Impact of surgery for colorectal cancer liver metastasis: Systematic review and meta-analysis

Table 1 Characteristics of included studies

Ref.	Type of study	Country	n2	Liver metastases/other %	CH (adj/neoadj %)	Resection %	R0 resection %	Median follow up (months)	HR for OS	Type of analysis (MVA/UVA)	NOS score
Aasebø et al[19], 2020	Prospective, cohort	Scandinavia	452	64/25 (lung)/29 (nodes)/20 peritoneum)	621	-	7	13	0.32 (0.20-0.52)	MVA	6
Afshari et al[20], 2019	Retrospective, case control	Sweden	281	88/14 (lung)	67.2/13.5	44	77.5	-	0.12 (0.06-0.24)	MVA	5
Ahmed et al[21], 2014	Retrospective, cohort	Canada	1378	100/50	42.31	14.4	-	7.1	0.54 (0.45-0.65)	MVA	6
Albertsmeier et al[22], 2017	Retrospective	Germany	456	74.8/25.2	-/23.3	49.6	36.4	26.4	0.31 (0.22-0.43)	MVA	7
Allard et al[23], 2017	Retrospective	Various	12406	100/9.8	-/40.8	100	87.62	29.4	0.35 (0.26-0.48)	MVA	7
Angelsen et al[24], 2017	Retrospective	Norway	2960	100/43.3	-	18.1	-	10.9	0.54 (0.34-0.86)	MVA	6
Badic et al[25], 2022	Retrospective, cohort	France	1115	40.5/4 (lung)/16 (peritoneum)	21.2	21.2	2	4.2	0.30 (0.24-0.38)	MVA	6
Bakalakos et al[26], 1998	Retrospective	United States	301	100	100	100	39.5	-	0.60 (0.44-0.82)	MVA	5
Beppu et al[27], 2014	Retrospective	Japan	71	100	100	37	25.3	21.8	0.19 (0.09-0.40)	MVA	7
Bhatti et al[28], 2022	Retrospective	Canada	28	100/46	100	53	-	16.5	0.62 (0.40-0.96)	MVA	7
Brouquet et al[29], 2011	Prospective	United States	65	100	100	72	-	50	0.13 (0.04-0.41)	MVA	8
Canseco et al[30], 2023	Retrospective	Taiwan	2612	100/45.5	22.8/11.9	24.4	-	60	0.15 (0.11-0.20)	MVA	8
Chen et al[31], 2018	Prospective	Taiwan	161	78.9	-/84.5	8	-	84	0.76 (0.43-1.33)	MVA	8
Chen et al[32], 2022	Retrospective	China	448	100	-	39.7	-	-	0.68 (0.53-0.87)	MVA	5
Cheng et al[33], 2022	Retrospective, cohort	China	1874	81.1/18.9	-	27.5	-	-	0.37 (0.29-0.47)	MVA	5
Cremolini et al[34], 2017	Pooled analysis of prospective trials	Italy	205	100	100	44.4	36.12	36.5	0.37 (0.22-0.62)	MVA	7
Cummings et al[35], 2007	Retrospective	United States	13599	100	-	6.1	-	-	0.33 (0.30-0.36)	UVA	5
D’Angelica et al[36], 2015	Prospective, phase 2	United States	45	100	71.1	47	40	39	0.16 (0.05-0.51)	MVA	7
Datta et al[37], 2022	Prospective	United States	128	100	100 (CH + HAI); 78.1 (CH)	40	27.3	65.5	0.24 (0.12-0.48)	MVA	8
de la Fouchardiere[38], 2019	Retrospective	France	287	51.9/25.8 (lung)/37.3 (peritoneum)	57.3/89.2 (L1)	15.3	-	47.5	0.47 (0.29-0.76)	MVA	8
Dexiang et al[39], 2012	Retrospective	China	1613	100/13.9	15.5 (CH + HAI); 8.1 (CH)	32.8	-	19	0.44 (0.33-0.59)	MVA	6
Díez-Alonso et al[40], 2021	Retrospective, cohort	Spain	104	100	-/57.7	67.9	-	-	0.44 (0.22-0.90)	MVA	5
