Advertisement

BMC Medical Genetics

, 20:22 | Cite as

Glutathione S-transferase pi 1 variant and squamous cell carcinoma susceptibility: a meta-analysis of 52 case-control studies

  • Shuang Wang
  • Jingqi Zhang
  • Fan Jun
  • Zhijie BaiEmail author
Open Access
Research article
  • 147 Downloads
Part of the following topical collections:
  1. Genetic epidemiology and genetic associations

Abstract

Background

There are several meta-analyses on the genetic relationship between the rs1695 polymorphism within the GSTP1 (glutathione S-transferase pi 1) gene and the risk of different SCC (squamous cell carcinoma) diseases, such as ESCC (oesophageal SCC), HNSCC (head and neck SCC), LSCC (lung SCC), and SSCC (skin SCC). Nevertheless, no unified conclusions have been drawn.

Methods

Herein, an updated meta-analysis was performed to evaluate the probable impact of GSTP1 rs1695 on the susceptibility to different SCC diseases under six genetic models (allele, carrier, homozygote, heterozygote, dominant, and recessive). Three online databases, namely, PubMed, WOS (Web of Science), and Embase (Excerpta Medica Database), were searched.

Results

Initially, we obtained a total of 497 articles. Based on our selection criteria, we eventually included 52 case-control studies (9763 cases/15,028 controls) from 47 eligible articles. As shown in the pooling analysis, there was no difference in the risk of overall SCC disease between cases and controls [allele, Pa (P value of association test) = 0.601; carrier, Pa = 0.587; homozygote, Pa = 0.689; heterozygote, Pa = 0.167; dominant, Pa = 0.289; dominant, Pa = 0.548]. Similar results were obtained after stratification by race (Asian/Caucasian), genotyping, control source, and disease type (ESCC/HNSCC/LSCC/SSCC) (all Pa > 0.05).

Conclusion

The rs1695 polymorphism within the GSTP1 gene is not associated with the risk of overall SCC or a specific SCC type, including ESCC, HNSCC, LSCC, and SSCC.

Keywords

GSTP1 Polymorphism Squamous cell carcinoma Susceptibility 

Abbreviations

AHR

Aryl hydrocarbon receptor

CADM1

Cell adhesion molecule 1

diASA-AMP

Di-allele-specific- amplification with artificially modified primers assay

Embase

Excerpta Medica Database

ESCC

Oesophageal squamous cell carcinoma

GST

Glutathione S-transferase

GSTA

Glutathione S-transferase alpha

GSTM1

Glutathione S-transferase mu 1

GSTP1

Glutathione S-transferase pi 1

GSTT1

Glutathione S-transferase theta 1

GWAS

Genome-wide association study

HB

Hospital-based

HNSCC

Head and neck squamous cell carcinoma

HWE

Hardy-Weinberg equilibrium

KLF5

Kruppel like factor 5

LSCC

Lung squamous cell carcinoma

MM

Malignant melanoma

OSCC

Oral squamous cell carcinoma

PB

Population-based

PCR

Polymerase chain reaction

PCR-RFLP

Polymerase chain reaction-restriction fragment length polymorphism

SBCC

Skin basal cell carcinoma

SCC

Squamous cell carcinoma

SEC16A

SEC16 homolog A, endoplasmic reticulum export factor

SSCC

Skin squamous cell carcinoma

SSCP

Single-stranded conformational polymorphism

UADTSCC

Upper aerodigestive tract squamous cell carcinoma

WOS

Web of Science

Background

SCC (squamous cell carcinoma), also termed “epidermal carcinoma,” is a malignant tumour that takes part in epidermis or adnexal cells and exhibits distinct degrees of keratosis [1, 2, 3]. SCC exists in the squamous epithelium of several places, e.g., skin, mouth, lung, lips, oesophagus, cervix, and vagina [4, 5, 6]. Based on GWAS (genome-wide association study) data, more and more reported genetic polymorphisms are believed to contribute to the aetiologies of different SCC types. For instance, a series of genes, including CADM1 (cell adhesion molecule 1), AHR (aryl hydrocarbon receptor), and SEC16A (SEC16 homolog A, endoplasmic reticulum export factor), may be related with the risk of SCC [7]. Two variants within the KLF5 (Kruppel-like factor 5) gene on chromosome 13q22.1, namely, rs1924966 and rs115797771, may be relevant to ESCC (oesophageal SCC) susceptibility [8]. Herein, we determined whether GSTP1 (glutathione S-transferase pi 1) gene polymorphism is associated with the susceptibility to different SCC patterns.

GSTP1, a member of the GST (glutathione S-transferase) family in humans, is associated with the biological detoxification or biotransformation process through catalysing the conjugation of many hydrophobic and electrophilic compounds with reduced glutathione [9, 10]. The GSTP1 gene, which is located on human chromosome 11q13, comprises seven exons and six introns [11]. Two common polymorphisms, namely, rs1695 A/G polymorphism in exon five (p.Ile105Val) and rs1138272 C/T polymorphism in exon six (p.Ala114Val), have been reported [12, 13].

Several SCC/GSTP1 rs1695-associated meta-analyses with conflicting conclusions have been reported. For instance, in 2009, Zendehdel et al. enrolled three case-control studies [14, 15, 16], performed a meta-analysis to assess the association between GSTP1 rs1695 and ESCC risk in Caucasian populations, and found a borderline significant association [16]. In 2014, Song et al. enrolled 21 case-control studies to perform a meta-analysis concerning the role of the GSTP1 rs1695 polymorphism in the risk of oesophageal cancers, including EAC (oesophageal adenocarcinoma) and ESCC [17]. The subgroup meta-analysis of ESCC containing thirteen case-control studies showed a positive correlation, particularly in the Caucasian population [17]. However, in 2015, Tan et al. performed another meta-analysis with twenty case-control studies on overall oesophageal cancer and reported negative results in both ESCC and EAC subgroups [18]. Accordingly, we performed an updated meta-analysis with a relatively larger sample size to reevaluate the potential impact of the GSTP1 rs1695 A/G polymorphism on the susceptibility to SCC diseases, mainly including ESCC, SSCC, HNSCC (head and neck SCC), and LSCC (lung SCC).

