Prognostic value of the Glasgow prognostic score in colorectal cancer: a meta-analysis of 9,839 patients

Figures & data

Figure 1 Flow diagram showing study retrieval and selection process.

Abbreviations: CRC, colorectal cancer; GPS, Glasgow prognostic score; mGPS, modified Glasgow prognostic score.

Table 1 Characteristics of included studies

Study	Year	Country	Design, center	Models	Endpoint	HRs	Sample size	Cutoff	Age (years)	Male (%)	TNM stages	Follow-up (months)	Therapies
Adachi et al^Citation20	2014	Japan	Prospective, one center	mGPS	OS	Reported	65	2	64 (17–38)	59. 6	I–IV	N/A	Resection
Chan et al^Citation33	2017	Australia	Retrospective, database	mGPS	OS	Reported	386	1	≤70: 107; >70: 279	44	I−III	52 (27–92)	Resection
Choi et al^Citation17	2014	Korea	Retrospective, one center	GPS	CSS	Reported	105	2	63 (32–86)	60	I–IV	44 (2–81)	Resection
Dréanic et al^Citation34	2013	France	Retrospective, one center	GPS	OS and CSS	Reported	49	1	<65: 29; ≥65: 20	63	IV	35 (16.5–74.7)	Chemotherapy
Eren et al^Citation35	2015	Turkey	Retrospective, one center	GPS	CSS	Reported	115	2	66 (32–91)	56	I–IV	20 (7–41)	Resection
Furukawa et al^Citation36	2011	Japan	Retrospective, one center	GPS	OS	Reported	40	2	66.1±9.6	75	IV	N/A	Chemotherapy
Ghanim et al^Citation37	2015	Austria	Retrospective, one center	mGPS	OS	Reported	52	1	62.7±11.4	53.8	III, IV	N/A	Resection
Hong et al^Citation38	2017	China	Retrospective, one center	mGPS	CSS	Reported	571	1	62.99±11.78	52	I−III	Median: 42	Resection
Ide et al^Citation39	2017	Japan	Retrospective, one center	mGPS	OS and CSS	Reported	115	1	64 (33–83)	71	I−III	65 (2–189)	Resection
Inoue et al^Citation40	2013	Japan	Retrospective, one center	mGPS	CSS	Reported	163	1	64 (29–85)	60	IV	621±145 days	Chemotherapy
Ishizuka et al^Citation13	2012	Japan	Retrospective, one center	GPS	CSS	Reported	271	1	67.4±11.1	66.4	0–IV	1,536±898 days	Resection
Ishizuka et al^Citation24	2016	Japan	Retrospective, one center	GPS	OS	Reported	627	2	67.7±11.7	63.8	0–IV	1,091±828 days	Resection
Kim et al^Citation41	2017	Korea	Retrospective, one center	mGPS	OS and CSS	Reported	503	2	62 (18–88)	63	IV	Median: 17.6	Chemotherapy
Kishiki et al^Citation21	2013	Japan	Retrospective, one center	mGPS	CSS	Reported	79	2	≤70: 43; >70: 36	53.2	IV	32 (1–66)	Resection
Kobayashi et al^Citation42	2010	Japan	Retrospective, one center	GPS	OS	Reported	63	1	<70: 41; ≥70: 22	69.8	IV	38 (30.5–45.6)	Resection
Køstner et al^Citation43	2016	Sweden; Finland; Norway	Retrospective, multiple centers	GPS	OS	Reported	492	1	65 (32–87)	62.8	IV	50 (2.2–177.6)	Resection
Leitch et al^Citation14	2007	UK	Retrospective, one center	mGPS	OS and CSS	Reported	R: 149; U: 84	2	R: <65: 48; 65–74: 52; >74: 49; U: <65: 34; 65–74: 27; >74: 23	R: 54.4; U: 57.1	R: I–III; U: IV	R: 48 (36–73); U: 12 (6–73)	Resection; chemotherapy
Lin et al^Citation44	2015	China	Retrospective, one center	GPS	OS	Reported	99	2	62.6±10.7	35.4	II	60	Resection
Maeda et al^Citation45	2013	Japan	Retrospective, one center	GPS	OS	Reported	94	2	<70: 62; ≥70: 32	54.3	IV	Median: 30	Resection
