Association of glutathione S-transferase T1, M1, and P1 polymorphisms in the breast cancer risk: a meta-analysis

Figures & data

Figure 1 Flowchart of study selection in this meta-analysis.

Abbreviation: HWE, Hardy–Weinberg equilibrium.

Table 1 Characteristics of the literature included in the meta-analysis

First author	Year	Country	Ethnicity	Sample size (cases/controls)	GSTM1				GSTT1				GSTP1						PHWE
					Cases		Controls		Cases		Controls		Cases			Controls
					Null	Present	Null	Present	Null	Present	Null	Present	Ile/Ile	Ile/Val	Val/Val	Ile/Ile	Ile/Val	Val/Val
Bailey et al^Citation19	1998	USA	Caucasian	164/162	91	73	100	62	47	117	44	118	–	–	–	–	–	–
Bailey et al^Citation19	1998	USA	Mixed	59/59	20	39	24	35	12	47	17	42	–	–	–	–	–	–
Zhao et al^Citation20	2001	USA	Caucasian	155/332	–	–	–	–	–	–	–	–	87	58	10	170	133	29	1.000
Amorim et al^Citation21	2002	Brazil	Caucasian	79/123	33	46	65	58	15	64	31	92	–	–	–	–	–	–
Amorim et al^Citation21	2002	Brazil	Mixed	128/256	50	78	103	153	32	96	65	191	–	–	–	–	–	–
Sohail et al^Citation22	2013	Pakistan	Asian	100/102	43	57	45	57	27	73	32	70	–	–	–	–	–	–
Zgheib et al^Citation23	2013	Lebanon	Asian	227/98	111	115	47	51	43	183	20	78	117	94	16	49	39	10	0.74
Sakoda et al^Citation24	2008	People’s Republic of China	Asian	615/878	321	294	428	450	–	–	–	–	378	215	20	569	277	30	0.15
Chang et al^Citation25	2006	People’s Republic of China	Asian	189/421	107	82	227	193	111	78	210	210	123	53	13	288	114	19	0.1
Ambrosone et al^Citation26	1999	USA	Caucasian	282/343	145	137	172	171	–	–	–	–	–	–	–	–	–	–
Saxena et al^Citation27	2012	India	Asian	215/215	–	–	–	–	–	–	–	–	81	89	45	101	75	39	0
Syamala et al^Citation28	2007	India	Asian	347/250	119	228	63	187	56	291	23	227	186	140	21	125	109	16	0.28
Mohamad^Citation29	2014	Saudi Arabia	Asian	100/48	–	–	–	–	–	–	–	–	58	40	2	28	18	2	1.000
Van Emburgh et al^Citation30	2008	USA	Caucasian	391/466	206	185	268	198	69	322	82	384	160	183	42	179	179	35	0.35
Rangel et al^Citation31	2015	Mexico	Caucasian	243/118	117	124	34	79	32	211	22	92	58	105	79	35	53	30	0.27
Ge et al^Citation32	2013	People’s Republic of China	Asian	920/783	–	–	–	–	–	–	–	–	540	325	55	519	230	34	0.2
Luo et al^Citation8	2012	People’s Republic of China	Asian	353/701	207	146	414	286	186	167	364	337	–	–	–	–	–	–
Christine et al^Citation33	1998	French	Caucasian	361/437	201	160	224	213	–	–	–	–	–	–	–	–	–	–
Hashemi et al^Citation34	2012	Iran	Asian	134/152	86	48	71	81	18	116	12	140	36	72	26	97	52	3	0.29
Zheng et al^Citation35	2002	USA	Caucasian	273/657	100	102	249	232	39	113	62	263	–	–	–	–	–	–
Ramalhinho et al^Citation36	2012	Portugal	Caucasian	101/121	66	35	45	76	47	54	24	97	54	35	12	55	48	16	0.31

Abbreviations: GST, glutathione S-transferase; Ile, isoleucine; Val, valine; “–”, no data; HWE, Hardy–Weinberg equilibrium.

