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Long-Term Outcome of Laparoscopic Versus Open Liver Resection for Hepatocellular Carcinoma: A Case-Controlled Study with Propensity Score Matching

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Abstract

Background

Laparoscopic liver resection (LR) for hepatocellular carcinoma (HCC) is usually applied to superficial and left-side small lesions. Therefore, well designed comparative studies about the results of LR versus open liver resection (OR) for HCC are difficult and still uncommon. The aim of this study was to compare the perioperative and long-term oncologic outcomes of LR versus OR for HCC between well-matched patient groups.

Methods

Between January 2000 and March 2012, 205 patients (43 with intent-to-treat with LR, 162 OR) underwent primary liver resection of less than three segments for HCC in our center. To select a comparison group, propensity score matching (PSM) was used at 1:1 ratio with covariates of baseline characteristics, including tumor characteristics. Outcomes were compared between the matched groups.

Results

The two groups were well balanced by PSM and 29 patients were matched respectively. In LR, there was more non-anatomical resection (65.5 vs. 34.5 %; p = 0.012), less postoperative ascites (0.0 vs. 17.2 %; p = 0.025), and shorter hospital stay (7.69 ± 2.94 vs. 13.38 ± 7.37 days; p < 0.001). With the exception of these, there were no significant differences in perioperative and long-term outcomes. The 1-, 3- and 5-year survivals were 100, 100 and 92.2 % in LR, and 96.5, 92.2 and 87.7 % in OR (p = 0.267), respectively. The 1-, 3- and 5-year disease-free survivals were 81.7, 61.7 and 54.0 % in LR, and 78.6, 60.9 and 40.1 % in OR, respectively (p = 0.929).

Conclusions

The outcome of LR for HCC was technically feasible and safe in selected patients, and LR showed similar perioperative and long-term oncologic outcomes when compared with OR matched with PSM.

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References

  1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893–2917

    Article  CAS  PubMed  Google Scholar 

  2. Forner A, Llovet JM, Bruix J (2012) Hepatocellular carcinoma. Lancet 379:1245–1255

    Article  PubMed  Google Scholar 

  3. Sherman M (2010) Hepatocellular carcinoma: epidemiology, surveillance, and diagnosis. Semin Liver Dis 30:3–16

    Article  CAS  PubMed  Google Scholar 

  4. Bruix J, Sherman M, American Association for the Study of Liver Diseases (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022

    Article  PubMed Central  PubMed  Google Scholar 

  5. Rahbari NN, Mehrabi A, Mollberg NM, Muller SA, Koch M, Buchler MW, Weitz J (2011) Hepatocellular carcinoma: current management and perspectives for the future. Ann Surg 253:453–469

    Article  PubMed  Google Scholar 

  6. Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS, Wakabayashi G, Belli G, Kaneko H, Ker CG, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D’Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey JN, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS (2009) The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 250:825–830

    Article  PubMed  Google Scholar 

  7. Hashizume M, Takenaka K, Yanaga K, Ohta M, Kajiyama K, Shirabe K, Itasaka H, Nishizaki T, Sugimachi K (1995) Laparoscopic hepatic resection for hepatocellular carcinoma. Surg Endosc 9:1289–1291

    Article  CAS  PubMed  Google Scholar 

  8. Mittler J, McGillicuddy JW, Chavin KD (2011) Laparoscopic liver resection in the treatment of hepatocellular carcinoma. Clin Liver Dis 15:371–384 vii–x

    Article  PubMed  Google Scholar 

  9. Yin Z, Fan X, Ye H, Yin D, Wang J (2013) Short- and long-term outcomes after laparoscopic and open hepatectomy for hepatocellular carcinoma: a global systematic review and meta-analysis. Ann Surg Oncol 20:1203–1215

    Article  PubMed  Google Scholar 

  10. Belli G, Limongelli P, Fantini C, D’Agostino A, Cioffi L, Belli A, Russo G (2009) Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg 96:1041–1048

    Article  CAS  PubMed  Google Scholar 

  11. Tranchart H, Di Giuro G, Lainas P, Roudie J, Agostini H, Franco D, Dagher I (2010) Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc 24:1170–1176

    Article  PubMed  Google Scholar 

  12. Sarpel U, Hefti MM, Wisnievsky JP, Roayaie S, Schwartz ME, Labow DM (2009) Outcome for patients treated with laparoscopic versus open resection of hepatocellular carcinoma: case-matched analysis. Ann Surg Oncol 16:1572–1577

