Meta-Analysis Open Access
Copyright ©The Author(s) 2016. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Feb 7, 2016; 22(5): 1911-1918
Published online Feb 7, 2016. doi: 10.3748/wjg.v22.i5.1911
Glutathione S-transferase M1 polymorphism and esophageal cancer risk: An updated meta-analysis based on 37 studies
Quan-Jun Lu, Ya-Cong Bo, Wolde Bekalo Sapa, Dan-Dan Duan, Yi-Wei Zhu, Department of Nutrition and Food Hygiene, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
Yan Zhao, Department of Epidemiology and Biostatistics, College of Public Health, Zhengzhou University, Zhengzhou 450001, Henan Province, China
Er-Jiang Zhao, Wei-Quan Lu, Affiliated Tumor Hospital of Zhengzhou University, Henan Tumor Hospital, Zhengzhou 450003, Henan Province, China
Ming-Jie Yao, School of Basic Medical Sciences, Peking University, Beijing 100191, China
Ling Yuan, Department of Radiotherapy, Affiliated Tumor Hospital of Zhengzhou University, Henan Tumor Hospital, Zhengzhou 450003, Henan Province, China
Author contributions: Lu QJ, Lu WQ and Yuan L conceived and designed the study; Bo YC, Zhao Y, Zhao EJ, Duan DD and Zhu YW selected the studies, extracted the data and performed the statistical analysis; Lu QJ and Bo YC drafted the manuscript; Sapa WB and Yao MJ revised the manuscript.
Supported by Science and Technology Project of The Health Department of Henan Province, China, No. 510102050432.
Conflict-of-interest statement: The authors declare that there are no conflicts of interest.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (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: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Ling Yuan, MD, Department of Radiotherapy, Affiliated Tumor Hospital of Zhengzhou University, Henan Tumor Hospital, No. 1 Jianshe East Rd, Erqi District, Zhengzhou 450003, Henan Province, China. hnyl2001@126.com
Telephone: +86-371-67781868 Fax: +86-371-67781868
Received: March 31, 2015
Peer-review started: April 1, 2015
First decision: June 19, 2015
Revised: October 6, 2015
Accepted: November 13, 2015
Article in press: November 13, 2015
Published online: February 7, 2016

Abstract

AIM: To evaluate the relationship between glutathione S-transferase M1 (GSTM1) polymorphism and susceptibility to esophageal cancer (EC).

METHODS: A comprehensive search of the United States National Library of Medicine PubMed database and the Elsevier, Springer, and China National Knowledge Infrastructure databases for all relevant studies was conducted using combinations of the following terms: “glutathione S-transferase M1”, “GSTM1”, “polymorphism”, and “EC” (until November 1, 2014). The statistical analysis was performed using the SAS software (v.9.1.3; SAS Institute, Cary, NC, United States) and the Review Manager software (v.5.0; Oxford, England); crude odds ratios (ORs) with 95% confidence intervals (CIs) were used to assess the association between the GSTM1 null genotype and the risk of EC.

RESULTS: A total of 37 studies involving 2236 EC cases and 3243 controls were included in this meta-analysis. We observed that the GSTM1 null genotype was a significant risk factor for EC in most populations (OR = 1.33, 95%CI: 1.12-1.57, Pheterogeneity < 0.000001, and I2 = 77.0%), particularly in the Asian population (OR = 1.53, 95%CI: 1.26-1.86, Pheterogeneity < 0.000001, and I2 = 77.0%), but not in the Caucasian population (OR = 1.02, 95%CI: 0.87-1.19, Pheterogeneity = 0.97, and I2 = 0%).

CONCLUSION: The GSTM1 null polymorphism may be associated with an increased risk for EC in Asian but not Caucasian populations.

Key Words: Meta-analysis, Glutathione S-transferase M1, Polymorphism, Esophageal cancer, Deletions

Core tip: Many previous studies have investigated the association between the glutathione S-transferase M1 (GSTM1) null genotype and the risk of esophageal cancer (EC), but these studies have provided controversial findings. The present study represents the largest meta-analysis to estimate the association between the GSTM1 polymorphism and EC risk. We investigated these two genotypes (GSTM1 null or GSTM1 present) in terms of EC morbidity.
INTRODUCTION

Esophageal cancer (EC), which is the sixth leading cause of cancer-associated death worldwide, has two major histological types: esophageal squamous cell carcinoma (ESCC) and esophageal adenocarcinoma (EADC)[1]. The five-year survival rate for EC is less than 20%[2]. A growing body of epidemiological evidence suggests that environmental factors together with genetic factors play important roles in the risk of developing EC[3,4]. The major risk factors for EC include alcohol consumption, smoking tobacco, and micronutrient deficiency[5]. Various factors and multiple processes lead to EC development. In addition to the above mentioned factors, genetic factors also account for EC cases.

