562207-d triple therapy
Fischbach et al[36]Western10810835NRNRNR
Kim et al[37]Asian999984NRNR7-d triple therapy or 7-d bismuth quadruple therapy
El-Zahabi et al[38]Asian19198NRNRND-day quadruple therapy
Hong et al[39]Asian909085NRNR14-d triple therapy or 14-d bismuth quadruple therapy
Wündisch et al[40]Western196193146NRNRNR
Akamatsu et al[41]Asian383829867-d triple therapy or ND-day quadruple therapy
Wündisch et al[42]Western12012096651014-d dual therapy or 10-d triple therapy
Montalban et al[43]Western242422NRNR14-d triple therapy
Chen et al[44]Asian313024NRNR14-d triple therapy
Taji et al[45]Asian1212713414-d triple therapy
Takenaka et al[46]Asian333126NRNRND-day triple therapy
Fischbach et al[47]Western808056NRNR7-d triple therapy
Sheu et al[48]Asian151511NRNR14-d triple therapy
Caletti et al[49]Western514525NRNR7-d triple therapy
Nakamura et al[50]Asian1717223714-d triple therapy
Liu et al[51]Western111111481114414-d dual therapy
Bertoni et al[52]Western626246NRNR7-d triple therapy; 14-d triple therapy or 14-d bismuth quadruple therapy
Ohashi et al[53]Asian131311NRNR14-d triple therapy
Kim et al[54]Asian202018NRNR7-d triple therapy or 7-d bismuth quadruple therapy
Matsushima et al[55]Asian141410NRNRND-day triple therapy
Kanda et al[56]Asian13129NRNRND-day dual therapy or ND-day triple therapy
Raderer et al[57]Western222115NRNRND-day dual therapy or ND-day triple therapy
Nakamura et al[58]Asian414129NRNRND-day triple or ND-day quadruple therapy
Ruskoné-Fourmestraux et al[59]Western343419NRNR14-d triple therapy
Thiede et al[60]Western979777NRNR14-d dual therapy or 7-d triple therapy
de Jong et al[61]Western232313NRNRND-day dual therapy; ND-day triple therapy or ND-day quadruple therapy
Urakami et al[62]Asian474442NRNR7-d-14-d triple therapy
Papa et al[63]Western777NRNR7-d triple therapy
Yamashita et al[64]Asian212114NRNR14-d triple therapy
Ohashi et al[65]Asian11119NRNR14-d triple therapy
Nakamura et al[66]Asian262513NRNR14-d dual therapy; 7-d triple therapy (14-d PPI); 14-d triple therapy
Savio et al[67]Western767671NRNRNR
Weston et al[68]Western655838NRNRND-day triple or ND-day quadruple therapy
Steinbach et al[69]Western282814NRNR21-d bismuth quadruple therapy
Nobre-Leitão et al[70]Western171717NRNR14-d triple therapy
Thiede et al[71]Western847968NRNRNR-day-dual or 7-d-triple therapy
Sackmann et al[72]Western222212NRNR14-d-dual therapy
Neubauer et al[73]Western505040NRNR14-d-dual therapy or 7-d-triple therapy
Pinotti et al[74]Western454430NRNR14-d-triple or quadruple therapy
Savio et al[75]Western131211NRNRNR-day-triple or quadruple therapy
Bayerdörffer et al[76]Western333323NRNR14-d-dual therapy
Roggero et al[77]Western26255NRNR14-d-triple therapy
Wotherspoon et al[78]Western665NRNRNR-day-dual or triple therapy
Risk of bias in studies

Risk of bias was assessed using JBI checklists (Figure 2). The included single-arm uncontrolled observational studies were classifiable and assessed as case series. The overall risk of bias was low to moderate in all but 1 study[36], with an average critical appraisal score across all studies of 79.02% (Figure 2A).

Figure 2
Figure 2 Risk of bias assessment by the Joanna Briggs Institute Critical Appraisal Tool. The critical appraisal checklist for case series consists of 10 questions: Q1: Were there clear criteria for inclusion in the case series? Q2: Was the condition measured in a standard, reliable way for all participants included in the case series? Q3: Were valid methods used for identification of the condition for all participants included in the case series? Q4: Did the case series have consecutive inclusion of participants? Q5: Did the case series have complete inclusion of participants? Q6: Was there clear reporting of the demographics of the participants in the study? Q7: Was there clear reporting of clinical information of the participants? Q8: Were the outcomes or follow-up results of cases clearly reported? Q9: Was there clear reporting of the presenting site(s)/clinic(s) demographic information? Q10: Was statistical analysis appropriate? The percentage of risk of bias was calculated by the number of “yes” answers selected in the checklist. Questions with “not applicable” answers were not considered in the calculation. The risk of bias was classified using the following categories: High (scores up to 49.0%), moderate (scores between 50.0% and 70.0%), and low (scores above 70.0%). A: Overall risk of bias; B: Risk of bias summary: Discriminated assessments for each question across all studies. N/A: Not applicable.

