Q2 Committee: David Geller, Giulio Belli, Bjørn Edwin, Paulo Herman, Daniel Cherqui
Q2: What are the comparative long term outcomes of LLR and OLR? (minor
and major)
Recommendations:
1. No RCT have been published to date comparing LLR to OLR
2. The best data comes from case-cohort matched studies comparing LLR to OLR for HCC
or limited mCRC.
3. With LLR for cancer, there are no reports or trocar or peritoneal seeding.
4. For HCC, 18 comparative studies have been published comparing LLR to OLR that
provide either 3 year or 5 year disease-free survival or overall survival. None of the
comparative studies showed inferiority for LLR for 3 year- or 5 year- DFS or OS for
HCC.
5. For mCRC, 11 comparative studies have been published comparing LLR to OLR for
limited mCRC (1 or 2 hepatic metastases). All of the studies show comparable 3 year- or
5 year- DFS or OS.
6. Hence, the aggregate data shows equivalent long-term overall survival comparing LLR to
OLR for HCC or limited mCRC.
7. Given the equivalent oncologic outcomes, then any short-term benefits reported for LLR
compared to OLR under CQ1 justify and favor LLR since there is no compromise of
long-term cancer outcomes.
8. LLR facilitates future liver surgery (transplant or resection) for recurrent tumor.
1
References
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5. Belli G, Fantini C, D'Agostino A, Cioffi L, Langella S, Russolillo N, Belli A. Laparoscopic
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6. Lee KF, Cheung YS, Chong CN, Tsang YY, Ng WW, Ling E, Wong J, Lai PB. Laparoscopic
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open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg. 2009; 96:1041-8.
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11. Sarpel U, Hefti MM, Wisnievsky JP, et al. Outcome for patients treated with laparoscopic versus
open resection of hepatocellular carcinoma: case-matched analysis. Ann Surg Oncol 2009;
16:1572-7.
2
12. Lai EC, Tang CN, Yang GP, Li MK. Minimally invasive surgical treatment of hepatocellular
carcinoma: long-term outcome. World J Surg. 2009; 33:2150-4.
13. Lai EC, Tang CN, Ha JP, Li MK. Laparoscopic liver resection for hepatocellular carcinoma: tenyear experience in a single center. Arch Surg 2009; 144:143-7.
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laparoscopy-assisted and open left lateral hepatectomy for hepatocellular carcinoma. Surg
Laparosc Endosc Percutan Tech. 2009; 19:e171-4
15. Dagher I, Belli G, Fantini C, Laurent A, Tayar C, Lainas P, Tranchart H, Franco D, Cherqui D.
Laparoscopic hepatectomy for hepatocellular carcinoma: a European experience. J Am Coll
Surg 2010; 211:16-23.
16. Tranchart H, Di Giuro G, Lainas P et al. Laparoscopic resection for hepatocellular carcinoma: a
matched-pair comparative study. Surg Endosc. 2010; 24:1170-6.
17. Ker CG, Chen JS, Kuo KK, Chuang SC, Wang SJ, Chang WC, Lee KT, Chen HY, Juan CC.
Liver Surgery for Hepatocellular Carcinoma: Laparoscopic versus Open Approach. Int J Hepatol.
2011:1-7.
18. Truant S, Bouras AF, Hebbar M, Boleslawski E, Fromont G, Dharancy S, Leteurtre E, Zerbib P,
Pruvot FR. Laparoscopic resection vs. open liver resection for peripheral hepatocellular
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25:3668-77
19. Lee KF, Chong CN, Wong J, Cheung YS, Wong J, Lai P. Long-term results of laparoscopic
hepatectomy versus open hepatectomy for hepatocellular carcinoma: a case-matched analysis.
World J Surg. 2011; 35:2268-74.
20. Hu BS, Chen K, Tan HM, Ding XM, Tan JW. Comparison of laparoscopic vs open liver
lobectomy(segmentectomy)for hepatocellular carcinoma. World J Gastroenterol. 2011;17:4725-8.
21. Kim K-J, Jeong C-Y, Jeong S-H, et al. Laparoscopic Liver Resection for Hepatocellular
Carcinoma. J Korean Surg Soc. 2011; 80:51.
22. Cheung TT, Poon RTP, Yuen WK, et al. Long-Term Survival Analysis of Pure Laparoscopic
Versus Open Hepatectomy for Hepatocellular Carcinoma in Patients With Cirrhosis. Annals of
Surgery. 2013; 257:506–511.
