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. 2018 Nov 12;18:1088. doi: 10.1186/s12885-018-5014-1

Association of Glutathione S-transferase gene polymorphism with bladder Cancer susceptibility

Tianbiao Zhou 1,✉,#, Hong-Yan Li 2,#, Wei-Ji Xie 1, Zhiqing Zhong 1, Hongzhen Zhong 1, Zhi-Jun Lin 1
PMCID: PMC6233535  PMID: 30419877

Abstract

Background

We conducted a meta-analysis to evaluate the relationship between the glutathione S-transferase μ1 (GSTM1)– and glutathione S-transferase θ1 (GSTT1)– null genotypes and susceptibility to bladder cancer.

Methods

We identified association reports from the databases of PubMed, Embase, the Cochrane Library and the China Biological Medicine Database (CBM disc) on July 1, 2017 and synthesized eligible investigations. Results were expressed using odds ratios (ORs) for dichotomous data, and we also calculated 95% confidence intervals (CIs).

Results

In this meta-analysis, we found that the GSTM1-null genotype was associated with bladder cancer risk in the overall population, and individually in whites, Africans and Asians (overall population: OR = 1.40, 95% CI: 1.31–1.48, P<0.00001; whites: OR = 1.39, 95% CI: 1.26–1.54, P<0.00001; Africans: OR = 1.54, 95% CI: 1.16–2.05, P = 0.003; Asians: OR = 1.45, 95% CI: 1.33–1.59, P<0.00001). The GSTT1-null genotype was associated with bladder cancer risk in the overall population, but not in whites, in Africans or Asians (overall population: OR = 1.11, 95% CI: 1.01–1.22, P = 0.03; whites: OR = 1.16, 95% CI: 0.99–1.36, P = 0.07; Africans: OR = 1.07, 95% CI: 0.65–1.76, P = 0.79; Asians: OR = 1.05, 95% CI: 0.91–1.22, P = 0.51). Interestingly, a dual-null GSTM1–GSTT1 genotype was associated with bladder cancer risk in the overall population and in Asians (overall population: OR = 1.48, 95% CI: 1.15–1.92, P = 0.002; Asians: OR = 1.62, 95% CI: 1.15–2.28, P = 0.006). In conclusion, the GSTM1-null, GSTT1-null and dual-null GSTM1–GSTT1 genotypes might be associated with the onset of bladder cancer, but additional genetic-epidemiological studies should be conducted to explore this association further.

Electronic supplementary material

The online version of this article (10.1186/s12885-018-5014-1) contains supplementary material, which is available to authorized users.

Keywords: Bladder cancer, Gene polymorphism, GSTM1, GSTT1, GSTP1, Meta-analysis

Background

Bladder cancer, also known as urothelial cancer of the bladder, is the most common malignancy affecting the urinary system [1–3]. Treatment of bladder cancer has not advanced in the past 30 years [1]. The disease has a multifactorial etiology that includes environmental factors such as cigarette smoking, arsenic exposure and occupational exposure as well as genetic factors [4–6]. Genetic factors are the one of the most important factors associated with the onset of bladder cancer [7]. Smoking is a major risk factor for the development of this cancer, but the functional consequences of the carcinogens in tobacco smoke in terms of bladder cancer–associated metabolic changes remain poorly defined. Current evidence indicates that some gene polymorphisms are associated with bladder cancer morbidity [8–12].

Glutathione S-transferases (GSTs) play an important role in detoxification of various toxic compounds, such as carcinogens, and are a family of enzymes that include the glutathione S-transferase μ1 (GSTM1), θ1 (GSTT1) and π1 (GSTP1) classes, etc. [13]. They are important phase II detoxifying enzymes that catalyze the conjugation of reduced glutathione (GSH) to hydrophobic, electrophilic xenobiotic substances [14]. Genetic risk to malignant tumors has led to the accumulating attention to the investigations of genes polymorphism involved in process of carcinogenesis [15]. The gene polymorphisms of GSTs might influence the detoxification activities of the enzymes, predisposing individuals to cancers, such as oral squamous-cell carcinoma, gynecological cancer, breast cancer, prostate cancer, hepatocellular carcinoma, and colorectal cancer [16–21].

In the past few decades, most of the epidemiological investigations have focused on the relationship between the null genotypes for GSTM1-GSTT1 and bladder cancer susceptibility. However, available evidence is inadequate due to the sparseness of data or disagreements among reported studies. We performed this meta-analysis to investigate whether the dual-null GSTM1-GSTT1 genotype was associated with bladder cancer susceptibility.

Methods

Search strategy

We retrieved relevant published articles from the electronic databases of PubMed, Embase, the Cochrane Library and the China Biological Medicine Database (CBM-disc) on July 1, 2017, and we recruited eligible original articles for our meta-analysis. Key search terms consisted of [“glutathione S-transferases” OR “GSTs” OR “GSTM1” OR “GSTT1”] and [“bladder cancers” OR “bladder cancer”]. We identified additional articles through references cited in retrieved articles, and we also examined citations of retrieved articles and the previous meta-analyses.