Previous studies have suggested that glutathione S-transferases (GSTs) are phase II metabolizing enzymes that detoxify free radicals and other carcinogens[6]. Therefore, individual variation in phases II enzyme activity may contribute to varying susceptibility to EC progression. The GST family plays an important role in the detoxification of a variety of electrophilic carcinogens through conjugation with glutathione, and there is a widely variable organ distribution of the four classes of GSTs, although all of these display esophageal expression: GSTA (a), GSTM (m), GSTP (p), and GSTT (h)[7,8]. Homozygous deletions of GSTM1 have been associated with the loss of enzymatic activity for the detoxification of carcinogens, which consequently confers a risk for some cancers, such as colorectal, pancreatic, esophageal, and head and neck cancers[9-12]. Therefore, the null genotype of GSTM1 might be associated with an increased risk of EC[13]. Many previous studies have investigated the association between the GSTM1 null genotype and the risk of EC, but these studies have provided controversial findings[8,14-18]. It remains uncertain whether the GSTM1 polymorphism is a risk factor for EC. Considering these controversial results, we conducted a meta-analysis summarizing reported case-control or prospective studies to assess the risk of EC.

MATERIALS AND METHODS
Search strategy

We conducted a comprehensive search of the US National Library of Medicine PubMed database and the Elsevier, Springer, and China National Knowledge Infrastructure databases for all relevant studies using combinations of the following terms: “glutathione S-transferase M1”, “GSTM1”, “polymorphism”, and “EC” (until November 1, 2014). Additional eligible studies were identified through references that were cited in the relevant articles. The full text of each potentially relevant paper was scrutinized to ensure that the following inclusion criteria were met: (1) the articles clearly described studies concerning the association of EC with GSTM1 polymorphism; (2) The study design should be observational (case-control or prospective); (3) Sufficient data for estimating the odds ratios (ORs) and 95% confidence intervals (CIs) were present; and (4) If more than one publication reported on the same population, we selected the study with the largest sample size.

Data extraction

Two researchers independently extracted the following data from each study that met the inclusion criteria: first author’s surname, year of publication, country, ethnicity of the subjects (stratified into Asian, Caucasian, and African populations), sources of the controls (categorized as population-based studies and hospital-based studies), histological type (adenocarcinoma and squamous cell carcinoma), number of different genotypes in cases and controls, smoking status, and the frequency of different genotypes in the cases and controls. Individuals with “present” genotype were defined as carriers with at least one of the functional alleles in accordance with the definition used in most studies, whereas individuals carrying none of the alleles were classified as the “null” genotype.

Statistical analysis

Crude ORs with 95%CIs were used to estimate the strength of the relationship between the GSTM1 polymorphism and EC risk. The pooled ORs were evaluated for null vs present genotypes. The heterogeneity was assessed using a χ2 analysis based on the Q-test[19]. The heterogeneity was considered significant for P < 0.05. In the presence of significant heterogeneity, a random-effects model (the DerSimonian and Laird method)[20] was used to calculate pooled estimates; otherwise, a fixed-effects model (the Mantel-Haenszel method) was used[21]. These two models provided similar results in the absence of heterogeneity. The potential publication bias was assessed using a funnel plot and linear regression asymmetry test[22].The statistical analyses were performed using the SAS (v.9.1.3; SAS Institute, Cary, NC, United States) and Review Manager software (v.5.0; Oxford, England) with two-sided P values and a 0.05 significance level.

RESULTS
Eligible studies

A total of 37 studies involving 2236 EC cases and 3243 controls were finally included in this meta-analysis[8,12-18,23-51]. The main characteristics of these studies are presented in Table 1. Among these studies, one case-control study was nested within a cohort study[51], and 25 studies provided data of the histological type of the EC cases. The smoking statuses of the cases and controls were recorded in six studies.