23. Kim H, Suh K-S, Lee K-W, et al. Long-term outcome of laparoscopic versus open liver resection
for hepatocellular carcinoma: a case-controlled study with propensity score matching. Surgical
Endoscopy. 2014; 28:950–960.
mCRC comparative series
24. Mala T, Edwin B, Gladhaug I, Fosse E, Søreide O, Bergan A, Mathisen O. A comparative study
of the short-term outcome following open and laparoscopic liver resection of colorectal
metastases. Surg Endosc. 2002; 16:1059-63
25. O'Rourke N, Shaw I, Nathanson L, Martin I, Fielding G. Laparoscopic resection of hepatic
colorectal metastases. HPB. 2004; 6:230-5.
26. Nguyen KT, Laurent A, Dagher I, Geller DA, Steel J, Thomas MT, Marvin M, Ravindra KV,
Mejia A, Lainas P, Franco D, Cherqui D, Buell JF, Gamblin TC. Minimally invasive liver
resection for metastatic colorectal cancer: a multi-institutional, international report of safety,
feasibility, and early outcomes. Ann Surg. 2009; 250:842-848.
27. Sasaki A, Nitta H, Otsuka K, Takahara T, Nishizuka S, Wakabayashi G. Ten-year experience of
totally laparoscopic liver resection in a single institution. Br J Surg 2009; 96:274-279.
28. Castaing D, Vibert E, Ricca L, Azoulay D, Adam R, Gayet B. Oncologic results of laparoscopic
versus open hepatectomy for colorectal liver metastases in two specialized centers. Ann Surg.
2009; 250:849-55.
3
29. Kazaryan AM, Marangos IP, Røsok BI, Rosseland AR, Villanger O, Fosse E, Mathisen O, Edwin
B. Laparoscopic resection of colorectal liver metastases: surgical and long-term oncologic
outcome. Ann Surg. 2010; 252:1005-12.
30. Nguyen KT, Geller DA. Outcomes of laparoscopic hepatic resection for colorectal cancer
metastases. J Surg Oncol. 2010; 102:975-7.
31. Abu Hilal M, Underwood T, Zuccaro M, Primrose J, Pearce N. Short- and medium-term results
of totally laparoscopic resection for colorectal liver metastases. Br J Surg. 2010; 97:927-3.
32. Nguyen KT, Marsh JW, Tsung A, Steel JL, Gamblin TC, Geller DA. Comparative benefits of
laparoscopic versus open hepatic resection: a critical appraisal. Arch Surg, 2011; 146:348-56.
33. Cannon RM, Scoggins CR, Callender, GG, et al. Laparoscopic versus open resection of hepatic
colorectal metastases. Surgery 2012; 152:567-573.
34. Topal H, Tiek J, Aerts R, et al. Outcome of laparoscopic major liver resection for colorectal
metastases. Surg Endosc 2012; 26:2451-2455.
35. Hu, MG, Ou-yang CG, Zhao GD, et al. Outcomes of open versus laparoscopic procedure for
synchronous radical resection of liver metastatic colorectal cancer: a comparative study. Surg
Laparosc Endosc Percutan Tech 2012; 22:364-369.
36. Guerron AD, Aliyev S, Agcaoglu O, et al. Laparoscopic versus open resection of colorectal liver
metastasis. Surg Endosc 2013; 27:1138-1143.
37. Cheung TT, Poon RT, Yuen WK, et al. Outcome of laparoscopic versus open hepatectomy for
colorectal liver metastases. ANZ J Surg 2013; 83:847-52.
38. Qiu J, Chen S, Pankaj P, et al. Laparoscopic hepatectomy for hepatic colorectal metastases - a
retrospective comparative cohort analysis and literature review. PLoS One 2013; 8:e60153.
Meta-Analysis papers
1. Simillis C, Constantinides VA, Tekkis PP, et al. Laparoscopic versus open hepatic resections for
benign and malignant neoplasms--a meta-analysis. Surgery 2007;141: 203-211.
2. Croome KP, Yamashita MH. Laparoscopic vs open hepatic resection for benign and malignant
tumors: An updated meta-analysis. Arch Surg. 2010; 145:1109-18.
