Associations between dopamine D2 receptor gene polymorphisms and schizophrenia risk: a PRISMA compliant meta-analysis

Figures & data

Figure 1 Flow diagram of the study selection process.

Abbreviations: CNKI, China National Knowledge Infrastructure; DRD2, dopamine D2 receptor.

Table 1 Characteristics of case–control studies on DRD2 gene polymorphisms and schizophrenia risk included in the meta-analysis

Author	Year	Country	Ethnicity	No of sample		Control sources	Mutation analysis method	Criteria	SNP	HWE (P-value)	Quality score
				Cases	Controls
Caprini et al^Citation28	2011	Scandinavia	Caucasians	837	1,471	PB	–	ICD-10 + DSM-III-R + DSM-IV	TaqID	Yes	5
Dollfus et al^Citation35	1996	France	Caucasians	62	161	PB	PCR-RFLP	DSM-III-R	TaqIA	Yes	8
Luo^Citation24	2008	China	Asians	211	201	PB	Direct sequencing	DSM-IV	−141C Ins/Del	Yes	6
Watanabe et al^Citation36	2012	Japan	Asians	648	664	PB	TaqMan	DSM-IV	Ser311Cys	Yes	7
Crawford et al^Citation31	1996	America	Caucasians	84	81	HB	Direct sequencing	DSM-III-R	Ser311Cys	Yes	6
Dubertret et al^Citation13	2010	France	Caucasians	50	50	PB	PCR	DSM-IV	TaqIB	–	–
									TaqIA	Yes	7
Himei et al^Citation37	2002	Japan	Asians	190	103	PB	PCR-RFLP	DSM-IV	Ser311Cys	Yes	7
									−141C Ins/Del	Yes	7
Jonsson et al^Citation87	1996	Sweden	Caucasians	118	78	PB	PCR	DSM-III-R	TaqIA	Yes	7
Kunii et al^Citation62	2014	Japan	Asians	12	12	PB	PCR-RFLP	DSM-IV	TaqIA	Yes	8
Srivastava et al^Citation4	2010	India	Caucasians (Indians)	233	224	PB	PCR-RFLP	DSM-IV	−141C Ins/Del	Yes	8
									TaqIA	Yes	8
									TaqIB	–	–
									Ser311Cys	Yes	8
Arinami et al^Citation47	1996	Japan	Asians	136	279	PB	PCR	ICD-10 + DSM-III-R	Ser311Cys	Yes	7
Arinami et al^Citation57	1997	Japan	Asians	260	312	PB	PCR-RFLP	DSM-III-R	−141C Ins/Del	Yes	7
Aslan et al^Citation23	2010	Turkey	Caucasians	99	109	PB	PCR	DSM-IV	TaqIA	No	6
Behravan et al^Citation11	2008	Iran	Caucasians	38	63	PB	PCR	DSM-IV	TaqIB	Yes	7
									TaqIA	No	6
Betcheva et al^Citation1	2009	Bulgaria	Caucasians	255	556	PB	PCR	DSM-IV	C957T	Yes	8
									C939T	Yes	8
Breen et al^Citation63	1999	England	Caucasians	439	437	PB	PCR	DSM-III-R + DSM-IV	−141C Ins/Del	Yes	7
Chen et al^Citation38	1996	China	Asians	114	88	PB	PCR	DSM-III-R	Ser311Cys	Yes	6
Cordeiro et al^Citation14	2009	Brazil	Mixed	229	733	PB	–	DSM-IV	−141C Ins/Del	Yes	8
Cordeiro and Vallada^Citation16	2014	Brazil	Mixed	235	834	PB	PCR	DSM-IV	TaqIA	Yes	8
Dubertret et al^Citation15	2004	France	Caucasians	103	83	PB	PCR-RFLP	DSM-IV	−141C Ins/Del	Yes	7
									TaqIB	–	–
									TaqID	–	–
									Ser311Cys	Yes	7
									TaqIA	Yes	7
Dubertret et al^Citation13	2010	France	Caucasians	144	142	PB	TaqMan	DSM-IV	TaqIA	Yes	8
									C957T	–	–
									Ser311Cys	Yes	8
									−141C Ins/Del	Yes	8
									TaqID	–	–
									TaqIB	–	–
Fan et al^Citation39	2010	China	Asians	421	404	PB	PCR	DSM-IV	Ser311Cys	Yes	7