Table 1 Characteristics of the studies included in this meta-analysis.
Ref.YearEthnicityCountrySource of controlsGenotype distribution
Case
Control
NullPresentNullPresent
Morita et al[49]1997AsianJapanPB23305577
Nimura et al[43]1997AsianChinaHB47426374
Hori et al[31]1997AsianJapanPB4153196232
Lin et al[27]1998AsianChinaPB20252124
Shao et al[36]1999AsianChinaHB68405557
van Lieshout et al[30]1999CaucasianThe NetherlandPB1717128119
Tan et al[14]2000AsianChinaPB461047674
Shi et al[40]2002AsianChinaHB67315169
Yokoyama et al[15]2002AsianJapanHB103131321313
Gao et al[42]2002AsianChinaPB1063513390
Casson et al[48]2003CaucasianCanadaPB26192520
Wang et al[50]2003AsianChinaPB27351919
Wang et al[44]2004AsianChinaHB74534457
Abbas et al[33]2004CaucasianFrenchPB39295961
Roth et al[51]2004AsianChinaNest4190145309
Han et al[39]2005AsianChinaHB46434851
Lu et al[28]2005AsianChinaPB36684100
Yin et al[35]2005AsianChinaHB69376145
Casson et al[45]2006CaucasianCanadaHB34225441
Jain et al[32]2006AsianIndiaHB39615186
Dong et al[47]2007AsianChinaHB76445169
Wideroff et al[41]2007CaucasianUnited StatesPB373012187
Rossini et al[29]2007CaucasianBrazilHB517499153
Li et al[34]2008AsianChinaPB77485570
Zendehdel et al[23]2009CaucasianSwedenPB8585230239
Ji et al[38]2010AsianChinaPB1117898127
Malik et al[26]2010AsianIndiaHB686779116
Liu et al[24]2010AsianChinaPB54433265
Moaven et al[12]2010AsianIranHB65835878
Li et al[16]2010BlackAfricaHB3320680200
Gao et al[37]2012AsianChinaHB22184535
Chen et al[17]2012AsianChinaHB68319096
Liu et al[46]2013AsianChinaHB476374146
Talukdar et al[25]2013AsianIndiaPB44684090
Sharma et al[13]2013AsianIndiaPB129186139297
Dura et al[8]2013CaucasianThe NetherlandPB228204318273
Djansugurova et al[18]2013AsianKazakhstanPB72432476
PB: Population-based study; HB: Hospital-based study.
Meta-analysis

Considering the obvious heterogeneity among the 37 included studies (P < 0.001, I2 = 77%), the random-effects model (DerSimonian-Laird method) was used to calculate the pooled ORs for the GSTM1 null vs GSTM1 present genotypes. Individuals with GSTM1 null genotypes were significantly associated with an increased risk for EC compared those carrying the GSTM1 present genotype (OR = 1.33, 95%CI: 1.12-1.57, Figure 1). In the sensitivity analysis, individual studies were sequentially removed. The results indicated that no individual study significantly affected the pooled OR, suggesting that these results were statistically robust.

Figure 1
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Figure 1 Forest plot for the association between the glutathione S-transferase M1 polymorphism and esophageal cancer risk.

In the subgroup analysis based on ethnicity, a positive correlation was observed between the GSTM1 null genotype and the EC risk in the Asian population (OR = 1.53, 95%CI: 1.26-1.86) but not in the Caucasian population (OR = 1.02, 95%CI: 0.87-11.19). However, the results of the stratified analysis based on histological type showed that the GSTM1 null genotype increased the risk of EC in patients whose histological type was unknown, but no statistically significant association was observed for either the ESCC patients or the EADC patients. Moreover, the heterogeneity was significantly reduced among Caucasian populations and studies based on the histological type of adenocarcinoma. Because only one study (14EADC, 137 ESCC) reported an association between the GSTM1 polymorphism and EADC in Asian populations, we only analyzed the data according to ESCC and EADC in Caucasian populations, and the results showed no statistically significant association between the GSTM1 polymorphism and ESCC or EADC. The main results of this meta-analysis and the heterogeneity test are shown in Table 2.

Table 2 Main results of the pooled odds ratios in this meta-analysis.
Null vs present
No. of studiesOR95%CIP value
Total371.331.12-1.570.00001
Ethnicity
Asian271.531.26-1.860.00001
Caucasian81.020.87-1.190.97
Histological type
ESCC221.150.91-1.450.00001
EADC80.980.81-1.180.93
NR121.821.58-2.090.007
Smoking status
Smokers60.970.53-1.770.00001
Nonsmokers60.970.57-1.640.001
Histological type of Caucasian
ESCC51.150.91-1.450.33
EADC80.980.81-1.180.93
The P value for heterogeneity. ESCC: Esophageal squamous cell carcinoma; EADC: Esophageal adenocarcinoma; NR: Not reported.
Publication bias

A funnel plot was used to graphically estimate the publication bias of the literature. As shown in Figure 2, the shape of the funnel plot was symmetrical in the overall population, suggesting the absence of publication bias. The results of Egger’s test showed statistical evidence for funnel plot symmetry (t = 1.76, P = 0.0873).

