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  • Research article
  • Open Access
  • Open Peer Review

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

Contributed equally
BMC Cancer201818:1088

https://doi.org/10.1186/s12885-018-5014-1

  • Received: 16 November 2017
  • Accepted: 30 October 2018
  • Published:
Open Peer Review reports

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.

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 [13]. 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 [46]. 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 [812].

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 [1621].

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 [2596], 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

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

In the subgroup of patients and controls who smoked cigarettes, we included 24 studies [25, 30, 34, 35, 42, 43, 47, 48, 50, 51, 5456, 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, 3234, 3640, 4245, 4753, 5561, 6369, 7274, 76, 77, 79, 8386, 89, 91, 92, 95108] 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

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

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

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

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

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

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

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, 110112], 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.

Notes

Declarations

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.

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Authors’ Affiliations

(1)
Department of Nephrology, The Second Affiliated Hospital of Shantou University Medical College, Shantou, 515041, China
(2)
Department of Nephrology, Huadu District People’s Hospital of Guangzhou, Southern Medical University, Guangzhou, China

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