									C957T	Yes	7
									C939T	Yes	7
Golimbet et al^Citation40	2011	Russia	Caucasians	366	387	PB	PCR	ICD-10	Ser311Cys	Yes	8
Gupta et al^Citation41	2009	India	Caucasians (Indians)	254	225	PB	PCR	DSM-IV	−141C Ins/Del	Yes	8
									Ser311Cys	Yes	8
									C957T	Yes	8
									C939T	Yes	8
Hanninen et al^Citation64	2006	Finland	Caucasians	188	384	PB	PCR	DSM-IV	C957T	Yes	8
Harano^Citation42	1997	Japan	Asians	70	101	HB	PCR	DSM-III-R	Ser311Cys	Yes	6
Hoenicka et al^Citation65	2006	Spain	Caucasians	131	364	PB	PCR	DSM-IV	C957T	Yes	7
Hori et al^Citation43	2001	Japan	Asians	241	201	PB	PCR	DSM-IV	Ser311Cys	Yes	7
									−141C Ins/Del	Yes	7
Iwata et al^Citation44	2003	Japan	Asians	51	63	PB	PCR-RFLP	DSM-IV	Ser311Cys	Yes	7
Jonsson et al^Citation66	1999	Sweden	Caucasians	129	179	HB	PCR	DSM-III-R	−141C Ins/Del	Yes	6
Jonsson et al^Citation45	2003	Sweden	Caucasians	173	236	HB	PCR	DSM-III-R	Ser311Cys	Yes	6
Kaneshima et al^Citation46	1997	Japan	Asians	78	112	PB	PCR	RDC + DSM-IV	Ser311Cys	Yes	7
Kukreti et al^Citation2	2006	India	Caucasians (Indians)	101	145	PB	PCR	DSM-IV	C957T	Yes	8
									C939T	Yes	8
Kurt et al^Citation67	2011	Turkey	Caucasians	73	60	PB	PCR-RFLP	DSM-IV	−141C Ins/Del	Yes	7
Lafuente et al^Citation68	2008	Spain	Caucasians	243	291	HB	PCR	DSM-IV	TaqIB	Yes	7
									TaqIA	Yes	7
									−141C Ins/Del	Yes	7
Laurent et al^Citation48	1994	France	Caucasians	113	184	PB	–	DSM-III-R	Ser311Cys	Yes	6
Lawford et al^Citation10	2005	Australia	Caucasians	154	148	PB	PCR	DSM-IV	C957T	Yes	7
Li et al^Citation70	1998	England	Caucasians	151	145	HB	PCR	DSM-IV + DSM-III-R	−141C Ins/Del	Yes	6
Monakhov et al^Citation69	2008	Russia	Caucasians	311	364	PB	PCR	DSM-IV	C957T	Yes	7
									C939T	Yes	7
									TaqIA	Yes	7
Ohara et al^Citation3	1996	Japan	Asians	153	121	PB	PCR	DSM-IV	Ser311Cys	Yes	7
Ohara et al^Citation71	1998	Japan	Asians	170	121	PB	PCR	DSM-IV	−141C Ins/Del	Yes	8
Parsons et al^Citation25	2007	Spain	Caucasians	119	165	PB	PCR-RFLP	DSM-IV	−141C Ins/Del	Yes	7
									TaqIA	No	6
Saiz et al^Citation72	2010	Spain	Caucasians	288	421	PB	PCR-RFLP	DSM-IV	−141C Ins/Del	Yes	9
Sanders et al^Citation49	2008	Europe	Caucasians	1,870	2,002	PB	TaqMan	DSM-IV	Ser311Cys	Yes	8
									−141C Ins/Del	Yes	8
Sasaki et al^Citation26	1996	Europe	Caucasians	273	255	HB	PCR	DSM-III-R	Ser311Cys	Yes	5
Spurlock et al^Citation50	1998	Europe	Caucasians	373	413	PB	PCR	DSM-III-R	Ser311Cys	Yes	7
Stöber et al^Citation73	1998	German	Caucasians	260	290	PB	PCR	ICD-10	−141C Ins/Del	Yes	7
Tallerico et al^Citation74	1999	America	Caucasians	50	51	PB	PCR	DSM-III-R	−141C Ins/Del	Yes	7
Tanaka et al^Citation51	1996	Japan	Asians	106	106	PB	PCR	DSM-III-R	Ser311Cys	Yes	7
Tsutsumi et al^Citation22	2011	Japan	Asians	407	384	PB	PCR-RFLP	DSM-IV	C957T	Yes	7
									Ser311Cys	No	6