Engstrand et al[41], 2018	Retrospective, cohort	Sweden	1026	68.8	56 (periop)	38	-	63.6	0.21 (0.13-0.33)	MVA	8
Famularo et al[42], 2023	Retrospective	Italy	847	100	69.5 (periop)	25.7	-	30	0.20 (0.08-0.48)	MVA	6
Folprecht et al[43], 2014	Retrospective	Germany, Austria	111	100	-/100	100	64.2	-	0.34 (0.14-0.83)	MVA	5
Galizia et al[44], 2013	Prospective	Italy	48	100	-/100	27.1	-	-	0.14 (0.03-0.65)	UVA	5
Ge et al[45], 2019	Retrospective, cohort	China	19796	70.6	-	-	-	-	0.48 (0.44-0.51)	MVA	5
Ghiringhelli et al[46], 2014	Retrospective	France	932	50/3.2 (lung)/13.1 (peritoneum)	58.3	-	11.2	60	0.18 (0.13-0.26)	MVA	6
Grande et al[47], 2016	Retrospective	Italy	751	41.1/10.3 (lung)/34.4 (multi)	46/78 (L1)	19	-	12	0.40 (0.30-0.53)	MVA	5
Habbous et al[48], 2023	Retrospective, cohort	Canada	1498	29 (liver and lung)/60 (lung)	-	-	49.5	34	0.80 (0.66-0.95)	MVA	7
Hackl et al[49], 2014	Retrospective	Germany	5772	24.7	26/48 (periop)	26	-	120	0.44 (0.39-0.50)	MVA	9
Huemer et al[50], 2023	Retrospective	Austria	117	68/34 (lung)/19 (peritoneum)	100	22	-	-	0.22 (0.09-0.54)	UVA	5
Imai et al[51], 2019	Prospective	Japan	163	100	47.2/55.8	100	-	38.8	0.07 (0.02-0.26)	MVA	7
Javed et al[52], 2022	Retrospective	France	105	100	-/63/87 (L1)	86	-	-	0.17 (0.08-0.34)	MVA	5
Jiao et al[53], 2023	Retrospective	China	4575	100	-	83.8	-	84	0.50 (0.39-0.64)	MVA	8
Joharatnam-Hogan et al[54], 2020	Retrospective	United Kingdom	125	44/7 (lung)/49 (multi)	18/34	-	-	54	0.47 (0.22-1.00)	UVA	8
Kataoka et al[55], 2014	Retrospective	Japan	145	100	39.1/-	52.2	-	25.2	0.25 (0.08-0.80)	MVA	6
't Lam-Boer et al[56], 2015	Retrospective	Netherlands	1617	100	62	100	-	-	0.32 (0.25-0.40)	MVA	5
Lan et al[57], 2016	Prospective	China	5239	68.2/19 (lung)/34 (peritoneum)	69/5.8	54.8	-	-	0.41 (0.32-0.51)	MVA	5
Lemini et al[58], 2019	Retrospective	United States	31172	81.3/12.2 (lung)	71.2	42.4	76.3	-	1.08 (0.95-1.23)	MVA	5
Leone et al[59], 2023	Prospective	Italy	167	100	100	23.9	-	48	0.31 (0.19-0.51)	-	7
Leporrier et al[60], 2006	Retrospective, population-based	France	358	100/18.4	100	17.3	-	26	0.79 (0.67-0.93)	MVA	6
Li et al[61], 2023	Retrospective, SEER population-based	China	2127	100	88.3	25.4	-	38	0.41 (0.23-0.73)	MVA	6
Lin et al[62], 2022	Retrospective	China	229	100	0/100	45.9	-	20	0.63 (0.33-1.21)	UVA	6
Luo et al[63], 2018	Retrospective, SEER population-based	China	20268	87.9/10 (lung)	-	11.5	-	-	0.66 (0.62-0.70)	MVA	5
Nakai et al[64], 2013	Prospective	Japan	21	100	100 (HAI)	38.1	-	-	0.08 (0.01-1.46)	MVA	5
Nogueira-Costa et al[65], 2020	Retrospective	Portugal	102	-	100	21.6	-	15	0.34 (0.15-0.77)	MVA	6
Norén et al[66], 2016	Retrospective	Sweden	3125	100	17.6	17.8	-	-	0.23 (0.19-0.27)	MVA	5