    Article  CAS  PubMed  Google Scholar 

  13. Belli G, Fantini C, D’Agostino A, Cioffi L, Langella S, Russolillo N, Belli A (2007) Laparoscopic versus open liver resection for hepatocellular carcinoma in patients with histologically proven cirrhosis: short- and middle-term results. Surg Endosc 21:2004–2011

    Article  CAS  PubMed  Google Scholar 

  14. Laurent A, Cherqui D, Lesurtel M, Brunetti F, Tayar C, Fagniez PL (2003) Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg 138:763–769 discussion 769

    Article  PubMed  Google Scholar 

  15. Kaneko H, Takagi S, Otsuka Y, Tsuchiya M, Tamura A, Katagiri T, Maeda T, Shiba T (2005) Laparoscopic liver resection of hepatocellular carcinoma. Am J Surg 189:190–194

    Article  PubMed  Google Scholar 

  16. Endo Y, Ohta M, Sasaki A, Kai S, Eguchi H, Iwaki K, Shibata K, Kitano S (2009) A comparative study of the long-term outcomes after laparoscopy-assisted and open left lateral hepatectomy for hepatocellular carcinoma. Surg Laparosc Endosc Percutan Tech 19:e171–e174

    Article  PubMed  Google Scholar 

  17. Lee KF, Chong CN, Wong J, Cheung YS, Wong J, Lai P (2011) Long-term results of laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma: a case-matched analysis. World J Surg 35:2268–2274

    Article  PubMed  Google Scholar 

  18. Li N, Wu YR, Wu B, Lu MQ (2012) Surgical and oncologic outcomes following laparoscopic versus open liver resection for hepatocellular carcinoma: a meta-analysis. Hepatol Res 42:51–59

    Article  PubMed  Google Scholar 

  19. McPhail MJ, Scibelli T, Abdelaziz M, Titi A, Pearce NW, Abu Hilal M (2009) Laparoscopic versus open left lateral hepatectomy. Expert Rev Gastroenterol Hepatol 3:345–351

    Article  PubMed  Google Scholar 

  20. Truant S, Bouras AF, Hebbar M, Boleslawski E, Fromont G, Dharancy S, Leteurtre E, Zerbib P, Pruvot FR (2011) Laparoscopic resection vs. open liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: a case-matched study. Surg Endosc 25:3668–3677

    Article  CAS  PubMed  Google Scholar 

  21. Cai XJ, Yang J, Yu H, Liang X, Wang YF, Zhu ZY, Peng SY (2008) Clinical study of laparoscopic versus open hepatectomy for malignant liver tumors. Surg Endosc 22:2350–2356

    Article  PubMed  Google Scholar 

  22. Cherqui D, Laurent A, Tayar C, Chang S, Van Nhieu JT, Loriau J, Karoui M, Duvoux C, Dhumeaux D, Fagniez PL (2006) Laparoscopic liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: midterm results and perspectives. Ann Surg 243:499–506

    Article  PubMed  Google Scholar 

  23. Rosenbaum PR, Rubin DB (1985) Constructing a control group using multivariate matched sampling methods that incorporate the propensity score. Am Stat 39:33–38

    Google Scholar 

  24. Lemeshow S, Hosmer DW Jr (1982) A review of goodness of fit statistics for use in the development of logistic regression models. Am J Epidemiol 115:92–106

    CAS  PubMed  Google Scholar 

  25. Hauck WW (1982) Re: “a review of goodness of fit statistics for use in the development of logistic regression models”. Am J Epidemiol 116:732

    CAS  PubMed  Google Scholar 

  26. D’Agostino RB Jr (1998) Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med 17:2265–2281

    Article  PubMed  Google Scholar 

  27. Xiong JJ, Altaf K, Javed MA, Huang W, Mukherjee R, Mai G, Sutton R, Liu XB, Hu WM (2012) Meta-analysis of laparoscopic vs open liver resection for hepatocellular carcinoma. World J Gastroenterol 18:6657–6668

    Article  PubMed  Google Scholar 

  28. Austin PC, Mamdani MM (2006) A comparison of propensity score methods: a case–study estimating the effectiveness of post-AMI statin use. Stat Med 25:2084–2106

    Article  PubMed  Google Scholar 

  29. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M (2009) The Clavien–Dindo classification of surgical complications: five-year experience. Ann Surg 250:187–196

    Article  PubMed  Google Scholar 

  30. Aldrighetti L, Guzzetti E, Pulitano C, Cipriani F, Catena M, Paganelli M, Ferla G (2010) Case-matched analysis of totally laparoscopic versus open liver resection for HCC: short and middle term results. J Surg Oncol 102:82–86