Inclusion and exclusion criteria

Inclusion criteria

(1) The endpoint of each study had to be bladder cancers. (2) The study had to include 2 comparison groups (bladder cancers vs. controls). (3) The study had to provide detailed data on genotype distribution.

Exclusion criteria

(1) Case reports, review articles and editorials. (1) Preliminary results not focused on GSTM1, GSTT1 or outcome. (3) Investigating the relationship of GST gene expression to disease. (4) Multiple publications.

Quality appraisal

To evaluate the quality of the recruited articles that met the above-listed inclusion criteria, we used a quality score based on 7 aspects of genetic-association studies (Additional file 1: Table S1). Thakkinstian et al. [22] created the quality score form in 2005; its range spans from 0 (worst quality) to 12 (best quality). Two researchers who were responsible for literature retrieval appraised quality independent of one another, and a discussion was made until every respect was entirely consistent by comparison.

Data extraction and synthesis

Two investigators independently excerpted the following information from each eligible study: first author’s surname, year of publication, and number of cases and controls for both the GSTM1 and GSTT1 genotypes. We calculated frequencies for both the disease group and the control group from the corresponding genotype distribution. Finally, we compared the results and resolved any disagreements by discussion. We tested the consistency of the data extracted by the 2 researchers, and any disagreement was again resolved by discussion.

Statistical analysis

We performed all statistical analyses using Cochrane Review Manager Software, version 5 (RevMan 5; Cochrane Library, UK). We used I2 to test heterogeneity among the included studies, and we counted the pooled statistic using a fixed-effects model (Cochran–Mantel–Haenszel method), but switched to a random-effects model (DerSimonian–Laird method) when the P-value of the heterogeneity test was < 0.1. Results were expressed with odds ratios (ORs) for dichotomous data, and we also calculated 95% confidence intervals (CIs). P < 0.05 was required for the pooled OR to be statistically significant. We graphically judged publication bias from the Begg adjusted-rank correlation test [23] and the Egger regression asymmetry test [24] using the Stata version 12.0 (Stata Corporation, College Station, TX), and P-values < 0.1 were considered significant.

Results

Study characteristics for the GSTM1-null genotype and bladder cancer risk

We included 72 studies [25–96], which contained 20,239 case series and 24,393 controls, in our assessment of the relationship between the GSTM1-null genotype and bladder cancer susceptibility (Fig. 1 and Table 1). We extracted data of interest: first author’s surname, year of publication and number of cases and controls for the GSTM1-null genotype (Table 1). Average distribution frequency of the GSTM1-null genotype was 56.15% in the bladder cancer group and 46.97% in the control group, indicating that the GSTM1-null genotype was higher in the bladder cancer cases than in the controls (case/control = 1.20).

Fig. 1.

Fig. 1

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Flow chart of the study search and selection

Table 1.

Characteristics of the studies evaluating effects of the GSTM1-null genotypes on bladder carcinogen risk