An increased risk of bias was due to “No” or “Unclear” answers to the following questions: (1) Was there clear reporting of the presenting site(s)/clinic(s) demographic information? (54/61 studies); (2) Did the case series have consecutive inclusion of participants (24/61 studies); (3) Did the case series have complete inclusion of participants? (22/61 studies); (4) Was there clear reporting of the demographics of the participants in the study? (6/61 studies); (5) Was statistical analysis appropriate? (6/61 studies); (6) Was the condition measured in a standard, reliable way for all participants included in the case series? (4/61 studies); (7) Was there clear reporting of clinical information of the participants? (4/61 studies); (8) Was there clear reporting of clinical information of the participants? (3/61 studies); (9) Were the outcomes or follow-up results of cases clearly reported? (8/61 studies); and (10) Were there clear criteria for inclusion in the case series? (2/61 studies). Figure 2B shows the discriminated assessments for each question across all studies.

P-MA of the CR

The overall CR of H. pylori-positive early-stage GML after bacterial eradication was 75.18% (95%CI: 70.45%-79.91%). P-MA highlighted substantial heterogeneity in CR rate reported across studies (I2 = 92%; P < 0.01) (Figure 3A).

Figure 3
Figure 3 Overall complete remission rate of Helicobacter pylori-positive early-stage gastric mucosa-associated lymphoid tissue lymphoma. A: After eradication therapy; B: After eradication therapy by study design. CI: Confidence interval.
Exploring heterogeneity - subgroup and meta-regression analysis

Considering the high heterogeneity across studies (I2 = 92%; P < 0.01), a subgroup analysis by study design was conducted. The subgroup analysis revealed that retrospective and prospective studies presented similar overall CR rate after eradication therapy: 75.51% (95%CI: 64.96%-86.07%; I2 = 96%; P < 0.01) and 75.08% (95%CI: 69.80-80.36; I2 = 89%; P < 0.01), respectively (Figure 3B). The meta-regression analysis indicated that the proportion of patients with t(11;18)(q21;q21)-positive GML and study risk of bias were sources of heterogeneity. More precisely, studies with greater than 30% of patients with t(11;18)(q21;q21)-positive GML and high risk of bias showed the pooled estimate of the CR rate decreased to 0.40 (95%CI: -0.59 to -0.22; P < 0.0001) and 0.43 (95%CI: -0.77 to -0.09; P = 0.0139), respectively. There was no significant difference in outcomes with respect to geographic region (Table 3).

Table 3 Meta-regression according to selected covariates.
Subgroup
Studies, n
Estimate
95%CI
P value
I2, %
Year
≤ 201554---92.5
> 201570.11-0.03 to 0.250.1188
Region92.8
Asian29---
Western32-0.06-0.15 to 0.030.2145
Proportion of patients with t(11;18)(q21;q21)-positive gastric MALT lymphoma
≤ 30%7
> 30%4-0.40-0.59 to -0.22< 0.000188.6
Risk of bias92.3
Low39---
Moderate210.02-0.07 to 0.120.6190
High1-0.43-0.77 to -0.090.0139
DISCUSSION

GML is rare and typically comprises a low-grade neoplasm[18]. H. pylori infection is predominant pathogenic mechanism underlying the development of GML[19], and international guidelines strongly recommend H. pylori eradication therapy for all patients irrespective of stage. In localized H. pylori-positive GML, bacterial eradication is the preferred initial treatment[79,80].

