Prognostic value of high IMP3 expression in solid tumors: a meta-analysis

Figures & data

Figure 1 Flowchart of the study selection process.

Table 1 Characteristics of studies included in the meta-analysis

Author	Year	Country or region	Cancer type	Case number	Method	Cutoff	High expression	Follow-up	Outcomes	Analysis	HR obtained	NOS score
Jiang et al^Citation8	2006	USA	RCC	371	IHC	Positive vs negative*	71 (19.1%)	Median 63 months	OS MFS	Multi	Report	9
Pei et al^Citation26	2015	USA	RCC	346	IHC	Positive vs negative	73 (21.1%)	>10 years	OS RFS	Multi	Report	8
Hoffmann et al^Citation25	2008	USA	RCC	716	IHC	Positive vs negative	213 (29.7%)	9.5 years	CSS MFS	Multi	Report	8
Park et al^Citation27	2014	Korea	RCC	148	IHC	>5% of cells stained	43 (29.1%)	Median 55.5 months	CSS	Multi	Report	7
Jiang et al^Citation28	2008	USA	RCC	317	IHC	Positive vs negative	40 (12.6%)	8.8 years	OS MFS	Multi	Report	9
Tantravahi et al^Citation29	2015	USA	RCC	27	IHC	>20% of cells stained	14 (51.9%)	>2 years	OS	Multi	Report	6
Del Gobbo et al^Citation34	2014	Italy	Lung cancer	74	IHC	Positive vs negative	24 (32.4%)	Mean 65.6 months	OS DFS	Uni	Report	7
Sun et al^Citation32	2015	China	Lung cancer	196	IHC	H-score >100 (0–300)	83 (42.3%)	Range (16.5–69.0) months	OS DFS	Multi	Report	8
Yan et al^Citation9	2016	China	Lung cancer	95	IHC	>25% of cells stained	39 (41.1%)	>5 years	OS	Multi	Report	7
Zhang et al^Citation33	2015	China	Lung cancer	186	IHC	>5% of cells stained	139 (74.7%)	>5 years	OS	Multi	Report	8
Lin et al^Citation30	2015	China	Lung cancer	92	IHC	Positive vs negative	62 (67.4%)	>5 years	OS	Multi	Report	8
Beljan Perak et al^Citation31	2012	Croatia	Lung cancer	90	IHC	>10% of cells stained	61 (67.8%)	>5 years	OS	Uni	SC	6
Clauditz et al^Citation35	2013	Germany	Oral cancer	145	IHC	>10% of cells stained	79 (54.5%)	Mean 41.3 months	OS	Multi	Report	8
Lin et al^Citation37	2011	Taiwan	Oral cancer	93	IHC	>25% of cells stained	51 (54.8%)	Mean 44.8 months	OS	Multi	Report	9
Li et al^Citation36	2010	Korea	Oral cancer	96	IHC	Positive vs negative	65 (67.7%)	Median 73 months	OS	Multi	Report	9
Kim and Cha^Citation10	2011	Korea	Oral cancer	95	IHC	Positive vs negative	67 (70.5%)	>5 years	OS	Multi	Report	7
Szarvas et al^Citation40	2012	Germany	Urothelial carcinoma	106	IHC	Staining index >7 (0–9)	17 (16.0%)	Median 15 months	OS CSS MFS	Multi	Report	7
Sitnikova et al^Citation39	2008	USA	Urothelial carcinoma	214	IHC	Positive vs negative	42 (19.6%)	Median 35 months	PFS DFS	Multi	Report	8
Lee et al^Citation41	2013	Multicenter	Urothelial carcinoma	622	IHC	Positive vs negative	76 (12.2%)	Median 27 months	OS CSS RFS	Multi	Report	9
Niedworok et al^Citation38	2015	Germany	Urothelial carcinoma	26	IHC	H-score >100 (0–300)	7 (26.9%)	Median 50 months	OS PFS	Uni	Report	7
Bi et al^Citation43	2016	China	Ovarian cancer	73	IHC	>10% of cells stained	46 (63.0%)	>5 years	OS	Uni	SC	7
Kobel et al^Citation16	2009	British and North America	Ovarian cancer	278	IHC	>5% of cells stained	147 (52.9%)	>4.6 years	CSS	Multi	Report	8
Hus et al^Citation42	2015	Taiwan	Ovarian cancer	140	IHC	The median value (IRS: 0–9)	NR	Median 39 months	PFS	Multi	Report	6
Noske et al^Citation17	2009	Germany	Ovarian cancer	68	IHC	IRS >6	32 (47.1%)	Median 37 months	OS	Uni	SC	7
Hu et al^Citation44	2014	China	HCC	160	IHC	Staining score (2–7 vs 0–1)	97 (60.6%)	Median 36 months	OS RFS	Uni	SC	8
Wachter et al^Citation45	2011	Germany	HCC	365	IHC	Staining group (2–3 vs 0–1)	67 (18.4%)	Mean 23.3 months	OS	Multi	Report	7