3. Zhou YM, Shao WY, Zhao YF, et al. Meta-analysis of laparoscopic versus open resection for
hepatocellular carcinoma. Dig Dis Sci 2011; 56:1937-1943.
4. Yin Z, Fan X, Ye H, et al. Short- and long-term outcomes after laparoscopic and open
hepatectomy for hepatocellular carcinoma: a global systematic review and meta-analysis. Ann
Surg Oncol 2013; 20:1203-1215.
5. Mirnezami R, Mirnezami AH, Chandrakumaran K, et al. Short- and long-term outcomes after
laparoscopic and open hepatic resection: systematic review and meta-analysis. HPB (Oxford)
2011; 13:295-308.
6. Li N, Wu YR, Wu B, et al. Surgical and oncologic outcomes following laparoscopic versus open
liver resection for hepatocellular carcinoma: A meta-analysis. Hepatol Res 2012; 42:51-59.
7. Fancellu A, Rosman AS, Sanna V, et al. Meta-analysis of trials comparing minimally-invasive
and open liver resections for hepatocellular carcinoma. J Surg Res 2011; 171:e33-e45.
8. Parks KR, Kuo YH, Davis JM, O' Brien B, Hagopian EJ. Laparoscopic versus open liver
resection: a meta-analysis of long-term outcome. HPB (Oxford). 2014;16:109-18.
9. Zhou Y, Xiao Y, Wu L, Li B, Li H. Laparoscopic liver resection as a safe and efficacious
alternative to open resection for colorectal liver metastasis: a meta-analysis. BMC Surg. 2013 Oct
1;13:44.
10. Rao A, Rao G, Ahmed I. Laparoscopic left lateral liver resection should be a standard operation.
Surg Endosc. 2011;25(5):1603-10.
4
11. Rao A, Rao G, Ahmed I. Laparoscopic or open liver resection? Let systematic review decide it.
Am J Surg. 2012; 204:222-31.
12. Rao AM, Ahmed I. Laparoscopic versus open liver resection for benign and malignant hepatic
lesions in adults. Cochrane Database Syst Rev. 2013
13. Mizuguchi T, Kawamoto M, Meguro M, Shibata T, Nakamura Y, Kimura Y, Furuhata T, Sonoda
T, Hirata K. Laparoscopic hepatectomy: a systematic review, meta-analysis, and power analysis.
Surg Today. 2011;41(1):39-47.
14. Xiong JJ, Altaf K, Javed MA, Huang W, Mukherjee R, Mai G, Sutton R, Liu XB, Hu WM. Metaanalysis of laparoscopic vs open liver resection for hepatocellular carcinoma. World J
Gastroenterol. 2012;18(45):6657-68
15. Luo LX, Yu ZY, Bai YN. Laparoscopic Hepatectomy for Liver Metastases from Colorectal
Cancer: A Meta-analysis. J Laparoendosc Adv Surg Tech A. 2014 Apr;24(4):213-22
16. Wei M, He Y, Wang J, Chen N, Zhou Z, Wang Z. Laparoscopic versus open hepatectomy with or
without synchronous colectomy for colorectal liver metastasis: a meta-analysis. PLoS One.
2014;9(1):e87461.
17. Schiffman SC, Kim KH, Tsung A, Marsh JW, Geller DA. Laparoscopic versus open liver
resection for metastatic colorectal cancer: A meta-analysis of 610 patients. Surgery, 2014, In
press.
