Association between the SLC6A4 gene and schizophrenia: an updated meta-analysis

Figures & data

Figure 1 Study selection process in this meta-analysis.

Abbreviations: CNKI, China National Knowledge Infrastructure; 5-HTTLPR, serotonin-transporter-linked polymorphic region; STin2 VNTR, second intron variable number of tandem repeats.

Table 1 Characteristics of the qualified studies in this meta-analysis

Authors	Year	Country	Ethnicity	Controls source	Mean age of the control group	Cases, n	Controls, n	Diagnostic criteria	Gender index (case)	Gender index (control)
Li and Li^Citation65	2013	People’s Republic of China	Han	Population-based	27.7±8.0	526	528	DSM-IV	1.000	1.000
Frtdtrique et al^Citation69	1997	France	Caucasians	Population-based	–	105	114	DSM-III-R	0.438	0.932
Pae et al^Citation36	2005	Korea	Korea	Hospital-based	–	111	172	DSM-IV	1.090	0.000
Saiz et al^Citation37	2007	Spain	Caucasians	Population-based	40.6±11.3	227	420	DSM-IV	0.667	0.961
Naylor et al^Citation38	1998	Australia	Caucasians	Population-based	–	58	62	DSM-III-R	–	–
Liu et al^Citation70	1999	People’s Republic of China	Han	Population-based	42.0±10.0	260	362	DSM-III-R	0.709	0.813
Ikeda et al^Citation39	2006	Japan	Japanese	Population-based	33.6±12.9	287	288	DSM-IV	0.939	0.92
Lin et al^Citation71	2009	People’s Republic of China	Han	Population-based	37.0±8.16	329	288	DSM-IV	0.621	0.811
Vijayan et al^Citation40	2009	Indian	Indian	Population-based	31.7±6.92	243	243	DSM-IV	–	–
Lee et al^Citation41	2009	Korea	Korea	Population-based	–	141	115	DSM-IV	–	–
Pae et al^Citation42	2003	Korea	Korea	Hospital-based	30.3±9.4	111	208	DSM-IV	1.096	0.818
Gu et al^Citation43	2013	People’s Republic of China	Han	Population-based	22.4±6.6	404	385	ICD-10	0.515	0.629
Kaiser et al^Citation16	2001	Germany	Caucasians	Population-based	30.1±7.6	684	587	DSM-IV	0.887	0.289
Tsai et al^Citation72	2002	People’s Republic of China	Han	Hospital-based	42.8±9.2	114	127	DSM-III-R	1.426	1.822
Herken et al^Citation44	2003	Turkey	Caucasians	Population-based	–	143	68	DSM-IV	1.860	–
Serretti et al^Citation45	2002	Raffaele	Caucasians	Hospital-based	46.0±15.5	261	457	DSM-IV	–	1.041
Tsai et al^Citation67	2000	People’s Republic of China	Han	Population-based	49.6±0.8	90	104	DSM-IV	0.525	2.596
Han et al^Citation46	2004	Korea	Korean	Hospital-based	–	168	158	DSM-IV	–	–
Zaboli et al^Citation47	2008	European	Caucasians	Population-based	41.0±11.2	155	246	DSM-III-R	0.667	0.629
Golimbet et al^Citation48	2017	Russian	Russian	Population-based	34.3±18.1	1,285	1,061	ICD-10	1.633	2.333