Figure 2 Forest plot for the association of GSTM1 null polymorphism and breast cancer risk for Asians.

Abbreviations: GSTM1, glutathione S-transferase M1; OR, odds ratio; CI, confidence interval.

Table 2 Meta-analysis of the association between GSTM1, GSTT1, and GSTP1 polymorphisms and breast cancer risk

Comparisons	Odds ratio	95% CI	P-value	Heterogeneity		Effects model
				I^2 (%)	P-value
GSTM1
Overall	1.13	0.97–1.32	0.019	66.00	<0.001	Random
Caucasian	1.13	0.85–1.52	0.398	79.50	<.001	Random
Asian	1.17	1.04–1.32	0.012	41.40	0.115	Fixed
Mixed	0.9	0.62–1.30	0.567	0.00	0.584	Fixed
GSTT1
Overall	1.15	0.93–1.42	0.189	60.00	0.002	Random
Caucasian	1.17	0.96–1.42	0.127	76.40	0.001	Random
Asian	1.19	1.01–1.41	0.039	43.30	0.117	Fixed
Mixed	0.88	0.57–1.34	0.544	0.00	0.378	Fixed
GSTP1
V vs I
Overall	1.21	0.99–1.48	0.066	81.30	<0.001	Random
Caucasian	1.16	1.01–1.34	0.042	25.40	0.259	Fixed
Asian	1.26	0.91–1.75	0.159	88.60	<0.001	Random
VV vs VV + VI
Overall	1.16	0.83–1.62	0.38	57.40	0.012	Random
Caucasian	1.14	0.86–1.52	0.355	0.00	0.42	Fixed
Asian	1.28	0.70–2.35	0.429	73.00	0.002	Random
VV + VI vs II
Overall	1.19	0.93–1.52	0.159	79.10	<0.001	Random
Caucasian	1.03	0.85–1.25	0.76	35.70	0.198	Fixed
Asian	1.34	0.94–1.93	0.11	85.80	<0.001	Random
VV vs II
Overall	1.24	0.81–1.89	0.32	71.10	<0.001	Random
Caucasian	1.14	0.84–1.57	0.388	30.40	0.23	Fixed
Asian	1.45	0.69–3.05	0.324	81.30	<0.001	Random

Abbreviations: GST, glutathione S-transferase; CI, confidence interval; I, Ile; Ile, isoleucine; V, Val; Val, valine.

Figure 3 Forest plot for the association of GSTT1 null polymorphism and breast cancer risk for Caucasians.

Abbreviations: GSTT1, glutathione S-transferase T1; OR, odds ratio; CI, confidence interval.

Figure 4 Forest plot for the association of GSTP1 Val105Ile (rs1695) polymorphism and breast cancer risk for Caucasians.

Abbreviations: GSTP1, glutathione S-transferase P1; OR, odds ratio; CI, confidence interval.

BaileyLRRoodiNVerrierCSYeeCJDupontWDParlFFBreast cancer and CYPIA1, GSTM1, and GSTT1 polymorphisms: evidence of a lack of association in Caucasians and African AmericansCancer Res199858165709426059

 PubMed Web of Science ®Google Scholar

ZhaoMFLewisRGustafsonDRWenWQCerhanJRZhengWNo apparent association of GSTP1 A(313)G polymorphism with breast cancer risk among postmenopausal Iowa womenCancer Epidemiol Biomarkers Prev200110121301130211751449

 PubMed Web of Science ®Google Scholar

da Fonte de AmorimLRossiniAMendonçaGCYP1A1, GSTM1, and GSTT1 polymorphisms and breast cancer risk in Brazilian womenCancer Lett2002181217918612175533

 PubMed Web of Science ®Google Scholar

SohailAKanwalNAliMEffects of glutathione-S-transferase polymorphisms on the risk of breast cancer: a population-based case-control study in PakistanEnviron Toxicol Pharmacol201335214315323376175

