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Hemorrhage control for laparoscopic hepatectomy: technical details and predictive factors for intraoperative blood loss

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Abstract

Background

Controlling bleeding during laparoscopic hepatectomy (LH) is technically demanding, but reportedly associated with less estimated blood loss (EBL) than open surgery. The present study aimed to describe and evaluate hemorrhage control techniques during LH and identify predictors of high intraoperative EBL.

Methods

The data of 438 consecutive patients undergoing LH between 1995 and 2012 were reviewed. Bleeding control was facilitated by the proper use of hemostatic devices and surgical maneuvers unique to LH and by preserving intra-abdominal pressure. EBL was evaluated among three groups of 146 patients in each group: 1995–2006 (group A), 2006–2009 (group B), and 2009–2012 (group C). We also sought factors that predicted EBL ≥800 mL.

Results

Mean EBL decreased overtime from groups A to C: group A, 378 ± 619 mL; group B, 293 ± 391 mL; groups C, 257 ± 366 mL; P = 0.127. Transfusion rate was 6.7 % in group A, 5.5 % in group B, and 4.8 % in group C (P = 0.743). Hypertension (odds ratio (OR) 2.82, 95 % confidence interval CI 1.37–5.78; P = 0.006), preoperative chemotherapy (OR 2.55, 95 % CI 1.26–5.31; P = 0.009), resection of posterosuperior segments (OR 3.73, 95 % CI 1.33–12.17; P = 0.012), and major hepatectomy (OR 4.21, 95 % CI 1.64–13.02; P < 0.001) independently predicted high EBL.

Conclusions

Improvements in bleeding control techniques over time have reduced EBL during LH. The use of these techniques and an understanding of the predictive factors for high EBL will help surgeons improve outcomes after LH.

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Abbreviations

LH:

Laparoscopic hepatectomy

OH:

Open hepatectomy

SD:

Standard deviation

EBL:

Estimated blood loss

References

  1. Vibert E, Perniceni T, Levard H, Denet C, Shahri NK, Gayet B (2006) Laparoscopic liver resection. Br J Surg 93:67–72

    Article  CAS  PubMed  Google Scholar 

  2. Otsuka Y, Tsuchiya M, Maeda T, Katagiri T, Isii J, Tamura A, Yamazaki K, Kubota Y, Suzuki T, Kagami S, Kaneko H (2009) Laparoscopic hepatectomy for liver tumors: proposals for standardization. J Hepatobiliary Pancreat Surg 16:720–725

    Article  PubMed  Google Scholar 

  3. Nitta H, Sasaki A, Fujita T, Itabashi H, Hoshikawa K, Takahara T, Takahashi M, Nishizuka S, Wakabayashi G (2010) Laparoscopy-assisted major liver resections employing a hanging technique: the original procedure. Ann Surg 251:450–453

    Article  PubMed  Google Scholar 

  4. Nguyen KT, Marsh JW, Tsung A, Steel JJ, Gamblin TC, Geller DA (2011) Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg 146:348–356

    Article  PubMed  Google Scholar 

  5. Cannon RM, Brock GN, Marvin MR, Buell JF (2011) Laparoscopic liver resection: an examination of our first 300 patients. J Am Coll Surg 213:501–507

    Article  PubMed  Google Scholar 

  6. Hwang DW, Han HS, Yoon YS, Cho JY, Kwon Y, Kim JH, Park JS, Yoon DS, Choi IS, Ahn KS, Kim YH, Kang KJ, Roh YH, Chu CW, Kim HC, Kang CM, Choi GH, Choi JS, Kim KS, Lee WJ, Yun SS, Kim HJ, Min SK, Lee HK, Song IS, Chun KS, Cho EH, Han SS, Park SJ (2013) Laparoscopic major liver resection in Korea: a multicenter study. J Hepatobiliary Pancreat Sci 20:125–130

    Article  PubMed  Google Scholar 

  7. Nguyen KT, Gamblin TC, Geller DA (2009) World review of laparoscopic liver resection-2,804 patients. Ann Surg 250:831–841

    Article  PubMed  Google Scholar 

  8. Croome KP, Yamashita MH (2010) Laparoscopic vs open hepatic resection for benign and malignant tumors: an updated meta-analysis. Arch Surg 145:1109–1118

    Article  PubMed  Google Scholar 

  9. Eiriksson K, Fors D, Rubertsson S, Arvidsson D (2011) High intra-abdominal pressure during experimental laparoscopic liver resection reduces bleeding but increases the risk of gas embolism. Br J Surg 98:845–852

    Article  CAS  PubMed  Google Scholar 

  10. Soubrane O, Schwarz L, Cauchy F, Perotto LO, Brustia R, Bernard D, Scatton O (2015) A conceptual technique for laparoscopic right hepatectomy based on facts and oncologic principles: the caudal approach. Ann Surg 261(6):1226–1231

    Article  PubMed  Google Scholar 

  11. 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 C-G, 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 J-N, 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. Ann Surg 250:825–830

