Laparoscopic liver resection: Experience based guidelines

Table 1 Laparoscopic liver resection learning curve key points

Knowledge of caudal view anatomy

Training in cadaveric and/or animal model

Clinical training should follow an increasing order of procedure difficulty (Difficult Scoring System for LLR[78] can be used to point difficulty levels)

Minor anterolateral resections

Minor anatomical resections (start with LLS)

Difficult resections

Major resections

Graft harvesting for LDLT

HALS and hybrid resections can be used in the early experience to overcome the learning curve

LLR: Laparoscopic liver resection; LLS: Left lateral sectionectomy; LDLT: Living donor liver transplantation; HALS: Hand-assisted liver surgery.

Table 2 Single center series of laparoscopic liver resection including more than 150 cases

Ref.	Cases	Malignancy	Minimally invasive approach (%)			Major resections	Conversion	Operative time	Blood loss	Transfusion	LOS	Complication	Mortality
	(n)	(%)	PLLR	HALS	Hybrid	(%)	(%)	(median/mean, min)	(median/mean, mL)	(%)	(median/mean, d)	(%)	(%)
Koffron et al[13]	300	34	80.3	10.6	9	39	7.3	99	102	0.6	1.9	9.3	0
Buell et al[165]	306	42	NR	NR	NR	45	2.4	162	222	7	2.9	16	1.6
Bryant et al[163]	166	60	95.2	4.8	0	18.6	9.6	180	329	5.4	6	15.1	0
Long et al[164]	173	100 (HCC)	100	0	0	8.3	2.3	112	194	NR	6.5	2.4	0
Cai et al[81]	365	27.1	100	0	0	22.2	17.2	150	370	NR	9.2	12.2	0
Gobardhan et al[93]	476	79	NR	NR	NR	33.8	4.2	NA	NA	4.6	NR	21	0.8
Troisi et al[99]	265	64.1	99.3	0	0.7	17.4	6.4	254	171	NR	5.5	14	0
University of Sao Paulo series 2015	214	65.9	75.2	5.6	19.2	14.5	6.5	205	240	7.4	4.5	15	0.5

PLLR: Pure laparoscopic liver resection; HALS: Hand-assisted liver surgery; HCC: Hepatocellular carcinoma; LOS: Length of stay; OLR: Open liver resection; NR: Not reported; NA: Not available.

Table 3 Studies of laparoscopic liver resection for benign liver diseases (studies with over 10 cases)

Ref.	Cases (n)	Type of study	Major hepatectomies (%)	Conversion (%)	Transfusion (%)	Complication (%)	Mortality (%)
Katkhouda et al[28]	121	Retrospective	0	8.3	0	0	0
Descottes et al[12]	87	Retrospective multicenter	3.4	10	6	5	0
Ardito et al[29]	50	Retrospective	16	8	2	10	0
Troisi et al[30]	20	Comparative (LLR × OLR)	2.5	10	10	20	0
Abu Hilal et al[32]	50	Retrospective	28	2	2	7	0
Abu Hilal et al[31]	13 HA only	Retrospective	62	0	7.7	7.7	0
Herman et al[17]	31 HA only	Retrospective	16.7	0	0	6.5	0
de'Angelis et al[197]	36 HA only	Comparative (LLR × OLR)	25	8.3	0	8.3	0
Dokmak et al[33]	31 LLS only	Comparative LLS (LLR × OLR)	0	6.5	NR	9.7	0
Ding et al[25]	49 hepatolithiasis only underwent LLS	Prospective randomized trial (LLR × OLR)	0	4.1	NR	6.1	0
University of Sao Paulo series 2015	73		15.1	0	4.1	6.9	0

¹Included LLR (n = 12) and cyst fenestration/pericystectomy (n = 31): Results of patients submitted to LLR. HA: Hepatocellular adenomas; LLR: Laparoscopic liver resection; LLS: Left lateral sectionectomy; OLR: Open liver resection; NR: Not reported.

