Prognostic Value of Long Noncoding RNAs in Patients with Gastrointestinal Cancer: A Systematic Review and Meta-Analysis

Table 1

Characteristics of studies and lncRNA expression related to OS in GIC patients.

References	lncRNAs ()	Year	Nations	Number ()	OS		Cut-off value	Detection methods	Sample types	Follow-up
					HR	95% CI
Sun et al. [13]	RNAGAS5^↓	2014	China	89 GC	2.43	1.29–4.59	Median	RT-PCR	Tissue	<40
Li et al. [29]	SNHG20^↑	2016	China	107 CRC	2.97	1.51–5.82	YI	RT-PCR	Tissue	<40
Kong et al. [15]^!	PVT1^↑	2015	China	80 GC	2.09	1.07–4.10	Median	RT-PCR	Tissue	<40
Qi et al. [31]	AGAP2-AS1^↑	2017	China	50 GC	2.67^#	1.45–4.93	Median	RT-PCR	Tissue	6–36^#
Chen et al. [32]	XIST^↑	2016	China	106 GC	3.11	1.67–3.78	Median	RT-PCR	Tissue	<120
Ye et al. [33]	lnc-GNAT1-1^↓	2016	China	68 CRC	2.16	1.01–4.63	Median	RT-PCR	Tissue	<20
Saito et al. [21]	ATB^↑	2015	Japan	183 GC	3.50	1.73–7.44	Median	RT-PCR	Tissue	0.192–134.4
Yuan et al. [35]^!	PVT1^↑	2016	China	111 GC	2.28	1.05–4.93	Median	RT-PCR	Tissue	20–48
Ye et al. [36]	CLMAT3^↑	2015	China	90 CRC	2.05	1.10–3.82	Dichotomize	RT-PCR	Tissue	<45
Zheng et al. [37]^!	UCA1^↑	2015	China	112 GC	2.35	1.22–4.52	Dichotomize	RT-PCR	Tissue	<92
Chen et al. [38]	NEAT1^↑	2015	China	96 EC	1.92	1.40–6.49	YI	RT-PCR	Tissue	<80
Wang et al. [39]^!	CCAT2^↑	2016	China	108 GC	2.11	1.44–3.20	Median	RT-PCR	Tissue	<70
Zhao et al. [22]	HOTAIR^↑	2015	China	168 GC	1.47	1.04–2.06	Median	RT-PCR	Tissue	<70
Zhang et al. [40]	Sox2ot^↑	2016	China	132 GC	2.05	1.28–3.30	Median	RT-PCR	Tissue	<96
Chen et al. [41]	HIF1A-AS2^↑	2015	China	83 GC	1.72	1.00–2.96	Median	RT-PCR	Tissue	<60
Li et al. [10]	HOTAIR^↑	2013	China	100 EC	1.91	1.06–4.00	125-fold	RT-PCR	Tissue	<60
Yue et al. [42]^!	FER1L4^↓	2015	China	70 CC	3.99	1.67–9.01	Median	RT-PCR	Tissue	<80
He et al. [43]	CCAT1^↑	2014	China	48 CC	2.09^#	1.42–3.06	Median	RT-PCR	Tissue	24–37^#
Yin et al. [44]	MEG3^↓	2015	China	62 CRC	0.13	0.02–0.99	Mean	RT-PCR	Tissue	<60
Nie et al. [45]	MIR31HG^↓	2016	China	48 CC	2.35^#	1.15–4.79	Median	RT-PCR	Tissue	3–36^#
Park et al. [46]	BM742401^↓	2013	Korea	113 GC	1.03	0.57–1.88	Median	RT-PCR	Tissue	<80
Liu et al. [23]	CRNDE-h^↑	2016	China	148 CRC	2.39	1.30–4.39	Median	RT-PCR	Serum	1–65
Li et al. [47]	PANDAR^↑	2017	China	102 CRC	3.08	0.84–7.89	Median	RT-PCR	Tissue	<60
Chen et al. [48]^!	H19^↑	2016	China	128 GC	1.96	0.97–3.97	Median	RT-PCR	Tissue	20–48
Zou et al. [49]^!	Sox2ot^↑	2016	China	155 GC	3.24	1.24–6.43	Median	RT-PCR	Tissue	<70