Author, year Country Ethnicity Source of controls Quality Score Case Control
– + total – + total
Bell 1993 USA Overall Population-based 9 111 89 200 85 115 200
Caucasian Population-based 61 39 100 50 50 100
African Population-based 50 50 100 35 65 100
Daly 1993 UK Caucasian Population-based 4 45 8 53 31 27 58
Zhong 1993 UK Caucasian Hospital-based 4 39 58 97 94 131 225
Lin 1994 USA, etc Overall Population-based 6 61 46 107 442 473 915
Caucasian Population-based 52 37 89 236 243 479
Asian Population-based 5 1 6 179 170 349
African Population-based 4 8 12 27 60 87
Okkels 1996 Denmark Caucasian Hospital-based 7 133 100 233 100 100 200
Anwar 1996 Egypt African Population-based 9 19 3 22 10 11 21
Brockmoller 1996 Germany Caucasian Hospital-based 8 217 157 374 192 181 373
Lafuente 1996 Egypt African Population-based 5 39 27 66 28 27 55
Katoh 1998 Japan Asian Hospital-based 9 66 46 112 50 62 112
Abdel-Rahman 1998 Egypt African Hospital-based 8 26 11 37 15 19 34
Salagovic 1999 Slovakia Caucasian Hospital-based 6 40 36 76 123 125 248
Mungan 2000 Netherlands Caucasian Hospital-based 4 38 23 61 30 39 69
Peluso 2000 Italy Caucasian Hospital-based 5 61 69 130 29 25 54
Schnakenberg 2000 Germany Caucasian Population-based 6 93 64 157 129 94 223
Steinhoff 2000 Germany Caucasian Hospital-based 7 80 55 135 57 70 127
Georgiou 2000 Greece Caucasian Hospital-based 6 56 33 89 56 91 147
Kim 2000 Korea Asian Hospital-based 6 78 34 112 128 97 225
Toruner 2001 Turkey Asian Hospital-based 8 75 46 121 55 66 121
Aktas 2001 Turkey Asian Population-based 4 56 47 103 70 132 202
Giannakopoulos 2002 Greece Caucasian Hospital-based 6 56 33 89 56 91 147
Kim 2002 Korea Asian Population-based 8 138 78 216 265 184 449
Lee 2002 Korea Asian Hospital-based 8 149 83 232 86 79 165
Ma 2002 China Asian Population-based 8 180 137 317 99 83 182
Schroeder 2003 USA Mix Hospital-based 8 137 93 230 101 112 213
Jong 2003 Korea Asian Population-based 9 75 51 126 99 105 204
Moore 2004 USA Mix Population-based 8 54 52 106 49 60 109
Srivastava 2004 India Asian Hospital-based 7 42 64 106 54 128 182
Hung 2004 France Caucasian Hospital-based 7 132 69 201 112 102 214
Saad 2005 UK Caucasian Population-based 8 45 27 72 40 41 81
Srivastava 2005 India Asian Population-based 10 140 230 370 43 63 106
Sobti 2005 India Asian Population-based 9 37 63 100 24 52 76
Garcia-Closas 2005 Spain Caucasian Hospital-based 9 716 422 1138 571 561 1132
Karagas 2005 USA Mix Population-based 9 210 134 344 309 233 542
Kim 2005 Korea Asian Hospital-based 7 92 61 153 73 80 153
McGrath 2006 USA Mix Population-based 11 109 82 191 483 439 922
Ouerhani 2006 Tunisia African Population-based 6 39 23 62 36 43 79
Murta-Nascimento 2007 Spain Caucasian Hospital-based 8 428 251 679 367 368 735
Moore 2007 Spain Caucasian Hospital-based 7 683 394 1077 524 498 1022
Cengiz 2007 Turkey Caucasian Hospital-based 6 34 17 51 22 31 53
Kellen 2007 Belgium Caucasian Population-based 8 312 267 579 597 466 1063
Zhao 2007 USA Caucasian Hospital-based 8 324 298 622 317 316 633
Shao 2008 China Asian Hospital-based 10 85 117 202 81 191 272
Yuan 2008 USA Mix Population-based 11 387 275 662 335 351 686
Covolo 2008 Italy Caucasian Hospital-based 7 128 69 197 111 100 211
Golka 2008 Germany Caucasian Hospital-based 7 184 109 293 88 88 176
Song 2009 China Asian Hospital-based 11 131 77 208 108 104 212
Altayli 2009 Turkey Caucasian Hospital-based 7 58 77 135 65 63 128
Grando 2009 Brazil Mix Population-based 7 40 60 100 33 67 100
Lin 2009 USA Mix Population-based 9 312 292 604 286 324 610
Zupa 2009 Italy Caucasian Population-based 8 13 10 23 68 53 121
Abd 2010 Egypt African Hospital-based 6 11 9 20 9 11 20
Moore 2011 USA Mix Hospital-based 10 653 400 1053 690 545 1235
Öztürk 2011 Turkey Caucasian Population-based 8 98 78 176 51 46 97
Rouissi 2011 Tunisia African Population-based 7 63 62 125 56 69 125
Salinas-Sonchez 2011 Spain Caucasian Hospital-based 5 109 92 201 78 115 193
Goerlitz 2011 Egypt African Hospital-based 9 344 274 618 332 289 621
Marenne 2012 Spain Caucasian Hospital-based 7 488 285 773 402 357 759
Ovsiannikov 2012 Germany Caucasian Hospital-based 6 102 94 196 123 112 235
Schwender 2012 Germany Caucasian Hospital-based 7 909 663 1572 863 876 1739
Henriquez-Hernondez 2012 Spain Caucasian Hospital-based 8 23 67 90 17 64 81
Lesseur 2012 New Hampshire Caucasian Hospital-based 9 378 275 653 508 420 928
Zhang 2012 USA Mix Hospital-based 10 381 329 710 402 380 782
Matic 2013 Serbia Caucasian Hospital-based 8 111 90 201 61 61 122
Savic-Radojevic 2013 Serbia Caucasian Hospital-based 6 45 35 80 32 28 60
Safarinejad 2013 Iran Asian Hospital-based 10 50 116 166 93 239 332
Wang 2013 China Asian Hospital-based 7 699 351 1050 834 570 1404
Berber 2013 Turkey Caucasian Hospital-based 7 54 60 114 51 63 114
Kang 2013 Korea Asian Hospital-based 9 65 45 110 103 117 220
Reszka 2014 Poland Caucasian Population-based 9 149 95 244 165 200 365
Ceylan 2015 Turkey Caucasian Hospital-based 8 22 43 65 31 39 70
Elhawary 2017 Saudi Arabia Asian Hospital-based 7 24 28 52 40 64 104
Ali 2017 Pakistan Asian Population-based 11 83 117 200 57 143 200
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In the subgroup of patients and controls who smoked cigarettes, we included 24 studies [25, 30, 34, 35, 42, 43, 47, 48, 50, 51, 54–56, 64, 65, 68, 69, 73, 76, 83, 85, 91, 92, 95] (data not shown) containing 3724 case series and 3160 controls. Average distribution frequency of the GSTM1-null genotype was 55.67% in the bladder cancer group and 47.57% in the control group, indicating that the GSTM1-null genotype was significantly higher in the bladder cancer cases compared with the controls (case/control = 1.17).