Table 4 Comparative studies of laparoscopic and open liver resection for hepatocellular carcinoma including more than 30 patients in each arm

Ref.	No. of patients		Blood loss (mean/median, mL)			Blood transfusion (%)			Conversion (%)	Complication (%)			Perioperative mortality (%)			5-yr overall survival (%)			5-yr recurrence free survival (%)
	LLR	OLR	LLR	OLR	P value	LLR	OLR	P value		LLR	OLR	P value	LLR	OLR	P value	LLR	OLR	P value	LLR	OLR	P value
Belli et al[34]	54	125	297	580	< 0.01	11	25.6	0.03	7	19	36	0.02	2	4	NS	671	-	NS	521	-	NS
Tranchart et al[35]	42	42	364	723	< 0.0001	9.5	16.7	NS	4.7	21.4	40.5	NS	2.4	2.4	NS	59.51	47.41	NS	60.91	54.31	NS
Truant et al[36]	36	61	452	447	NS	2.8	3.8	NS	19.4	25	35.8	NS	0	7.5	NS	70	46	NS	35.5	33.6	NS
Lee et al[37]	33	50	150	240	NS	6.1	10	NS	18.2	6.1	24	0.033	0	0	NS	76	76.1	NS	45.3	55.9	NS
Hu et al[110]	30	30	520 g	480 g	NS	NA	NA	-	0	13.3	10	NS	0	0	NS	50	50.3	NS	NR	NR	-
Ker et al[38]	116	208	139	1147	< 0.001	6.9	50.9	< 0.001	5.2	6	30.2	< 0.001	0	2.9	NS	62.2	71.8	NS	NR	NR	-
Cheung et al[39]	32	64	150	300	0.001	0	4.7	NS	NR	6.3	18.8	NS	0	1.6	NS	76.6	57	NS	54.5	44.3	NS
Ai et al[40]	97	178	460	454	NS	4.6	2.8	NS	9.28	9	30	0.001	0	0	NS	861	881	NS	661	671	NS
Memeo et al[41]	45	45	200	200	NS	0	0	NS	NR	20	45	0.01	2	13	0.04	59	44	NS	19	23	NS
Kim et al[42]	70	70	NA	NA	-	24.3	40.8	0.001	8.57	7.1	14.5	NS	NR	NR	-	65.3	65.7	NS	58.3	62.6	NS
Kim et al[198]	43	162	484	261	NS	3.4	0	NS	23.3	13.8	37.9	NS	0	0	NS	92.2	87.7	NS	54	40.1	NS
Ahn et al[43]	51	51	350	355.2	NS	5.9	9.8	NS	Excluded	5.8	9.8	NR	0	0	NS	80.1	85.7	NS	67.8	54.8	NS
Yamashita et al[44]	63	99	455	436	NS	6	2	NS	NA	10	26	0.046	0	0	NS	69	77	NS	33	41	NS
Yoon et al[45]	58	174	NA	NA	-	3.4	7.5	0.04	0	6.9	22.4	0.02	NR	NR	-	882	682	NS	562	622	NS
Martin et al[46]	100	254	336	755	< 0.001	1.2	2.4	0.043	NR	44	57	NS	6	8	NS	60.71	41.81	NS	201	261	NS
Lee et al[47]	43	86	300	700	0.004	NR	NR	-	14	23.3	39.5	NS	NR	NR	-	89.7	87.3	NS	53.5	58.6	NS
Han et al[48]	88	88	500	525	NS	20	26.1	NS	9.1	12.5	20.4	0.042	1.1	1.1	NS	76.4	73.2	NS	44.2	41.2	NS
Xiao et al[49]	41	86	272.2	170.8	0.001	7.3	13.9	NS	7.32	17.1	37.3	0.021	0	0	NS	781	76.71	NS	70.71	68.61	NS

¹Data computed for 3-yr survival;

²Data computed for 4-yr survival. LLR: Laparoscopic liver resection; OLR: Open liver resection; NR: Not reported; NS: Non significant.

Table 5 Comparative studies of laparoscopic and open liver resection for colorectal liver metastases including more than 30 patients in each arm

Ref.	No. of patients		Blood loss (mean/median, mL)			Blood transfusion (%)			Conversion (%)	Complication (% )			Perioperative mortality (%)			5-yr overall survival (%)			5-yr recurrence free survival (%)
	LLR	OLR	LLR	OLR	P value	LLR	OLR	P value		LLR	OLR	P value	LLR	OLR	P value	LLR	OLR	P value	LLR	OLR	P value
Castaing et al[50]	60	60	NR	NR	-	15	36	0.007	10	27	28	NS	1.7	1.7	NS	64	56	NS	30	20	NS
Abu Hilal et al[51]	55	119	363	500	NR	3.6	NR	NR	12	15	20.2	NR	0	2	NR	NR	NR	NR	NR	NR	-
Cannon et al[52]	35	140	202	392	< 0.001	17	25	NS	NR	23	50	0.004	0	1.4	NS	36	42	NS	15	22	NS
Qiu et al[53]	30	140	215	390	< 0.001	10	25	< 0.05	6.6	26.2	55	< 0.001	0	0	NS	NR	NR	-	NR	NR	-
Guerron et al[54]	40	40	376	753	0.041	5	20	0.04	5	15	20	NS	0	0	NS	NR	NR	NS	NR	NR	NS
Kubota et al[55]	43	62	287.3	579.3	< 0.001	2.4	21	0.004	NR	2.4	9.7	NS	0	0	NS	88.41	74.21	NS1	NR	NR	-
Montalti et al[56]	57	57	454.2	691.5	0.003	NR	NR	-	15.8	15.8	31.6	0.03	0	0	NS	60	65	NS	29	38	NS
de'Angelis et al[57]	52	52	200	300	0.001	5.8	21.2	NS	5.8	17.3	22	NS	0	3.8	NS	73.1	62.5	NS	21.1	21.1	NS
Hasegawa et al[58]	102	69	127	620	0.000	NR	NR	NR	1	8.8	24.6	0.005	0.98	1.4	NS	56.8	48.8	NS	39.7	28.6	NS