Herken et al^Citation73	2002	Turkish	Turkish	Population-based	–	128	135	DSM-IV	–	–
Peitl et al^Citation49	2017	Croatia	Croatia	Population-based	37.6±11.5	300	291	DSM-IV	0.376	0.865
Carlstrom et al^Citation76	2012	Scandinavia	Caucasians	Population-based	–	837	1,473	DSM-IV	–	–
Terzic et al^Citation50	2015	Ljubljana	Slovenian	Population-based	–	138	94	DSM-IV	–	–
Lu et al^Citation68	2012	the Netherland and Germany	Caucasians	Population-based	–	2,030	1,288	DSM-IV	–	–
Golimbet et al^Citation51	2010	Russian	Russian	Population-based	55.6±20.5	58	62	ICD-10	0.277	0.824
Golimbet et al^Citation52	2003	Russian	Russian	Hospital-based	31.6±13.5	110	124	ICD-10	0.746	1.696
Stober et al^Citation53	1998	German	Caucasians	population-based	29.9±10.0	180	223	ICD-10	0.622	0.701
Collier et al^Citation74	1996	European	Caucasians	Population-based	–	129	187	DSM-III-R	–	–
Kotler et al^Citation54	1999			Population-based	28.0±15.0	82	821	ICD-10	0.586	1.61
Rao et al^Citation55	1998	The USA	Caucasians	Population-based	30.0±10.0	80	127	DSM-IV	0.667	1.953
Rao et al^Citation55	1998	The USA	African American	Population-based	30.0±8.0	47	37	DSM-IV	0.741	1.313
Pakhomova et al^Citation56	2011	Russian	Russian	Population-based	18.9±6.7	65	111	ICD-10	0.444	0.609
Mendes de Oliveira et al^Citation57	1998	European	Caucasians	Hospital-based	–	39	89	DSM-IV	–	–
Bayle et al^Citation58	2003	French	Caucasians	Hospital-based	35.0±10.0	185	159	DSM-IV	0.434	0.529
Mata et al^Citation59	2004	Spain	Caucasians	Population-based	26.9±5.5	187	278	DSM-IV	0.680	0.887
Sanjuan et al^Citation60	2006	Spain	Caucasians	Population-based	–	158	138	DSM-IV	0.500	–
Pal et al^Citation79	2009	Croatian	Caucasians	Population-based	50.3±7.5	104	131	ICD-10	0.705	–
Chong et al^Citation61	2000		East Asia	Population-based	–	338	103	DSM-IV	0.565	–
Pae et al^Citation62	2006	Koreans	Koreans	Hospital-based	–	152	152	DSM-IV	–	–
Young et al^Citation63	2006	The USA	Caucasians	Population-based	–	12	15	DSM-IV	–	–
Jing et al^Citation64	2016	People’s Republic of China	Han	Population-based	30.9±6.7	624	683	DSM-IV	0.830	0.882
Li et al^Citation78	2013	People’s Republic of China	Han	Population-based	33.1±11.8	189	300	DSM-IV	2.316	2.297
Yang et al^Citation75	2001	People’s Republic of China	Han	Population-based	–	260	362	DSM-III-R	–	–
Zuo et al^Citation66	2003	People’s Republic of China	Han	Hospital-based	–	157	185	CCMD-II-R	0.622	0.312
Xuan et al^Citation77	2012	People’s Republic of China	Han	Population-based	–	132	150	DSM-IV	1.000	1.000