5
Q2: What are the comparative long term outcomes of LLR and OLR ?(minor and major)
Author
Year
Journal
# pts (n)
Study
type
Tumor
LLR / OLR
Median F/U
(mos)
Median DFS
(mos)
Median OS
(mos)
3 yr DFS
(%)
5 yr DFS
(%)
3 yr OS (%)
5 yr OS
(%)
LLR / OLR
LLR / OLR
LLR / OLR
LLR / OLR
LLR / OLR
LLR / OLR
LLR /
OLR
p
values
Kim
2014
Surg Endo
29 / 29
Comparative
HCC
48 / 60
NA
NA
62 / 61
54 / 40
100 / 92
92 / 88
NS
Cheung
2013
Ann Surg
32 / 64
Comparative
HCC
NA
79 / 29
92 / 71
73 / 50
55 / 44
88 / 73
77 / 57
NS
Kobayashi
2013
Surg Endo
56 / 27
Comparative
HCC
19 / 68
NA
NA
50 / 62
NA
100 / 100
NA
NS
Ker
2011
Int J Hepat
116 / 208
Comparative
HCC
94 / 94
NA
NA
NA
NA
70 / 76
62 / 72
NS
Truant
2011
Surg Endo
35 / 53
Comparative
HCC
36 / 36
NA
NA
NA
36 / 34
NA
70 / 46
NS
Lee
2011
W J Surg
33 / 50
Comparative
HCC
35 / 29
NA
NA
51 / 56
45 / 56
82 / 81
76 / 76
NS
Hu
2011
W J Gastro
30 / 30
Comparative
HCC
NA
NA
NA
NA
NA
76 / 77
50 / 53
NS
Kim
2011
J Kor Surg
26 / 29
Comparative
HCC
22 / 25
NA
NA
NA
57 / 56
NA
NA
NS
Tranchart
2010
Surg Endo
42 / 42
Comparative
HCC
30 / 35
NA
NA
61 / 54
46 / 37
74 / 73
60 / 47
NS
Aldrighetti
2010
J Surg Onc
16 / 16
Comparative
HCC
32 / 32
23 / 31
40 / 48
NA
NA
NA
NA
NS
Belli
2009
Br J Surg
54 / 125
Comparative
HCC
24 / 24
38 / -
63 / -
52 / 55
NA
67 / 63
NA
NS
Sarpel
2009
AnnSurg Onc
20 / 56
Comparative
HCC
24 / 18
NA
NA
NA
NA
NA
95 / 75
NS
Endo
2009
Surg Lap ET
41923
Comparative
HCC
NA
NA
NA
NA
24 / 19
NA
57 / 48
NS
Lai
2009
Arch Surg
25 / 33
Comparative
HCC
29 / 29
NA
NA
52 / 56
NA
60 / 60
NA
NS
6
Q2: What are the comparative long term outcomes of LLR and OLR ?(minor and major)
Cai
2008
Surg Endo
31 / 31
Comparative
HCC
NA
NA
70 / 61
NA
NA
67 / 74
56 / 54
NS
Kaneko
2005
Am J Surg
30 / 28
Comparative
HCC
NA
NA
NA
45 / 50
31 / 29
80 / 77
61 / 62
NS
Laurent
2003
Arch Surg
13 / 13
Comparative
HCC
NA
NA
NA
56 / 54
NA
89 / 55
NA
0.04
Shimada
2001
Surg Endo
17 / 38
Comparative
HCC
17 / 29
NA
NA
NA
72 / 72
NA
48 / 38
NS
Soubrane
2014
HPB
351 / -
Survey
HCC
NA
NA
NA
56 / -
40 / -
70 / -
66 / -
Herman
2014
J Lap AdvSurg TA
30 / -
Descriptive
HCC
NA
NA
30 / -
58 / -
NA
76 / -
NA
Dagher
2011
Surg Endo
32 / -
Descriptive
HCC
26 / -
NA
NA
55 / -
NA
72 / -
NA
Belli
2011
Dig Surg
65 / -
Descriptive
HCC
NA
42 / -
75 / -
62 / -
32 / -
70 / -
55 / -
Dagher
2010
JACS
167 / -
Descriptive
HCC
30 / -
NA
NA
47 / -
32 / -
69 / -
65 / -
Yoon
2010
Surg Endo
69 / -
Descriptive
HCC
21 / -
NA
NA
60 / -
NA
90 / -
NA
Sasaki
2009
Br J Surg
37 / -
Descriptive
HCC
36 / -
NA
NA
NA
NA
73 / -
53 / -
Bryant
2009
Ann Surg
63 / -
Descriptive
HCC
26 / -
NA
NA
46 / -
34 / -
70 / -
65 / -
Lai
2009
W J Surg
30 / -
Descriptive
HCC