Jiang et al. [50]	TUG1^↑	2016	China	218 EC	1.40	1.01–1.95	NR	RT-PCR	Tissue	12–72
Svoboda et al. [51]	HOTAIR^↑	2014	Czech	84 CRC	5.9	1.34–26.1	Median	RT-PCR	Blood	12–54
Wang et al. [52]^!	OTUB1-isoform 2^↑	2016	China	156 GC	1.54	1.04–2.27	Median	RT-PCR	Tissue	<80
Guo et al. [53]	FTX^↑	2015	China	187 CRC	2.37	1.42–2.74	Median	RT-PCR	Tissue	<60
Pan et al. [54]	FOXCUT^↑	2014	China	82 EC	2.13^#	1.38–3.29	Mean	RT-PCR	Tissue	1–72
Zhou et al. [55]	LET^↓	2014	China	93 GC	2.28	1.30–5.18	Mean	RT-PCR	Tissue	<60
Hu et al. [56]	linc-UBC1^↑	2015	China	85 GC	3.56^#	1.71–7.39	Median	RT-PCR	Tissue	<100
Wang et al. [57]	CCAT2^↑	2015	China	86 GC	2.41	1.19–5.42	Mean	RT-PCR	Tissue	<60
Ren et al. [58]	HOTTIP^↑	2015	China	156 CRC	2.15	1.31–3.42	Median	RT-PCR	Tissue	33–65
Liu et al. [59]^!	DANCR^↑	2015	China	104 CRC	2.13	1.16–7.06	Median	RT-PCR	Tissue	<60
Wang et al. [60]^!	ZEB1-AS1^↑	2015	China	87 EC	2.37	1.28–6.12	Median	RT-PCR	Tissue	<61
Li et al. [61]	BANCR^↑	2015	China	184 GC	1.51	1.03–2.23	Median	RT-PCR	Tissue	5–93
Ma [62]^!	PANDAR^↑	2016	China	100 GC	3.68	1.13–12.06	NR	RT-PCR	Tissue	2–36
Huang et al. [63]	MALAT1^↑	2016	China	132 EC	6.64	2.95–14.95	NR	RT-PCR	Tissue	<60
Ni et al. [64]	UCA1^↑	2015	China	54 CRC	3.11^#	0.59–16.39	Median	RT-PCR	Tissue	9–51^#
Wu et al. [25]	uc002yug.2^↑	2014	China	684 EC	2.61	1.50–3.78	NR	RT-PCR	Tissue	<140
Sun et al. [16]	HOXA11-AS^↑	2016	China	85 GC	2.85^#	1.65–4.91	Median	ISH	Tissue	9–36
Peng et al. [65]^!	NEAT1^↑	2016	China	56 CRC	1.70^#	1.04–2.80	NR	RT-PCR	Tissue	<60
Jiao et al. [66]	UCA1^↑	2016	China	66 EC	2.24^#	1.17–4.29	Median	RT-PCR	Tissue	5–30^#
Liu and Shangguan [67]	CARLo-5^↑	2017	China	240 GC	2.41	1.13–5.94	0.041	RT-PCR	Tissue	<60
Ma et al. [11]	CCAL^↑	2016	China	252 CRC	2.25	1.35–3.74	Median	RT-PCR	Tissue	<100
Yang et al. [18]	GHET1^↑	2014	China	42 GC	1.90^#	0.53–6.85	Median	RT-PCR	Tissue	7–40^#
Wu et al. [68]	HOTAIR^↑	2014	China	120 CC	3.92	1.23–12.50	5-fold	RT-PCR	Tissue	10–72
Zhou et al. [69]^!	ROR^↑	2016	China	60 CC	7.22	2.43–17.43	Median	RT-PCR	Tissue	<80
Yang et al. [70]^!	Loc554202^↓	2016	China	178 CRC	2.45	1.34–7.74	Median	RT-PCR	Tissue	<70
Lü et al. [71]	BC032469^↑	2016	China	58 GC	2.78^#	0.95–8.09	Mean	RT-PCR	Tissue	<23
Su et al. [72]	BLACAT1^↑	2017	China	48 CRC	1.50	1.32–1.70	Mean	RT-PCR	Tissue	<60
Hu et al. [12]	GAPLINC^↑	2014	China	90 GC	1.54	1.22–1.94	Median	ISH	Tissue	<80