Methods

Electronic database retrieval

We reviewed three on-line databases, including PubMed, WOS (Web of Science), and Embase (Excerpta Medica Database), through January 2018 using the following main search keywords: Carcinoma, Squamous Cell; Carcinomas, Squamous Cell; Squamous Cell Carcinomas; Squamous Cell Carcinoma; Carcinoma, Squamous; Carcinomas, Squamous; Squamous Carcinoma; Squamous Carcinomas; Carcinoma, Epidermoid; Carcinomas, Epidermoid; Epidermoid Carcinoma; Epidermoid Carcinomas; Carcinoma, Planocellular; Carcinomas, Planocellular; Planocellular Carcinoma; Planocellular Carcinomas; SCC; GSTP1; Glutathione S-Transferase pi; Glutathione S Transferase pi; GST Class-phi; Class-phi, GST; GST Class phi; Glutathione Transferase P1–1; Glutathione Transferase P1 1; Transferase P1–1, Glutathione; GSTP1 Glutathione D-Transferase; D-Transferase, GSTP1 Glutathione; GSTP1 Glutathione D Transferase; Glutathione D-Transferase, GSTP1; Polymorphism; Polymorphism, Genetic; Polymorphisms, Genetic; Genetic Polymorphisms; Genetic Polymorphism; Polymorphism (Genetics); Polymorphisms (Genetics); and Polymorphism; Polymorphisms.

Eligible article screening

We performed a literature search and screened the retrieved articles as per the PRISMA (preferred reporting items for systematic reviews and meta-analyses) guidelines [19]. Selection criteria included duplicated articles; data from animal or cell experiments; meeting abstract or meta-analysis; review, trials or case reports; data of GSTP1 expression; not SCC or GSTP1; lack confirmed histopathological data; combined GA + AA genotype frequency; without the control data; and P value of HWE (Hardy-Weinberg equilibrium) less than 0.05. Eligible case-control studies provided sufficient genotype frequency data of the GSTP1 gene rs1695 polymorphism in each case and control group.

Data extraction

Two investigators independently extracted the data and evaluated the methodological quality of each article by means of the NOS (Newcastle-Ottawa Scale) system. One table contains the following basic information: first author, publication year, region, race, genotyping assay, genotype frequency, disease type, control source, P values of HWE, study number, and sample size of the case/control.

Data synthesis

We utilized STATA software (StataCorp LP, College Station, TX, USA) for the following statistical analyses. The allele (allele G vs. A), carrier (carrier G vs. A), homozygote (GG vs. AA), heterozygote (AG vs. AA), dominant (AG + GG vs. AA), and recessive (GG vs. AA+AG) models were utilized to target the GSTP1 gene rs1695 G/A polymorphism. We calculated the OR (odds ratio), 95% CIs (confidence intervals) and Pa (P value of association test) values to estimate the association. When the Ph (P value of heterogeneity) was > 0.1 or I2 was < 50.0%, a fixed-effects model was adopted. Otherwise, a random-effects model was selected.

Considering the factors of race, genotyping assay, control source, and disease type, we performed the corresponding subgroup meta-analyses. We also carried out Egger’s/Begg’s tests to determine a potential publication bias. The presence of a publication bias was considered when PE (P value of Egger’s test) and PB (P value of Begg’s test) were below 0.05. Sensitivity analysis was applied to assess data stability and robustness.

Results

Article retrieval and screening

The article retrieval and selection processes during our meta-analysis were conducted as described in the flow chart shown in Fig. 1. After our literature search, a total of 497 articles were obtained. Then, 168 articles with duplicated data and 214 articles meeting the exclusion criteria were excluded. Next, we assessed the eligibility of the remaining 115 full-text articles. After the exclusion of 68 ineligible articles, a total of 47 articles containing 52 case-control studies [14, 15, 16, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63] were ultimately recruited for our meta-analysis. Table 1 summarizes the extracted basic information.
Fig. 1

Flow chart of eligible article selection

Table 1

Basic information of the eligible articles in the meta-analysis

First author

Year

Region

Race

Assay

Case

Disease type

Control

Control source

P HWE

AA

AG

GG

AA

AG

GG

Abbas

2004

France

Caucasian

PCR-RFLP

21

21

3

ESCC

59

56

9

PB

0.38

Cabelguenne

2001

France

Caucasian

PCR-RFLP

89

57

16

HNSCC

146

139

25

HB

0.31

Cai

2006

China

Asian

PCR-RFLP

143

58

3

ESCC

265

116

12

PB

0.87

Cho

2006

Korea

Asian

Gene sequencing

201

85

7

HNSCC

211

112

10

HB

0.29

Dura

2013

Netherlands

Caucasian

PCR

48

42

15

ESCC

246

261

84

PB

0.27

Dzian

2012

Netherlands

Caucasian

PCR-RFLP

56

45

11

LSCC

153

115

22

PB/HB

0.95

Evans

2004

USA

Caucasian

PCR-RFLP

123

132

27

HNSCC

97

85

24

PB

0.42

Fryer

2005

Australia

Caucasian

PCR-RFLP

59

51

18

SSCC

95

90

25

HB

0.60

Harth

2008

Germany

Caucasian

PCR-melting-curve

145

122

45

HNSCC

130

138

32

HB

0.62

Jain

2006

India

Asian

PCR-RFLP

46

23

7

ESCC

72

56

9

HB

0.67

Jourenkova

1999a

France

Caucasian

PCR-RFLP

49

53

15

HNSCC

86

64

22

HB

0.07

Jourenkova

1999b

France

Caucasian

PCR-RFLP

62

52

15

HNSCC

86

64

22

HB

0.07

Jourenkova

1998

France

Caucasian

PCR-RFLP

46

41

11

LSCC

86

64

22

HB

0.07

Kelders

2002

Netherlands

Caucasian

PCR-RFLP

36

38

13

HNSCC

26

18

7

HB

0.20

Kihara

1999

Japan

Asian

PCR-RFLP

84

32

9

LSCC

184

65

8

HB

0.45

Larsen

2006

Australia

Caucasian

PCR-RFLP

230

213

51

LSCC

161

169

49a

HB

0.66

  

Australia

Caucasian

PCR-RFLP

230

213

51

LSCC

112

100

35b

PB

0.11

Leichsenring

2006

Brazil

Mixed

PCR-RFLP

30

34

8

HNSCC

30

25

5

PB

0.95

Leite

2007

Brazil

Mixed

PCR-RFLP

14

13

2

SSCC

60

46

18

PB

0.07

Lewis

2002

UK

Caucasian

PCR-RFLP

14

17

1

LSCC

64

74

13

HB

0.19

Li

2010

South African

Black African

PCR-RFLP

56

59

26

ESCC

76

83

27

PB

0.58

   

Mixed

PCR-RFLP

34

52

11

ESCC

30

51

13

PB

0.24

Li

2007

USA

Caucasian

PCR-RFLP

336

356

111

HNSCC

333

385

121

PB

0.57

Liang

2005

China

Asian

diASA-AMP

58

32

4

LSCC

132

86

9

HB

0.27

Liu

2010

China

Asian

PCR-RFLP

66

29

0

ESCC

61

27

3

PB

1.00

Malik

2010

India

Asian

PCR-RFLP

53

36

14

ESCC

111

75

9

PB

0.41

Matejcic

2011

South African

Black African

TaqMan genotyping

79

155

91

ESCC

100

242

132

PB

0.57

  