    Article  PubMed  Google Scholar 

  31. Hu BS, Chen K, Tan HM, Ding XM, Tan JW (2011) Comparison of laparoscopic vs open liver lobectomy (segmentectomy) for hepatocellular carcinoma. World J Gastroenterol 17:4725–4728

    Article  PubMed  Google Scholar 

  32. Ker CG, Chen JS, Kuo KK, Chuang SC, Wang SJ, Chang WC, Lee KT, Chen HY, Juan CC (2011) Liver surgery for hepatocellular carcinoma: laparoscopic versus open approach. Int J Hepatol 2011:596792

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Kim HH, Park EK, Seoung JS, Hur YH, Koh YS, Kim JC, Cho CK, Kim HJ (2011) Liver resection for hepatocellular carcinoma: case-matched analysis of laparoscopic versus open resection. J Korean Surg Soc 80:412–419

    Article  PubMed Central  PubMed  Google Scholar 

  34. Zhou YM, Shao WY, Zhao YF, Xu DH, Li B (2011) Meta-analysis of laparoscopic versus open resection for hepatocellular carcinoma. Dig Dis Sci 56:1937–1943

    Article  PubMed  Google Scholar 

  35. Fancellu A, Rosman AS, Sanna V, Nigri GR, Zorcolo L, Pisano M, Melis M (2011) Meta-analysis of trials comparing minimally-invasive and open liver resections for hepatocellular carcinoma. J Surg Res 171:e33–e45

    Article  PubMed  Google Scholar 

  36. Stoot JH, Wong-Lun-Hing EM, Limantoro I, Visschers R, Busch OR, Van Hillegersberg R, De Jong KM, Rijken AM, Kazemier G, Olde Damink SW, Lodewick TM, Bemelmans MH, van Dam RM, Dejong CH (2012) Laparoscopic liver resection in The Netherlands: how far are we? Dig Surg 29:70–78

    Article  PubMed  Google Scholar 

  37. Rao A, Rao G, Ahmed I (2012) Laparoscopic or open liver resection? Let systematic review decide it. Am J Surg 204:222–231

    Article  PubMed  Google Scholar 

  38. Han H-S (2013, May) Prospective randomized trial of laparoscopic versus open liver resection with hepatocellular carcinoma. http://clinicaltrials.gov/ct2/show/NCT00606385

  39. Austin PC (2011) Optimal caliper widths for propensity-score matching when estimating differences in means and differences in proportions in observational studies. Pharm Stat 10:150–161

    Article  PubMed Central  PubMed  Google Scholar 

  40. Kaneko H (2005) Laparoscopic hepatectomy: indications and outcomes. J Hepatobiliary Pancreat Surg 12:438–443

    Article  PubMed  Google Scholar 

  41. Mizuguchi T, Kawamoto M, Meguro M, Shibata T, Nakamura Y, Kimura Y, Furuhata T, Sonoda T, Hirata K (2011) Laparoscopic hepatectomy: a systematic review, meta-analysis, and power analysis. Surg Today 41:39–47

    Article  PubMed  Google Scholar 

  42. Hasegawa K, Kokudo N, Imamura H, Matsuyama Y, Aoki T, Minagawa M, Sano K, Sugawara Y, Takayama T, Makuuchi M (2005) Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg 242:252–259

    Article  PubMed  Google Scholar 

  43. Kobayashi A, Miyagawa S, Miwa S, Nakata T (2008) Prognostic impact of anatomical resection on early and late intrahepatic recurrence in patients with hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 15:515–521

    Article  PubMed  Google Scholar 

  44. Eguchi S, Kanematsu T, Arii S, Okazaki M, Okita K, Omata M, Ikai I, Kudo M, Kojiro M, Makuuchi M, Monden M, Matsuyama Y, Nakanuma Y, Takayasu K, Liver Cancer Study Group of Japan (2008) Comparison of the outcomes between an anatomical subsegmentectomy and a non-anatomical minor hepatectomy for single hepatocellular carcinomas based on a Japanese nationwide survey. Surgery 143:469–475

    Article  PubMed  Google Scholar 

  45. Kamiyama T, Nakanishi K, Yokoo H, Kamachi H, Matsushita M, Todo S (2010) The impact of anatomical resection for hepatocellular carcinoma that meets the Milan criteria. J Surg Oncol 101:54–60

