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Laparoscopic and open minor liver resection for hepatocellular carcinoma with clinically significant portal hypertension: a multicenter study using inverse probability weighting approach

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Abstract

Background

Liver resection offers substantial advantages over open liver resection (OLR) for patients with hepatocellular carcinoma (HCC) in terms of reduced intraoperative blood loss and morbidity. However, there is limited evidence comparing the indications and perioperative outcomes with the open versus laparoscopic approach for resection. This study aimed to compare postoperative outcomes between patients undergoing laparoscopic liver resection (LLR) and OLR for HCC with clinically significant portal hypertension (CSPH).

Methods

A total of 316 HCC patients with CSPH (the presence of gastroesophageal varices or platelet count < 100,000/ml and spleen diameter > 12 cm) undergoing minor liver resection at eight centers were included in this study. To adjust for confounding factors between the LLR and OLR groups, an inverse probability weighting method analysis was performed.

Results

Overall, 193 patients underwent LLR and 123 underwent OLR. After weighting, LLR was associated with a lower volume of intraoperative blood loss and the incidence of postoperative complications (including pulmonary complications, incisional surgical site infection, and paralytic ileus) compared to the OLR group. The 3-, 5-, and 7-year postoperative recurrence-free survival rates were 39%, 26%, and 22% in the LLR group and 49%, 18%, and 18% in the OLR group, respectively (p = 0.18). And, the 3-, 5-, and 7-year postoperative overall survival rates were 71%, 56%, and 44% in the LLR group and 76%, 51%, 44% in the OLR group, respectively (p = 0.87).

Conclusions

LLR for HCC patients with CSPH is clinically advantageous by lowering the volume of intraoperative blood loss and incidence of postoperative complications, thereby offering feasible long-term survival.

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References

  1. Bruix J, Gores GJ, Mazzaferro V (2014) Hepatocellular carcinoma: clinical frontiers and perspectives. Gut 63:844–855

    Article  CAS  PubMed  Google Scholar 

  2. Nababan SHH, Lesmana CRA (2022) Portal hypertension in nonalcoholic fatty liver disease: from pathogenesis to clinical practice. J Clin Transl Hepatol 10:979–985

    Article  PubMed  PubMed Central  Google Scholar 

  3. Sakiani S, Heller T (2022) Current and investigational drugs in early clinical development for portal hypertension. Front Med (Lausanne) 9:974182

    Article  PubMed  Google Scholar 

  4. European Association for the Study of the Liver (2018) EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 69:182–236

    Article  Google Scholar 

  5. Liu J, Zhang H, Xia Y, Yang T, Gao Y, Li J et al (2019) Impact of clinically significant portal hypertension on outcomes after partial hepatectomy for hepatocellular carcinoma: a systematic review and meta-analysis. HPB (Oxford) 21:1–13

    Article  PubMed  Google Scholar 

  6. Ishizawa T, Hasegawa K, Aoki T, Takahashi M, Inoue Y, Sano K et al (2008) Neither multiple tumors nor portal hypertension are surgical contraindications for hepatocellular carcinoma. Gastroenterology 134:1908–1916

    Article  PubMed  Google Scholar 

  7. Oba A, Ishizawa T, Mise Y, Inoue Y, Ito H, Ono Y et al (2019) Possible underestimation of blood loss during laparoscopic hepatectomy. BJS Open 3:336–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Takahara T, Wakabayashi G, Beppu T, Aihara A, Hasegawa K, Gotohda N et al (2015) Long-term and perioperative outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma with propensity score matching: a multi-institutional Japanese study. J Hepato-Bil Pancreat Sci 22:721–727

    Article  Google Scholar 

  9. Ishizawa T, Hasegawa K, Kokudo N, Sano K, Imamura H, Beck Y et al (2009) Risk factors and management of ascites after liver resection to treat hepatocellular carcinoma. Arch Surg 144:46–51

    Article  PubMed  Google Scholar 

  10. Uchiyama H, Harimoto N, Itoh S, Yoshizaumi T, Ikegami T, Maehara Y (2017) Pleural effusion after hepatectomy for hepatocellular carcinoma: risk factor analyses and its impact on oncological outcomes. World J Surg 41:1089–1099

    Article  PubMed  Google Scholar 

  11. Zhao Y, Jin Y, Wu Y (2016) Postoperative infectious complications after liver resection for hepatocellular carcinoma. J Cancer Res Ther 12:C268-270

    Article  PubMed  Google Scholar 

  12. Li YR, Chen JD, Huang J, Wu FX, Jin GZ (2022) Post-hepatectomy liver failure prediction and prevention: development of a nomogram containing postoperative anticoagulants as a risk factor. Ann Hepatol 27:100744

