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 Table of Contents  
Year : 2018  |  Volume : 14  |  Issue : 1  |  Page : 176-183

Association of glutathione S-transferase M1 polymorphisms in the colorectal cancer risk: A meta-analysis

1 Department of Pathophysiology, West China School of Basic Medical Sciences & Forensic Medicine, Sichuan University, Chengdu, Sichuan Province, China
2 Sichuan University-West China Medicine Technology Transfer Center, West China Hospital, Sichuan University, Chengdu, Sichuan Province, China
3 Department of Oncology, Chengdu First People's Hospital, Chengdu, Sichuan Province, China

Date of Web Publication8-Mar-2018

Correspondence Address:
Prof. Ying Huang
Department of Pathophysiology, West China School of Basic Medical Sciences & Forensic Medicine, Sichuan University, Chengdu 610041, Sichuan Province
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcrt.JCRT_446_16

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 > Abstract 

Purpose: The glutathione S-transferase M1 (GSTM1) as a member of phase II detoxification enzymes is expressed in many tissues and plays a critical role in preventing the occurrence of cancer. Published data regarding the associations between the GSTM1 polymorphism and colorectal cancer (CRC) risk are inconclusive.
Materials and Methods: A meta-analysis of 55 case–control studies involving 17,498 cases and 26,441 controls were performed to assess the strength of association using odds ratio (OR) with 95% confidence interval (CI).
Results: The meta-analysis of those studies suggested that GSTM1 null genotype was significantly associated with CRC risk (OR = 1.13, 95% CI = 1.06–1.20, P < 0.0001). In the subgroup analysis by ethnicity, significant risks were associated with GSTM1 null genotype in Caucasians (OR = 1.18, 95% CI = 1.07–1.29, P = 0.001), Asians (OR = 1.11, 95% CI = 1.02–1.22, P = 0.02), and mixed group (OR = 1.01, 95% CI = 0.90–1.14, P = 0.85). In the subgroup analysis by study design, significant elevated risks were associated with GSTM1 null genotype in hospital-based case–control study group (OR = 1.20, 95% CI = 1.10–1.31, and P < 0.0001) but not in population-based case–control study group (OR = 1.03, 95% CI = 0.96–1.10, P = 0.43).
Conclusions: Based on our meta-analysis, the GSTM1 null genotype is a risk factor for CRC.

Keywords: Colorectal cancer, glutathione S-transferase M1, meta-analysis, polymorphism

How to cite this article:
Huang M, Zeng Y, Zhao F, Huang Y. Association of glutathione S-transferase M1 polymorphisms in the colorectal cancer risk: A meta-analysis. J Can Res Ther 2018;14:176-83

How to cite this URL:
Huang M, Zeng Y, Zhao F, Huang Y. Association of glutathione S-transferase M1 polymorphisms in the colorectal cancer risk: A meta-analysis. J Can Res Ther [serial online] 2018 [cited 2021 Jun 13];14:176-83. Available from: https://www.cancerjournal.net/text.asp?2018/14/1/176/226741

Min Huang, Yan Zeng and Fen Zhao contributed equally to this work.

 > Introduction Top

Colorectal cancer (CRC) is the third most common cancer and the second leading cause of mortality in developed countries.[1],[2] The occurrence of CRC is a multistage procedure mediated by genetic factors and local environmental factors.[3] This suggests that genetic differences, such as polymorphism, may contribute to the occurrence of CRC. At present, many published studies have focused on genetic variation and susceptibility to CRC.

Glutathione S-transferase (GST) comprises a number of isozymes and catalyzes reactions between glutathione and lipophilic compounds, which neutralize the toxic compounds and xenobiotics.[4] Glutathione S-transferase M1 (GSTM1) as a member of the GSTs participates in the neutralization process and plays critical roles in protecting hosts against cancer.[5] The GSTM1 gene which located on the short arm of chromosome 1 has been found variants in the population.[4] The deletion mutation in GSTM1 genotypes is related to the decreased enzyme activity that detoxifies carcinogens, which seems to increase the risk of cancer.[6] Although there have been a large number of researches investigated the deletion mutations polymorphism with CRC, the results were controversially. For a more comprehensive summary about the connection of GSTM1 and CRC, we performed a meta-analysis of case–control study on the association between CRC susceptibility and the polymorphism in GSTM1 gene.

 > Materials and Methods Top

Literature search and inclusion criteria

A systematic literature search was carried out in PubMed, Medline (Ovid), Embase, Chinese biomedical database (CBM), China national knowledge infrastructure, Weipu, and Wanfangdatabase to identify studies involving association between the GSTM1 polymorphism and CRC risk. The search terms were used as follows: GSTM1 in combination with polymorphism or variant or mutation and colorectal neoplasm or CRC or colorectal carcinoma. The search results were limited to English and Chinese languages. Studies included in meta-analysis met the following inclusion criteria: (1) the study evaluated the association between GSTM1 polymorphism and CRC, (2) the design had to be a case–control study, and (3) the cases and controls were available for estimate an odds ratio (OR) with its 95% confidence interval (CI). Studies were excluded if one of the following conditions existed: (1) no controls, (2) genotype not reported, and (3) abstracts and reviews. If more than one article was published by the same authors who used the same case series, studies with the largest size of samples or recently published were included.