Okuno et al[67], 2020	Prospective, phase 2	Japan	34	100/23.5	100	61.7	-	72.6	0.19 (0.06-0.60)	MVA	8
Padman et al[68], 2013	Retrospective, cohort	Australia	455	100	26.6	45.7	-	16.7	0.38 (0.28-0.52)	MVA	6
Park et al[69], 2013	Retrospective, cohort	South Korea	847	100	-	16.5	-	-	0.32 (0.19-0.54)	MVA	6
Qiao et al[70], 2022	Retrospective, cohort	China	7583	68/14.9	-	34.3	-	-	0.74 (0.69-0.79)	MVA	6
Raoof et al[71], 2020	Retrospective, cohort	United States	16382	100/55.8	54.2	10	-	-	0.84 (0.79-0.89)	MVA	6
Robinson et al[72], 1999	Retrospective, cohort	United States	48	100	-	52	-	-	0.29 (0.15-0.56)	MVA	5
Rouyer et al[73], 2018	Retrospective, cohort	France	360	72.2/80	100	21	57.9	24	0.09 (0.02-0.41)	MVA	7
Rouyer et al[74], 2016	Retrospective, cohort	France	389	100/62.5	99	27.2	16.9	36	0.41 (0.19-0.88)	MVA	7
Sarkar et al[75], 2023	Retrospective, cohort	United States	72376	100/40.5	29/9.4	35.6	-	-	0.41 (0.35-0.49)	MVA	6
Shindoh et al[76], 2013	Retrospective, cohort	United States	123	100	-/61.8	70.7	-	50.2	0.33 (0.19-0.57)	UVA	8
Siebenhüner et al[77], 2020	Retrospective, cohort	Swiss	10325	92.2/20.6	-	28.1	-	19	0.73 (0.68-0.78)	MVA	6
Thomasset et al[78], 2013	Retrospective, cohort	United Kingdom	269	100	-	58	-	-	0.70 (0.53-0.92)	UVA	5
Villard et al[79], 2021	Retrospective, cohort	Sweden	100	100	-/100	31	-	-	0.54 (0.33-0.88)	MVA	5
Wang et al[80], 2010	Retrospective, cohort	China	293	100	-	49	-	-	0.40 (0.18-0.90)	MVA	5
Ye et al[81], 2021	Retrospective, cohort	China	93	76.3/23.7	-	34.4	-	26.7	0.46 (0.22-0.96)	MVA	5
Yi et al[82], 2020	Retrospective, cohort	China	27878	72.2/30.6	-	14.5	-	-	0.75 (0.72-0.78)	MVA	6
Zaydfudim et al[83], 2015	Retrospective, cohort	United States	31574	100	2.5/1.1	6.9	-	-	0.40 (0.38-0.42)	MVA	6
Zhang et al[84], 2020	Retrospective, National Cancer Database	United States	58171	70/30	-	8.7	44.6	60	0.42 (0.38-0.46)	MVA	8

¹First-line.

²R0-R1.

CH: Chemotherapy; HAI: Hepatic arterial infusion; HR: Hazard ratio; OS: Overall survival; MVA: Multivariate analysis; UVA: Univariate analysis; L1: First chemotherapy line; periop: Perioperative; multi: Multiple sites; NOS: Newcastle-Ottawa Scale.

Table 2 Summary characteristics of included studies

Characteristic	Value
Included studies, n	67
Total patients, n	368380
Study design	Retrospective 55 (82%); prospective 12 (18%)
Publication years	1998-2023
Sample size (per study)	Median 448 (IQR 124-2786)
Geographic region (approximately)	Asia 22; non-Asia 44; multi-region 1
Median follow-up	37 months (not reported in 42% of studies)
Systemic therapy reporting	Not available in 17 studies

IQR: Interquartile range.