Chen et al^Citation46	2013	China	HCC	92	IHC	Positive vs negative	65 (70.7%)	>3 years	OS	Multi	Report	7
Yuan et al^Citation48	2009	Taiwan	Colorectal cancer	186	IHC	>50% of cells stained	66 (35.5%)	Median >5 years	OS	Multi	Report	8
Li et al^Citation49	2009	China	Colorectal cancer	203	IHC	Staining score (2–7 vs 0–1)	132 (65.0%)	Median 61 months	OS DFS	Multi	Report	9
Lochhead et al^Citation12	2012	USA	Colorectal cancer	671	IHC	Intense or moderate vs weak or absent	234 (34.9%)	Median 160 months	OS CSS	Multi	Report	8
Lin et al^Citation30	2013	China	Colorectal cancer	186	IHC	Positive vs negative	143 (76.9%)	>2 years	OS	Multi	Report	7
Ikenberg et al^Citation15	2010	Switzerland	Prostate cancer	425	IHC	Positive vs negative	354 (83.3%)	Median 63 months	RFS	Uni	Report	9
Chromecki et al^Citation14	2011	USA	Prostate cancer	232	IHC	>10% of cells stained	42 (18.1%)	Median 69.8 months	RFS	Multi	Report	9
Szarvas et al^Citation50	2014	Germany	Prostate cancer	124	IHC	>10% of cells stained	30 (24.2%)	Median 155 months	OS CSS	Uni	Report	8
Wang et al^Citation52	2014	China	Pancreatic cancer	50	qPCR	Cutoff value based on the ROC curve	30 (60.0%)	>2 years	OS	Multi	Report	7
Schaeffer et al^Citation51	2010	Canada	Pancreatic cancer	127	IHC	IHC score >5	80 (63.0%)	Mean 13 months	OS	Multi	Report	8
Morimatsu et al^Citation53	2012	Japan	Pancreatic cancer	32	IHC	>50% of cells stained	17 (53.1%)	Median 33.6 months	CSS	Uni	SC	6
Wang et al^Citation54	2010	China	Gastric cancer	92	IHC	Positive vs negative	75 (81.5%)	>2 years	OS	Uni	SC	7
Okada et al^Citation11	2011	Japan	Gastric cancer	96	IHC	>10% of cells stained	71 (74.0%)	Median 5.5 years	OS DFS	Multi	Report	8
Chen et al^Citation46	2013	Taiwan	ICC	61	IHC	>10% of cells stained	25 (41.0%)	Mean 33.5 months	OS DFS	Uni	SC	7
Gao et al^Citation56	2014	China	ICC	72	IHC	Positive vs negative	59 (81.9%)	Median 14.9 months	OS	Multi	Report	8
Li et al^Citation57	2011	China	Tongue carcinoma	65	IHC	Positive vs negative	50 (76.9%)	Median 36 months	CSS	Uni	SC	8
Asioli et al^Citation58	2010	USA	Thyroid carcinoma	103	IHC	Final score >2 (0–6)	61 (59.2%)	>5 years	OS DFS MFS	Multi	Report	9
Zhou et al^Citation59	2014	China	Sacral chordoma	32	IHC	Staining score (2–7 vs 0–1)	20 (62.5%)	Median 110 months	DFS	Uni	SC	8
Barton et al^Citation60	2013	USA	PA/PMA	77	IHC	Three groups (1–2 vs 0)	24 (31.2%)	Mean 8.8 years	PFS	Uni	Report	7
Chen et al^Citation61	2011	Taiwan	Neuroblastoma	90	IHC	>10% of cells stained	52 (57.8%)	Median 39.5 months	OS	Multi	Report	8
Hao et al^Citation62	2011	USA	Meningioma	107	IHC	Positive vs negative	7 (6.5%)	Median 53 months	OS RFS	Multi	Report	7
Sheen et al^Citation63	2014	Taiwan	Melanoma	97	IHC	>10% of cells stained	72 (74.2%)	Median 5.2 years	OS	Multi	Report	7
Walter et al^Citation64	2009	USA	Breast cancer	138	IHC	>10% of cells stained	45 (32.6%)	Median 71.5 months	OS	Multi	Report	7
Zhang et al^Citation33	2015	China	Giant cell tumor	38	IHC	Staining score (3–7 vs 0–2)	13 (34.2%)	Median 88.0 months	RFS	Uni	SC	6
Riener et al^Citation66	2009	Switzerland	Bile duct carcinoma	115	IHC	Intense or moderate vs weak or absent	67 (58.3%)	Median 9 months	CSS	Multi	Report	8
Takata et al^Citation67	2014	Japan	Esophageal carcinoma	191	IHC	>10% of cells stained	113 (59.2%)	Mean 41 months	OS	Multi	Report	9
Wei et al^Citation13	2014	China	Cervical carcinoma	96	IHC	>10% of cells stained	54 (56.3%)	Median 58.1 months	OS	Multi	Report	8

Note:

* Positive vs negative: tumor cells with any detectable staining were considered positive.