South African

Mixed

TaqMan genotyping

69

112

48

ESCC

145

191

92

PB

0.05

McWilliams

2000

USA

Mixed

PCR-RFLP

60

73

13

HNSCC

58

51

15

HB

0.47

Miller

2006

USA

Caucasian

PCR-RFLP

190

173

49

LSCC

579

623

141

PB

0.16

Moaven

2010

Iran

Asian

PCR-RFLP

84

50

14

ESCC

74

54

8

PB

0.65

Nazar

2003

USA

Mixed

PCR-RFLP

35

29

9

LSCC

199

234

54

PB

0.23

Olshan

2000

USA

Mixed

PCR-RFLP

40

62

7

HNSCC

68

80

20

HBc

0.63

  

USA

Mixed

PCR-RFLP

18

38

7

HNSCC

7

13

5

HBd

0.82

Oude

2003

Netherlands

Caucasian

PCR-RFLP

116

90

29

HNSCC

125

121

39

PB

0.27

Peters

2006

USA

Mixed

PCR-RFLP

303

311

76

HNSCC

333

329

86

PB

0.73

Ramsay

2001

UK

Caucasian

SSCP

10

10

0

SSCC

53

71

17

HB

0.36

Risch

2001

Germany

Caucasian

PCR-RFLP

76

77

18

LSCC

167

151

35

HB

0.92

Rossini

2007

Brazil

Mixed

PCR-RFLP

42

65

18

ESCC

116

108

28

PB

0.71

Ruwali

2009

India

Caucasian

PCR-RFLP

224

112

14

HNSCC

199

138

13

PB

0.06

Ruwali

2011

India

Caucasian

PCR-RFLP

316

162

22

HNSCC

285

195

20

PB

0.06

Ryberg

1997

Norway

Caucasian

PCR-RFLP

20

34

13

LSCC

153

117

27

PB

0.50

Schneider

2004

Germany

Caucasian

PCR-melting-curve

81

75

27

LSCC

298

254

70

PB/HB

0.16

Soucek

2010

Czech/Polish

Caucasian

TaqMan drug metabolism genotyping

56

53

7

HNSCC

57

50

10

PB

0.52

Soya

2007

India

Asian

PCR-RFLP

219

162

27

UADTSCC

120

88

12

PB

0.42

Stücker

2002

France

Caucasian

PCR-RFLP

54

46

15

LSCC

124

120

20

HB

0.22

Tan

2000

China

Asian

PCR-RFLP

93

48

9

ESCC

91

53

6

PB

0.62

To

2002

Spain

Caucasian

PCR-RFLP

101

84

19

HNSCC

100

78

23

PB

0.20

To

1999

Spain

Caucasian

PCR-RFLP

29

20

3

LSCC

64

54

14

PBb

0.61

  

Spain

Caucasian

PCR-RFLP

29

20

3

LSCC

90

90

20

PBe

0.72

van

1999

Netherlands

Caucasian

PCR-RFLP

5

6

2

ESCC

146

89

12

PB

0.74

Zendehdel

2009

Sweden

Caucasian

Pyrosequencing

26

42

10

ESCC

208

207

38

PB

0.18

PCR polymerase chain reaction, PCR-RFLP polymerase chain reaction-restriction fragment length polymorphism, diASA-AMP di-allele-specific-amplification with artificially modified primers assay, SSCP Single-stranded conformational polymorphism, ESCC oesophageal squamous cell carcinoma, HNSCC head and neck squamous cell carcinoma, LSCC lung squamous cell carcinoma, SSCC skin squamous cell carcinoma, OSCC oral squamous cell carcinoma, UADTSCC upper aerodigestive tract squamous cell carcinoma, PB population-based, HB hospital-based, PHWE P value of hardy-weinberg equilibrium

aCOPD patients without LSCC, bhealthy smokers; ccontrol from Caucasian population; dcontrol from Black African population; econtrol from general population

Overall meta-analysis

First, we performed the overall meta-analysis, which included 52 case-control studies with 9763 cases and 15,028 controls (Table 2). The fixed-effects model was applied in all meta-analyses, because no substantial between-study heterogeneity was detected [Table 2, I2 value < 50.0%, Ph > 0.1]. As shown in Table 2, no altered susceptibility to SCC disease in cases was observed compared with controls [allele, Pa = 0.601; carrier, Pa = 0.587; homozygote, Pa = 0.689; heterozygote, Pa = 0.167; dominant, Pa = 0.289; dominant, Pa = 0.548]. These data suggest that the rs1695 polymorphism within the GSTP1 gene does not contribute to the risk of overall SCC.
Table 2

Meta-analysis of the GSTP1 rs1695 A/G polymorphism

Statistical analysis

Index

Allele

Carrier

Homozygote

Heterozygote

Dominant

Recessive

Association

OR

0.99

0.99

1.02

0.96

0.97

1.03

 

95% CIs

0.95~1.03

0.94~1.03

0.93~1.12

0.91~1.02

0.92~1.03

0.94~1.12

 

P a

0.601

0.587

0.689

0.167

0.289

0.548

Sample size

case

9763

9763

9763

9763

9763

9763

 

control

15,028

15,028

15,028

15,028

15,028

15,028

 

study

52

52

52

52

52

52

Heterogeneity

I2

15.5%

0.0%

9.7%

7.7%

11.8%

1.2%

 

P h

0.174

0.999

0.278

0.318

0.239

0.450

 

Model

Fixed

Fixed

Fixed

Fixed

Fixed

Fixed

Egger’s test

t

1.14

1.38

0.13

2.36

2.16

−0.31

 

P E

0.259

0.175

0.899

0.022

0.036

0.760

Begg’s test

z

0.53

0.84

0.77

1.96

1.82

1.29

 

P B

0.597

0.398

0.444

0.049

0.068

0.198

OR odds ratio, CIs confidence intervals, Pa, P value of association test, Ph, P value of heterogeneity test, PE, P value of Egger’s test, PB, P value of Begg’s test

Subgroup analysis

Next, we performed additional subgroup meta-analyses according to the factors of race (Asian/Caucasian), genotyping assay (PCR-RFLP), control source (PB/HB), and disease type (ESCC/HNSCC/LSCC/SSCC). As shown in Tables 3 and 4, there were no significant associations in any subgroup analysis for all genetic models tested (all Pa > 0.05). The forest plot of the subgroup analysis by disease type under the allele model is shown in Fig. 2.
Table 3

Subgroup analysis of the GSTP1 rs1695 A/G polymorphism by race, genotyping assay and control source

Factor

Subgroup

Index

Allele

Carrier

Homozygote

Heterozygote

Dominant

Recessive

Race

Asian

OR (95% CIs)

1.00 (0.89~1.12)

0.98 (0.86~1.11)

1.29 (0.94~1.76)

0.90 (0.78~1.04)