Study characteristics for GSTT1-null genotype and bladder cancer risk

We included 61 studies [29, 32–34, 36–40, 42–45, 47–53, 55–61, 63–69, 72–74, 76, 77, 79, 83–86, 89, 91, 92, 95–108] containing 13,041 case series and 16,739 controls in our assessment of the relationship between the GSTT1-null genotype and bladder cancer risk (Fig. 1 and Table 2). Average distribution frequency of the GSTT1-null genotype was 29.58% in the bladder cancer group and 26.67% in the control group, indicating that the GSTT1 -null genotype was higher in the bladder cancer cases compared with the controls (case/control = 1.11).

Table 2.

Characteristics of the studies evaluating effects of the GSTT1-null genotype of on bladder carcinogen risk

Author, Year Country Ethnicity Source of controls Quality score Case Control
– + total – + total
Brockmoller 1996 Germany Caucasian Hospital-based 8 66 308 374 78 295 373
Kempkes 1996 Germany Caucasian Population-based 7 20 93 113 31 139 170
Abdel-Rahman 1998 Egypt African Hospital-based 8 17 20 37 5 29 34
Katoh 1998 Japan Caucasian Hospital-based 9 46 66 112 59 53 112
Kim 1998 Korea Asian Hospital-based 7 18 49 67 29 38 67
Lee 1999 Korea Asian Hospital-based 7 93 65 158 66 65 131
Salagovic 1999 Slovakia Caucasian Hospital-based 6 21 55 76 42 206 248
Georgiou 2000 Greece Caucasian Hospital-based 6 5 84 89 16 131 147
Peluso 2000 Italy Caucasian Hospital-based 5 14 108 122 6 48 54
Kim 2000 Korea Asian Hospital-based 6 47 65 112 101 119 220
Steinhoff 2000 Germany Caucasian Hospital-based 7 20 115 135 17 110 127
Schnakenberg 2000 Germany Asian Hospital-based 6 28 129 157 48 175 223
Toruner 2001 Turkey Asian Hospital-based 8 24 97 121 21 100 121
Giannakopoulos 2002 Greece Caucasian Hospital-based 6 5 84 89 16 131 147
Lee 2002 Korea Asian Hospital-based 8 135 97 232 85 80 165
Ma 2002 China Asian Population-based 8 29 32 61 88 94 182
Kim 2002 Korea Asian Population-based 8 91 125 216 228 221 449
Gago-Dominguez 2003 USA Mix Population-based 8 50 146 196 34 142 176
Jong 2003 Korea Asian Hospital-based 9 68 58 126 113 91 204
Chen 2004 China Asian Population-based 8 32 30 62 51 30 81
Moore 2004 USA Mix Population-based 8 17 89 106 12 97 109
Hung 2004 France Caucasian Hospital-based 7 43 158 201 33 181 214
Srivastava 2004 India Asian Hospital-based 7 28 78 106 29 153 182
Sanyal 2004 Sweden Caucasian Population-based 8 66 204 270 12 110 122
Broberg 2005 Sweden Caucasian Population-based 9 7 54 61 22 132 154
Garcia-Closas 2005 Spain Caucasian Hospital-based 9 230 899 1129 248 873 1121
Saad 2005 UK Caucasian Population-based 8 26 46 72 14 67 81
Karagas 2005 USA Mix Population-based 9 53 83 136 301 458 759
Golka 2005 Dortmund Caucasian Hospital-based 8 30 106 136 38 125 163
Kim 2005 Korea Asian Hospital-based 7 71 82 153 89 64 153
Srivastava 2005 India Asian Population-based 10 28 78 106 79 291 370
Shao 2005 China Asian Population-based 7 204 201 405 195 194 389
Sobti 2005 India Asian Population-based 9 30 70 100 11 65 76
McGrath 2006 USA Mix Population-based 11 35 156 191 148 776 924
Ouerhani 2006 Tunisia African Population-based 6 26 36 62 35 44 79
Kogevinas 2006 Spain Caucasian Hospital-based 8 24 75 99 17 74 91
Cengiz 2007 Turkey Caucasian Hospital-based 6 18 33 51 11 42 53
Kellen 2007 Belgium Caucasian Population-based 8 30 164 194 61 319 380
Zhao 2007 USA Caucasian Hospital-based 8 103 520 623 115 519 634
Covolo 2008 Italy Caucasian Hospital-based 7 42 155 197 33 178 211
Yuan 2008 USA Mix Population-based 11 140 518 658 124 556 680
Song 2008 China Asian Hospital-based 7 71 37 108 58 54 112
Altayli 2009 Turkey Caucasian Hospital-based 7 31 104 135 9 119 128
Grando 2009 Brazil Mix Population-based 7 51 49 100 37 63 100
Song 2009 China Asian Hospital-based 11 110 98 208 105 107 212
Cantor 2010 Spain Caucasian Hospital-based 9 136 542 678 160 550 710
Moore 2011 USA Mix Hospital-based 10 210 794 1004 237 942 1179
Rouissi 2011 Tunisia African Population-based 7 30 95 125 38 87 125
Goerlitz 2011 Egypt African Hospital-based 9 147 470 617 156 464 620
Salinas-Sánchez 2011 Spain Caucasian Hospital-based 5 42 148 190 25 138 163
Lesseur 2012 New Hampshire Caucasian Hospital-based 9 106 556 662 143 780 923
Ovsiannikov 2012 Germany Caucasian Hospital-based 6 33 163 196 47 188 235
Henriquez-Hernondez 2012 Spain Caucasian Hospital-based 8 60 30 90 40 41 81
Berber 2013 Turkey Caucasian Hospital-based 7 31 83 114 16 98 114
Matic 2013 Serbia Caucasian Hospital-based 8 56 145 201 34 88 122
Safarinejad 2013 Iran Asian Hospital-based 10 35 131 166 69 263 332
Kang 2013 Korea Asian Hospital-based 9 64 46 110 128 92 220
Reszka 2014 Poland Caucasian Population-based 9 30 212 242 77 288 365
Ceylan 2015 Turkey Caucasian Hospital-based 8 19 46 65 9 61 70
Ali 2017 Pakistan Asian Population-based 11 34 166 200 26 174 200
Elhawary 2017 Saudi Arabia Asian Hospital-based 7 6 46 52 8 96 104
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In the subgroup of patients and controls who smoked cigarettes, we included 21 studies [34, 42, 43, 47, 48, 50, 51, 55, 56, 64, 65, 68, 69, 73, 76, 83, 85, 91, 92, 95, 97] (data not shown) containing 3170 case series and 2793 controls. Average distribution frequency of the GSTT1-null genotype was 29.29% in the bladder cancer group and 28.65% in the control group-that is, similar in both groups (case/control = 1.02).

Study characteristics for the dual-null GSTM1-GSTT1 genotype and bladder cancer risk

We included 18 studies [32, 37, 39, 43, 47, 48, 52, 55, 58, 60, 63, 65, 67, 79, 84, 85, 89, 96] containing 2426 case series and 3874 controls in our assessment of the relationship between the dual-null GSTM1-GSTT1 genotype and bladder cancer risk (Fig. 1 and Table 3). Average distribution frequency of the dual-null GSTM1-GSTT1 genotype was 16.78% in the bladder cancer group and 11.45% in the control group. Therefore, the dual-null GSTM1-GSTT1 genotype was significantly higher in the bladder cancer cases compared with the controls (case/control = 1.47).

Table 3.

Characteristics of the studies evaluating effects of the GSTM1-GSTT1 dual-null genotype on bladder carcinogen risk

Author, Year Country Ethnicity Source of controls Quality score Case Control
null-null non-null-null total null-null non-null-null total
Abdel-Rahman 1998 Egypt African Hospital-based 8 14 23 37 3 31 34
Steinhoff 2000 Germany Caucasian Hospital-based 7 12 123 135 4 123 127
Schnakenberg 2000 Germany Caucasian Population-based 6 12 145 157 31 192 223
Ma 2002 China Asian Population-based 8 16 45 61 54 128 182
Lee 2002 Korea Asian Hospital-based 8 83 149 232 37 128 165
Srivastava 2004 India Asian Hospital-based 7 16 90 106 9 173 182
Moore 2004 USA Mix Population-based 8 9 97 106 6 103 109
Hung 2004 France Caucasian Hospital-based 7 28 173 201 19 195 214
Srivastava 2005 India Asian Population-based 10 17 89 106 32 338 370
McGrath 2006 USA Mix Population-based 11 18 173 191 78 844 922
Song 2009 China Asian Hospital-based 11 77 131 208 50 162 212
Salinas-Sonchez 2011 Spain Caucasian Hospital-based 5 20 131 151 6 88 94
Ovsiannikov 2012 Germany Caucasian Hospital-based 6 17 179 196 29 206 235
Henriquez-Hernondez 2012 Spain Caucasian Hospital-based 8 17 73 90 8 73 81
Berber 2013 Turkey Caucasian Hospital-based 7 11 103 114 7 107 114
Safarinejad 2013 Iran Asian Hospital-based 10 38 128 166 73 259 332
Ceylan 2015 Turkey Caucasian Hospital-based 8 8 57 65 8 62 70
Elhawary 2017 Saudi Arabia Asian Hospital-based 7 0 104 104 0 208 208
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Association of the GSTM1-null genotype with bladder cancer risk

