Overexpression of G protein-coupled receptor 31 as a poor prognosticator in human colorectal cancer

doi:10.3748/wjg.v24.i41.4679

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World Journal of Gastroenterology

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World J Gastroenterol. Nov 7, 2018; 24(41): 4679-4690
Published online Nov 7, 2018. doi: 10.3748/wjg.v24.i41.4679

Table 1 Clinicopathological characteristics of patients with different G protein-coupled receptor 31 expression levels in colorectal cancer n (%)

Variable	GPR31 expression
	Training cohort				Validation cohort
	Cases	Low	High	P value	Cases	Low	High	P value
Age (yr)	321	57.7 ± 14.3	59.6 ± 13.7	0.223	145	61.6 ± 13.4	64.0 ± 13.1	0.324
Gender				0.674				0.921
Female	148	89 (60.1)	59 (39.9)		53	39 (73.6)	14 (26.4)
Male	173	108 (62.4)	65 (37.6)		92	67 (72.8)	25 (27.2)
BMI (kg/m²)	315	21.1 ± 4.0	21.5 ± 3.1	0.350	71	21.8 ± 3.1	22.8 ± 2.2	0.192
Preoperative ileus				0.051				0.402
Yes	25	20 (80.0)	5 (20.0)		33	26 (78.8)	7 (21.2)
No	294	177 (60.2)	117 (39.8)		112	80 (71.4)	32 (28.6)
CEA (ng/mL)				0.949				0.954
< 5	200	125 (62.5)	75 (37.5)		90	66 (73.3)	24 (26.7)
≥ 5	97	61 (62.9)	36 (37.1)		42	31 (73.8)	11 (26.2)
CA199 (ng/mL)				0.399				0.534
< 37	218	142 (65.1)	76 (34.9)		105	77 (73.3)	28 (26.7)
≥ 37	64	38 (59.4)	26 (40.6)		21	14 (66.7)	7 (33.3)
Tumor location				0.764				0.404
Colon	156	93 (59.6)	63 (40.4)		64	49 (76.6)	15 (23.4)
Rectal	163	103 (63.2)	60 (36.8)		81	57 (70.4)	24 (29.6)
Size (cm)	320	5.1 ± 2.2	4.9 ± 2.0	0.380	143	4.8 ± 2.0	4.5 ± 1.7	0.446
Histopathology				0.551				0.406
Adenocarcinoma	283	172 (60.8)	111 (39.2)		128	95 (74.2)	33 (25.8)
Others	38	25 (65.8)	13 (34.2)		17	11 (64.7)	6 (35.3)
Differentiation				0.464				0.305
Well/moderate	271	164 (60.5)	107 (39.5)		112	84 (75.0)	28 (25.0)
Poor	50	33 (66.0)	17 (34.0)		29	19 (65.5)	10 (34.5)
pT classification				0.592				0.006^a
T1/T2	60	35 (58.3)	25 (41.7)		39	35 (89.7)	4 (10.3)
T3/T4	261	162 (62.1)	99 (37.9)		106	71 (67.0)	35 (33.0)
pN classification				0.643				0.767
N0	194	117 (60.3)	77 (39.7)		81	60 (74.1)	21 (25.9)
N1	124	78 (62.9)	46 (37.1)		64	46 (71.9)	18 (28.1)
pM classification				0.007^a				0.018^a
M0	298	189 (63.4)	109 (36.6)		127	97 (76.4)	30 (23.6)
M1	23	8 (34.8)	15 (65.2)		18	9 (50.0)	9 (50.0)
TNM stage				0.885				0.360
I/II	188	116 (61.7)	72 (38.3)		76	58 (76.3)	18 (23.7)
III/IV	133	81 (60.9)	52 (39.1)		69	48 (69.6)	21 (30.4)

^aP < 0.05; GPR31: G protein-coupled receptor 31; BMI: Body mass index; CEA: Carcinoembryonic antigen; CA199: Carbohydrate antigen 19-9.