0.94 (0.82~1.08)

1.35 (0.99~1.83)

  

P a

0.948

0.716

0.114

0.139

0.361

0.058

  

Case/control

1696/2139

1696/2139

1696/2139

1696/2139

1696/2139

1696/2139

  

Study number

10

10

10

10

10

10

Race

Caucasian

OR (95% CIs)

0.98 (0.93~1.03)

0.98 (0.82~1.04)

1.00 (0.89~1.12)

0.94 (0.87~1.01)

0.95 (0.89~1.02)

1.02 (0.91~1.14)

  

P a

0.358

0.447

0.984

0.099

0.153

0.716

  

Case/control

5968/9719

5968/9719

5968/9719

5968/9719

5968/9719

5968/9719

  

Study number

30

30

30

30

30

30

genotyping assay

PCR-RFLP

OR (95% CIs)

0.99 (0.94~1.03)

0.99 (0.93~1.04)

1.01 (0.91~1.12)

0.96 (0.90~1.03)

0.97 (0.91~1.03)

1.01 (0.91~1.12)

  

P a

0.542

0.579

0.874

0.260

0.351

0.824

  

Case/control

8008/11,342

8008/11,342

8008/11,342

8008/11,342

8008/11,342

8008/11,342

  

Study number

42

42

42

42

42

42

control source

PB

OR (95% CIs)

0.98 (0.94~1.03)

0.98 (0.93~1.04)

1.00 (0.90~1.12)

0.96 (0.89~1.03)

0.96 (0.90~1.03)

1.02 (0.92~1.13)

  

P a

0.519

0.572

0.943

0.214

0.287

0.751

  

Case/control

6697/10,170

6697/10,170

6697/10,170

6697/10,170

6697/10,170

6697/10,170

  

Study number

31

31

31

31

31

31

control source

HB

OR (95% CIs)

0.98 (0.91~1.06)

0.98 (0.90~1.07)

1.00 (0.84~1.20)

0.95 (0.86~1.06)

0.96 (0.87~1.07)

1.01 (0.85~1.19)

  

P a

0.586

0.638

0.977

0.377

0.461

0.944

  

Case/control

2771/3946

2771/3946

2771/3946

2771/3946

2771/3946

2771/3946

  

Study number

19

19

19

19

19

19

Pa, P value of association test

PCR-RFLP polymerase chain reaction-restriction fragment length polymorphism, PB population-based, HB hospital-based, OR odds ratio, CIs confidence intervals

Table 4

Subgroup analysis of the GSTP1 rs1695 A/G polymorphism by SCC type

Subgroup

Index

Allele

Carrier

Homozygote

Heterozygote

Dominant

Recessive

ESCC

OR (95% CIs)

1.05 (0.96~1.15)

1.03 (0.93~1.14)

1.15 (0.95~1.39)

1.00 (0.88~1.14)

1.03 (0.92~1.17)

1.13 (0.95~1.34)

 

P a

0.263

0.568

0.155

0.970

0.575

0.160

 

Case/control

1934/3951

1934/3951

1934/3951

1934/3951

1934/3951

1934/3951

 

Study number

15

15

15

15

15

15

HNSCC

OR (95% CIs)

0.95 (0.89~1.01)

0.96 (0.89~1.03)

0.94 (0.82~1.09)

0.94 (0.87~1.02)

0.93 (0.86~1.01)

0.95 (0.83~1.09)

 

P a

0.112

0.247

0.408

0.131

0.102

0.459

 

Case/control

4671/4961

4671/4961

4671/4961

4671/4961

4671/4961

4671/4961

 

Study number

18

18

18

18

18

18

LSCC

OR (95% CIs)

1.00 (0.93~1.08)

1.00 (0.92~1.09)

1.04 (0.88~1.24)

0.97 (0.87~1.07)

0.98 (0.89~1.09)

1.06 (0.90~1.25)

 

P a

0.940

0.973

0.616

0.526

0.741

0.485

 

Case/control

2574/5421

2574/5421

2574/5421

2574/5421

2574/5421

2574/5421

 

Study number

15

15

15

15

15

15

SSCC

OR (95% CIs)

0.91 (0.70~1.19)

0.94 (0.69~1.28)

0.83 (0.46~1.49)

0.94 (0.64~1.36)

0.91 (0.64~1.30)

0.86 (0.49~1.51)

 

P a

0.493

0.688

0.532

0.728

0.605

0.597

 

Case/control

177/475

177/475

177/475

177/475

177/475

177/475

 

Study number

3

3

3

3

3

3

ESCC oesophageal squamous cell carcinoma, HNSCC head and neck squamous cell carcinoma, LSCC lung squamous cell carcinoma, SSCC skin squamous cell carcinoma, OR odds ratio, CIs confidence intervals, Pa, P value of association test

Fig. 2

Data of subgroup analysis by SCC type (allele model)

Furthermore, we included all case-controls studies regarding the specific SCC type and conducted a series of subgroup analyses by race and control source. However, similar results were obtained (data not shown). As a result, the GSTP1 gene rs1695 polymorphism is not likely related to the genetic susceptibility of a specific SCC type, including ESCC, HNSCC, LSCC, and SSCC.

Publication bias and sensitivity analysis

The publication bias analysis data obtained from Egger’s and Begg’s tests are shown in Table 2. There was no remarkable publication bias in most genetic models (PE > 0.05, PB > 0.05), except for the heterozygote (PE = 0.022, PB = 0.049) and dominant (PE = 0.036) models. The funnel plot (allele model) is displayed in Fig. 3a-b. Moreover, our sensitivity analysis led us to consider the stability of the data. Figure 4 shows a representative example of the sensitivity analysis (allele model).
Fig. 3

Funnel plot of publication bias analysis. a Egger’s test; b Begg’s test

Fig. 4

Sensitivity analysis data (allele model)

Discussion

In the current meta-analysis, we first focused on the genetic relationship between the GSTP1 rs1695 A/G polymorphism and the risk of overall SCC and then conducted subgroup analyses by the specific histological status. After rigorous screening, four main types of SCC, namely, ESCC, HNSCC, ESCC, and SSCC, were targeted.

ESCC, a type of squamous epithelium differentiation of a malignant tumour within the oesophagus, accounts for the vast majority of oesophageal cancers [64, 65]. ESCC often presents in physiological or pathological stenosis of the oesophagus, and genetic factors, carcinogens, and/or chronic irritants may contribute to the pathogenesis of ESCC [64, 65]. The GSTP1 rs1695 A/G polymorphism is significantly related to the risk of ESCC in the Kashmiri population [42]. Similarly, GSTP1 rs1695 may be an independent risk factor for ESCC in Western populations [53]. Nevertheless, different associations were detected in other reports. For instance, no difference between unrelated controls and ESCC cases was observed in a French population [14] or a Chinese population [61]. Therefore, a meta-analysis was required to comprehensively evaluate the role of the GSTP1 rs1695 A/G polymorphism in ESCC risk. Herein, we recruited 15 case-control studies involving 1934 cases and 3951 controls and performed a new meta-analysis to examine the association between the GSTP1 rs1695 A/G polymorphism and ESCC susceptibility. The carrier (carrier G vs. A) model, as well as the allele, homozygote, heterozygote, dominant and recessive genetic models, was used. Our results in the stratified analysis of specific ESCCs are consistent with the data of Tan et al. [18].