Maillet et al^Citation46	2014	France	Retrospective, one center	GPS	OS and CSS	Extracted from survival plots	80	2	65 (36–83)	56.3	IV	14 (1–58)	Chemotherapy
McSorley et al^Citation47	2017	UK	Retrospective, one center	mGPS	CSS	Reported	70	1	<65: 33; 65–74: 29; >74: 8	54.3	I−III	25 (8–78)	Resection
Moug et al^Citation48	2010	UK	Retrospective, two centers	mGPS	OS	Reported	206	1	69.9±10.6	55.3	I−III	44.4 (1.2–81.6)	Resection
Nakagawa et al^Citation49	2014	Japan	Retrospective, one center	mGPS	CSS	Reported	343	1	62.83±3.85	63.8	IV	N/A	Resection
Ni et al^Citation50	2016	China	Retrospective, one center	GPS	OS	Reported	148	1	60.2 (20–74)	65.5	IV	12 (0.4–67)	Chemotherapy
Nozoe et al^Citation15	2014	Japan	Retrospective, one center	mGPS	OS	Reported	272	2	70.4 (24–90)	58.8	I–IV	N/A	Resection
Okimoto et al^Citation25	2017	Japan	Retrospective, one center	GPS	OS and CSS	Reported	134	1	63 (30–87)	67	IV	43 (5–155)	Resection
Okugawa et al^Citation51	2018	Japan	Retrospective, two centers	mGPS	OS	Reported	T: 125; V: 545	2	T: 72.7±11.9; V: 66.9±11.3	T: 56.8; V: 58.9	I–IV	N/A	Resection
Read et al^Citation19	2006	Australia	Retrospective, two centers	GPS	OS	Extracted from survival plots	51	1	64 (40–79)	58.8	IV	Median: 29.8	Chemotherapy
Sharma et al^Citation52	2008	Australia	Retrospective, multiple centers	GPS	OS	Extracted from survival plots	52	2	Median: 70.5	64	IV	N/A	Chemotherapy
Shibutani et al (1)^Citation31	2015	Japan	Retrospective, one center	GPS	OS and CSS	Extracted from survival plots	110	1	64 (27–86)	57.3	IV	N/A	Chemotherapy
Shibutani et al (2)^Citation31	2015	Japan	Retrospective, one center	GPS	OS	Reported	254	1	66 (26–86)	54.7	II, III	N/A	Resection
Shimura et al^Citation32	2017	Japan	Retrospective, one center	mGPS	OS	Reported	92	2	65 (31–90)	61.9	IV	16.2 (0.2–110.4)	Resection
Sirniö et al^Citation26	2018	Finland	Prospective, one center	mGPS	OS and CSS	Reported	271	1	69.5±11.6	50.9	I–IV	Median: 64.3	Resection
Son et al^Citation53	2013	Korea	Retrospective, one center	mGPS	OS	Reported	624	2	<60: 295; ≥60: 329	58.9	I−III	42 (1–66)	Resection
Song et al^Citation54	2015	Korea	Retrospective, one center	mGPS	OS	Reported	177	1	52 (25–81)	46.9	IV	3.1 (0.1–33.3)	Chemotherapy
Sugimoto et al^Citation16	2012	Japan	Retrospective, one center	GPS	CSS	Reported	366	2	≤70: 240; >70: 126	57.1	II−III	Median: 70.8	Resection
Sun et al^Citation55	2014	China	Retrospective, one center	mGPS	OS and CSS	Reported	255	1	59.47±12.63	52.9	I−III	N/A	Resection
Toiyama et al^Citation56	2011	Japan	Retrospective, one center	mGPS	OS and CSS	Reported	219	1	66 (29–91)	62.1	II, III	56.9±63.8	Resection
Tokunaga et al^Citation57	2017	Japan	Retrospective, one center	mGPS	OS and CSS	Reported	468	1	68 (19–93)	59.2	I−III	48.5 (2–124)	Resection
Watt et al^Citation58	2016	UK	Retrospective, one center	mGPS	OS and CSS	Reported	813	1	<65: 268; 65–74: 286; >74: 259	54.6	0−III	T: 116 (72–180); V: 31 (10–71)	Resection
Yamamoto et al^Citation59	2012	Japan	Retrospective, two centers	mGPS	CSS	Reported	42	2	<70: 12; ≥70: 30	61.9	IV	Median: 424 days	Chemotherapy