Verga et al^Citation52	1997	Italy	Caucasians	103	97	PB	PCR	DSM-III-R	Ser311Cys	Yes	7
Fujiwara et al^Citation54	1997	Japan	Asians	52	26	PB	PCR	DSM-IV + ICD-10	Ser311Cys	Yes	7
Kampman et al^Citation75	2003	Finland	Caucasians	93	94	PB	PCR	DSM-IV	−141C Ins/Del	Yes	7
Morimoto et al^Citation55	2002	Japan	Asians	48	48	PB	PCR	DSM-IV + ICD-10	Ser311Cys	Yes	7
Vijayan et al^Citation19	2007	India	Caucasians (Indians)	213	196	PB	PCR	DSM-IV	TaqIB	Yes	8
									TaqIA	Yes	8
									TaqID	Yes	8
									C939T	Yes	8
									Ser311Cys	Yes	8
Xiao et al^Citation76	2013	China	Asians	120	100	PB	PCR	DSM-IV-TR	−141C Ins/Del	Yes	7
Comings et al^Citation77	1991	America	Caucasians	87	69	HB	PCR	DSM-III-R	TaqIA	Yes	7
Sanders et al^Citation78	1993	America	Caucasians	55	51	PB	PCR-RFLP	DSM-III-R + RDC	TaqIA	Yes	8
Campion et al^Citation79	1994	France	Caucasians	80	80	PB	PCR-RFLP	DSM-III-R	TaqIA	Yes	7
Itokawa et al^Citation58	1993	Japan	Asians	50	110	PB	PCR-RFLP SSCP analysis	DSM-III-R	Ser311Cys	Yes	7
Nothen et al^Citation34	1993	German	Caucasians	60	60	PB	PCR	DSM-III-R	TaqIA	Yes	7
Arinami et al^Citation9	1994	Japan	Asians	156	300	HB	PCR	DSM-III-R	Ser311Cys	Yes	6
Asherson et al^Citation59	1994	England	Caucasians	112	64	PB	PCR	DSM-III-R	Ser311Cys	Yes	6
Gejman et al^Citation61	1994	America	Caucasians	106	113	HB	PCR-RFLP	DSM-III-R	Ser311Cys	Yes	7
Hattori et al^Citation27	1994	Japan	Asian	100	100	PB	PCR-RFLP	DSM-III-R	Ser311Cys	No	6
Nanko et al^Citation60	1994	Japan	Asian	100	100	PB	PCR	DSM-III-R	Ser311Cys	Yes	6
Nothen et al^Citation34	1993	German	Caucasians	179	138	PB	PCR	DSM-III-R	Ser311Cys	Yes	7
Shaikh et al^Citation29	1994	England	Caucasians	147	100	HB	PCR	DSM-III-R	Ser311Cys	No	5
Sobell et al^Citation30	1994	America	Caucasians	338	1,914	HB	–	–	Ser311Cys	Yes	5
Inada et al^Citation80	1999	Japan	Asian	234	94	PB	PCR	ICD-10	−141C Ins/Del	Yes	8
Serretti et al^Citation81	2000	Italy	Caucasians	366	267	HB	–	–	Ser311Cys	Yes	–
Itokawa et al^Citation53	2010	Japan	Asian	156	300	HB	SSCP	DSM-III-R	Ser311Cys	Yes	7
				291	579		PCR
Li^Citation82	2014	China	Asian	915	421	PB	PCR-AFLP Sequenom MassARRAY	ICD-10 + CCMD-II-R	TaqIA	Yes	7
Fan et al^Citation56	1996	China	Asian	105	108	PB	PCR	ICD-10	Ser311Cys	Yes	7
Liu et al^Citation33	2012	China	Asian	317	310	PB	PCR	DSM-IV	TaqIA	Yes	7
Liu et al^Citation83	2009	China	Asian	128	124	PB	PCR-RFLP	CCMD-3	−141C Ins/Del	Yes	7
Luo^Citation24	2008	China	Asian	512	480	PB	PCR	DSM-IV	−141C Ins/Del	Yes	7
									Ser311Cys	No	6
									C957T	Yes	7
									C939T	Yes	7
									TaqIA	No	6
Shen et al^Citation84	2011	China	Asian	120	100	PB	PCR	DSM-IV	−141C Ins/Del	Yes	7
Zhang et al^Citation85	2003	China	Asian	67	77	PB	PCR	CCMD-II-R	TaqIA	Yes	6
Zheng^Citation18	2012	China	Asian	92	96	PB	PCR	–	C957T	Yes	6
									C939T	Yes	6
									Ser311Cys	Yes	6
Liang^Citation86	2005	China	Asian	101	105	PB	PCR	DSM-IV + CCMD-3	−141C Ins/Del	Yes	7