Similarly, inconsistent results regarding an association between the GSTP1 rs1695 A/G polymorphism and LSCC risk have been reported in different races and geographical locations [24, 31, 33, 34, 37, 40, 45, 47, 52, 56, 57, 60, 63]. Here, we failed to detect a positive correlation between GSTP1 rs1695 and LSCC susceptibility, consistent with the prior meta-analysis of Feng in 2013 [66] and Xu in 2014 [67].

Head and neck cancer comprises cancers of the mouth, nose, sinuses, salivary glands, throat, and lymph nodes in the neck, and HNSCC is the major pathologic type [68]. In 2012, Lang et al. enrolled 28 case-control studies to perform a meta-analysis regarding the genetic effect of the GSTP1 rs1695 A/G polymorphism on overall head and neck cancer [69]. The authors were unable to identify a positive association between the GSTP1 rs1695 A/G polymorphism and the risk of overall head and neck cancer. Nevertheless, the potential role of GSTP1 rs1695 in the susceptibility to HNSCC was not assessed. Therefore, we performed a subgroup meta-analysis of HNSCC involving 18 case-control studies, but did not identify an association between GSTP1 rs1695 and HNSCC risk.

SSCC, SBCC (skin basal cell carcinoma) and (MM malignant melanoma) are the three main types of cutaneous cancer [4]. Herein, we did not identify an association between the GSTP1 rs1695 A/G polymorphism and SSCC risk, consistent with the prior meta-analyses regarding the correlation between GSTP1 rs1695 and the susceptibility to cutaneous cancer in 2015 [70, 71].

Human GST family genes, mainly including GSTA (glutathione S-transferase alpha), GSTM1 (glutathione S-transferase mu 1), GSTT1 (glutathione S-transferase theta 1) and GSTP1, encode phase II enzymes and are thus important for the body defence, metabolic detoxification of mutagens or chemical drugs, or cellular elimination of carcinogens [9, 10]. The rs1695 A/G polymorphism within the GSTP1 gene can result in the substitution of Ile (isoleucine) for Val (valine) at amino acid position 105, which may lower the cytosolic enzyme activity of GSTP1 protein [72, 73]. Although significant associations were not obtained in our overall meta-analysis or subgroup analyses by pathological type, we cannot rule out the potential genetic effect of the GSTP1 rs1695 A/G polymorphism.

There are still some limitations to our meta-analysis that should be clarified. Even though our findings were considered reliable by our sensitivity analysis and publication bias assessment, more eligible investigations are still warranted to further enhance the statistical power. We note that population-based controls were not utilized in each case-control study. The currently available data of genotypic and allelic frequency from the on-line databases led us to only target the rs1695 polymorphism of the GSTP1 gene. Other possible functional polymorphisms of the GSTP1 gene, such as rs1138272, or relative haplotypes will be important to examine in the future. We should also pay attention to the genetic relationship between GSTP1/GSTM1/GSTT1 polymorphisms and the risk of SCC.

Conclusion

In general, based on the currently published data, the GSTP1 gene rs1695 polymorphism is not associated with the susceptibility to overall SCC diseases, including ESCC, HNSCC, LSCC, and skin SCC. The confirmation or refutation of this conclusion merits further evidence.

Notes

Acknowledgements

Not applicable.

Funding

This study was supported in part by a grant of Science Foundation from Tianjin Municipal Commission of Health and Family Planning (2015KY11).

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

SW and ZB designed the study. SW, JZ and FJ extracted, analyzed, and interpreted the data. SW and ZB drafted the manuscript. All authors read and approved the final version of the manuscript.

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.