34 / -
NA
NA
NA
36 / -
NA
50 / -
Santambrogio
2009
LangArchSurg
22 / -
Descriptive
HCC
12 / -
NA
NA
49 / -
NA
73 / -
NA
Chen
2008
AnnSurg Onc
116 / -
Descriptive
HCC
94 / -
NA
NA
NA
NA
66 / -
59 / -
Cherqui
2006
Ann Surg
27 / -
Descriptive
HCC
24 / -
NA
NA
64 / -
NA
93 /-
NA
7
Q2: What are the comparative long term outcomes of LLR and OLR ?(minor and major)
Vibert
2006
Br J Surg
14 / -
Author
Year
Journal
# pts (n)
Descriptive
Study
type
HCC
40 / -
NA
NA
68 / -
NA
66 / -
NA
Tumor
Median F/U
(mos)
Median DFS
(mos)
Median OS
(mos)
3 yr DFS
(%)
5 yr DFS
(%)
3 yr OS (%)
5 yr OS
(%)
LLR / OLR
LLR / OLR
LLR / OLR
LLR / OLR
LLR / OLR
LLR / OLR
LLR / OLR
LLR /
OLR
p
values
Montalti
2014
EJSO
57 / 57
Comparative
mCRC
41 / 54
NA
NA
39 / 42
29 / 38
75 / 75
60 / 65
NS
Iwahashi
2013
Surg Endo
21 / 21
Comparative
mCRC
NA
NA
NA
14 / 33
14 / 25
84 / 89
42 / 51
NS
Guerron
2013
Surg Endo
40 /40
Comparative
mCRC
16 / 16
23/ 23
NA
NA
NA
89/81(2yr)
NA
NS
Qiu
2013
PlosOne
30 / 30
Comparative
mCRC
NA
NA
NA
NA
NA
NA
NA
Cannon
2012
Surgery
35 / 140
Comparative
mCRC
NA
NA
NA
37 / 39
15 / 22
63 / 60
36 / 42
NS
Cheung
2012
ANZJ Surg
20 / 40
Comparative
mCRC
NA
9.8 / 10.9
69 / 42
42 / 18
42 / 18
54 / 65
54 / 22
NS
Topal
2012
Surg End
20 / 20
Comparative
mCRC
NA
NA
NA
NA
43 / 23
NA
48 / 46
NS
Hu
2012
SurgLapEPT
13 / 13
Comparative
mCRC
NA
NA
NA
NA
NA
55 / 54
27 / 31
NS
Nguyen
2011
Arch Surg
24 / 25
Comparative
mCRC
27 / 29
NA
NA
63 / 46
NA
75 / 79
NA
NS
Abu Hilal
2010
Br J Surg
50 / 85
Comparative
mCRC
22 / 22
NA
NA
NA
NA
NA
NA
Castaing
2009
Ann Surg
60 / 60
Comparative
mCRC
30 / 33
47 / 40
NA
47 / 40
35 / 27
82 / 70
64 / 56
8
NS
Q2: What are the comparative long term outcomes of LLR and OLR ?(minor and major)
Abu Hilal
2012
Arch Surg
83 / -
Descriptive
mCRC
NA
64 (2 yr) / -
NA
64 (2 yr) / -
NA
80 (2 yr) / -
NA
Shafaee
2011
JACS
55 / -
Descriptive
mCRC
24 / -
NA
NA
27 / -
Repeat LLR
83 / -
55 / -
Kazaryan
2010
Ann Surg
122 / -
Descriptive
mCRC
19 / -
NA
NA
46 / -
42 / -
68 / -
51 / -
Nguyen
2009
Ann Surg
109 / -
Descriptive
mCRC
20 / -
NA
NA
43 / -
43 / -
69 / -
50 / -
Sasaki
2009
Br J Surg
39 / -
Descriptive
mCRC
22 / -
NA
NA
NA
NA
64 / -
64 / -
Bryant
2009
Ann Surg
22 / -
Descriptive
mCRC
36 / -
NA
NA
71 / -
47 / -
79 / -
64 / -
Ito
2009
JOGS
13 / -
Descriptive
mCRC
28 / -
NA
NA
NA
NA
NA
NA
Vibert
2006
Br J Surg
30 / -
Descriptive
mCRC
30 / -
NA
NA
74 / -
NA
87 / -
NA
Nathan
2010
JACS
/ 949
Descriptive
mCRC
/ 65
/ 45
Ito
2008
Ann Surg
/1,049
Descriptive
mCRC
/ 65
/ 45
Blazer
2008
J Clin Onc
/ 305
Descriptive
mCRC
/ 65
/ 42
Adam
2008
J Clin Onc
/ 738
Descriptive
mCRC
/ 61
/ 45
Zakaria
2007
Ann Surg
/ 662
Descriptive
mCRC
/ 55
/ 37
Open
mCRC
9