    Article  PubMed  Google Scholar 

  46. Arii S, Tanaka S, Mitsunori Y, Nakamura N, Kudo A, Noguchi N, Irie T (2010) Surgical strategies for hepatocellular carcinoma with special reference to anatomical hepatic resection and intraoperative contrast-enhanced ultrasonography. Oncology 78(Suppl 1):125–130

    Article  PubMed  Google Scholar 

  47. Chen HY, Juan CC, Ker CG (2008) Laparoscopic liver surgery for patients with hepatocellular carcinoma. Ann Surg Oncol 15:800–806

    Article  PubMed  Google Scholar 

  48. Dagher I, Belli G, Fantini C, Laurent A, Tayar C, Lainas P, Tranchart H, Franco D, Cherqui D (2010) Laparoscopic hepatectomy for hepatocellular carcinoma: a European experience. J Am Coll Surg 211:16–23

    Article  PubMed  Google Scholar 

  49. Teramoto K, Kawamura T, Takamatsu S, Noguchi N, Nakamura N, Arii S (2003) Laparoscopic and thoracoscopic partial hepatectomy for hepatocellular carcinoma. World J Surg 27:1131–1136

    Article  PubMed  Google Scholar 

  50. Reddy YP, Sheridan WG (2000) Port-site metastasis following laparoscopic cholecystectomy: a review of the literature and a case report. Eur J Surg Oncol 26:95–98

    Article  CAS  PubMed  Google Scholar 

  51. Paolucci V (2001) Port site recurrences after laparoscopic cholecystectomy. J Hepatobiliary Pancreat Surg 8:535–543

    Article  CAS  PubMed  Google Scholar 

  52. Sakata N, Suzuki M, Shibuya K, Takeda K, Matsuno S (2002) Unexpected bile duct carcinoma presenting with port-site metastasis after laparoscopic cholecystectomy for cholecystolithiasis. J Hepatobiliary Pancreat Surg 9:511–514

    Article  PubMed  Google Scholar 

  53. Nasiri S, Gafuri A, Karamnejad M, Farshidfar F (2009) Four port-site recurrences of gall bladder cancer after laparoscopic cholecystectomy. ANZ J Surg 79:75–76

    Article  PubMed  Google Scholar 

  54. Singla S, Singla S, Budhiraja S (2009) Port site metastasis after laparoscopic cholecystectomy. Indian J Surg 71:41–42

    Article  PubMed Central  PubMed  Google Scholar 

  55. Raznatovic ZJ, Zaric ND, Galun DA, Lekic NS, Micev M, Djordjevic VR, Djurasic LM, Kerkez MD (2012) Multiple port-site metastasis of incidental gallbladder carcinoma after laparoscopic cholecystectomy. Acta Chir Iugosl 59:105–109

    Article  PubMed  Google Scholar 

  56. Barbulescu M, Alecu L, Boeti P, Popescu I (2012) Port-site metastasis after laparoscopic surgery for colorectal cancer—still a real concern? Case report and review of the literature. Chirurgia (Bucur) 107:103–107

    CAS  Google Scholar 

  57. Itano O, Watanabe T, Jinno H, Suzuki F, Baba H, Otaka H (2003) Port site metastasis of sigmoid colon cancer after a laparoscopic sigmoidectomy: report of a case. Surg Today 33:379–382

    Article  PubMed  Google Scholar 

  58. Koga C, Tanemura M, Wada H, Kobayashi S, Marubashi S, Eguchi H, Mori M, Doki Y, Nagano H (2011) A case report of port-site metastasis of pancreatic cancer after laparoscope assisted distal pancreatectomy. Gan To Kagaku Ryoho 38:2454–2456

    PubMed  Google Scholar 

  59. Davies AR, Ahmed W, Purkiss SF (2008) Port site metastasis following diagnostic laparoscopy for a malignant gastro-intestinal stromal tumour. World J Surg Oncol 6:55

    Article  PubMed Central  PubMed  Google Scholar 

  60. Chen YY, Yen HH (2011) Subcutaneous metastases after laparoscopic-assisted partial hepatectomy for hepatocellular carcinoma. Surg Laparosc Endosc Percutan Tech 21:e41–e43

    Article  PubMed  Google Scholar 

  61. Palomba S, Falbo A, Russo T, La Sala GB (2012) Port-site metastasis after laparoscopic surgical staging of endometrial cancer: a systematic review of the published and unpublished data. J Minim Invasive Gynecol 19:531–537

    Article  PubMed  Google Scholar 

  62. Kadi N, Isherwood M, Al-Akraa M, Williams S (2012) Port-site metastasis after laparoscopic surgery for urological malignancy: forgotten or missed. Adv Urol 2012:609531