References

  1. 1.
    Que SKT, Zwald FO, Schmults CD. Cutaneous squamous cell carcinoma: management of advanced and high-stage tumors. J Am Acad Dermatol. 2018;78(2):249–61.PubMedGoogle Scholar
  2. 2.
    Wang C, Wang J, Chen Z, Gao Y, He J. Immunohistochemical prognostic markers of esophageal squamous cell carcinoma: a systematic review. Chin J Cancer. 2017;36(1):65.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Bann DV, Deschler DG, Goyal N. Novel Immunotherapeutic Approaches for Head and Neck Squamous Cell Carcinoma. Cancers (Basel). 2016;8(10).Google Scholar
  4. 4.
    Liu N, Liu GJ, Liu J. Genetic association between TNF-alpha promoter polymorphism and susceptibility to squamous cell carcinoma, basal cell carcinoma, and melanoma: a meta-analysis. Oncotarget. 2017;8(32):53873–85.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Zhang X, He R, Ren F, Tang R, Chen G. Association of miR-146a rs2910164 polymorphism with squamous cell carcinoma risk: a meta-analysis. J buon. 2015;20(3):829–41.PubMedGoogle Scholar
  6. 6.
    Yu H, Li H, Zhang J, Liu G. Influence of MDM2 polymorphisms on squamous cell carcinoma susceptibility: a meta-analysis. Onco Targets Ther. 2016;9:6211–24.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Chahal HS, Lin Y, Ransohoff KJ, Hinds DA, Wu W, Dai HJ, Qureshi AA, Li WQ, Kraft P, Tang JY, et al. Genome-wide association study identifies novel susceptibility loci for cutaneous squamous cell carcinoma. Nat Commun. 2016;7:12048.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Chang J, Wei L, Miao X, Yu D, Tan W, Zhang X, Wu C, Lin D. Two novel variants on 13q22.1 are associated with risk of esophageal squamous cell carcinoma. Cancer Epidemiol Biomark Prev. 2015;24(11):1774–80.Google Scholar
  9. 9.
    Schnekenburger M, Karius T, Diederich M. Regulation of epigenetic traits of the glutathione S-transferase P1 gene: from detoxification toward cancer prevention and diagnosis. Front Pharmacol. 2014;5:170.PubMedPubMedCentralGoogle Scholar
  10. 10.
    Marchewka Z, Piwowar A, Ruzik S, Dlugosz A. Glutathione S - transferases class pi and mi and their significance in oncology. Postepy Hig Med Dosw (Online). 2017;71(0):541–50.Google Scholar
  11. 11.
    Yuan Y, Qian ZR, Sano T, Asa SL, Yamada S, Kagawa N, Kudo E. Reduction of GSTP1 expression by DNA methylation correlates with clinicopathological features in pituitary adenomas. Mod Pathol. 2008;21(7):856–65.PubMedGoogle Scholar
  12. 12.
    Hollman AL, Tchounwou PB, Huang HC. The association between Gene-environment interactions and diseases involving the human GST superfamily with SNP variants. Int J Environ Res Public Health. 2016;13(4):379.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Karaca S, Karaca M, Cesuroglu T, Erge S, Polimanti R. GSTM1, GSTP1, and GSTT1 genetic variability in Turkish and worldwide populations. Am J Hum Biol. 2015;27(3):310–6.PubMedGoogle Scholar
  14. 14.
    Abbas A, Delvinquiere K, Lechevrel M, Lebailly P, Gauduchon P, Launoy G, Sichel F. GSTM1, GSTT1, GSTP1 and CYP1A1 genetic polymorphisms and susceptibility to esophageal cancer in a French population: different pattern of squamous cell carcinoma and adenocarcinoma. World J Gastroenterol. 2004;10(23):3389–93.PubMedPubMedCentralGoogle Scholar
  15. 15.
    van Lieshout EM, Roelofs HM, Dekker S, Mulder CJ, Wobbes T, Jansen JB, Peters WH. Polymorphic expression of the glutathione S-transferase P1 gene and its susceptibility to Barrett's esophagus and esophageal carcinoma. Cancer Res. 1999;59(3):586–9.PubMedGoogle Scholar
  16. 16.
    Zendehdel K, Bahmanyar S, McCarthy S, Nyren O, Andersson B, Ye W. Genetic polymorphisms of glutathione S-transferase genes GSTP1, GSTM1, and GSTT1 and risk of esophageal and gastric cardia cancers. Cancer Causes Control. 2009;20(10):2031–8.PubMedGoogle Scholar
  17. 17.
    Song Y, Du Y, Zhou Q, Ma J, Yu J, Tao X, Zhang F. Association of GSTP1 Ile105Val polymorphism with risk of esophageal cancer: a meta-analysis of 21 case-control studies. Int J Clin Exp Med. 2014;7(10):3215–24.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Tan X, Chen M. Association between glutathione S-transferases P1 Ile105Val polymorphism and susceptibility to esophageal cancer: evidence from 20 case-control studies. Mol Biol Rep. 2015;42(2):399–408.PubMedGoogle Scholar
  19. 19.
    Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Cabelguenne A, Loriot MA, Stucker I, Blons H, Koum-Besson E, Brasnu D, Beaune P, Laccourreye O, Laurent-Puig P, De Waziers I. Glutathione-associated enzymes in head and neck squamous cell carcinoma and response to cisplatin-based neoadjuvant chemotherapy. Int J Cancer. 2001;93(5):725–30.PubMedGoogle Scholar
  21. 21.
    Cai L, Mu LN, Lu H, Lu QY, You NC, Yu SZ, Le AD, Zhao J, Zhou XF, Marshall J, et al. Dietary selenium intake and genetic polymorphisms of the GSTP1 and p53 genes on the risk of esophageal squamous cell carcinoma. Cancer Epidemiol Biomark Prev. 2006;15(2):294–300.Google Scholar
  22. 22.
    Cho CG, Lee SK, Nam SY, Lee MS, Lee SW, Choi EK, Park HJ, Kim SY. Association of the GSTP1 and NQO1 polymorphisms and head and neck squamous cell carcinoma risk. J Korean Med Sci. 2006;21(6):1075–9.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Dura P, Salomon J, Te Morsche RH, Roelofs HM, Kristinsson JO, Wobbes T, Witteman BJ, Tan AC, Drenth JP, Peters WH. No role for glutathione S-transferase genotypes in Caucasian esophageal squamous cell or adenocarcinoma etiology: an European case-control study. BMC Gastroenterol. 2013;13:97.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Dzian A, Halasova E, Matakova T, Kavcova E, Smolar M, Dobrota D, Hamzik J, Mistuna D. Lung adenocarcinoma and squamous cell carcinoma in association with genetic polymorphisms of GSTs in Slovak population. Neoplasma. 2012;59(2):160–7.PubMedGoogle Scholar
  25. 25.
    Evans AJ, Henner WD, Eilers KM, Montalto MA, Wersinger EM, Andersen PE, Cohen JI, Everts EC, McWilliams JE, Beer TM. Polymorphisms of GSTT1 and related genes in head and neck cancer risk. Head Neck. 2004;26(1):63–70.PubMedGoogle Scholar
  26. 26.