    Article  PubMed  Google Scholar 

  12. Tranchart H, O’Rourke N, Van Dam R, Gaillard M, Lainas P, Sugioka A, Wakabayashi G, Dagher I (2015) Bleeding control during laparoscopic liver resection: a review of literature. J Hepatobiliary Pancreat Sci 22:371–378

    Article  PubMed  Google Scholar 

  13. Gayet B, Cavaliere D, Vibert E, Perniceni T, Levard H, Denet C, Christidis C, Blain A, Mal F (2007) Totally laparoscopic right hepatectomy. Am J Surg 194:685–689

    Article  PubMed  Google Scholar 

  14. Gumbs AA, Gayet B (2013) Adopting Gayet’s techniques of totally laparoscopic liver surgery in the United States. Liver Cancer 2:5–15

    Article  PubMed  PubMed Central  Google Scholar 

  15. Pringle JHV (1908) Notes on the arrest of hepatic hemorrhage due to trauma. Ann Surg 48:541–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ishizawa T, Zuker NB, Conrad C, Lei HJ, Ciacio O, Kokudo N, Gayet B (2013) Using a ‘no drain’ policy in 342 laparoscopic hepatectomies: which factors predict failure. HPB (Oxford) 16(5):494–499

    Article  Google Scholar 

  17. Strasberg SM, Phillips C (2013) Use and dissemination of the brisbane 2000 nomenclature of liver anatomy and resections. Ann Surg 257:377–382

    Article  PubMed  Google Scholar 

  18. Couinaud C (1999) Liver anatomy: portal (and suprahepatic) or biliary segmentation. Dig Surg 16(6):459-467

    Article  CAS  PubMed  Google Scholar 

  19. Juza RM, Pauli EM (2014) Clinical and surgical anatomy of the liver: a review for clinicians. Clin Anat 27:764–769

    Article  PubMed  Google Scholar 

  20. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  21. Aickin M, Gensler H (1996) Adjusting for multiple testing when reporting research results: the Bonferroni vs Holm methods. Am J Public Health 86:726–728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Imamura H, Seyama Y, Kokudo N, Maema A, Sugawara Y, Sano K, Takayama T, Makuuchi M (2003) One thousand fifty-six hepatectomies without mortality in 8 years. Arch Surg 138:1198–206; discussion 206

  23. Nanashima A, Abo T, Hamasaki K, Wakata K, Kunizaki M, Tou K, Takeshita H, Hidaka S, Sawai T, Tsuchiya T, Nagayasu T (2013) Predictors of intraoperative blood loss in patients undergoing hepatectomy. Surg Today 43:485–493

    Article  PubMed  Google Scholar 

  24. Hanazaki K, Matsushita A, Nakagawa K, Misawa R, Amano J (2005) Risk factors of long-term survival and recurrence after curative resection of hepatocellular carcinoma. Hepatogastroenterology 52:552–557

    PubMed  Google Scholar 

  25. Katz SC, Shia J, Liau KH, Gonen M, Ruo L, Jarnagin WR, Fong Y, D’Angelica MI, Blumgart LH, Dematteo RP (2009) Operative blood loss independently predicts recurrence and survival after resection of hepatocellular carcinoma. Ann Surg 249:617–623

    Article  PubMed  Google Scholar 

  26. Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transpl 48:452–458

    Article  CAS  Google Scholar 

  27. Topal B, Fieuws S, Aerts R, Vandeweyer H, Penninckx F (2008) Laparoscopic versus open liver resection of hepatic neoplasms: comparative analysis of short-term results. Surg Endosc 22:2208–2213

    Article  CAS  PubMed  Google Scholar 

  28. 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 

  29. Bryant R, Laurent A, Tayar C, Cherqui D (2009) Laparoscopic liver resection-understanding its role in current practice: the Henri Mondor Hospital experience. Ann Surg 250:103–111

    Article  PubMed  Google Scholar 

  30. 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 

  31. Buell JF, Thomas MT, Rudich S, Marvin M, Nagubandi R, Ravindra KV, Brock G, McMasters KM (2008) Experience with more than 500 minimally invasive hepatic procedures. Ann Surg 248:475–486

    PubMed  Google Scholar 

  32. Koffron AJ, Auffenberg G, Kung R, Abecassis M (2007) Evaluation of 300 minimally invasive liver resections at a single institution: less is more. Ann Surg 246:385–92; discussion 92-4

  33. Aloia T, Sebagh M, Plasse M, Karam V, Levi F, Giacchetti S, Azoulay D, Bismuth H, Castaing D, Adam R (2006) Liver histology and surgical outcomes after preoperative chemotherapy with fluorouracil plus oxaliplatin in colorectal cancer liver metastases. J Clin Oncol 24:4983–4990

    Article  CAS  PubMed  Google Scholar 

  34. Bilchik AJ, Poston G, Curley SA, Strasberg S, Saltz L, Adam R, Nordlinger B, Rougier P, Rosen LS (2005) Neoadjuvant chemotherapy for metastatic colon cancer: a cautionary note. J Clin Oncol 23:9073–9078

    Article  CAS  PubMed  Google Scholar 

  35. Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, