Influence of MDM2 polymorphisms on squamous cell carcinoma susceptibility: a meta-analysis

Figures & data

Figure 1 Flow diagram of article-search strategy for meta-analysis.

Abbreviation: SCC, squamous cell carcinoma.

Table 1 Characteristics of studies included for meta-analysis

Study	Country	Ethnicity	SNPs	Case		SCC type	Control		Source of control	Genotyping assay	HUE P-value
				Total	MM/Mm/mm		Total	MM/Mm/mm
Alhopuro et al^Citation31	Finland	Caucasian	rs2279744	157	58/75/24	HNSCC	185	56/98/31	PB	PCR-RFLP and sequencing	0.28
Almquist et al^Citation4	USA	Caucasian	rs2279744	559	234/261/64	SSCC	674	323/284/67	PB	Sequenom platform	0.69
Cao et al^Citation43	People’s Republic of China	Asian	rs2279744	351	50/170/131	ESCC	642	117/299/226	PB	PIRA-PCR	0.3
			rs3730485	351	181/146/24	ESCC	642	310/285/47			0.09
Chen et al^Citation13	USA	Caucasian	rs2279744	325	146/132/47	OSCC	335	112/165/58	HB	PCR-RFLP	0.84
			rs937283	325	69/209/47	OSCC	335	114/169/52			0.41
Er et al^Citation30	People’s Republic of China	Asian	rs2279744	121	47/31/43	ESCC	142	41/78/23	PB	PCR-RFLP	0.16
Hamid et al^Citation25	Mixed	Asian	rs2279744	207	48/104/55	OSCC	116	30/58/28	PB	PCR-RFLP
Hong et al^Citation33	People’s Republic of China	Asian	rs2279744	758	203/348/207	ESCC	1,420	418/711/291	PB	PCR-RFLP	0.72
Huang et al^Citation40	People’s Republic of China	Asian	rs2279744	351	80/176/95	OSCC	1,272	274/653/345	PB	MALDI-TOF	0.29
Jiang et al^Citation39	People’s Republic of China	Asian	rs2279744	96	44/35/17	CSCC	140	30/84/26	PB	PCR-RFLP and sequencing	0.02
Kohno et al^Citation44	Japan	Asian	rs2279744	377	68/183/126	LSCC	325	79/151/95	HB	Pyrosequencing	0.22
Li et al^Citation46	People’s Republic of China	Asian	rs2279744	132	37/70/25	ESCC	132	47/71/14	PB	PCR-RFLP	0.09
Liu et al^Citation34	USA	Caucasian	rs2279744	423	178/186/59	LSCC	1,360	530/626/204	HB	TaqMan assay sequencing	0.39
Loginov et al^Citation38	Russia	Caucasian	rs2279744	59	50/9/0	LSCC	160	156/4/0	PB	PCR-RFLP	0.87
Ma et al^Citation42	People’s Republic of China	Asian	rs2279744	226	49/119/58	ESCC	226	50/118/58	PB	PCR-RFLP	0.49
			rs3730485	226	120/91/15	ESCC	226	118/92/16			0.74
Misra et al^Citation18	India	Asian	rs2279744	297	70/147/80	OSCC	328	59/181/88	PB	PCR-RFLP	0.04
Nakashima et al^Citation37	Japan	Asian	rs2279744	103	29/46/28	HNSCC	120	37/50/33	PB	Sequencing and real-time PCR	0.07
Nan et al^Citation47	USA	Caucasian	rs2279744	281	117/119/45	SSCC	851	380/356/115	PB	PCR-RFLP	0.03
Park et al^Citation36	South Korea	Asian	rs2279744	270	57/128/85	LSCC	582	122/299/161	PB	PCR-RFLP	0.44
Roszak et al^Citation32	Poland	Caucasian	rs2279744	379	139/169/71	CSCC	481	202/204/75	PB	PCR-RFLP and sequencing	0.05
Singhal et al^Citation45	India	Asian	rs2279744	182	63/74/45	CSCC	182	108/52/22	PB	PCR-RFLP and sequencing	0.00
Tu et al^Citation35	People’s Republic of China	Asian	rs2279744	189	44/93/52	OSCC	116	29/55/32	PB	Sequencing	0.58
Yang et al^Citation29	People’s Republic of China	Asian	rs937283	307	163/126/18	ESCC	311	161/126/24	PB	TaqMan assay	0.92
Yu et al^Citation41	USA	Caucasian	rs2279744	1,083	463/486/134	HNSCC	1,090	488/472/130	PB	PCR-RFLP	0.33
			rs937283	1,078	369/522/187	HNSCC	1,089	355/529/205		TaqMan assay	0.75
Zhang et al^Citation12	People’s Republic of China	Asian	rs2279744	132	37/70/25	ESCC	132	47/71/14	PB	PCR-RFLP	0.09
			rs3730485	132	17/59/56	ESCC	132	13/48/71			0.26
Zhang et al^Citation48	People’s Republic of China	Asian	rs2279744	476	113/241/122	LSCC	1,420	418/711/291	PB	ARMS-PCR	0.72
Zhou et al^Citation24	People’s Republic of China	Asian	rs2279744	146	37/58/51	Laryngeal SCC	212	35/109/68	PB	Pyrosequencing	0.43

Note: P<0.05 in bold.

Abbreviations: SNPs, single-nucleotide polymorphisms; M, major allele; m, minor allele; HNSCC, head and neck squamous cell carcinoma; SSCC, skin SCC; ESCC, esophageal SCC; OSCC, oral SCC; LSCC, lung SCC; CSCC, cervical SCC; PB, population-based; HB, hospital-based; PCR-RFLP, polymerase chain-reaction restriction fragment-length polymorphism; PIRA-PCR, primer-introduced restriction-analysis PCR; MALDI-TOF, matrix-assisted laser desorption/ionization time of flight; ARMS-PCR, amplification refractory mutation-system (tetra-primer) PCR; HUE, Hardy–Weinberg equilibrium.

Figure 2 Meta-analysis of the association between MDM2 rs2279744 and SCC susceptibility under the G vs T model.

Notes: (A) Forest plot; (B) Egger’s funnel plot of publication-bias; (C) sensitivity analysis. Weights are from random-effect analysis.
Abbreviations: SCC, squamous cell carcinoma; OR, odds ratio; CI, confidence interval.

Figure 3 Meta-analysis of the association between MDM2 rs2279744 and SCC susceptibility under the GG vs TT model.

Notes: (A) Forest plot; (B) Egger’s funnel plot of publication-bias; (C) sensitivity analysis. Weights are from random-effect analysis.
Abbreviations: SCC, squamous cell carcinoma; OR, odds ratio; CI, confidence interval.

Figure 4 Meta-analysis of the association between MDM2 rs2279744 and SCC susceptibility under the TG vs TT model.

Notes: (A) Forest plot; (B) Egger’s funnel plot of publication-bias; (C) sensitivity analysis. Weights are from random-effect analysis.
Abbreviations: SCC, squamous cell carcinoma; OR, odds ratio; CI, confidence interval.

Figure 5 Meta-analysis of the association between MDM2 rs2279744 and SCC susceptibility under the TG + GG vs TT model.

Notes: (A) Forest plot; (B) Egger’s funnel plot of publication-bias; (C) sensitivity analysis. Weights are from random-effect analysis.
Abbreviations: SCC, squamous cell carcinoma; OR, odds ratio; CI, confidence interval.

Figure 6 Meta-analysis of the association between MDM2 rs2279744 and SCC susceptibility under the GG vs TT + TG model.

Notes: (A) Forest plot; (B) Egger’s funnel plot of publication-bias; (C) sensitivity analysis. Weights are from random-effect analysis.
Abbreviations: SCC, squamous cell carcinoma; OR, odds ratio; CI, confidence interval.

Table 2 Meta analysis of the association between MDM2 polymorphisms (rs2279744, rs937283, and rs3730485) and SCC susceptibility

SNP	Comparison	No of case-control studies	Case/control total sample size	Test of association			Heterogeneity		Model	Begga		Egger
				OR	95% CI	P-value	I^2 (%)	P-value		z	P-value	t	P-value
rs2279744	G vs T	25	7,680/12,643	1.09	1–1.19	0.041	70	<0.001	R	0.05	0.963	0.43	0.671
rs2279744	GG vs TT	24	7,621/12,483	1.17	1.02–1.36	0.030	59.1	<0.001	R	0.05	0.96	−0.33	0.744
rs2279744	TG vs TT	25	7,680/12,643	1	0.87–1.15	0.975	72.9	<0.001	R	0.79	0.427	−0.48	0.637
rs2279744	TG + GG vs TT	25	7,680/12,643	1.06	0.92–1.21	0.422	73.7	<0.001	R	0.47	0.64	−0.18	0.861
rs2279744	GG vs TT + TG	24	7,621/12,483	1.18	1.07–1.3	0.001	36.3	0.04	R	0.74	0.457	0.52	0.607
rs2279744	carrier G vs T	25	7,680/12,643	1.06	1–1.13	0.064	31.5	0.068	R	0.09	0.926	0.78	0.446
rs937283	G vs A	3	1,710/1,735	1.02	0.84–1.24	0.803	67	0.048	R	0	1	0.57	0.668
rs937283	GG vs AA	3	1,710/1,735	0.99	0.69–1.43	0.957	52	0.124	R	0	1	0.33	0.795
rs937283	AG vs AA	3	1,710/1,735	1.22	0.78–1.9	0.377	85.7	0.001	R	1.04	0.296	1.05	0.485
rs937283	AG + GG vs AA	3	1,710/1,735	1.17	0.77–1.77	0.461	85.3	0.001	R	1.04	0.296	1.01	0.498
rs937283	GG vs AA + AG	3	1,710/1,735	0.89	0.74–1.08	0.231	0	0.84	F	1.04	0.296	−1.02	0.493
rs937283	carrier G vs A	3	1,710/1,735	1	0.89–1.12	0.992	9.8	0.33	F	0	1	0.59	0.659
rs3730485	− vs +	3	709/1,000	0.89	0.76–1.04	0.130	0	0.428	F	0	1	−0.81	0.567
rs3730485	−/− vs +/+	3	709/1,000	0.82	0.56–1.19	0.294	0	0.7	F	1.04	0.296	−0.69	0.614
rs3730485	+/− vs +/+	3	709/1,000	0.91	0.73–1.13	0.387	0	0.909	F	0	1	0.64	0.637
rs3730485	+/−, −/− vs +/+	3	709/1,000	0.89	0.73–1.1	0.275	0	0.809	F	0	1	−0.53	0.688
rs3730485	−/− vs +/+, +/−	3	709/1,000	0.79	0.58–1.09	0.146	0	0.5	F	0	1	0.62	0.648
rs3730485	Carrier − vs +	3	709/1,000	0.92	0.77–1.09	0.315	0	0.684	F	0	1	−0.81	0.566

Notes:

a Continuity-corrected; significant P-values in bold.

Abbreviations: SCC, squamous cell carcinoma; OR, odds ratio; CI, confidence interval; F, fixed-effect model; R, random-effect model.

Table 3 Subgroup analysis by ethnicity, source of controls, and HWE for association between MDM2 rs2279744 and SCC susceptibility