    Fryer AA, Ramsay HM, Lovatt TJ, Jones PW, Hawley CM, Nicol DL, Strange RC, Harden PN. Polymorphisms in glutathione S-transferases and non-melanoma skin cancer risk in Australian renal transplant recipients. Carcinogenesis. 2005;26(1):185–91.PubMedGoogle Scholar
  27. 27.
    Harth V, Schafer M, Abel J, Maintz L, Neuhaus T, Besuden M, Primke R, Wilkesmann A, Thier R, Vetter H, et al. Head and neck squamous-cell cancer and its association with polymorphic enzymes of xenobiotic metabolism and repair. J Toxicol Environ Health A. 2008;71(13–14):887–97.PubMedGoogle Scholar
  28. 28.
    Jain M, Kumar S, Rastogi N, Lal P, Ghoshal UC, Tiwari A, Pant MC, Baiq MQ, Mittal B. GSTT1, GSTM1 and GSTP1 genetic polymorphisms and interaction with tobacco, alcohol and occupational exposure in esophageal cancer patients from North India. Cancer Lett. 2006;242(1):60–7.PubMedGoogle Scholar
  29. 29.
    Jourenkova-Mironova N, Voho A, Bouchardy C, Wikman H, Dayer P, Benhamou S, Hirvonen A. Glutathione S-transferase GSTM1, GSTM3, GSTP1 and GSTT1 genotypes and the risk of smoking-related oral and pharyngeal cancers. Int J Cancer. 1999a;81(1):44–8.PubMedGoogle Scholar
  30. 30.
    Jourenkova-Mironova N, Voho A, Bouchardy C, Wikman H, Dayer P, Benhamou S, Hirvonen A. Glutathione S-transferase GSTM3 and GSTP1 genotypes and larynx cancer risk. Cancer Epidemiol Biomark Prev. 1999b;8(2):185–8.Google Scholar
  31. 31.
    Jourenkova-Mironova N, Wikman H, Bouchardy C, Voho A, Dayer P, Benhamou S, Hirvonen A. Role of glutathione S-transferase GSTM1, GSTM3, GSTP1 and GSTT1 genotypes in modulating susceptibility to smoking-related lung cancer. Pharmacogenetics. 1998;8(6):495–502.PubMedGoogle Scholar
  32. 32.
    Kelders WP, Oude Ophuis MB, Roelofs HM, Peters WH, Manni JJ. The association between glutathione S-transferase P1 genotype and plasma level in head and neck cancer. Laryngoscope. 2002;112(3):462–6.PubMedGoogle Scholar
  33. 33.
    Kihara M, Kihara M, Noda K. Lung cancer risk of the GSTM1 null genotype is enhanced in the presence of the GSTP1 mutated genotype in male Japanese smokers. Cancer Lett. 1999;137(1):53–60.PubMedGoogle Scholar
  34. 34.
    Larsen JE, Colosimo ML, Yang IA, Bowman R, Zimmerman PV, Fong KM. CYP1A1 Ile462Val and MPO G-463A interact to increase risk of adenocarcinoma but not squamous cell carcinoma of the lung. Carcinogenesis. 2006;27(3):525–32.PubMedGoogle Scholar
  35. 35.
    Leichsenring A, Losi-Guembarovski R, Maciel ME, Losi-Guembarovski A, Oliveira BW, Ramos G, Cavalcanti TC, Bicalho MG, Cavalli IJ, Colus IM, et al. CYP1A1 and GSTP1 polymorphisms in an oral cancer case-control study. Braz J Med Biol Res. 2006;39(12):1569–74.PubMedGoogle Scholar
  36. 36.
    Leite JL, Morari EC, Granja F, Campos GM, Guilhen AC, Ward LS. Influence of the glutathione s-transferase gene polymorphisms on the susceptibility to basal cell skin carcinoma. Rev Med Chil. 2007;135(3):301–6.PubMedGoogle Scholar
  37. 37.
    Lewis SJ, Cherry NM, Niven RM, Barber PV, Povey AC. GSTM1, GSTT1 and GSTP1 polymorphisms and lung cancer risk. Cancer Lett. 2002;180(2):165–71.PubMedGoogle Scholar
  38. 38.
    Li D, Dandara C, Parker MI. The 341C/T polymorphism in the GSTP1 gene is associated with increased risk of oesophageal cancer. BMC Genet. 2010;11:47.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Li DH, Wang LE, Chang P, El-Naggar AK, Sturgis EM, Wei QY. In vitro benzo a pyrene diol epoxide-induced DNA adducts and risk of squamous cell carcinoma of head and neck. Cancer Res. 2007;67(12):5628–34.PubMedGoogle Scholar
  40. 40.
    Liang G, Pu Y, Yin L. Rapid detection of single nucleotide polymorphisms related with lung cancer susceptibility of Chinese population. Cancer Lett. 2005;223(2):265–74.PubMedGoogle Scholar
  41. 41.
    Liu R, Yin L, Pu Y, Li Y, Liang G, Zhang J, Li X. Functional alterations in the glutathione S-transferase family associated with enhanced occurrence of esophageal carcinoma in China. J Toxicol Environ Health A. 2010;73(7):471–82.PubMedGoogle Scholar
  42. 42.
    Malik MA, Upadhyay R, Mittal RD, Zargar SA, Mittal B. Association of xenobiotic metabolizing enzymes genetic polymorphisms with esophageal cancer in Kashmir Valley and influence of environmental factors. Nutr Cancer. 2010;62(6):734–42.PubMedGoogle Scholar
  43. 43.
    Matejcic M, Li D, Prescott NJ, Lewis CM, Mathew CG, Parker MI. Association of a deletion of GSTT2B with an altered risk of oesophageal squamous cell carcinoma in a south African population: a case-control study. PLoS One. 2011;6(12):e29366.PubMedPubMedCentralGoogle Scholar
  44. 44.
    McWilliams JE, Evans AJ, Beer TM, Andersen PE, Cohen JI, Everts EC, Henner WD. Genetic polymorphisms in head and neck cancer risk. Head Neck. 2000;22(6):609–17.PubMedGoogle Scholar
  45. 45.
    Miller DP, Asomaning K, Liu G, Wain JC, Lynch TJ, Neuberg D, Su L, Christiani DC. An association between glutathione S-transferase P1 gene polymorphism and younger age at onset of lung carcinoma. Cancer. 2006;107(7):1570–7.PubMedGoogle Scholar
  46. 46.
    Moaven O, Raziee HR, Sima HR, Ganji A, Malekzadeh R, A'Rabi A, Abdollahi A, Memar B, Sotoudeh M, Naseh H, et al. Interactions between glutathione-S-transferase M1, T1 and P1 polymorphisms and smoking, and increased susceptibility to esophageal squamous cell carcinoma. Cancer Epidemiol. 2010;34(3):285–90.PubMedGoogle Scholar
  47. 47.
    Nazar-Stewart V, Vaughan TL, Stapleton P, Van Loo J, Nicol-Blades B, Eaton DL. A population-based study of glutathione S-transferase M1, T1 and P1 genotypes and risk for lung cancer. Lung Cancer. 2003;40(3):247–58.PubMedGoogle Scholar
  48. 48.
    Olshan AF, Weissler MC, Watson MA, Bell DA. GSTM1, GSTT1, GSTP1, CYP1A1, and NAT1 polymorphisms, tobacco use, and the risk of head and neck cancer. Cancer Epidemiol Biomark Prev. 2000;9(2):185–91.Google Scholar
  49. 49.
    Oude Ophuis MB, Roelofs HM, van den Brandt PA, Peters WH, Manni JJ. Polymorphisms of the glutathione S-transferase P1 gene and head and neck cancer susceptibility. Head Neck. 2003;25(1):37–43.PubMedGoogle Scholar
  50. 50.
    Peters ES, McClean MD, Marsit CJ, Luckett B, Kelsey KT. Glutathione S-transferase polymorphisms and the synergy of alcohol and tobacco in oral, pharyngeal, and laryngeal carcinoma. Cancer Epidemiol Biomark Prev. 2006;15(11):2196–202.Google Scholar
  51. 51.