Abbreviations: CCMD-II-R, Chinese Classification of Mental Disorders, Second Edition, Revised; DSM-III-R, Diagnostic and Statistical Manual of Mental Disorders, Third Edition, Revised; DSM-IV, Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition; ICD-10, International Classification of Diseases-10.

Table 2 Genotype distribution and allele frequency of 5-HTTLPR

Authors	Year	Genotype distribution						PHWE	Allele frequency
		Cases, n			Controls, n				Cases, %		Controls, %
		LL	LS	SS	LL	LS	SS		L	S	L	S
Pae et al^Citation36	2005	4	35	72	10	49	113	0.143	43	179	69	275
Saiz	2007	64	104	59	124	203	93	0.566	232	222	451	389
Naylor et al^Citation38	1998	11	30	17	19	29	14	0.646	52	64	67	57
Ikeda et al^Citation39	2006	16	82	189	12	101	175	0.588	114	460	125	451
Vijayan et al^Citation40	2009	40	123	79	62	118	61	0.748	203	281	242	240
Lee et al^Citation41	2009	7	52	82	3	45	67	0.151	66	216	51	179
Pae et al^Citation42	2003	4	35	72	11	58	139	0.140	43	179	80	336
Gu et al^Citation43	2013	14	101	289	7	90	288	0.992	129	679	104	666
Kaiser et al^Citation16	2001	253	324	107	207	286	94	0.772	830	538	700	474
Herken et al^Citation44	2003	30	70	40	17	24	27	0.022	130	150	58	78
Serretti et al^Citation45	2002	89	121	51	165	217	75	0.800	299	223	547	367
Tsai et al^Citation67	1999	9	28	53	15	30	59	0.002	46	134	60	148
Han et al^Citation46	2004	7	52	109	8	54	96	0.910	66	270	70	246
Zaboli et al^Citation47	2008	56	73	26	75	126	45	0.532	185	125	276	216
Golimbet et al^Citation48	2017	486	595	204	413	503	145	0.677	1,567	1,003	1,329	793
Peitl et al^Citation49	2017	118	124	58	103	138	50	0.746	360	240	344	238
Terzic	2015	52	71	15	47	34	13	0.104	175	101	128	60
Lu et al^Citation68	2012	407	626	254	690	992	345	0.719	1,440	1,134	2,372	1,682
Golimbet et al^Citation51	2010	27	20	11	22	28	12	0.567	74	42	72	52
Golimbet et al^Citation52	2003	42	46	22	45	57	22	0.594	130	90	147	101
Stober	1998	58	90	32	79	112	42	0.834	206	154	270	196
Kotler et al^Citation54	1999	24	38	20	210	446	165	0.010	86	78	866	776
Rao et al^Citation55	1998	28	32	20	43	59	25	0.559	88	72	145	109
Rao et al^Citation55	1998	25	18	4	18	12	7	0.079	68	26	48	26
Pakhomova	2011	20	37	8	43	48	20	0.310	77	53	134	88
Mendes de Oliveira et al^Citation57	1998	12	21	6	39	43	16	0.480	45	33	121	75
Bayle et al^Citation58	2003	48	99	38	40	83	36	0.573	195	175	163	155
Mata et al^Citation59	2004	41	102	44	63	124	91	0.100	184	190	250	306
Sanjuan et al^Citation60	2006	33	78	47	44	68	26	0.976	144	172	156	120
Chong et al^Citation61	2000	33	130	175	13	32	58	0.019	196	480	58	148
Pae et al^Citation62	2006	5	46	101	9	47	96	0.322	56	248	65	239
Young	2006	2	5	5	6	7	2	0.985	9	15	19	11
Jing et al^Citation64	2016	51	267	306	66	248	369	0.012	369	879	380	986
Li et al^Citation78	2013	5	35	149	24	134	142	0.325	45	333	182	418
Zuo	2003	15	50	92	21	49	115	0.000	80	234	91	279

Abbreviations: 5-HTTLPR, serotonin-transporter-linked polymorphic region; P_HWE, P-value of Hardy–Weinberg equilibrium.

Table 3 Pooled association of SLC6A4 polymorphisms with schizophrenia

Loci	Genetic model	Studies (n)	Statistical	OR	95% CI	Pz	I^2	Ph	Pe
5-HTTLPR	Allele contrast	35	Random	0.934	0.868–1.004	0.066	53.6	0.000	0.587
	Homozygous codominant	35	Random	1.142	0.782–0.980	0.021	15.6	0.206	0.912
	Heterozygous codominant	35	Random	1.066	0.980–1.161	0.138	7.7	0.340	0.165
	Dominant	35	Random	1.085	0.999–1.178	0.054	10.4	0.294	0.211
	Recessive	35	Random	1.082	0.961–1.218	0.195	57.8	0.000	0.846
STin2 VNTR	10R vs others	17	Random	0.884	0.725–1.077	0.221	82.8	0.000	0.951
	12R vs others	17	Random	1.134	0.931–1.381	0.21	82.8	0.000	0.936
	10R/10R vs others	17	Random	0.907	0.624–1.319	0.611	78.9	0.000	0.401
	10R/12R vs others	17	Random	0.789	0.646–0.963	0.020	71.1	0.000	0.748
	12R/12R vs others	17	Random	1.936	1.238–3.029	0.004	94.7	0.000	0.474
rs1042173	Contrast	4	Random	1.094	0.962–1.245	0.17	22.7	0.275	0.412
	Homozygous codominant	4	Random	1.214	0.921–1.600	0.169	26.4	0.253	0.336
	Heterozygous codominant	4	Random	1.011	0.812–1.260	0.920	18.0	0.301	0.941
	Dominant	4	Random	1.077	0.856–1.354	0.528	26.9	0.250	0.722
	Recessive	4	Random	1.199	0.994–1.445	0.057	14.5	0.320	0.155
rs140700	Allele contrast	4	Random	1.052	0.519–1.734	0.863	92.9	0.000	0.359
	Homozygous codominant	4	Random	0.809	0.236–2.774	0.736	63.7	0.041	0.223
	Heterozygous codominant	4	Random	0.971	0.500–1.884	0.931	91.9	0.000	0.685
	Dominant	4	Random	1.003	0.503–1.999	0.993	93.2	0.000	0.560
	Recessive	4	Random	0.830	0.284–2.422	0.733	53.5	0.092	0.333