In this meta-analysis, we found that the GSTM1-null genotype was associated with bladder cancer risk in the overall population, and individually in whites, Africans and Asians (overall population: OR = 1.40, 95% CI: 1.31–1.48, P<0.00001; whites: OR = 1.39, 95% CI: 1.26–1.54, P<0.00001; Africans: OR = 1.54, 95% CI: 1.16–2.05, P = 0.003; Asians: OR = 1.45, 95% CI: 1.33–1.59, P<0.00001); as well as in controls from both hospital-based and population-based studies that included both high- and low-quality studies (Fig. 2 for the overall population; Table 4). In the meta-analysis for all patients and controls who smoked cigarettes, we found that the GSTM1-null genotype was associated with bladder cancer risk in the overall population, Asians and controls from both hospital-based and population-based studies that included both high- and low-quality studies. However, we did not find this relationship in whites or Africans (Table 4).

Fig. 2.

Fig. 2

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Association between the GSTM1-null genotype and bladder cancer susceptibility in the overall population

Table 4.

Meta-analysis of the association of null genotypes of GSTM1, GSTT1 and dual-null genotype of GSTM1/GSTT1 with bladder carcinogens risk

Genetic contrasts Group and subgroups Studies Number Q test P value Model selected OR (95% CI) P
GSTM1
 - vs + Overall 72 <0.00001 Random 1.40 (1.31,1.48) <0.00001
Caucasian 37 <0.00001 Random 1.39 (1.26,1.54) <0.00001
Asian 20 0.39 Fixed 1.45 (1.33,1.59) <0.00001
African 9 0.10 Random 1.54 (1.16,2.05) 0.003
Hospital-based 46 0.0001 Random 1.42 (1.32,1.52) <0.00001
Population-based 26 0.003 Random 1.36 (1.21,1.53) <0.00001
High quality 54 0.0002 Random 1.37 (1.28,1.45) <0.00001
Low quality 18 0.0009 Random 1.58 (1.29,1.94) <0.0001
GSTM1 (smoking)
 - vs + Overall 24 0.02 Random 1.37 (1.19,1.59) <0.0001
Caucasian 10 0.007 Random 1.17 (0.85,1.59) 0.33
Asian 7 0.63 Fixed 1.67 (1.32,2.11) <0.0001
African 3 0.22 Fixed 1.44 (0.95,2.17) 0.08
High quality 17 0.02 Random 1.35 (1.14,1.60) 0.0005
Low quality 7 0.27 Fixed 1.48 (1.12,1.96) 0.006
GSTT1
 - vs + Overall 61 <0.00001 Random 1.11 (1.01,1.22) 0.03
Caucasian 29 <0.00001 Random 1.16 (0.99,1.36) 0.07
Asian 21 0.01 Random 1.05 (0.91,1.22) 0.51
African 4 0.03 Random 1.07 (0.65,1.76) 0.79
Hospital-based 40 <0.0001 Random 1.11 (0.99,1.24) 0.07
Population-based 21 0.0002 Random 1.12 (0.94,1.35) 0.20
High quality 52 <0.00001 Random 1.14 (1.03,1.26) 0.01
Low quality 9 0.23 Fixed 0.93 (0.75,1.14) 0.49
GSTT1 (smoking)
Overall 21 0.67 Fixed 1.06 (0.93,1.20) 0.38
Caucasian 9 0.84 Fixed 1.14 (0.91,1.43) 0.24
Asian 7 0.62 Fixed 1.00 (0.77,1.30) 0.99
African 2 0.41 Fixed 0.60 (0.36,1.02) 0.06
High quality 16 0.52 Fixed 1.06 (0.93,1.22) 0.37
Low quality 5 0.64 Fixed 1.01 (0.70,1.48) 0.94
Dual-null genotype of GSTM1/GSTT1
Overall 18 0.003 Random 1.48 (1.15,1.92) 0.002
Caucasian 8 0.03 Random 1.30 (0.83,2.03) 0.25
Asian 7 0.04 Random 1.62 (1.15,2.28) 0.006
Hospital-based 13 0.03 Random 1.71 (1.28,2.28) 0.0003
Population-based 5 0.06 Random 1.07 (0.67,1.71) 0.77
High quality 15 0.11 Fixed 1.61 (1.36,1.91) <0.00001
Low quality 3 0.04 Random 0.86 (0.40,1.85) 0.70
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Association of the GSTT1-null genotype with bladder cancer risk