Comparison	Ethnicity		HWE		Source of control
	Asian	Caucasian	Y	N	PB	HB
G vs T
No of case-control studies	17	8	21	4	22	3
Case/control total sample size	4,414/7,507	3,266/5,136	6,824/11,142	856/1,501	6,555/10,623	1,125/2,020
OR (95% CI)	1.12 (1.01–1.24)	1.03 (0.89–1.19)	1.09 (1.01–1.17)	1.09 (0.69–1.71)	1.12 (1.03–1.22)	0.94 (0.72–1.23)
P-value	0.027	0.669	0.026	0.711	0.011	0.662
GG vs TT
No of case-control studies	17	7	20	4	21	3
Case/control total sample size	4,414/7,507	3,207/4,976	6,765/10,982	856/1,501	6,496/10,463	1,125/2,020
OR (95% CI)	1.26 (1.04–1.52)	1.03 (0.84–1.27)	1.18 (1.03–1.34)	1.13 (0.55–2.34)	1.22 (1.05–1.41)	0.94 (0.58–1.53)
P-value	0.016	0.755	0.015	0.74	0.008	0.805
TG vs TT
No of case-control studies	17	8	21	4	22	3
Case/control total sample size	4,414/7,507	3,266/5,136	6,824/11,142	856/1,501	6,555/10,623	1,125/2,020
OR (95% CI)	0.97 (0.8–1.1)	0.97 (0.8–1.19)	1.02 (0.89–1.16)	0.87 (0.42–1.77)	1.01 (0.87–1.18)	0.9 (0.6–1.36)
P-value	0.781	0.805	0.818	0.691	0.857	0.629
TG + GG vs TT
No of case-control studies	17	8	21	4	22	3
Case/control total sample size	4,414/7,507	3,266/5,136	6,824/11,142	856/1,501	6,555/10,623	1,125/2,020
OR (95% CI)	1.06 (0.88–1.28)	1.04 (0.84–1.28)	1.07 (0.95–1.2)	0.94 (0.45–1.94)	1.08 (0.94–1.25)	0.91 (0.6–1.4)
P-value	0.527	0.736	0.279	0.86	0.269	0.682
GG vs TT + TG
No of case-control studies	17	7	20	4	21	3
Case/control total sample size	4,414/7,507	3,207/4,976	6,765/10,982	856/1,501	6,496/10,463	1,125/2,020
OR (95% CI)	1.25 (1.11–1.42)	1.05 (0.92–1.2)	1.17 (1.06–1.29)	1.27 (0.88–1.83)	1.22 (1.1–1.35)	0.99 (0.78–1.24)
P-value	<0.001	0.501	0.002	0.197	<0.001	0.911
Carrier G vs T
No of case-control studies	17	8	21	4	22	3
Case/control total sample size	4,414/7,507	3,266/5,136	6,824/11,142	856/1,501	6,555/10,623	1,125/2,020
OR (95% CI)	1.08 (1.01–1.16)	1.03 (0.91–1.16)	1.06 (1.01–1.12)	1.07 (0.77–1.5)	1.08 (1.01–1.15)	1.06 (1–1.13)
P-value	0.023	0.672	0.031	0.676	0.018	0.618

Note: Significant P-values in bold.

Abbreviations: HWE, Hardy–Weinberg equilibrium; SCC, squamous cell carcinoma; PB, population-based; HB, hospital-based; Y, P-value of HWE >0.05; n, P-value of HWE <0.05; OR, odds ratio; CI, confidence interval.

Table 4 Subgroup analysis by disease type for association between MDM2 rs2279744 and SCC susceptibility

Comparison	HNSCC	SSCC	ESCC	OSCC	CSCC	LSCC
G vs T
No of case-control studies	3	2	6	5	3	5
Case/control total sample size	1,186/1,210	840/1,525	1,720/2,694	1,369/2,167	657/803	1,605/3,847
OR (95% CI)	1.03 (0.92–1.15)	1.16 (1.02–1.32)	1.19 (1.09–1.3)	0.92 (0.81–1.05)	1.19 (0.62–2.25)	1.16 (0.95–1.42)
P-value	0.659	0.022	<0.001	0.223	0.603	0.153
GG vs TT
No of case-control studies	3	2	6	5	3	4
Case/control total sample size	1,186/1,210	840/1,525	1,720/2,694	1,369/2,167	657/803	1,546/3,687
OR (95% CI)	1.03 (0.82–1.31)	1.3 (0.98–1.71)	1.46 (1.23–1.74)	0.86 (0.7–1.07)	1.33 (0.5–3.52)	1.23 (0.92–1.65)
P-value	0.788	0.067	<0.001	0.173	0.569	0.161
TG vs TT
No of case-control studies	3	2	6	5	3	5
Case/control total sample size	1,186/1,210	840/1,525	1,720/2,694	1,369/2,167	657/803	1,605/3,847
OR (95% CI)	1.02 (0.83–1.26)	1.19 (0.99–1.43)	0.98 (0.72–1.34)	0.82 (0.65–1.04)	0.96 (0.35–0.62)	1.21 (0.88–1.67)
P-value	0.83	0.062	0.916	0.103	0.941	0.249
TG + GG vs TT
No of case-control studies	3	2	6	5	3	5
Case/control total sample size	1,186/1,210	840/1,525	1,720/2,694	1,369/2,167	657/803	1,605/3,847
OR (95% CI)	1.02 (0.82–1.26)	1.22 (1.02–1.45)	1.14 (0.94–1.38)	0.84 (0.66–1.06)	1.06 (0.39–2.85)	1.26 (0.91–1.75)
P-value	0.886	0.028	0.179	0.135	0.913	0.164
GG vs TT + TG
No of case-control studies	3	2	6	5	3	4
Case/control total sample size	1,186/1,210	840/1,525	1,720/2,694	1,369/2,167	657/803	1,546/3,687
OR (95% CI)	1.01 (0.81–1.26)	1.19 (0.92–1.55)	1.48 (1.12–1.94)	0.98 (0.83–1.16)	1.42 (0.88–2.31)	1.18 (1–1.38)
P-value	0.911	0.181	0.005	0.801	0.154	0.045
Carrier G vs T
No of case-control studies	3	2	6	5	3	5
Case/control total sample size	1,186/1,210	840/1,525	1,720/2,694	1,369/2,167	657/803	1,605/3,847
OR (95% CI)	1.02 (0.9–1.16)	1.11 (0.96–1.29)	1.12 (1.01–1.24)	0.94 (0.84–1.06)	1.15 (0.71–1.86)	1.11 (0.92–1.34)
P-value	0.766	0.148	0.028	0.326	0.581	0.268

Note: Significant P-values in bold.

Abbreviations: HNSCC, head and neck squamous cell carcinoma; SSCC, skin SCC; ESCC, esophageal SCC; OSCC, oral SCC; CSCC, cervical SCC; LSCC, lung SCC; OR, odds ratio; CI, confidence interval.

Table 5 Meta-analysis of association between MDM2ITP53 mutations and SCC susceptibility

Mutation	Genotype		No of case-control studies	Case/control total sample size	Test of association			Heterogeneity		Model	Begga		Egger
	MDM2 rs2279744	TP53 Arg72Pro			OR	95% CI	P-value	I^2 (%)	P-value		z	P-value	t	P-value
MDM2^+/TP53^−	T/G or G/G	Arg/Arg	5	1,293/2,375	1.15	0.77–1.72	0.506	73.5	0.004	R	1.71	0.086	3.29	0.046
MDM2^−/TP5T	T/T	Arg/Pro or Pro/Pro	4	1,017/1,532	0.71	0.5–1	0.051	56.9	0.073	R	0.34	0.734	−1	0.424
MDM2^+/TP53^+, overall	T/G or G/G	Arg/Pro or Pro/Pro	9	2,474/4,319	1.52	I.I 9–1.95	0.001	43.1	0.08	R	0.1	0.917	0.1 1	0.918
MDM2^+/TP53^+, Asian	T/G or G/G	Arg/Pro or Pro/Pro	6	1,863/2,473	1.49	1.06–2.11	0.022	50	0.075	R	0	1	−0.75	0.541
MDM2^+/TP53^+, Caucasian	T/G or G/G	Arg/Pro or Pro/Pro	3	611/1,846	1.59	0.97–2.61	0.066	49.1	0.14	R	1.04	0.296	2.43	0.022

Notes:

a Continuity-corrected; significant P-values in bold.

Abbreviations: SCC, squamous cell carcinoma; OR, odds ratio; CI, confidence interval; R, random-effect model.

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