Abbreviations: 5-HTTLPR, serotonin-transporter-linked polymorphic region; P_z, P_h, and P_e, P-values of association, heterogeneity, and publication bias tests, respectively; R, repeats; STin2 VNTR, second intron variable number of tandem repeats.

Table 4 Subgroup association of SLC6A4 polymorphisms with schizophrenia

Loci	Subgroup analysis	Studies (n)	OR	95% CI	Pz	I^2	Ph
5HTTLPR	Caucasians	21	1.053	0.974–1.138	0.192	1.6	0.437
	East Asia	12	1.204	0.953–1.521	0.119	4.1	0.404
	African American	1	0.834	0.352–1.975	0.679	0.0	0.000
	Indians	1	1.749	1.120–2.731	0.014	0.0	0.000
	Population-based	26	1.089	0.982–1.209	0.131	28.3	0.090
	Hospital-based	9	1.094	0.897–1.335	0.273	0.0	0.939
STin2 VNTR 1010	Caucasians	9	0.883	0.645–1.207	0.435	63.7	0.005
	East Asia	7	0.857	0.310–2.374	0.767	75.5	0.00
	Indians	1	0.639	0.368–1.108	0.111	–	0.000
	Population-based	16	0.930	0.639–1.354	0.704	79.8	0.000
	Hospital-based	1	0.155	0.008–3.040	0.220	–	–
1012	Caucasians	9	0.944	0.832–1.072	0.374	0.0	0.706
	East Asia	7	0.617	0.389–0.978	0.040	80.8	0.000
	Indians	1	0.635	0.441–0.913	0.014	–	–
	Population-based	16	0.794	0.646–0.976	0.028	72.8	0.000
	Hospital-based	1	0.667	0.290–1.536	0.341	–	–
1212	Caucasians	9	1.042	0.916–1.186	0.531	0.0	0.885
	East Asia	7	4.482	2.312–8.689	0.000	92.1	0.000
	Indians	1	1.573	1.086–2.280	0.170	–	–
	Population-based	16	1.755	1.124–2.742	0.013	94.5	0.000
	Hospital-based	1	10.689	5.303–21.544	0.000	–	–
rs1042173	Caucasians	2	1.299	1.0791.565	0.006	0.0	0.421
	East Asia	1	0.834	0.5171.346	0.458	–	–
	Indians	1	1.213	0.7981.843	0.365	–	–
rs140700	Caucasians	2	1.253	0.8271.896	0.287	42.6	0.187
	East Asia	2	0.757	0.2152.670	0.665	93.5	0.000

Abbreviations: 5-HTTLPR, serotonin-transporter-linked polymorphic region; P_z and P_h, P-values of association and heterogeneity, respectively; STin2 VNTR, second intron variable number of tandem repeats.