Abbreviations: CSS, cancer-specific survival; DFS, disease-free survival; HCC, hepatocellular carcinoma; HR, hazard ratio; ICC, intrahepatic cholangiocarcinoma; IHC, immunohistochemistry; IRS, immunoreactivity score; MFS, metastasis-free survival; NOS, Newcastle–Ottawa Scale; NR, not reported; OS, overall survival; PA/PMA, pilocytic astrocytoma and pilomyxoid astrocytoma; PFS, progression-free survival; qPCR, quantitative polymerase chain reaction; RFS, recurrence-free survival; RCC, renal cell carcinoma; SC, survival curve.

Figure 2 Forest plot of studies evaluating HR of high IMP3 expression in solid tumors for OS.

Notes: A pooled analysis showed that high IMP3 expression was associated with poor OS in solid tumors (HR =2.08, 95% CI: 1.80–2.42, P<0.001). Weights are from random-effects analysis.
Abbreviations: CI, confidence interval; HRs, hazard ratios; IMP3, insulin-like growth factor II mRNA-binding protein 3; OS, overall survival.

Figure 3 Subgroup analysis of OS stratified by tumor types, funnel plot of OS for publication bias, and sensitive analysis of OS.

Notes: (A) High IMP3 expression was significantly associated with poor OS in RCC, lung cancer, oral cancer, urothelial carcinoma, HCC, colorectal cancer, pancreatic cancer, gastric cancer, and ICC but not in ovarian cancer. (B) The funnel plot for OS was asymmetric, which indicated the probability of publication bias. (C) Sensitivity analysis by sequential omission of individual studies did not alter the significance, which confirmed the credibility of outcomes.
Abbreviations: CI, confidence interval; HCC, hepatocellular carcinoma; HR, hazard ratio; ICC, intrahepatic cholangiocarcinoma; In, natural logarithm; IMP3, insulin-like growth factor II mRNA-binding protein 3; OS, overall survival; RCC, renal cell carcinoma; SE, standard error.

Table 2 Subgroup analysis and meta-regression of the studies regarding overall survival

Subgroups	Studies	Patients	Pooled HR and 95% CI	P-value	Heterogeneity (I^2)	Meta-regression P-value
Ethnicity						0.748
Caucasian	18	3,827	2.08 (1.54–2.81)	<0.001	76.3%
Asian	22	2,598	1.96 (1.73–2.22)	<0.001	9.6%
No of patients						0.659
>100	20	4,850	2.08 (1.71–2.53)	<0.001	62.3%
<100	20	1,575	2.11 (1.66–2.67)	<0.001	57.6%
Cutoff						0.421
Positive vs negative	13	2,562	2.50 (1.96–3.19)	<0.001	53.9%
>10% of cells stained	11	1,201	1.95 (1.50–2.53)	<0.001	29.7%
>25% of cells stained	2	188	1.63 (1.06–2.52)	0.027	46.5%
Others	14	2,474	1.87 (1.42–2.46)	<0.001	65.6%
Cancer stage						0.017
Nonmetastatic	14	2,918	2.01 (1.77–2.29)	<0.001	23.4%
Mixed (metastatic and nonmetastatic)	26	3,507	1.77 (1.58–1.97)	<0.001	16.8%
HR obtain method						0.326
Reported	34	5,881	2.14 (1.84–2.50)	<0.001	55.5%
Extracted	6	544	1.70 (1.03–2.82)	0.040	76.2%
Analysis						0.319
Univariable analysis	9	768	1.76 (1.09–2.85)	0.020	74.7%
Multivariable analysis	31	5,657	2.14 (1.84–2.48)	<0.001	52.9%

Abbreviations: CI, confidence interval; HR, hazard ratio.

Figure 4 Forest plot of studies evaluating HRs of high IMP3 expression in solid tumors for CSS and DFS.

Notes: (A) High IMP3 expression was associated with poor CSS in solid tumors (HR =1.75, 95% CI: 1.50–2.05, P<0.001). (B) High IMP3 expression was associated with poor DFS in solid tumors (HR =3.30, 95% CI: 1.82–5.99, P<0.001). Weights are from random-effects analysis.
Abbreviations: CI, confidence interval; CSS, cancer-specific survival; DFS, disease-free survival; HRs, hazard ratios; IMP3, insulin-like growth factor II mRNA-binding protein 3; OS, overall survival.

Figure 5 Forest plot of studies evaluating HRs of high IMP3 expression in solid tumors for RFS, PFS, and MFS.