    Article  CAS  PubMed  Google Scholar 

  13. Imai D, Maeda T, Wang H, Shimagaki T, Sanefuji K, Kayashima H et al (2021) Risk factors for and outcomes of intraoperative blood loss in liver resection for hepatocellular tumors. Am Surg 87:376–383

    Article  PubMed  Google Scholar 

  14. Molina V, Sampson-Davila J, Ferrer J, Fondevila C, Diaz Del Gobbo R, Calatayud D et al (2018) Benefits of laparoscopic liver resection in patients with hepatocellular carcinoma and portal hypertension: a case-matched study. Surg Endosc 32:2345–2354

    Article  PubMed  Google Scholar 

  15. Lim C, Osseis M, Lahat E, Doussot A, Sotirov D, Hemery F et al (2019) Safety of laparoscopic hepatectomy in patients with hepatocellular carcinoma and portal hypertension: interim analysis of an open prospective study. Surg Endosc 33:811–820

    Article  PubMed  Google Scholar 

  16. Zheng J, Feng X, Liang Y, Cai J, Shi Z, Kirih MA et al (2021) Safety and feasibility of laparoscopic liver resection for hepatocellular carcinoma with clinically significant portal hypertension: a propensity score-matched study. Surg Endosc 35:3267–3278

    Article  PubMed  Google Scholar 

  17. Casellas-Robert M, Lim C, Lopez-Ben S, Llado L, Salloum C, Codina-Font J et al (2020) Laparoscopic liver resection for hepatocellular carcinoma in Child-Pugh A patients with and without portal hypertension: a multicentre study. World J Surg 44:3915–3922

    Article  PubMed  Google Scholar 

  18. Harada N, Maeda T, Yoshizumi T, Ikeda T, Kayashima H, Ikegami T et al (2016) Laparoscopic liver resection is a feasible treatment for patients with hepatocellular carcinoma and portal hypertension. Anticancer Res 36:3489–3497

    CAS  PubMed  Google Scholar 

  19. Azoulay D, Ramos E, Casellas-Robert M, Salloum C, Llado L, Nadler R et al (2021) Liver resection for hepatocellular carcinoma in patients with clinically significant portal hypertension. JHEP Rep 3:100190

    Article  PubMed  Google Scholar 

  20. Llovet JM, Bru C, Bruix J (1999) Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 19:329–338

    Article  CAS  PubMed  Google Scholar 

  21. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, Montalto F, Ammatuna M, Morabito A, Gennari L (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334:693–699

    Article  CAS  PubMed  Google Scholar 

  22. Ueno M, Hayami S, Sonomura T, Kawai M, Hirono S, Okada KI et al (2019) Concomitant use of indocyanine green fluorescence imaging and interventional radiology for detection of liver segments during laparoscopic anatomical liver resection: pilot feasibility study. Surg Laparosc Endosc Percutan Tech 29:242–246

    Article  PubMed  Google Scholar 

  23. Ishizawa T, Gumbs AA, Kokudo N, Gayet B (2012) Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 256:959–964

    Article  PubMed  Google Scholar 

  24. Lim C, Ishizawa T, Miyata A, Mise Y, Sakamoto Y, Hasegawa K et al (2016) Surgical indications and procedures for resection of hepatic malignancies confined to segment VII. Ann Surg 263:529–537

    Article  PubMed  Google Scholar 

  25. Liang X, Zheng J, Xu J, Tao L, Cai J, Liang Y et al (2021) Laparoscopic anatomical portal territory hepatectomy using Glissonean pedicle approach (Takasaki approach) with indocyanine green fluorescence negative staining: how I do it. HPB (Oxford) 23:1392–1399

    Article  PubMed  Google Scholar 

  26. Hu JX, Dai WD, Miao XY, Zhong DW, Huang SF, Wen Y et al (2009) Anatomic resection of segment VIII of liver for hepatocellular carcinoma in cirrhotic patients based on an intrahepatic Glissonian approach. Surgery 146:854–860

    Article  PubMed  Google Scholar 

  27. Wada H, Eguchi H, Nagano H, Kubo S, Nakai T, Kaibori M et al (2018) Perioperative allogenic blood transfusion is a poor prognostic factor after hepatocellular carcinoma surgery: a multi-center analysis. Surg Today 48:73–79

    Article  PubMed  Google Scholar 

  28. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213

    Article  PubMed  PubMed Central  Google Scholar 

  29. Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L et al (2011) Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the international study group of liver surgery. Surgery 149:680–688

    Article  PubMed  Google Scholar 

  30. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR (1999) Guideline for prevention of surgical site infection, 1999. Hospital infection control practices advisory committee. Infect Control Hosp Epidemiol 1999(20):250–278

    Google Scholar 

  31. Famularo S, Donadon M, Cipriani F, Ardito F, Iaria M, Carissimi F et al (2021) The impact of postoperative ascites on survival after surgery for hepatocellular carcinoma: a national study. J Gastrointest Surg 25:2823–2834