Table 2 Univariate analysis of G protein-coupled receptor 31 expression and clinicopathologic variables on overall survival

Variable	Training cohort			Validation cohort
Variable	All cases	Hazard ratio (95%CI)	P value	All cases	Hazard ratio (95%CI)	P value
Age (yr)			0.010^a			0.054
< 58.4	153	1.0			1.0
≥ 58.4	168	1.832 (1.158-2.898)			1.937 (0.987-3.800)
Gender			0.817			0.933
Female	148	1.0			1.0
Male	173	1.053 (0.680-1.631)			1.026 (0.562-1.874)
BMI (kg/m²)			0.474			0.959
< 21.4	159	1.0			1.0
≥ 21.4	154	0.980 (0.927-1.036)			1.026 (0.394-2.673)
Preoperative ileus			0.07			0.77
Yes	25	1.0			1.0
No	294	1.438 (0.716-2.890)			0.901 (0.449-1.810)
CEA (ng/mL)			< 0.001^b			0.034^a
< 5	200	1.0			1
≥ 5	97	2.435 (1.509-3.927)			1.919 (1.050-3.508)
CA199 (ng/mL)			0.010^a			0.279
< 37	218	1.0			1.0
≥ 37	64	1.988 (1.179-3.351)			1.504 (0.719-3.148)
Tumor location			0.303			0.911
Colon	156	1.0			1
Rectal	163	1.250 (0.818-1.910)			0.968 (0.545-1.720)
Size (cm)			0.355			0.193
< 5.0	156	1.0			1.0
≥ 5.0	164	1.230 (0.793-1.907)			0.654 (0.345-1.239)
Histopathology			0.091			0.537
Adenocarcinoma	283	1.0			1.0
Others	38	1.671 (0.922-3.031)			1.311 (0.556-3.090)
Differentiation			0.001^a			0.07
Well/moderate	271	1.0			1.0
Poor	50	2.363 (1.435-3.890)			1.811 (0.952-3.443)
pT classification			0.039^a			0.001^a
T1/T2	60	1.0			1.0
T3/T4	261	2.079 (1.038-4.163)			7.055 (2.191-22.722)
pN classification			< 0.001^b			< 0.001^b
N0	194	1.0			1.0
N1	124	2.293 (1.471-3.576)			3.130 (1.716-5.709)
pM classification			< 0.001^b			< 0.001^b
M0	298	1.0			1.0
M1	23	9.857 (5.825-16.680)			5.212 (2.764-9.828)
GPR31 expression			< 0.001^b			< 0.001^b
Low	197	1.0			1.0
High	124	2.888 (1.844-4.523)			3.413 (1.920-6.066)

^aP < 0.05;

^bP < 0.001; CI: Confidence interval; GPR31: G protein-coupled receptor 31; BMI: Body mass index; CEA: Carcinoembryonic antigen; CA199: Carbohydrate antigen 19-9.

Table 3 Univariate analysis of G protein-coupled receptor 31 expression and clinicopathologic variables on disease-free survival

Variable	Training cohort			Validation cohort
Variable	All cases	Hazard ratio (95%CI)	P value	All cases	Hazard ratio (95%CI)	P value
Age (yr)			0.021^a			0.182
< 58.4	153	1.0			1.0
≥ 58.4	168	1.683 (1.082-2.619)			1.481 (0.832-2.636)
Gender			0.832			0.959
Female	148	1.0			1.0
Male	173	0.955 (0.624-1.462)			0.986 (0.573-1.697)
BMI (kg/m2)			0.388			0.938
< 21.4	159	1.0			1.0
≥ 21.4	154	0.977 (0.926-1.030)			1.035 (0.431-2.488)
Preoperative ileus			0.461			0.925
Yes	25	1.0			1.0
No	294	1.299 (0.647-2.607)			0.971 (0.524-1.800)
CEA (ng/mL)			0.001^a			0.057
< 5	200	1.0			1.0
≥ 5	97	2.233 (1.400-3.563)			1.709 (0.985-2.966)
CA199 (ng/mL)			0.014^a			0.415
< 37	218	1.0			1.0
≥ 37	64	1.920 (1.143-3.225)			1.334 (0.668-2.666)
Tumor location			0.101			0.199
Colon	156	1.0			1.0
Rectal	163	1.416 (0.934-2.147)			0.713 (0.425-1.195)
Size (cm)			0.210			0.686
< 5.0	156	1.0			1.0
≥ 5.0	164	1.316 (0.857-2.022)			0.893 (0.514-1.549)
Histopathology			0.112			0.108
Adenocarcinoma	283	1.0			1.0
Others	38	1.617 (0.894-2.924)			1.793 (0.879-3.658)
Differentiation			0.002^a			0.069
Well/moderate	271	1.0			1.0
Poor	50	2.200 (1.342 -3.607)			1.732 (0.958-3.132)
pT classification			0.020^a			0.001^a
T1/T2	60	1.0			1.0
T3/T4	261	2.269 (1.135-4.537)			9.173 (2.867-29.350)
pN classification			< 0.001^b			< 0.001^b
N0	194	1.0			1.0
N1	124	2.228 (1.446-3.434)			2.667 (1.567-4.538)
pM classification			< 0.001^b			< 0.001^b
M0	298	1.0			1.0
M1	23	8.856 (5.259-14.913)			5.210 (2.895-9.375)
GPR31 expression			< 0.001^b			< 0.001^b
Low	197	1.0			1.0
High	124	2.576 (1.671-3.969)			3.277 (1.942-5.530)