Notes: (A) High IMP3 expression was associated with poor RFS in solid tumors (HR =2.11, 95% CI: 1.43–3.12, P<0.001). (B) High IMP3 expression was associated with poor PFS in solid tumors (HR =2.18, 95% CI: 1.11–4.29, P=0.023). (C) High IMP3 expression was associated with poor MFS in solid tumors (HR =4.91, 95% CI: 2.05–11.73, P<0.001). Weights are from random-effects analysis.
Abbreviations: CI, confidence interval; HRs, hazard ratios; IMP3, insulin-like growth factor II mRNA-binding protein 3; MFS, metastasis-free survival; PFS, progression-free survival; RFS, recurrence-free survival.

Table S1 Checklist of PRISMA 2009

Section/topic	#	Checklist item	Reported on page #
Title
Title	1	Identify the report as a systematic review, meta-analysis, or both.	1
Abstract
Structured summary	2	Provide a structured summary including, as applicable: background; objectives; data sources; study eligibility criteria, participants, and interventions; study appraisal and synthesis methods; results; limitations; conclusions and implications of key findings; systematic review registration number.	2
Introduction
Rationale	3	Describe the rationale for the review in the context of what is already known.	3
Objectives	4	Provide an explicit statement of questions being addressed with reference to participants, interventions, comparisons, outcomes, and study design (PICOS).	3,4
Methods
Protocol and registration	5	Indicate if a review protocol exists, if and where it can be accessed (eg, Web address), and, if available, provide registration information including registration number.	No
Eligibility criteria	6	Specify study characteristics (eg, PICOS, length of follow-up) and report characteristics (eg, years considered, language, publication status) used as criteria for eligibility, giving rationale.	4,5
Information sources	7	Describe all information sources (eg, databases with dates of coverage, contact with study authors to identify additional studies) in the search and date last searched.	4
Search	8	Present full electronic search strategy for at least one database, including any limits used, such that it could be repeated.	4
Study selection	9	State the process for selecting studies (ie, screening, eligibility, included in systematic review, and, if applicable, included in the meta-analysis).	5
Data collection process	10	Describe method of data extraction from reports (eg, piloted forms, independently, in duplicate) and any processes for obtaining and confirming data from investigators.	5
Data items	11	List and define all variables for which data were sought (eg, PICOS, funding sources) and any assumptions and simplifications made.	5,6
Risk of bias in individual studies	12	Describe methods used for assessing risk of bias of individual studies (including specification of whether this was done at the study or outcome level), and how this information is to be used in any data synthesis.	5,6
Summary measures	13	State the principal summary measures (eg, risk ratio, difference in means).	5,6
Synthesis of results	14	Describe the methods of handling data and combining results of studies, if done, including measures of consistency (eg, I^2) for each meta-analysis.	6
Risk of bias across studies	15	Specify any assessment of risk of bias that may affect the cumulative evidence (eg, publication bias, selective reporting within studies).	6
Additional analyses	16	Describe methods of additional analyses (eg, sensitivity or subgroup analyses, meta-regression), if done, indicating which were pre-specified.	6
Results
Study selection	17	Give numbers of studies screened, assessed for eligibility, and included in the review, with reasons for exclusions at each stage, ideally with a flow diagram.	7
Study characteristics	18	For each study, present characteristics for which data were extracted (eg, study size, PICOS, follow-up period) and provide the citations.	7
Risk of bias within studies	19	Present data on risk of bias of each study and, if available, any outcome level assessment (see item 12).	7–14
Results of individual studies	20	For all outcomes considered (benefits or harms), present, for each study: (a) simple summary data for each intervention group; (b) effect estimates and confidence intervals, ideally with a forest plot.	7–14
Synthesis of results	21	Present results of each meta-analysis done, including confidence intervals and measures of consistency.	7–14
Risk of bias across studies	22	Present results of any assessment of risk of bias across studies (see item 15).	7–14
Additional analysis	23	Give results of additional analyses, if done (eg, sensitivity or subgroup analyses, meta-regression [see Item 16]).	7–14
Discussion
Summary of evidence	24	Summarize the main findings including the strength of evidence for each main outcome; consider their relevance to key groups (eg, healthcare providers, users, and policy makers).	14,15
Limitations	25	Discuss limitations at study and outcome level (eg, risk of bias), and at review-level (eg, incomplete retrieval of identified research, reporting bias).	15,16
Conclusions	26	Provide a general interpretation of the results in the context of other evidence, and implications for future research.	17
Funding
Funding	27	Describe sources of funding for the systematic review and other support (eg, supply of data); role of funders for the systematic review.	None

Notes: Reproduced from Moher D, Liberati A, Tetzlaff J, et al, Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement. PLoS Med. 2009:6(7): e1000097.¹

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