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Pearce NW, Di Fabio F, Teng MJ, Syed S, Primrose JN, Abu Hilal M (2011) Laparoscopic right hepatectomy: a challenging, but feasible, safe and efficient procedure. Am J Surg 202:e52–e58

    Article  PubMed  Google Scholar 

  64. Tsai TJ, Chouillard EK, Gumbs AA (2012) Laparoscopic right hepatectomy with intrahepatic transection of the right bile duct. Ann Surg Oncol 19:467–468

    Article  PubMed  Google Scholar 

  65. Han HS, Yoon YS, Cho JY, Ahn KS (2010) Laparoscopic right hemihepatectomy for hepatocellular carcinoma. Ann Surg Oncol 17:2090–2091

    Article  PubMed  Google Scholar 

  66. Kobayashi S, Nagano H, Marubashi S, Wada H, Eguchi H, Takeda Y, Tanemura M, Sekimoto M, Doki Y, Mori M (2010) A single-incision laparoscopic hepatectomy for hepatocellular carcinoma: initial experience in a Japanese patient. Minim Invasive Ther Allied Technol 19:367–371

    Article  PubMed  Google Scholar 

  67. Gaujoux S, Kingham TP, Jarnagin WR, D’Angelica MI, Allen PJ, Fong Y (2011) Single-incision laparoscopic liver resection. Surg Endosc 25:1489–1494

    Article  PubMed  Google Scholar 

  68. Hu MG, Zhao GD, Xu DB, Liu R (2011) Transumbilical single-incision laparoscopic hepatectomy: an initial report. Chin Med J (Engl) 124:787–789

    Google Scholar 

  69. Shetty GS, You YK, Choi HJ, Na GH, Hong TH, Kim DG (2012) Extending the limitations of liver surgery: outcomes of initial human experience in a high-volume center performing single-port laparoscopic liver resection for hepatocellular carcinoma. Surg Endosc 26:1602–1608

    Article  PubMed  Google Scholar 

  70. Pan M, Jiang Z, Cheng Y, Xu X, Zhang Z, Zhou C, He G, Xu T, Liu H, Gao Y (2012) Single-incision laparoscopic hepatectomy for benign and malignant hepatopathy: initial experience in 8 Chinese patients. Surg Innov 19:446–451

    Article  PubMed  Google Scholar 

  71. Choi HJ, You YK, Na GH, Hong TH, Shetty GS, Kim DG (2012) Single-port laparoscopy-assisted donor right hepatectomy in living donor liver transplantation: sensible approach or unnecessary hindrance? Transplant Proc 44:347–352

    Article  CAS  PubMed  Google Scholar 

  72. Aikawa M, Miyazawa M, Okamoto K, Toshimitsu Y, Okada K, Ueno Y, Yamaguchi S, Koyama I (2012) Single-port laparoscopic hepatectomy: technique, safety, and feasibility in a clinical case series. Surg Endosc 26:1696–1701

    Article  PubMed  Google Scholar 

  73. Lai EC, Tang CN, Li MK (2012) Robot-assisted laparoscopic hemi-hepatectomy: technique and surgical outcomes. Int J Surg 10:11–15

    Article  PubMed  Google Scholar 

  74. Ji WB, Wang HG, Zhao ZM, Duan WD, Lu F, Dong JH (2011) Robotic-assisted laparoscopic anatomic hepatectomy in China: initial experience. Ann Surg 253:342–348

    Article  PubMed  Google Scholar 

  75. Ho CM, Wakabayashi G, Nitta H, Ito N, Hasegawa Y, Takahara T (2013) Systematic review of robotic liver resection. Surg Endosc 27:732–739

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

For statistical treatment and analysis in the present study, we received complete assistance for PSM and substantial counsel for analysis of the outcomes of our study from the Medical Research Collaborating Center in the Seoul National University Hospital Biomedical Research Institute.

Disclosures

Drs. Hyeyoung Kim, Kyung-Suk Suh, Kwang-Woong Lee, Nam-Joon Yi, Geun Hong, Suk-Won Suh, Tae Yoo, Min-Su Park, YoungRok Choi, and Hae Won Lee have no conflicts of interest or financial ties to disclose.

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Kim, H., Suh, KS., Lee, KW. et al. Long-Term Outcome of Laparoscopic Versus Open Liver Resection for Hepatocellular Carcinoma: A Case-Controlled Study with Propensity Score Matching. Surg Endosc 28, 950–960 (2014). https://doi.org/10.1007/s00464-013-3254-3

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