    Article  PubMed  Google Scholar 

  32. Kubo S, Tsukamoto T, Hirohashi K, Tanaka H, Shuto T, Takemura S et al (2004) Correlation between preoperative serum concentration of type IV collagen 7s domain and hepatic failure following resection of hepatocellular carcinoma. Ann Surg 239:186–193

    Article  PubMed  PubMed Central  Google Scholar 

  33. Rosenbaum PR, Rubin DB (1984) Reducing bias in observational studies using subclassification on the propensity score. J Am Stat Assoc 79:516–524

    Article  Google Scholar 

  34. Premkumar M, Anand AC (2022) Overview of complications in cirrhosis. J Clin Exp Hepatol 12:1150–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wang J, Zhang Z, Shang D, Li J, Liu C, Yu P et al (2022) Noninvasively assessed portal hypertension grade predicts post-hepatectomy liver failure in patients with HepatocellCarcinoma: a multicenter study. Front Oncol 12:934870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Yoshino K, Yoh T, Taura K, Seo S, Ciria R, Briceno-Delgado J (2021) A systematic review of prediction models for post-hepatectomy liver failure in patients undergoing liver surgery. HPB (Oxford) 23:1311–1320

    Article  PubMed  Google Scholar 

  37. Choi SB, Kim HJ, Song TJ, Ahn HS, Choi SY (2014) Influence of clinically significant portal hypertension on surgical outcomes and survival following hepatectomy for hepatocellular carcinoma: a systematic review and meta-analysis. J Hepato-Bil Pancreat Sci 21:639–647

    Article  Google Scholar 

  38. He W, Zeng Q, Zheng Y, Chen M, Shen J, Qiu J et al (2015) The role of clinically significant portal hypertension in hepatic resection for hepatocellular carcinoma patients: a propensity score matching analysis. BMC Cancer 15:263

    Article  PubMed  PubMed Central  Google Scholar 

  39. Westerkamp AC, Lisman T, Porte RJ (2009) How to minimize blood loss during liver surgery in patients with cirrhosis. HPB (Oxford) 11:453–458

    Article  PubMed  Google Scholar 

  40. Hackl C, Schlitt HJ, Renner P, Lang SA (2016) Liver surgery in cirrhosis and portal hypertension. World J Gastroenterol 22:2725–2735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Miyagi S, Nakanishi C, Hara Y, Kamei T, Kawagishi N, Ohuchi N (2015) An evaluation of the safety of pure laparoscopic hepatectomy in patients with liver cirrhosis: investigations including serum albumin and ascites. Surg Laparosc Endosc Percutan Tech 25:209–211

    Article  PubMed  Google Scholar 

  42. Han HS, Shehta A, Ahn S, Yoon YS, Cho JY, Choi Y (2015) Laparoscopic versus open liver resection for hepatocellular carcinoma: case-matched study with propensity score matching. J Hepatol 63:643–650

    Article  PubMed  Google Scholar 

  43. Tanaka S, Kawaguchi Y, Kubo S, Kanazawa A, Takeda Y, Hirokawa F et al (2019) Validation of index-based IWATE criteria as an improved difficulty scoring system for laparoscopic liver resection. Surgery 165:731–740

    Article  PubMed  Google Scholar 

  44. Fuks D, Cauchy F, Fteriche S, Nomi T, Schwarz L, Dokmak S et al (2016) Laparoscopy decreases pulmonary complications in patients undergoing major liver resection: a propensity score analysis. Ann Surg 263:353–361

    Article  PubMed  Google Scholar 

  45. Scuderi V, Barkhatov L, Montalti R, Ratti F, Cipriani F, Pardo F et al (2017) Outcome after laparoscopic and open resections of posterosuperior segments of the liver. Br J Surg 104:751–759

    Article  CAS  PubMed  Google Scholar 

  46. Alukal JJ, Thuluvath PJ (2019) Gastrointestinal failure in critically ill patients with cirrhosis. Am J Gastroenterol 114:1231–1237

    Article  PubMed  Google Scholar 

  47. Xiong JJ, Nunes QM, Huang W, Tan CL, Ke NW, Xie SM et al (2013) Laparoscopic vs open total gastrectomy for gastric cancer: a meta-analysis. World J Gastroenterol 19:8114–8132

    Article  PubMed  PubMed Central  Google Scholar 

  48. Liang W, Li J, Zhang W, Liu J, Li M, Gao Y et al (2019) Prolonged postoperative ileus in gastric surgery: is there any difference between laparoscopic and open surgery? Cancer Med 8:5515–5523

    Article  PubMed  PubMed Central  Google Scholar 

  49. Hajibandeh S, Hajibandeh S, Bill V (2020) Meta-analysis of enhanced recovery after surgery (ERAS) protocols in emergency abdominal surgery. World J Surg 44:1336–1348