^aP < 0.05;

^bP < 0.001; CI: Confidence interval; GPR31: G protein-coupled receptor 31; BMI: Body mass index; CEA: Carcinoembryonic antigen; CA199: Carbohydrate antigen 19-9.

Table 4 Cox multivariate analysis of prognostic factors on overall survival and disease-free survival

Variable	Training cohort			Validation cohort
Variable	Hazards ratio	95%CI	P value	Hazards ratio	95%CI	P value
Overall survival
Age (≥ 58.4 vs < 58.4)	2.344	1.365-4.025	0.002^a	1.722	0.788-3.760	0.173
CEA, ng/mL (≥ 5 vs < 5)	2.236	1.284-3.894	0.004^a	1.437	0.745-2.773	0.279
CA199, ng/mL (≥ 37 vs < 37)	1.382	0.780-2.448	0.267	1.189	0.543-2.604	0.665
Differentiation (poor vs well/moderate)	1.913	1.045-3.503	0.036^a	0.940	0.420-2.103	0.880
pT classification (T3/T4 vs T1/T2)	1.489	0.619-3.581	0.374	7.890	1.028-60.588	0.047^a
pN classification (N1 vs N0)	1.855	1.116-3.084	0.017^a	2.210	1.059-4.613	0.035^a
pM classification (M1 vs M0)	11.836	5.801-24.148	< 0.001^b	2.706	1.307-5.604	0.007^a
GPR31 expression (high vs low)	1.896	1.123-3.202	0.017^a	2.254	1.168-4.349	0.015^a
Disease-free survival
Age (≥ 58.4 vs < 58.4)	2.003	1.200-3.344	0.008^a	1.159	0.598-2.247	0.661
CEA, ng/mL (≥ 5 vs < 5)	1.965	1.147-3.366	0.014^a	1.247	0.686-2.267	0.469
CA199, ng/mL (≥ 37 vs < 37)	1.459	0.824-2.585	0.195	1.103	0.529-2.300	0.794
Differentiation (poor vs well/moderate)	1.609	0.884-2.929	0.119	0.881	0.424-1.830	0.734
pT classification (T3/T4 vs T1/T2)	1.749	0.719-4.254	0.218	13.092	1.738-98.636	0.013*
pN classification (N1 vs N0)	1.809	1.108-2.953	0.018^a	1.787	0.936-3.412	0.079
pM classification (M1 vs M0)	10.233	5.128-20.420	< 0.001^b	2.741	1.408-5.334	0.003^a
GPR31 expression (high vs low)	1.766	1.069-2.917	0.026^a	1.825	1.001-3.325	0.049^a

^aP < 0.05;

^bP < 0.001; CI: Confidence interval; GPR31: G protein-coupled receptor 31; BMI: Body mass index; CEA: Carcinoembryonic antigen; CA199: Carbohydrate antigen 19-9.

Citation: Rong YM, Huang XM, Fan DJ, Lin XT, Zhang F, Hu JC, Tan YX, Chen X, Zou YF, Lan P. Overexpression of G protein-coupled receptor 31 as a poor prognosticator in human colorectal cancer. World J Gastroenterol 2018; 24(41): 4679-4690
URL: https://www.wjgnet.com/1007-9327/full/v24/i41/4679.htm
DOI: https://dx.doi.org/10.3748/wjg.v24.i41.4679