In this study, we found that the GSTT1-null genotype was associated with bladder cancer risk in the overall population, and controls from hospital-based studies that included high-quality studies; but not with bladder cancer risk in whites, Africans, Asians or controls from population-based studies that included low-quality studies (overall population: OR = 1.11, 95% CI: 1.01–1.22, P = 0.03; whites: OR = 1.16, 95% CI: 0.99–1.36, P = 0.07; Africans: OR = 1.07, 95% CI: 0.65–1.76, P = 0.79; Asians: OR = 1.05, 95% CI: 0.91–1.22, P = 0.51; Fig. 3 for overall population; Table 4). However, in controls from either hospital-based or population-based studies that included both high- and low-quality studies, or in the meta-analysis for all patients and controls who smoked cigarettes, we found that the GSTT1-null genotype was not associated with bladder cancer risk in the overall population, or in individual white, African or Asian populations (Table 4).

Fig. 3.

Fig. 3

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Association between the GSTT1-null genotype and bladder cancer susceptibility in the overall population

Association of dual-null GSTM1-GSTT1 genotype with bladder cancer risk

We found an association between the dual-null GSTM1-GSTT1 genotype and bladder cancer risk in the overall population, Asians and controls from hospital-based studies that included high-quality studies (overall population: OR = 1.48, 95% CI: 1.15–1.92, P = 0.002; Asians: OR = 1.62, 95% CI: 1.15–2.28, P = 0.006; Fig. 4 for overall population; Table 4). However, the dual-null GSTM1-GSTT1 genotype was not associated with onset of bladder cancer in whites or in controls from population-based studies that included low-quality studies (whites: OR = 1.30, 95% CI: 0.83–2.03, P = 0.25; Table 4).

Fig. 4.

Fig. 4

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Association between the dual-null GSTM1–GSTT1 genotype and bladder cancer risk in the overall population

Evaluation of publication bias

We performed a publication bias test for the association of the GSTM1-null, GSTT1-null and dual-null GSTM1-GSTT1 genotypes with bladder cancer risk in the overall population. There was no bias for the association of the dual-null GSTM1-GSTT1 genotype with bladder cancer risk, but there was for the GSTM1- and GSTT1-null genotypes (GSTM1-null: Begg P = 0.100, Egger P = 0.052; GSTT1-null: Begg P = 0.001, Egger P = 0.002; dual-null GSTM1–GSTT1: Begg P = 0.343, Egger P = 0.236; Fig. 5).

Fig. 5.

Fig. 5

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Publication bias. a GSTM1-null genotype. b GSTT1-null genotype. c Dual-null GSTM1–GSTT1 genotype

Discussion

Research on single-nucleotide polymorphisms have focused mainly on their impact on tumor suppressor genes, metabolic-enzyme genes, and DNA repair genes, etc. Understanding disease susceptibility and pathogenesis and using them to guide diagnosis and individual treatment choice constitute an important new therapeutic approach [109]. In this study, we found that the average distribution frequency of the GSTM1-null genotype was significantly higher in bladder cancer cases than in controls (case/control = 1.20). In the subgroup of patients and controls who smoked cigarettes, it was also higher in the bladder cancer case group compared with the control group (case/control = 1.17). This might indicate that the GSTM1-null genotype was associated with bladder cancer risk in the overall population, including whites, Africans, Asians, and controls from both hospital-based and population-based studies that included both high- and low-quality studies. In the meta-analysis for all patients and controls who smoked cigarettes, we found that the GSTM1-null genotype was associated with bladder cancer risk in the overall population, Asians, and controls from both hospital-based and population-based studies that included both high- and low-quality studies. The sample size of our meta-analysis was larger than those of other meta-analyses [61, 110–112], and therefore our results might be more robust. However, our tests for publication bias, the GSTM1 studies were found to be positive. Therefore, the positive association between the GSTM1-null genotype and bladder cancer should be reassessed in the future.

The average distribution frequency of the GSTT1-null genotype was higher in the bladder cancer case group than in the control group (case/control = 1.11). In the subgroup of patients and controls who smoked cigarettes, it was similar in both groups (case/control = 1.02). This might tell us that the GSTT1-null genotype was associated with bladder cancer risk. For confirmation, we performed a meta-analysis, which further showed the GSTT1-null genotype to be associated with bladder cancer risk in the overall population, whites and controls from hospital-based studies that included high-quality studies. In the meta-analysis for all patients and controls who smoked cigarettes, we found that the GSTT1-null genotype was not associated with bladder cancer risk in the overall population, whites, Africans, Asians or controls from both hospital-based and population-based studies that included both high- and low-quality studies. Our results indicate that the GSTT1-null genotype does not predict the risk of bladder cancer. The sample size of our meta-analysis was larger than those of other meta-analyses [111, 112], suggesting that our conclusion might be more robust. However, publication bias was also found for GSTT1. Therefore, further studies are required.