¹Data computed for 3-yr survival. LLR: Laparoscopic liver resection; OLR: Open liver resection; NR: Not reported; NS: Non significant.

Table 6 Meta-analysis published comparing open vs laparoscopic liver resection

Ref.	No. of studies/period	Type of studies	End point	No. of OLR × LLR	Conversion rate	Favors ORL	Favors LLR	Equal OLR × LLR
Simillis et al[151]	8	Observational	Short-term outcomes	244 (59.7%) × 165 (40.3%)	3.7%	Need and duration of portal clamping	Operative blood loss	Blood transfusion rate
		Nonrandomized					Return to oral intake	Operative time
		Comparative					LOS	Incidence of portal triad clamping
	1998-2005	Benign and malignant disease						Adverse events
								Oncologic clearance
Croome et al[150]	26	Observational	Short and long-term outcomes	1019 (53.9%) × 871 (46.1%)	3.5%	Lower risk of margins smaller than 1 cm	Operative blood loss	Blood transfusion rate
		Nonrandomized					Return to oral intake	Operative time
		Comparative					Need for intravenous narcotics	Incidence of portal triad clamping
	1998-2009	Benign and malignant disease					Overall complication rate	Oncologic clearance
							All cause mortality in 2-5 yr	Recurrence risk
Mirnezami et al[149]	26	Observational	Short and long-term outcomes	961 (57%) × 717 (43%)	7%	Operative time	Operative blood loss	Portal trial clamping time
		Nonrandomized					Return to oral intake	Margin size
		Comparative					Overall and specific complications	Hepatic tumor recurrence for HCC
	1998-2009	Benign and malignant disease					Incidence of portal triad clamping	DFS for HCC
							Lower risk of margins smaller than 1 cm
							Lower rate of positive margins
							Increased overall survival for HCC
Zhou et al[118]	10	Observational	Short and long-term outcomes	281 (56.9%) × 213 (43.1%)	6.1%	-	Operative blood loss	Operative time
		Nonrandomized					Blood transfusion rate	Postoperative mortality
		Comparative					Overall and liver specific complications	Size of resection margins
	2001-2010	HCC only					LOS	DFS
								Overall survival
Mizuguchi et al[152]	11	Observational	Short-term outcomes	253 (52.2%) × 232 (47.8%)	NR	-	Operative blood loss	Operative time
		Nonrandomized					Postoperative complications
		Comparative					LOS
	2001-2008	Benign and malignant disease
Fancellu et al[111]	9	Observational	Short and long-term outcomes	363 (61.5%) × 227 (38.5%)	4%	-	Rate of positive margins	Liver haemorrhage
		Nonrandomized					Operative blood loss	Bile leakage
		Comparative					Blood transfusion rate	OS
	2001-2010	HCC only					LOS	DFS
							Overall and liver specific complications
Rao et al[94]	7	Observational	Short-term outcomes	111 (45.3%) × 134 (54.7%)	2.7%	-	Postoperative complications	Operative blood loss
		Nonrandomized					Operative time	Blood transfusion rate
	2005-2009	Comparative only patients undergoing laparoscopic × open LLS					LOS	Rate of positive margins
Li et al[173]	10	Observational	Short and long-term outcomes	383 (61%) × 244 (39%)	6.6%	-	Operative blood loss	Operative time
		Nonrandomized					Blood transfusion rate	Surgical margin size
		Comparative					Postoperative complications	Rate of positive margins
	2001-2011	HCC only					LOS	Tumor recurrence
Rao et al[148]	32	Observational	Short and long-term outcomes	1305 (52.9%) x 1161 (47.1%)	2.3%	Operative time	Operative blood loss	Overall and liver specific complications
		Nonrandomized					Blood transfusion rate	Operative mortality
		Comparative					LOS	Margin width
	1998-2009	Benign and malignant disease					Return to oral intake	DFS
							Rate of positive margins	OS
							Overall complication rate	Recurrence rate
Xiong et al[117]	15	Observational	Short and long-term outcomes	316 (57.5%) × 234 (42.5%)	0% to 19.4%	-	Operative blood loss	Operative time