Note: Age and follow-up periods were expressed as mean ± SD or median (range).

Abbreviations: CSS, cancer-specific survival; GPS, Glasgow prognostic score; mGPS, modified Glasgow prognostic score; N/A, not available; OS, overall survival; R, resectable; T, training; TNM, tumor, node, metastases; U, unresectable; V, validation.

Figure 2 Subgroup analysis showing correlation between GPS and prognosis of CRC patients according to models.

Note: (A) Overall survival and (B) cancer-specific survival.

Abbreviations: CRC, colorectal cancer; df, degrees of freedom; GPS, Glasgow prognostic score; mGPS, modified Glasgow prognostic score; LG, low group; HG, high group; SE, standard error.

Figure 3 Subgroup analysis showing correlation between GPS and prognosis of CRC patients according to therapeutic strategies.

Note: (A) Overall survival and (B) cancer-specific survival.

Abbreviations: CRC, colorectal cancer; df, degrees of freedom; GPS, Glasgow prognostic score; LG, low group; HG, high group; SE, standard error.

Figure 4 Subgroup analysis showing correlation between GPS and prognosis of CRC patients according to cutoff values.

Note: (A) Overall survival and (B) cancer-specific survival.

Abbreviations: CRC, colorectal cancer; df, degrees of freedom; GPS, Glasgow prognostic score; LG, low group; HG, high group; SE, standard error.

Figure 5 Subgroup analysis showing correlation between GPS and prognosis of CRC patients according to the region of publication.

Note: (A) Overall survival and (B) cancer-specific survival.

Abbreviations: CRC, colorectal cancer; df, degrees of freedom; GPS, Glasgow prognostic score; LG, low group; HG, high group; SE, standard error.

Figure 6 Subgroup analysis showing correlation between GPS and prognosis of CRC patients according to patient age.

Note: (A) Overall survival and (B) cancer-specific survival.

Abbreviations: CRC, colorectal cancer; df, degrees of freedom; GPS, Glasgow prognostic score; LG, low group; HG, high group; SE, standard error.

Figure 7 Subgroup analysis showing correlation between GPS and prognosis of CRC patients according to sample size.

Note: (A) Overall survival and (B) cancer-specific survival.

Abbreviations: CRC, colorectal cancer; df, degrees of freedom; GPS, Glasgow prognostic score; LG, low group; HG, high group; SE, standard error.

Figure 8 Subgroup analysis showing correlation between GPS and prognosis of CRC patients according to TNM stages.

Note: (A) Overall survival and (B) cancer-specific survival.

Abbreviations: CRC, colorectal cancer; df, degrees of freedom; GPS, Glasgow prognostic score; LG, low group; HG, high group; SE, standard error; TNM, tumor, node, metastases.

Figure 9 Sensitivity analysis and funnel plot of OS of patients with CRC.

Notes: Sensitivity analysis for (A) overall patients focusing on OS and (B) patients after removing studies with potential publication bias. Funnel plot for (C) overall patients focusing on OS and (D) patients after removing studies with potential publication bias.

Abbreviations: CRC, colorectal cancer; OS, overall survival; SE, standard error.

Table 2 Results of subgroup analyses of overall survival and cancer-specific survival

Subgroups	Independent cohorts	Sample size	HR (95% CI) (H/L)	P-value	Study heterogeneity
					χ^2	df	I^2 (%)	P-value
Overall survival	32	7,714	2.20 (1.88, 2.57)	<0.00001	91.05	31	66	<0.00001
Models
GPS	14	2,293	2.08 (1.69, 2.55)	<0.00001	19.95	13	35	0.10
mGPS	18	5,421	2.23 (1.79, 2.78)	<0.00001	70.68	17	76	<0.00001
Therapies
Resection	23	6,504	2.30 (1.90, 2.79)	<0.00001	70.01	22	69	<0.00001
Chemotherapy	9	1,210	1.95 (1.46, 2.62)	<0.00001	19.36	8	59	0.01
Cutoff value
1	18	4,263	1.85 (1.58, 2.16)	<0.00001	37.66	17	55	0.003
2	14	3,451	3.02 (2.21, 4.13)	<0.00001	39.04	13	67	0.0002
Regions
Asia	21	5,113	2.44 (1.98, 3.02)	<0.00001	56.26	20	64	<0.0001
Others	11	2,601	1.79 (1.47, 2.18)	<0.00001	20.44	10	51	0.03
Age, years
Mean/median <65	11	1,709	1.91 (1.50, 2.43)	<0.00001	21.98	10	55	0.02
Mean/median ≥65	17	5,091	2.46 (1.93, 3.13)	<0.00001	67.21	16	76	<0.00001
Sample size
Sample <300	24	3,256	2.43 (1.97, 3.00)	<0.00001	60.13	23	62	<0.0001
Sample ≥300	8	4,458	1.86 (1.50, 2.31)	<0.00001	21.04	7	67	0.004
TNM stages
0–III	12	3,588	1.95 (1.57, 2.42)	<0.00001	31.86	10	69	0.0004
IV	14	2,085	1.95 (1.56, 2.42)	<0.00001	26.46	13	51	0.01
Cancer-specific survival	23	5,375	1.86 (1.59, 2.17)	<0.00001	45.42	22	52	0.002
Models
GPS	8	1,230	2.38 (1.63, 3.46)	<0.00001	12.75	7	45	0.08
mGPS	15	4,145	1.73 (1.47, 2.03)	<0.00001	28.10	14	50	0.01
Therapies
Resection	16	4,344	2.06 (1.67, 2.53)	<0.00001	35.67	15	58	0.002
Chemotherapy	7	1,031	1.47 (1.24, 1.74)	<0.00001	6.06	6	1	0.42
Cutoff value
1	14	3,852	1.74 (1.48, 2.05)	<0.00001	21.26	13	39	0.07
2	9	1,523	2.34 (1.61, 3.40)	<0.00001	24.07	8	67	0.002
Regions
Asia	15	3,744	2.01 (1.65, 2.44)	<0.00001	27.86	14	50	0.01
Others	8	1,631	1.56 (1.24, 1.96)	<0.00001	10.65	7	34	0.15
Age, years
Mean/median <65	9	2,299	1.83 (1.47, 2.27)	<0.00001	16.28	8	51	0.04
Mean/median ≥65	10	2,512	1.73 (1.34, 2.24)	<0.00001	17.68	9	49	0.04
Sample size
Sample <300	17	2,311	2.02 (1.64, 2.49)	<0.00001	27.01	16	41	0.04
Sample ≥300	6	3,064	1.61 (1.32, 1.96)	<0.00001	10.35	5	52	0.07
TNM stages
0–III	9	3,026	2.01 (1.57, 2.58)	<0.00001	19.29	8	59	0.01
IV	10	1,587	1.80 (1.43, 2.27)	<0.00001	15.76	9	43	0.07