Average distribution frequency of the dual-null GSTM1-GSTT1 genotype in the bladder cancer group was slightly higher than in the control group (case/control = 1.47), indicating a possible association between the dual-null GSTM1-GSTT1 genotype and bladder cancer risk. Meta-analysis further revealed an association between the dual-null GSTM1-GSTT1 genotype and bladder cancer risk in the overall population, Asians and controls from hospital-based studies that included high-quality studies. No publication bias was found for this meta-analysis, and the conclusion was robust.

In a previous study, García-Closas et al. [61] conducted a meta-analysis of 28 studies of GSTM1 and reported that the GSTM1-null genotype both increased the overall risk of bladder cancer and posed similar relative risks for both smokers and non-smokers. This finding suggested that GSTM1 lowers the risk of bladder cancer through mechanisms that are not specific to the detoxification of polycyclic aromatic hydrocarbons in tobacco smoke. Engel et al. [110] performed a meta-analysis of GSTM1 and bladder cancer that included 17 studies and reported that the GSTM1-null status is associated with a modest increase in the risk of bladder cancer, and that there was no evidence of multiplicative interaction between the GSTM1-null genotype and once and current smoking in relation to bladder cancer. A meta-analysis by Yu et al. [112] included 48 case–control studies for GSTM1-null and 57 studies for GSTT1, and suggested that the GSTM1- and GSTT1-null genotypes might both be related to higher bladder cancer risk. Yu et al. [111] also performed a meta-analysis to investigate the association between GSTM1-GSTT1 deletion polymorphisms and bladder cancer susceptibility, including 46 studies of GSTM1-null, 54 of GSTT1 and 10 of dual-null GSTM1-GSTT1. All 3 genotypes were associated with increased bladder cancer risk. In our meta-analysis, we included 72 studies for GSTM1-null, 62 for GSTT1-null and 18 for dual-null GSTM1-GSTT1 genotypes. These results from the meta-analyses mentioned above were similar to our results. However, the sample size of our meta-analysis was larger than the previous meta-analyses, and the results from our studies might be more robust. Furthermore, we initially conducted a meta-analysis that showed no evidence of multiplicative interaction between the GSTT1-null genotype and smoking in relation to bladder cancer.

Smoking is a known risk factor for bladder cancer [113], and the products of GSTs help detoxify the polycyclic aromatic hydrocarbons found in tobacco smoke [114]. Our study suggests that the GSTM1-null genotype might play a role in such detoxification, but the GSTT1-null genotype does not. However, more studies should be conducted to confirm this.

GSTM1-null, GSTT1-null and dual-null GSTM1-GSTT1 genotypes play an important role in detoxification of various toxic compounds, such as carcinogens. In this meta-analysis, it indicated that GSTM1-null, GSTT1-null and dual-null GSTM1-GSTT1 genotypes were risk factors to susceptibility of bladder cancer, and took part in the pathogenesis of bladder cancer.

There were limitations in our meta-analysis. First, age might be a source of heterogeneity, but it was difficult to stratify the different ages in the reports prior to pooling the results, for the reason that the ages from most of the included studies were different. So, no conclusions can be drawn regarding the impact of GSTs on age of onset. Furthermore, heterogeneity and publication bias were both significant for GSTM1-null and GSTT1-null. Subgroup analyses were performed to find out any effect modifier, but the reason was not clear.

Conclusion

Our results supported that the GSTM1-null, GSTT1-null and dual-null GSTM1–GSTT1 genotypes might be associated with the onset of bladder cancers. However, more association investigations are required to further clarify these relationships.

Additional file

Additional file 1: (42KB, doc)

Table S1. Scale for Quality Assessment. (DOC 42 kb)

Acknowledgements

Not applicable.

Funding

This study was supported by Guangzhou Medical Key Discipline Construction Project. The funding paid the publication fee for this paper.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Authors’ contributions

TBZ was in charge of conceived and designed the study. TBZ, HYL, WJX, ZQZ, HZZ were responsible for collection of data and performing the statistical analysis and manuscript preparation. TBZ and ZJL were responsible for checking the data. All authors were responsible for drafting the manuscript, read and approved the final version.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Tianbiao Zhou, Email: zhoutb@aliyun.com.

Hong-Yan Li, Email: lihy0726@126.com.

Wei-Ji Xie, Email: weijixiest@126.com.

Zhiqing Zhong, Email: zhiqingzhongstu@163.com.

Hongzhen Zhong, Email: hongzhenzhongstu@163.com.

Zhi-Jun Lin, Email: zhijunlin@yeah.net.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Additional file 1: (42KB, doc)

Table S1. Scale for Quality Assessment. (DOC 42 kb)

Data Availability Statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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