    Ramsay HM, Harden PN, Reece S, Smith AG, Jones PW, Strange RC, Fryer AA. Polymorphisms in glutathione S-transferases are associated with altered risk of nonmelanoma skin cancer in renal transplant recipients: a preliminary analysis. J Invest Dermatol. 2001;117(2):251–5.PubMedGoogle Scholar
  52. 52.
    Risch A, Wikman H, Thiel S, Schmezer P, Edler L, Drings P, Dienemann H, Kayser K, Schulz V, Spiegelhalder B, et al. Glutathione-S-transferase M1, M3, T1 and P1 polymorphisms and susceptibility to non-small-cell lung cancer subtypes and hamartomas. Pharmacogenetics. 2001;11(9):757–64.PubMedGoogle Scholar
  53. 53.
    Rossini A, Rapozo DCM, Soares Lima SC, Guimarães DP, Ferreira MA, Teixeira R, Kruel CDP, Barros SGS, Andreollo NA, Acatauassú R, et al. Polymorphisms of GSTP1 and GSTT1, but not of CYP2A6, CYP2E1 or GSTM1, modify the risk for esophageal cancer in a western population. Carcinogenesis. 2007;28(12):2537–42.PubMedGoogle Scholar
  54. 54.
    Ruwali M, Pant MC, Shah PP, Mishra BN, Parmar D. Polymorphism in cytochrome P450 2A6 and glutathione S-transferase P1 modifies head and neck cancer risk and treatment outcome. Mutat Res. 2009;669(1–2):36–41.PubMedGoogle Scholar
  55. 55.
    Ruwali M, Singh M, Pant MC, Parmar D. Polymorphism in glutathione S-transferases: susceptibility and treatment outcome for head and neck cancer. Xenobiotica. 2011;41(12):1122–30.PubMedGoogle Scholar
  56. 56.
    Ryberg D, Skaug V, Hewer A, Phillips DH, Harries LW, Wolf CR, Ogreid D, Ulvik A, Vu P, Haugen A. Genotypes of glutathione transferase M1 and P1 and their significance for lung DNA adduct levels and cancer risk. Carcinogenesis. 1997;18(7):1285–9.PubMedGoogle Scholar
  57. 57.
    Schneider J, Bernges U, Philipp M, Woitowitz HJ. GSTM1, GSTT1, and GSTP1 polymorphism and lung cancer risk in relation to tobacco smoking. Cancer Lett. 2004;208(1):65–74.PubMedGoogle Scholar
  58. 58.
    Soucek P, Susova S, Mohelnikova-Duchonova B, Gromadzinska J, Moraviec-Sztandera A, Vodicka P, Vodickova L. Polymorphisms in metabolizing enzymes and the risk of head and neck squamous cell carcinoma in the Slavic population of the Central Europe. Neoplasma. 2010;57(5):415–21.PubMedGoogle Scholar
  59. 59.
    Soya SS, Vinod T, Reddy KS, Gopalakrishnan S, Adithan C. Genetic polymorphisms of glutathione-S-transferase genes (GSTM1, GSTT1 and GSTP1) and upper aerodigestive tract cancer risk among smokers, tobacco chewers and alcoholics in an Indian population. Eur J Cancer. 2007;43(18):2698–706.PubMedGoogle Scholar
  60. 60.
    Stücker I, Hirvonen A, De Waziers I, Cabelguenne A, Mitrunen K, Cénée S, Koum-Besson E, Hémon D, Beaune P, Loriot MA. Genetic polymorphisms of glutathione S-transferases as modulators of lung cancer susceptibility. Carcinogenesis. 2002;23(9):1475–81.PubMedGoogle Scholar
  61. 61.
    Tan W, Song N, Wang GQ, Liu Q, Tang HJ, Kadlubar FF, Lin DX. Impact of genetic polymorphisms in cytochrome P450 2E1 and glutathione S-transferases M1, T1, and P1 on susceptibility to esophageal cancer among high-risk individuals in China. Cancer Epidemiol Biomark Prev. 2000;9(6):551–6.Google Scholar
  62. 62.
    To-Figueras J, Gene M, Gomez-Catalan J, Pique E, Borrego N, Caballero M, Cruellas F, Raya A, Dicenta M, Corbella J. Microsomal epoxide hydrolase and glutathione S-transferase polymorphisms in relation to laryngeal carcinoma risk. Cancer Lett. 2002;187(1–2):95–101.PubMedGoogle Scholar
  63. 63.
    To-Figueras J, Gene M, Gomez-Catalan J, Pique E, Borrego N, Carrasco JL, Ramon J, Corbella J. Genetic polymorphism of glutathione S-transferase P1 gene and lung cancer risk. Cancer Causes Control. 1999;10(1):65–70.PubMedGoogle Scholar
  64. 64.
    Song Q, Jiang D, Wang H, Huang J, Liu Y, Xu C, Hou Y. Chromosomal and genomic variations in esophageal squamous cell carcinoma: a review of technologies, applications, and prospections. J Cancer. 2017;8(13):2492–500.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Luo LN, He LJ, Gao XY, Huang XX, Shan HB, Luo GY, Li Y, Lin SY, Wang GB, Zhang R, et al. Evaluation of preoperative staging for esophageal squamous cell carcinoma. World J Gastroenterol. 2016;22(29):6683–9.PubMedPubMedCentralGoogle Scholar
  66. 66.
    Feng X, Zhou HF, Zheng BS, Shi JJ, Luo C, Qin JJ. Association of glutathione S-transferase P1 gene polymorphism with the histological types of lung cancer: a meta-analysis. Mol Biol Rep. 2013;40(3):2439–47.PubMedGoogle Scholar
  67. 67.
    Xu CH, Wang Q, Zhan P, Qian Q, Yu LK. GSTP1 Ile105Val polymorphism is associated with lung cancer risk among Asian population and smokers: an updated meta-analysis. Mol Biol Rep. 2014;41(7):4199–212.PubMedGoogle Scholar
  68. 68.
    Szyszko TA, Cook GJR. PET/CT and PET/MRI in head and neck malignancy. Clin Radiol. 2018;73(1):60–9.PubMedGoogle Scholar
  69. 69.
    Lang J, Song X, Cheng J, Zhao S, Fan J. Association of GSTP1 Ile105Val Polymorphism and Risk of Head and Neck Cancers: A Meta-Analysis of 28 Case-Control Studies. PLoS One. 2012;7(11):e48132.Google Scholar
  70. 70.
    Lei Z, Liu T, Li X, Xu X, Fan D. Contribution of glutathione S-transferase gene polymorphisms to development of skin cancer. Int J Clin Exp Med. 2015;8(1):377–86.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Zhou CF, Ma T, Zhou DC, Shen T, Zhu QX. Association of glutathione S-transferase pi (GSTP1) Ile105Val polymorphism with the risk of skin cancer: a meta-analysis. Arch Dermatol Res. 2015;307(6):505–13.PubMedGoogle Scholar
  72. 72.
    Watson MA, Stewart RK, Smith GB, Massey TE, Bell DA. Human glutathione S-transferase P1 polymorphisms: relationship to lung tissue enzyme activity and population frequency distribution. Carcinogenesis. 1998;19(2):275–80.PubMedGoogle Scholar
  73. 73.
    Zhong SL, Zhou SF, Chen X, Chan SY, Chan E, Ng KY, Duan W, Huang M. Relationship between genotype and enzyme activity of glutathione S-transferases M1 and P1 in Chinese. Eur J Pharm Sci. 2006;28(1–2):77–85.PubMedGoogle Scholar

Copyright information

© The Author(s). 2019

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors and Affiliations

  1. 1.Department of Plastic and Burn SurgeryTianjin First Center HospitalTianjinChina
  2. 2.Department of Urology SurgeryTianjin First Center HospitalTianjinChina

Personalised recommendations