Abbreviations: AFLP, amplified fragment length polymorphism; CC, complication or comorbidity; CCMD, Chinese Classification of Mental Disorders; DSM, The Diagnostic and Statistical Manual of Mental Disorder; HB, hospital-based; PB, population-based; HWE, Hardy–Weinberg equilibrium; ICD-10, International Statistical Classification of Diseases and Related Health Problems – 10th version; PCR, polymerase chain reaction; RDC, Research Diagnostic Criteria; SNP, single-nucleotide polymorphisms; RFLP, restriction fragment length polymorphism.

Figure 2 Calculated OR and 95% CI for the associations between DRD2 gene polymorphism and schizophrenia risk.

Notes: (A) rs1801028; (B) rs6277; (C) rs1799732; (D) rs1800497. weights are from random effects analysis.
Abbreviations: CI, confidence interval; DRD2, dopamine D2 receptor; OR, odds ratio.

Table 2 Subgroup analysis of case–control studies on DRD2 gene polymorphisms and schizophrenia risk

SNP	Subgroup type	Subgroup	N	P-value	OR	95% CI	I^2 (%)
rs1801028	Control sources	Population-based	31	0.99	1.00	0.88, 1.14	0
		Hospital-based	11	<0.01	1.91	1.39, 2.61	31
	Ethnicity	Caucasians	19	0.09	1.22	0.97, 1.54	41
		Asians	23	0.04	1.25	1.01, 1.55	31
rs6277	Ethnicity	Caucasians	8	<0.01	0.72	0.66, 0.79	0
		Asians	4	0.37	1.17	0.83, 1.64	46
rs1799732	Control sources	Population-based	24	0.36	0.92	0.78, 1.10	77
		Hospital-based	3	0.46	0.81	0.47, 1.41	71
	Ethnicity	Caucasians	15	0.33	1.11	0.90, 1.36	71
		Asians	11	0.004	0.76	0.63, 0.92	56
		Mixed	1	0.002	0.61	0.44, 0.83	–
rs1800497	Control sources	Population-based	20	0.02	0.84	0.72, 0.97	71
		Hospital-based	2	0.46	1.50	0.51, 4.47	86
	Ethnicity	Caucasians	16	0.24	0.88	0.72, 1.08	71
		Asians	5	0.29	0.85	0.63, 1.15	82
		Mixed	1	0.06	0.82	0.66, 1.01	–

Abbreviations: CI, confidence intervals; DRD2, dopamine D2 receptor; OR, odds ratios; SNP, single-nucleotide polymorphisms.

Figure 3 Sensitivity analysis via deletion of each individual study reflecting the relative influence of each individual dataset on the pooled ORs for the rs1801028.

Abbreviations: CI, confidence interval; OR, odds ratio.

Figure 4 Cumulative meta-analyses according to publication year for the rs1801028.

Figure 5 Trim-and-fill plot to correct publication bias for the rs1801028.

Abbreviation: SE, standard error.

Table S1 Scale for quality assessment

Criteria	Score
Representativeness of cases
Consecutive/randomly selected form case population with clearly defined sampling frame	2
Consecutive/randomly selected form case population without clearly defined sampling frame or with extensive	1
Not described	0
Definition of the DR
Population- or health-based	2
Hospital-bases	1
Not described	0
Hardy–Weinberg equilibrium in controls
Hardy–Weinberg equilibrium	2
Hardy–Weinberg disequilibrium	1
Genotyping examination
Genotyping done under “blinded” condition	1
Unblinded done or not mentioned	0
Association assessment
Assess association between genotypes and head and neck cancer with appropriate statistics and adjustment for confounders	2
Assess association between genotypes and head and neck cancer with appropriate statistics and without adjustment for confounders	1
Inappropriate statistics used	0

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