Data extraction

Two independent reviewers collected the data using the inclusion criteria listed above. The title and abstract of articles were screened to determine their relevance first. If the title and abstract were ambiguous, full articles were then scrutinized. In case of disagreement, a third author would assess these articles. A standardized data form was used and it included first author's name, year of publication, original country, ethnicity, study design, total number of cases and control, and genotyping method.

Statistical analysis

The strength of association between GSTM1 polymorphism and CRC risk was assessed by OR with 95% CI. We estimated GSTM1 genotypes using (null or present) model. Then, the relationship between genotype and susceptibility to CRC was examined. The pooled OR was calculated by a fixed-effects model or a random-effects model according to the heterogeneity. Heterogeneity was checked by a χ2-based Q-statistic and P < 0.10 was considered statistically significant. P ≥ 0.10 for the Q-test indicated the lack of heterogeneity among the studies, and so the summary OR estimate of each study was calculated by the fixed-effects model.[7] Otherwise, the random-effects model was used.[8] The statistical significance of OR was analyzed by Z-test, and P < 0.05 was considered statistically significant. To evaluate the ethnicity-specific and study design-specific effects, we performed the analysis of stratification on ethnicity and study design. For the subgroup analysis by ethnicity, the study populations were stratified into three groups: the Caucasian, Asian, and mixed (if it was difficult to distinguish the ethnicity of participants according to the data presented, the study was termed “mixed”). Subjects were categorized into different classifications according to the study design: Hospital-based case–control study (HCC) and population-based case–control study (PCC). Sensitivity analysis was also performed by sequence excluding individual study to check the robustness of the result.[9] The possible publication bias was examined visually in a Begg's funnel plot and the degree of asymmetry was tested by Egger's test (P< 0.05 was considered representative of statistically significant publication bias).[10] Statistical analysis was performed using software Review Manager (RevMan) 5.2 (Cochrane Collaboration, 2008; www.cc-ims.net/RevMan) and Stata 10.0 (StataCorp, College Station, Texas).

 > Results Top

Study inclusion and characteristics

As shown in [Figure 1], the initial search identified 213 results from the selected electronic databases. After reading the titles and abstracts, 126 potential articles were included for full-text view. After reading full texts, 68 studies were excluded for being irrelevant to CRC risk and GSTM1 polymorphism. Therefore, 58 full-text articles remained for data extraction. Two articles were excluded for not presenting usable data.[11],[12] An additional article was excluded for repeating or overlapping.[13] Finally, a total of 55 case–control studies published in 55 articles which met our inclusion criteria were identified, including 17,498 cases and 26,441 controls. The characteristics of each case–control study are listed in [Table 1]. There were 26 case–controls of Caucasian,[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39] 23 of Asian,[40],[41],[42],[43],[44],[45],[46],[47],[48],[49],[50],[51],[52],[53],[54],[55],[56],[57],[58],[59] and 6 of mixed group.[60],[61],[62],[63],[64],[65] Fifty-two eligible reports were written in English and 3 studies were Chinese.
Figure 1: Flow diagram of included/excluded studies

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Table 1: Characteristics of the studies included in meta-analysis

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Quantitative data synthesis

The meta-analysis results suggested that GSTM1 null genotype was significantly associated with CRC risk (OR = 1.13, 95% CI = 1.06–1.20, P < 0.0001) [Figure 2]. Subgroup analyses by ethnicity and study design status were performed. For ethnicity, the analysis was stratified into three subgroups: the Caucasian (6530 cases and 9594 controls), Asian (7560 cases and 12237 controls), and mixed ethnicity (3408 cases and 4610 controls). Significantly elevated CRC risk was associated with the GSTM1 null/present genotype in Caucasians and Asians (OR = 1.18, 95% CI = 1.07–1.29, P = 0.001 and OR = 1.11, 95% CI = 1.02–1.22, P = 0.02, respectively). However, no significantly increased risks were found among the mixed ethnicity (OR = 1.01, 95% CI = 0.90–1.14, and P = 0.85) [Figure 3]a. In the subgroup analysis by study design status [Figure 3]b, the analysis was stratified into two subgroups: PCC and HCC, obviously increased risk was identified among HCC (OR = 1.20, 95% CI = 1.10–1.31, and P < 0.0001) but no significantly increased risks among PCC (OR = 1.03, 95% CI = 0.96–1.10, and P = 0.43).
Figure 2: Meta-analysis with of the association between glutathione S-transferase M1 polymorphism and colorectal cancer

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Figure 3: Subgroup analysis of the association between glutathione S-transferase M1 polymorphism and colorectal cancer. (a) Subgroup analysis by ethnicity. (b) Subgroup analysis by study design

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Sensitivity and publication analysis