 PubMed Web of Science ®Google Scholar

ZgheibNKShamseddineAAGeryessEGenetic polymorphisms of CYP2E1, GST, and NAT2 enzymes are not associated with risk of breast cancer in a sample of Lebanese womenMutat Res2013747–7484047

 PubMed Web of Science ®Google Scholar

SakodaLCBlackstonCRXueKGlutathione S-transferase M1 and P1 polymorphisms and risk of breast cancer and fibrocystic breast conditions in Chinese womenBreast Cancer Res Treat2008109114315517624589

 PubMed Web of Science ®Google Scholar

ChangTWWangSMGuoYLTsaiPCHuangCJHuangWGlutathione S-transferase polymorphisms associated with risk of breast cancer in southern TaiwanBreast200615675476116713266

 PubMed Web of Science ®Google Scholar

AmbrosoneCBColesBFFreudenheimJLShieldsPGGlutathione-S-transferase (GSTM1) genetic polymorphisms do not affect human breast cancer risk, regardless of dietary antioxidantsJ Nutr19991292S suppl565S568S10064333

 PubMed Web of Science ®Google Scholar

SaxenaADhillonVSShahidMGSTP1 methylation and polymorphism increase the risk of breast cancer and the effects of diet and lifestyle in breast cancer patientsExp Ther Med2012461097110323226781

 PubMed Web of Science ®Google Scholar

SyamalaVSSreejaLSyamalaVInfluence of germline polymorphisms of GSTT1, GSTM1, and GSTP1 in familial versus sporadic breast cancer susceptibility and survivalFam Cancer20087321322018080216

 PubMed Web of Science ®Google Scholar

KhabazMNPolymorphism of the glutathione S-transferase P1 gene (Gst-Pi) in breast carcinomaPol J Pathol201465214114625119175

 PubMed Web of Science ®Google Scholar

Van EmburghBOHuJJLevineEAPolymorphisms in CYP1B1, GSTM1, GSTT1 and GSTP1, and susceptibility to breast cancerOncol Rep20081951311132118425393

 PubMed Web of Science ®Google Scholar

Jaramillo-RangelGOrtega-MartinezMCerda-FloresRMBarrera-SaldanaHAPolymorphisms in GSTM1, GSTT1, GSTP1, and GSTM3 genes and breast cancer risk in northeastern MexicoGenet Mol Res20151426465647126125851

 PubMed Web of Science ®Google Scholar

GeJTianAXWangQSThe GSTP1 105Val allele increases breast cancer risk and aggressiveness but enhances response to cyclophosphamide chemotherapy in North ChinaPLoS One201386e6758923826324

 PubMed Web of Science ®Google Scholar

LuoJGaoYTChowWHUrinary polyphenols, glutathione S-transferases copy number variation, and breast cancer risk: results from the Shanghai women’s health studyMol Carcinog201251537938821557334

 PubMed Web of Science ®Google Scholar

MaugardCMCharrierJBignonYJAllelic deletion at glutathione S-transferase M1 focus and its association with breast cancer susceptibilityChem Biol Interact1998111–112365375

 PubMed Web of Science ®Google Scholar

HashemiMEskandari-NasabEFazaeliAAssociation between polymorphisms of glutathione S-transferase genes (GSTM1, GSTP1 and GSTT1) and breast cancer risk in a sample Iranian populationBiomark Med20126679780323227845

 PubMed Web of Science ®Google Scholar

ZhengWWenWQGustafsonDRGrossMCerhanJRFolsomARGSTM1 and GSTT1 polymorphisms and postmenopausal breast cancer riskBreast Cancer Res Treat200274191612150456

 PubMed Web of Science ®Google Scholar

RamalhinhoACFonseca-MoutinhoJABreitenfeld GranadeiroLAPositive association of polymorphisms in estrogen biosynthesis gene, CYP19A1, and metabolism, GST, in breast cancer susceptibilityDNA Cell Biol20123161100110622300440

 PubMed Web of Science ®Google Scholar