This study aimed to provide an up-to-date, comprehensive synthesis of evidence regarding H. pylori eradication as the sole initial therapy for early-stage GML. We identified prospective and retrospective uncontrolled, single-arm observational studies with a total of 3315 patients with early-stage GML, of which 3003 were H. pylori-positive. A total of 2936 patients in whom H. pylori was successfully eradicated were included in the analysis. The unavailability of robust comparative studies (e.g., prospective cohort studies) precluded pairwise meta-analysis (PW-MA); instead, a P-MA was conducted. In contrast to comparative PW-MA, which calculates a pooled estimate of effect over 2 groups, P-MA enables the calculation of a grouped overall proportion[81,82]. Though single-group analysis may not produce measures of relative association, it can be useful for estimating the impact of a treatment on a given condition in the absence of higher-quality evidence. This represents an alternative for informed decision making, especially in our field where robust comparative studies are scarce.

P-MA highlighted that the overall CR rate of H. pylori-positive early-stage GML after bacterial eradication was 75.18% (95%CI: 70.45%-79.91%), suggesting that H. pylori eradication as the sole initial therapy for early-stage GML is effective. These results are similar to those found in a pooled data analysis published in 2010 by Zullo et al[12] [77.5% (95%CI: 75.3%-79.7%)]. On the other hand, the substantial heterogeneity observed across studies (I2 = 92%; P < 0.01) limits, though does not preclude, the interpretation of the pooled overall CR rate. Subgroup analysis revealed that retrospective and prospective studies estimated similar overall CR rates after eradication therapy [75.51% (95%CI: 64.96%-86.07%; I2 = 96%; P < 0.01) and 75.08% (95%CI: 69.80%-80.36%; I2 = 89%; P < 0.01), respectively]. Nevertheless, meta-regression analysis indicated that the proportion of patients with t(11;18)(q21;q21)-positive GML and the studies’ risk of bias were sources of heterogeneity. More precisely, studies with greater than 30% of patients with t(11;18)(q21;q21)-positive GML or high risk of bias decrease in 0.40 (95%CI: -0.59 to -0.22; P < 0.0001) and 0.43 (95%CI: -0.77 to -0.09; P = 0.0139) the pooled estimate of the CR rate, respectively. In this sense, we reiterate the results of Zullo et al[12] which highlight the presence of the t(11;18)(q21; q21) translocation as a predictor of lymphoma remission after bacterial eradication. In contrast to the previous pooled analysis[12], our study did not observe significant differences in lymphoma remission between Western and Asian countries.

Hence, our results reaffirm that H. pylori eradication should be given as the first-line treatment for localized low-grade GML[8]. The anti-H. pylori regimen should be chosen based on regional microbial susceptibility; in many regions, BQT or high-dose PPI clarithromycin-containing triple therapy may be recommended as first-line empirical treatment[83]. In case of eradication failure, second-line treatment should be attempted following the currently recommended algorithm for empirical H. pylori eradication or as guided by individual antibiotic susceptibility testing. For patients with GML refractory to H. pylori eradication, irradiation and systemic oncological therapies should be used, depending on the stage of the disease. Radiotherapy (RT) is the first-line choice for the treatment of localized GML. Chemotherapy, immunotherapy, or combination chemoimmunotherapy are mainly considered if RT is not feasible or otherwise not indicated[84,85].

To our knowledge, our study is the first systematic review with meta-analysis to assess the CR rate of H. pylori-positive early-stage GML after H. pylori eradication. Our work has strengths in its design and execution, such as the use of random-effects meta-analysis to address heterogeneity between included studies, subgroup analyses by study design, and meta-regression to explore possible sources of heterogeneity. Nonetheless, the present analysis has several limitations inherent to the included studies and study design. Due to the unavailability of language resources (e.g., professional translators), we could not include studies in languages other than English. Although limiting study inclusion based on the language of publication is a common practice in systematic reviews, it introduces the risk of ignoring key data, referred to as language bias, which may limit the interpretation of our findings[86].

Moreover, discriminated assessments for each JBI Critical Appraisal Tool question across all reports showed that the included series had serious gaps in clinical and demographic information reporting. Thus, exploring possible sources of heterogeneity and identifying predictors of lymphoma remission was difficult. Furthermore, incomplete and non-consecutive inclusion of patients in several studies compromises the reliability of their results and increases the risk of bias. Another limitation was the failure to report the confirmation method for H. pylori eradication, which could be a covariate explaining the heterogeneity between studies. Inadequate reporting was an important reason for the exclusion of studies during screening and a complicating factor for data extraction. Observational studies evaluating the CR of GML after bacterial eradication should stratify the observed outcome according to H. pylori infection status. Furthermore, it is necessary to discriminate the lymphoma stage in H. pylori-positive patients undergoing treatment. In fields in which reliable and robust studies are scarce, proper reporting of the available evidence is vital to inform clinical practice. Therefore, this meta-analysis should be interpreted in the context of these limitations.