Fu et al. [73]	NEAT1^↑	2016	China	140 GC	1.61	1.03–2.53	Median	RT-PCR	Tissue	<96
Yao et al. [26]	RP11-766N7.4^↓	2017	China	50 EC	2.14^#	1.10–4.15	Median	RT-PCR	Tissue	32–60^#
Xie et al. [74]	SPRY4-IT1^↑	2014	China	92 EC	2.05	1.04–4.03	Median	RT-PCR	Tissue	3–60
Peng [75]^!	SPRY4-IT1^↑	2015	China	175 GC	0.82	0.31–1.57	Median	RT-PCR	Tissue	<60
Nie et al. [76]^!	ZFAS1^↑	2016	China	54 GC	2.08^#	1.11–3.93	Median	RT-PCR	Tissue	3–36^#
Ohtsuka et al. [77]	H19^↑	2016	USA	117 CC	1.28	1.08–1.50	0.64	RT-PCR	Tissue	<90
Li et al. [20]	MALAT1^↑	2017	China	68 CRC	2.17^#	1.32–3.55	Median	RT-PCR	Tissue	1–51^#
Zhou et al. [78]	AFAP1-AS1^↑	2016	China	162 EC	1.89	1.22–2.92	Median	RT-PCR	Tissue	6–72
Sun et al. [80]^!	RP11-119F7.4^↓	2015	China	96 GC	1.20^#	0.84–1.71	Median	RT-PCR	Tissue	<100
Zhang et al. [81]^!	ANRIL^↑	2014	China	120 GC	1.74	1.04–2.93	3-fold	RT-PCR	Tissue	<60
Li et al. [82]^!	NEAT1^↑	2015	China	239 CRC	1.70	1.18–2.45	2-fold	RT-PCR	Tissue	<60
Chen et al. [83]	LINC00152^↑	2016	China	97 GC	1.66	1.01-2.73	Median	RT-PCR	Tissue	<60
Chen et al. [19]	FEZF1-AS1^↑	2016	China	153 CRC	2.40	1.07–5.41	NR	ISH	Tissue	<100
Han et al. [84]^!	H19^↑	2016	China	83 CRC	1.43	1.24–1.79	3-fold	RT-PCR	Tissue	<50
Yang et al. [85]	GAPLINC^↑	2016	China	180 CRC	2.21	1.38–3.57	NR	ISH	Tissue	<100
Jin et al. [86]	HULC^↑	2016	China	54 GC	1.92^#	1.00–3.67	2-fold	RT-PCR	Serum	11–32^#
Cao et al. [87]^!	BC200^↑	2016	China	70 EC	2.24	1.12–4.49	Median	RT-PCR	Tissue	<50
Cao et al. [88]	SPRY4-IT1^↑	2016	China	84 CRC	3.21	1.55–6.67	2.87-fold	RT-PCR	Tissue	3–36
Gao et al. [89]	linc-UBC1^↑	2017	China	96 CRC	2.43	1.09–5.42	Median	RT-PCR	Tissue	<60
Wang et al. [90]^!	AFAP1-AS1^↑	2016	China	52 CRC	2.36	1.11–5.01	Median	RT-PCR	Tissue	<50
Ge et al. [91]	PCAT-1^↑	2013	China	108 CRC	3.12	1.36–7.19	NR	RT-PCR	Tissue	<100
Deng et al. [92]	91H^↑	2014	China	72 CRC	3.66	1.66–8.10	2.86-fold	RT-PCR	Tissue	2–36
Sun et al. [93]^!	AK098081^↑	2016	China	84 CRC	1.90	1.39–2.58	Mean	RT-PCR	Tissue	1–118^#
Xu et al. [94]^!	FENDRR^↓	2014	China	158 GC	1.76	1.04–3.12	Median	RT-PCR	Tissue	20–48
Bian et al. [96]	UCA1^↑	2016	China	90 CRC	2.40	1.04-5.50	Median	RT-PCR	Tissue	<100
Zuo et al. [97]	UCA1^↑	2017	China	37 GC	2.92	1.07–7.96	Median	RT-PCR	Tissue	<40
Lu et al. [98]	PANDAR^↑	2017	China	124 CRC	3.53	1.41–4.45	Median	RT-PCR	Tissue	<60
Lv et al. [99]	MEG3^↓	2016	China	96 EC	2.12	1.05–4.27	NR	RT-PCR	Tissue	<120
Xu et al. [100]	TUSC7^↓	2017	China	63 CRC	2.92	1.03–8.33	NR	RT-PCR	Tissue	<120