Abbreviations: df, degrees of freedom; GPS, Glasgow prognostic score; H, high group; L, low group; mGPS, modified Glasgow prognostic score; TNM, tumor, node, metastases.

Table S1 Summary of risk of bias

Study	Study participation	Study attrition	Prognostic factor measurement	Outcome measurement	Study confounding	Statistical analysis and reporting
Adachi et al^Citation1	−	−	±	−	−	±
Chan et al^Citation2	−	−	−	−	±	±
Choi et al^Citation3	−	−	±	−	±	−
Dréanic et al^Citation4	−	±	−	±	±	−
Eren et al^Citation5	−	−	±	−	±	−
Furukawa et al^Citation6	±	±	−	−	−	−
Ghanim et al^Citation7	±	±	−	−	−	−
Hong et al^Citation8	−	−	−	−	±	−
Ide et al^Citation9	−	−	±	−	±	−
Inoue et al^Citation10	−	−	−	−	±	−
Ishizuka et al^Citation11	−	−	−	−	−	−
Ishizuka et al^Citation12	−	−	−	−	±	±
Kim et al^Citation13	−	−	−	−	±	−
Kishiki et al^Citation14	−	−	−	−	±	−
Kobayashi et al^Citation15	±	−	−	−	±	−
Køstner et al^Citation16	−	−	−	−	±	−
Leitch et al^Citation17	−	−	−	−	−	±
Lin et al^Citation18	±	−	−	−	±	±
Maeda et al^Citation19	±	−	−	−	±	−
Maillet et al^Citation20	±	−	−	−	±	−
McSorley et al^Citation21	±	−	−	−	−	±
Moug et al^Citation22	−	−	−	±	±	±
Nakagawa et al^Citation23	−	±	−	−	±	−
Ni et al^Citation24	−	−	±	−	±	−
Nozoe et al^Citation25	−	±	−	−	±	±
Okimoto et al^Citation26	−	−	−	−	±	−
Okugawa et al^Citation27	−	±	−	−	−	−
Read et al^Citation28	±	−	−	−	−	−
Sharma et al^Citation29	±	±	−	−	±	−
Shibutani et al (1)^Citation30	−	±	−	−	±	−
Shibutani et al (2)^Citation30	−	−	−	−	±	−
Shimura et al^Citation31	−	−	±	−	−	−
Sirniö et al^Citation32	−	−	−	−	±	−
Son et al^Citation33	−	−	−	−	±	−
Song et al^Citation34	−	−	−	−	−	±
Sugimoto et al^Citation35	±	−	−	−	±	−
Sun et al^Citation36	−	±	−	−	±	−
Toiyama et al^Citation37	−	−	−	−	−	±
Tokunaga et al^Citation38	−	−	−	−	±	−
Watt et al^Citation39	−	−	−	±	±	−
Yamamoto et al^Citation40	±	−	−	−	±	±

Note: The risk of bias for each domain is graded as low (−), moderate (±), or high (+).

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