CONCLUSION

This comprehensive evidence synthesis suggests the effectiveness of H. pylori eradication as the sole initial therapy for early-stage GML. Although the substantial heterogeneity observed across studies limits the interpretation of the pooled overall CR rate, our study is a relevant alternative for informing clinical practice. Further robust comparative observational studies are needed to identify predictive factors for GML remission following H. pylori eradication and to provide more reliable evidence in our field.

ARTICLE HIGHLIGHTS
Research background

Gastric mucosa-associated lymphoid tissue (MALT) lymphoma (GML) is usually a low-grade, B-cell neoplasia strongly associated with Helicobacter pylori (H. pylori)-induced chronic gastritis. As such, clinical practice guidelines currently recommend H. pylori eradication as the preferred initial treatment for early-stage GML.

Research motivation

Studies that aim to evaluate the effects of H. pylori eradication on early-stage GML are generally small and heterogenous single-arm uncontrolled observational studies. Hence, we recognized the need for an updated powerful statistical synthesis of the available evidence regarding the practical effect of H. pylori eradication as sole initial therapy for early-stage GML.

Research objectives

We aimed to perform a systematic review with an up-to-date proportional meta-analysis (P-MA) to assess the complete remission (CR) rate of H. pylori-positive early-stage GML after bacterial eradication therapy.

Research methods

We performed independent computer-assisted searches of PubMed/MEDLINE, Embase and Cochrane Central databases culling reports published before September 2022. Prospective and retrospective observational studies evaluating the CR rate of early-stage GML after bacterial eradication therapy in H. pylori-positive patients were eligible for inclusion. The risk of bias was assessed using the JBI Critical Appraisal Tools. We followed the random-effects model to calculate the pooled estimate of the complete histopathological remission rate and respective confidence intervals (95%CI). We used Cochran’s Q test and I2 statistic to assess the heterogeneity and inconsistency, and we set the threshold for heterogeneity as P < 0.01 and > 50%, respectively. Subgroup and meta-regression analyses were conducted to explore potential sources of heterogeneity.

Research results

P-MA highlighted that the overall CR of H. pylori-positive early-stage GML after bacterial eradication was 75.18% (95%CI: 70.45%-79.91%). On the other hand, the substantial heterogeneity observed across studies (I2 = 92%; P < 0.01) limits, but does not preclude, the interpretation of the pooled overall CR rate. Subgroup analysis revealed that retrospective and prospective studies presented similar overall CR rate estimates after eradication therapy: 75.51% (95%CI: 64.96%-86.07%; I2 = 96%; P < 0.01) and 75.08% (95%CI: 69.80%-80.36%; I2 = 89%; P < 0.01), respectively. Nevertheless, meta-regression analysis indicated that the proportion of patients with t(11;18)(q21;q21)-positive GML and the studies’ risk of bias were sources of heterogeneity. More precisely, studies with greater than 30% of patients with t(11;18)(q21;q21)-positive GML and high risk of bias decrease in 0.40 (95%CI: -0.59 to -0.22; P < 0.0001) and 0.43 (95%CI: -0.77 to -0.09; P = 0.0139) the pooled estimate of the CR rate, respectively.

Research conclusions

Comprehensive evidence synthesis suggests the effectiveness of H. pylori eradication as the sole initial therapy for early-stage GML. Although the substantial heterogeneity observed across studies limits the interpretation of the pooled overall CR rate, the present study is a relevant alternative for informing clinical practice.

Research perspectives

Inadequate reporting was an important reason for the exclusion of studies during screening and a complicating factor for data extraction. As reliable and robust studies are scarce in our field, we emphasize that proper reporting of the available evidence is vital to inform clinical practice. Further robust comparative observational studies are needed to identify predictive factors for GML remission following H. pylori eradication and to provide more reliable evidence in our field.

Footnotes

Provenance and peer review: Invited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Gastroenterology and hepatology

Country/Territory of origin: Brazil

Peer-review report’s scientific quality classification

Grade A (Excellent): A

Grade B (Very good): B

Grade C (Good): 0

Grade D (Fair): 0

Grade E (Poor): 0

P-Reviewer: Haddadi S, Algeria; Viazis N, Greece S-Editor: Wang JJ L-Editor: Filipodia P-Editor: Wang JJ

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