    Article  PubMed  Google Scholar 

  50. Morise Z, Kawabe N, Kawase J, Tomishige H, Nagata H, Ohshima H et al (2013) Pure laparoscopic hepatectomy for hepatocellular carcinoma with chronic liver disease. World J Hepatol 5:487–495

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  52. Troisi RI, Berardi G, Morise Z, Cipriani F, Ariizumi S, Sposito C et al (2021) Laparoscopic and open liver resection for hepatocellular carcinoma with Child–Pugh B cirrhosis: multicentre propensity score-matched study. Br J Surg 108:196–204

    Article  CAS  PubMed  Google Scholar 

  53. Zhu P, Liao W, Zhang WG, Chen L, Shu C, Zhang ZW et al (2023) A Prospective Study Using propensity score matching to compare long-term survival outcomes after robotic-assisted, laparoscopic, or open liver resection for patients with BCLC stage 0-A hepatocellular carcinoma. Ann Surg 277:e103–e111

    Article  PubMed  Google Scholar 

  54. Rayman S, Sucandy I, Ross SB, Crespo K, Syblis C, Rosemurgy A (2023) A propensity score matched analysis of robotic and open hepatectomy for treatment of liver tumors. Clinical outcomes, oncological survival, and costs comparison. J Robot Surg 17:2399–407

    Article  PubMed  Google Scholar 

  55. Gumbs AA, Lorenz E, Tsai TJ, Starker L, Flanagan J, Benedetti Cacciaguerra A, Yu NJ, Bajul M, Chouillard E, Croner R, Abu Hilal M (2022) Study: international multicentric minimally invasive liver resection for colorectal liver metastases (SIMMILR-CRLM). Cancers (Basel). https://doi.org/10.3390/cancers14061379

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Hepatobiliary-Pancreatic Surgery, Osaka Metropolitan University Graduate School of Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka, 545-0051, Japan

    Hiroji Shinkawa, Shogo Tanaka, Shoji Kubo & Takeaki Ishizawa

  2. Department of Surgery, Hirakata Hospital, Kansai Medical University, Hirakata, Osaka, Japan

    Masaki Kaibori & Hisashi Kosaka

  3. Department of Medical Statistics, Osaka Metropolitan University Graduate School of Medicine, Osaka, Japan

    Daijiro Kabata

  4. Department of Surgery, Faculty of Medicine, Kindai University, Osakasayama, Osaka, Japan

    Takuya Nakai & Chihoko Nobori

  5. Second Department of Surgery, Wakayama Medical University, Wakayama, Japan

    Masaki Ueno & Shinya Hayami

  6. Department of Surgery, Nara Medical University, Kashihara, Nara, Japan

    Daisuke Hokuto & Satoshi Yasuda

  7. Division of Digestive Surgery, Department of Surgery, Kyoto Prefectural University of Medicine, Kyoto, Japan

    Hisashi Ikoma & Ryo Morimura

  8. Department of Surgery, Shiga University of Medical Science, Otsu, Shiga Prefecture, Japan

    Hiroya Iida & Haruki Mori

  9. Department of General and Gastroenterological Surgery, Osaka Medical and Pharmaceutical University, Takatsuki, Osaka, Japan

    Koji Komeda & Shuji Kagota

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  1. Hiroji Shinkawa
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  19. Takeaki Ishizawa
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Correspondence to Hiroji Shinkawa.

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Disclosures

Hiroji Shinkawa, Masaki Kaibori, Daijiro Kabata, Takuya Nakai, Masaki Ueno, Daisuke Hokuto, Hisashi Ikoma, Hiroya Iida, Koji Komeda, Shogo Tanaka, Hisashi Kosaka, Chihoko Nobori, Shinya Hayami, Satoshi Yasuda, Ryo Morimura, Haruki Mori, Shuji Kagota, Shoji Kubo, and Takeaki Ishizawa have no conflicts of interest or financial ties to disclose.

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464_2023_10591_MOESM1_ESM.tif

Supplementary material 1 (TIF 801 kb) Long-term survival outcomes after liver resection in patients of hepatocellular carcinoma with clinically significant portal hypertension in the entire cohort. (A) Recurrence-free survival rates

464_2023_10591_MOESM2_ESM.tif

Supplementary material 1 (TIF 796 kb) Long-term survival outcomes after liver resection in patients of hepatocellular carcinoma with clinically significant portal hypertension in the entire cohort. (B) Overall survival rates

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Shinkawa, H., Kaibori, M., Kabata, D. et al. Laparoscopic and open minor liver resection for hepatocellular carcinoma with clinically significant portal hypertension: a multicenter study using inverse probability weighting approach. Surg Endosc 38, 757–768 (2024). https://doi.org/10.1007/s00464-023-10591-z

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