		Nonrandomized					Blood transfusion rate	Pulmonary complications
		Comparative					LOS	Bleeding
	2001-2011	HCC only					Incidence of liver failure and ascites	Bile leakage
								Operative mortality
								Rate of positive margins
								Tumor recurrence
Rao et al[172]	10	Observational	Short-term outcomes	404 (57.7%) × 296 (42.3%)	NR	-	Operative blood loss	Operative time
		Nonrandomized					Blood transfusion rate	Ascitis
	2002-2009	Comparative					Negative margins rate	Postoperative liver failure
		Malignant tumors					Overall complication rate	DFS
							LOS	OS
								Recurrence rate
Yin et al[174]	15	Observational	Short and long-term outcomes	753 (60.8%) × 485 (39.2%)	2.6%	-	Operative blood loss	Surgical margins
		Nonrandomized					Blood transfusion rate	Operative time
		Comparative					Postoperative morbidity	Negative margins rate
	2001-2011	HCC only					LOS	Recurrence rate
								OS
								RFS
Zhou et al[129]	8	Observational	Short and long-term outcomes	427 (61.4%) × 268 (38.6%)	8.2%	-	Operative blood loss	Operative time
		Nonrandomized					Blood transfusion rate
		Comparative					Postoperative morbidity
	2002-2013	CRLM only					LOS
							Negative margin
							OS
							DFS
Twaij et al[168]	4	Observational	Short and long-term outcomes	270 (64.3%) × 150 (35.7%)	7% to 19.4%	-	Surgical margin size	Operative time
		Nonrandomized					Operative blood loss	OS
		Comparative					Blood transfusion rate	DFS
	2009-2013	HCC only with cirrhosis					Postoperative morbidity
Parks et al[167]	15	Observational	Short and long-term outcomes	556 (55.5%) × 446 (44.5%)	4.2%	-	Operative blood loss	Operative time
		Nonrandomized					LOS	30-d mortality
		Comparative						OS
	2001-2011	Malignant tumors
Luo et al[128]	7	Observational	Short and long-term outcomes	383 (61.4%) × 241 (38.6%)	NR	Margin size	Operative blood loss	Operative time
		Nonrandomized					Blood transfusion rate	LOS
		Comparative					Postoperative complications	OS
	2002-2013	CRLM only					Rate of R1 margins	DFS
Wei et al[127]	14	Observational	Short and long-term outcomes	599 (61.4%) × 376 (38.6%)	NR	-	Operative blood loss	Operative time
		Nonrandomized					Blood transfusion rate	Perioperative mortality
	2002-2013	Comparative					LOS	OS
		CRLM only					Postoperative complications	DFS
		13 studies comparing simultaneous
		laparoscopic × open resections					1Simultaneous resection	1Simultaneous resection
							LOS	Morbidity, operative time, operative blood loss
Schiffman et al[130]	8	Observational	Short and long-term outcomes	368 (60.3%) × 242 (39.7%)	NR	-	Operative blood loss	Operative time
		Nonrandomized					Blood transfusion rate	Number of major resections
		Comparative					Overall complication rate	Mean number of resected tumors
	2009-2013	CRLM only					LOS	Tumor size
								Positive margins
								Margin width
								OS
								DFS
Jackson et al[153]	46	Observational	Short-term outcomes	1741 (47.8%) × 1901 (52.2%)	5.68%	Cost	Operative blood loss	Operative time
		Nonrandomized					Negative margin	30-d mortality
	2001-2013	Comparative					LOS
		Benign and malignant disease					Postoperative complications
Morise et al[169]	21	Observational	Ascitis	602 (63.1%)	NR	-	Less ascites	-
		Nonrandomized		× 352 (36.9%)			Less postoperative liver failure
	2001-2014	Comparative
		HCC only	Postoperative liver failure	220 (54.6%) × 183 (45.7%)

¹Results of a subset of studies (3) comparing simultaneous resection of the primary tumor and liver metastases. CRLM: Colorectal cancer liver metastases; DFS: Disease free survival; HCC: Hepatocellular carcinoma; LLR: Laparoscopic liver resection; LLS: Left lateral sectionectomy; LOS: Length of stay; OLR: Open liver resection; OS: Overall survival; NR: Not reported.