Ma et al. [101]	DUXAP8^↑	2016	China	72 GC	2.37^#	1.39–4.05	Median	RT-PCR	Tissue	5–36^#
Fei et al. [103]^!	LINC00982^↓	2016	China	106 GC	2.87	1.34–6.17	Median	RT-PCR	Tissue	20–48
Chen et al. [104]^!	SNHG15^↑	2016	China	106 GC	2.93	1.30–6.58	Median	RT-PCR	Tissue	20–48
Tan et al. [105]	SPRY4-IT1^↑	2017	China	106 CRC	2.34	1.14–4.83	Mean	RT-PCR	Tissue	<70
Wang and Xing [106]	ZFAS1^↑	2016	China	159 CRC	1.88^∗	1.01–3.53	Median	RT-PCR	Tissue	<101
Yao et al. [107]	MALAT-1^↑	2016	China	137 EC	1.27^#	0.90–1.80	0.5-fold	RT-PCR	Tissue	3–36^#
Liu et al. [108]^!	BANCR^↑	2016	China	142 EC	0.95^∗	0.21–0.95	Median	RT-PCR	Tissue	1–60^#
Chen et al. [109]	HOTAIR^↑	2013	China	78 EC	2.40	1.35–4.28	Mean	RT-PCR	Tissue	2–60
Hu et al. [102]^a	Linc00152^↑	2016	China	205 EC	1.89	1.22–2.58	Upper 95% CI in control group	RT-PCR	Plasma	<60
	POU3F3^↑				1.82	1.17–2.51
	CFLAR^↑				1.68	1.08–2.32
Yu et al. [110]	u50535^↑	2018	China	98CRC	4.01	1.06–15.14	NR	RT-PCR	Tissue	<60
Jiang et al. [111]	CRNDE^↑	2017	China	251CRC	1.69	1.05–2.74	NR	ISH	Tissue	1–117
Cui et al. [112]	HEIH^↑	2018	China	84CRC	1.46	1.02–2.08	Median	RT-PCR	Tissue	<60
Wu et al. [113]^!	GHRLOS^↓	2017	China	366CRC	1.96	1.34–2.86	1/2-fold	RT-PCR	Tissue	5–85
Li et al. [115]	ZEB1-AS1^↑	2017	China	24GC	2.36	1.41–3.96	Median	RT-PCR	Tissue	72
Huang et al. [116]	LINC00673^↑	2017	China	73GC	2.38	1.12–5.06	2-fold	RT-PCR	Tissue	<20
Li et al. [117]	PVT1^↑	2017	China	104ESCC	2.75	1.35–5.59	Median	RT-PCR	Tissue	<80
Shi et al. [118]	ZFAS1^↑	2017	China	246ESCC	1.59	1.07–2.36	Median	RT-PCR	Tissue	114
Wu et al. [119]	XIST^↑	2017	China	127ESCC	2.4	1.44–4.01	Median	RT-PCR	Tissue	<80
Ba et al. [120]	LINC00673^↑	2017	China	79GC	2.56	1.01–4.54	Median	RT-PCR	Tissue	<50
Zhu et al. [121]	SNHG1^↑	2017	China	108CRC	3.17	1.55–6.21	Median	RT-PCR	Tissue	<50
Yang et al. [122]	LINC01133^↓	2018	China	149ESCC	2.18	1.23–3.85	Median	RT-PCR	Tissue	<60

^aOne study involved lncRNA Linc00152, lncRNA POU3F3, and lncRNA CFLAR. indicates adjusted HR; # indicates calculated HR of OS and follow-up time; ! indicates studies included OS and DFS; ↑ or ↓ indicates upregulated or downregulated with poor prognosis. OS: overall survival; DFS: disease-free survival; HR: hazard ratio; CI: confidence interval; EC: esophageal cancer; GC: gastric cancer; CRC: colorectal cancer; GIC: gastrointestinal cancer; NR: no report; YI: Youden index; RT-PCR: reverse transcription PCR; ISH: in situ hybridization.