Figure 2
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Figure 2 Funnel plot evaluating the risk of publication bias in this meta-analysis.
DISCUSSION

GSTM1 is a member of the family of cytosolic GSTs, which are phase II xenobiotic-metabolizing enzymes. These enzymes play a crucial role in the detoxification and elimination of electrophilic carcinogens through conjugation with glutathione[12]. Many studies have investigated the association between the GSTM1 null genotype and various types of cancer, such as colorectal carcinoma, lung cancer, liver cancer, and EC, but the findings are controversial, particularly those obtained for EC[52,53]. The results of this meta-analysis showed that the GSTM1 null genotype is significantly associated with an increased risk of EC in the overall population. Furthermore, in the subgroup analysis by ethnicity, we detected a significant association between the GSTM1 polymorphism and EC risk in Asians but not in Caucasians, suggesting that the GSTM1 null polymorphism might contribute to increased susceptibility to EC in Asians. Similar results have been obtained in several previous meta-analyses[54,55]. However, other studies have shown conflicting results. A pooled analysis of 20 studies from the Archives of Medical Research revealed that there was no evidence of increased risk of EC associated with the GSTM1 null genotype[56]. The result might reflect a relatively small sample size and, to a lesser extent, different ethnicities, different histological types and the source of the controls.

In the present meta-analysis, most of the included studies concerned Asian populations. This phenomenon might be attributed to the occurrence of EC, which displays a remarkable geographical difference. Specifically, the ‘‘EC belt’’, which stretches from North Central China westward through Central Asia and northern Iran, exhibits a particularly high EC incidence in Asian populations[57], which explains why many of the studies were conducted in Asian countries.

In the subgroup analysis based on histological type, no significant association was detected between the GSTM1 polymorphism and ESCC or EADC risk, indicating that histological type might affect the statistical correlation between the GSTM1 polymorphism and EC. Similar results have been reported in previous studies[23,55,58], indicating that further clarification of the histological type might avoid the interference of some confounding factors.

Several potential limitations of the present meta-analysis should also be acknowledged. Only one of the included studies was conducted in Africa, and it did not provide sufficient data for the subgroup analysis based on ethnicity. Therefore, we could not include the African population in the subgroup analysis based on ethnicity. Moreover, only published studies were included in the present meta-analysis, which might have biased the results.

In conclusion, this meta-analysis demonstrated that the GSTM1 null polymorphism might be associated with an increased risk for EC in Asian populations but not in Caucasian populations. Larger well-designed epidemiological studies are warranted to verify these findings.

COMMENTS
Background

Esophageal cancer (EC), which is the sixth leading cause of cancer-associated death worldwide, has two major histological types: esophageal squamous cell carcinoma and esophageal adenocarcinoma. The five-year survival rate for EC is less than 20%. Previous studies have suggested that glutathione S-transferase (GSTs) are phase II metabolizing enzymes that detoxify free radicals and other carcinogens. Therefore, individuals with low phase II activity might have a higher risk of developing cancer. The GST family plays an important role in the detoxification of a variety of electrophilic carcinogens through conjugation with glutathione, and there is a widely variable organ distribution of the four classes of GSTs, namely, GSTA (a), GSTM (m), GSTP (p), and GSTT (h), although all show esophageal expression.

Research frontiers

A growing body of epidemiological evidence suggests that environmental factors together with genetic factors play important roles in the risk of developing esophageal carcinoma: alcohol consumption, smoking tobacco, and micronutrient deficiency are considered the major risk factors for EC. The GSTM1 null genotype has been associated with an increased risk of EC. Many previous studies have investigated the association between the GSTM1 null genotype and the risk of esophageal carcinoma, but these studies provide controversial findings.

Innovations and breakthroughs

The results of the present study indicated that the GSTM1 null polymorphism might be associated with an increased risk of EC in Asian populations but not in Caucasian populations, which would be helpful for the identification of individuals at an increased risk of developing EC.

Applications

The present study enhances the current understanding of the effects of GSTM1 on EC. Larger well-designed epidemiological studies are warranted to confirm the precise mechanism underlying the involvement of the GSTM1 gene in EC progression.

Terminology

GSTM1 is a primary member of the GST family, which comprises enzymes that play important roles in the detoxification of a variety of electrophilic carcinogens through conjugation with glutathione. Homozygous deletions of GSTM1 might disrupt enzymatic detoxification of carcinogens and consequently confer risk for some cancers, such as colorectal, pancreatic, esophageal, and head and neck cancers.

Peer-review

The present study analyzed the effect of the GST1 polymorphism on EC risk. The meta-analysis of 37 studies showed that the GSTM1 null polymorphism is associated with a significantly increased risk of EC.

Footnotes

P- Reviewer: Corrales FJ, Ghiorzo P, Nagahara H S- Editor: Ma YJ L- Editor: Wang TQ E- Editor: Zhang DN

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