The one-way sensitivity analyses were performed to assess the stability of the results, namely, a single study in the meta-analysis was deleted each time to reflect the influence of the individual data set to the pooled OR. After sequentially excluding each case–control study, statistically similar results were obtained (P< 0.05), confirming the stability of this meta-analysis. The detailed data were not presented. We assessed publication bias by Begg's funnel plot. The shape of funnel plots [Figure 4] did not reveal evidence of obvious asymmetry in all comparison models.
Figure 4: Inverted funnel plot for publication bias in studies on the glutathione S-transferase M1 polymorphism

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 > Discussion Top

Previous evidence suggested that the pathogenesis of CRC was nonclear and influenced by genetic factors, smoking status, diet structure, and other environmental factors.[5] GSTM1 as the most main members of GSTs has the ability to regulate the conversion of toxic compounds to hydrophilic metabolites, ultimately preventing the occurrence of cancer.[6] The expression of GSTM1 is found in almost all tissues, and in liver, reproductive tract, and colon, the expressions are highly showed. GSTM1 null genotype is the most common polymorphism and its incidence rate is approximately 50% in human (ranging from 22% in Africa to 62% in Europe).[66] It has been proven that GSTM1 null genotype was associated with the risk of several cancers, including CRC.[67],[68]

During the past 20 years, many researchers studied the concerning polymorphisms of genes involved in the pathogenesis of CRC. The GSTM1 null genotype in the etiology of CRC is one of the most widely studied. A large number of researches suggested that this polymorphism is associated with risk of CRC. To date, conclusions of the association of GSTM1 polymorphism with CRC are still uncertain. Thus, we performed a meta-analysis of 55 case–control studies, including 17,954 cases and 26,819 controls to comprehensively assess the association. Considering the complexity of the pathogenesis of CRC, subgroup analyses were performed by ethnicity and study designs.

By analyzing our results, we found the significant association between GSTM1 null variant and CRC under the random-effects model. Considering that the genetic background might cause the possible presence of heterogeneity between the studies and affect the results of genetic association studies, we further performed the analysis of subgroup on ethnicity and study design. In the stratified analysis by ethnicity, we found that the GSTM1 null genotype had influenced the risk of CRC in Caucasian and Asian, but not in mixed group. Possible explanation to these different results may be that the mixed group not only contains Caucasian and Asian but also African or Oceanian and no adequate data were available to analysis the association. When summarizing the results of stratification analysis by study design, the HCC group was more strongly associated with the risk of CRC in GSTM1 polymorphisms compared with PCC group. This reason may be that the hospital-based studies have some biases because such controls may be just the representative of a sample of ill-defined reference population and may not represent the general population very well.

To minimize the possible of heterogeneity, we used the explicit criteria for study inclusion and performed data extraction and data analysis strictly. However, heterogeneity is a problem when interpreting the results of the present meta-analysis. In overall analysis, we found moderate heterogeneity between studies. After subgroup analyses by ethnicity and study design, the heterogeneity was effectively removed in mixed group and PCC group or decreased in Caucasian, Asian, and HCC groups. The presence of heterogeneity can result from genetic heterogeneity between the samples that were drawn from geographically diverse populations. Another important factor contributing to heterogeneity was that homogeneity in either the case or control groups was uncertain. In addition, we attempted to determine if the heterogeneity might also be explained by other variables such as stages of CRC, smoking status, diet structure, and environmental factors included in the different studies, but are unable to provide a reliable answer to this question because of insufficient information for these variables.

We have to mention a previously published study by Economopoulos et al.[69] They also investigated the association between GSTM1 polymorphism and CRC risk. There were some differences between these two studies. First, the current meta-analysis included more case-control studies compared with Economopoulos et al.'s study. And then, some issues that might influence the results of meta-analysis were assessed in our study, such as sensitivity analysis and publication bias. In addition, the current study was a meta-analysis only focused on GSTM1 polymorphism, while Economopoulos's study was more devoted with the other polymorphisms. Despite of these differences, we also found significant sign of associations between GSTM1 polymorphism and CRC risk, which is consistent with Economopoulos et al.'s study, strongly suggesting that this GSTM1 null genotype was contribute to CRC pathogenesis.

Some limitations of this meta-analysis should be acknowledged when explaining our results. First, the overall outcomes were based on individual unadjusted ORs, while a more precise estimation should be conducted adjusted by confounding factors such as smoking status, diet structure, and environmental factors. Second, the results should be cautiously interpreted because controls were not uniformly defined. Third, in our meta-analysis, as only certain published studies written in English or Chinese were included, which indicates that some potential published studies in other languages or unpublished studies could be missed, publication bias is very likely to occur although it was not shown in the statistical test. And the last, this meta-analysis only estimated the Caucasian and Asian and there is no adequate sample sizes to analyze the other race populations. Therefore, more subjects of different ethnicities would be required to accurately clarify whether ethnicity has a biological influence on cancer susceptibility.

In conclusion, this meta-analysis suggests that the GSTM1 polymorphism is a risk factor for CRC, which may be beneficial for further medical research concerning and personalized therapy for CRC patients. To further assess gene and environment combined effects on GSTM1 polymorphisms and CRC, studies with different environmental backgrounds are urgently needed.


The authors would like to thank Dr. Shouchun Cheng for the suggestion that have been given in this meta-analysis.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1]


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