Table 5 Genotype distribution and allele frequency of STin2 VNTR

Authors	Year	Genotype distribution						Allele frequency
		Case			Control			Case					Control
		10	12	Others	10	12	Others	1010	1012	1212	Others	1010	1012	1212	Others
Frtdtrique	1997	84	120	6	79	143	6	24	36	39	6	18	41	50	5
Saiz	2007	171	281	2	305	530	5	42	86	97	2	64	177	174	5
Liu et al^Citation70	1999	22	498	0	58	665	1	2	18	240	0	5	48	308	1
Ikeda et al^Citation39	2006	51	523	0	46	530	0	1	49	237	0	3	40	245	0
Lin et al^Citation71	2009	55	425	0	107	457	0	6	43	191	0	9	89	184	0
Vijayan et al^Citation40	2009	137	343	0	189	297	0	24	89	127	0	36	117	90	0
Lee et al^Citation41	2009	36	246	0	23	207	0	4	28	109	0	3	17	95	0
Kaiser et al^Citation16	2001	493	835	40	485	668	21	95	291	259	39	108	259	199	21
Tsai et al^Citation72	2002	10	218	0	22	232	0	0	10	104	0	3	16	108	0
Herken et al^Citation44	2003	82	204	0	31	59	0	12	58	73	0	8	15	22	0
Zaboli et al^Citation47	2008	122	184	0	176	302	0	30	62	61	0	29	118	92	0
Herken et al^Citation73	2002	72	184	0	71	198	1	9	54	65	0	7	57	70	1
Stober	1998	141	217	2	204	254	8	29	83	66	2	54	96	75	8
Collier et al^Citation74	1996	94	162	2	169	202	3	19	56	52	2	42	85	57	3
Mata et al^Citation59	2004	103	221	0	178	288	0	15	73	74	0	37	104	92	0
Li et al^Citation78	2013	333	45	0	418	182	0	149	35	5	0	142	134	24	0
Yang	2001	22	498	0	58	665	1	2	18	240	0	5	48	308	1

Abbreviation: STin2 VNTR, second intron variable number of tandem repeats.

Table 6 Genotype distribution and allele frequency of rs1042173

Authors	Year	Genotype distribution						PHWE	Allele frequency
		Cases, n			Controls, n				Cases, %		Controls, %
		GG	GT	TT	GG	GT	TT		G	T	G	T
Vijayan et al^Citation40	2009	63	119	50	55	112	67	0.538	245	219	222	246
Zaboli et al^Citation47	2008	39	78	38	58	129	59	0.444	156	154	245	247
Carlstrom	2012	207	402	223	291	770	410	0.039	816	848	1,352	1,590
Xuan et al^Citation77	2012	77	43	12	94	48	8	0.568	197	67	236	64

Abbreviation: P_HWE, P-value of Hardy–Weinberg equilibrium.

Table 7 Genotype distribution and allele frequency of rs140700

Authors	Year	Genotype distribution						PHWE	Allele frequency
		Cases, n			Controls, n				Cases, %		Controls, %
		GG	GA	AA	GG	GA	AA		G	A	G	A
Li et al^Citation78	2013	369	127	30	259	212	57	0.173	865	187	730	326
Lin et al^Citation71	2009	277	30	2	244	18	1	0.295	584	34	506	20
Carlstrom	2012	689	140	2	1,233	221	10	0.977	1,518	144	2,687	241
Pal et al^Citation79	2009	80	19	5	112	18	1	0.769	179	29	242	20

Abbreviation: P_HWE, P-value of Hardy–Weinberg equilibrium.

Figure 2 Funnel plot analysis on the detection of publication bias in the association between 5-HTTLPR (SS + LS vs LL) and schizophrenia.

Abbreviation: 5-HTTLPR, serotonin-transporter-linked polymorphic region.

Figure 3 Funnel plot analysis on the detection of publication bias in the association between STin2 VNTR (10R/10R vs others) and schizophrenia.

Abbreviation: STin2 VNTR, second intron variable number of tandem repeats.

Figure 4 Funnel plot analysis on the detection of publication bias in the association between STin2 VNTR (10R/12R vs others) and schizophrenia.

Abbreviation: STin2 VNTR, second intron variable number of tandem repeats.

Figure 5 Funnel plot analysis on the detection of publication bias in the association between STin2 VNTR (12R/12R vs others) and schizophrenia.

Abbreviation: STin2 VNTR, second intron variable number of tandem repeats.

Figure 6 Funnel plot analysis on the detection of publication bias in the association between rs1042173 (GG vs GT + TT) and schizophrenia.

Figure 7 Funnel plot analysis on the detection of publication bias in the association between rs140700 (AA + AG vs GG) and schizophrenia.

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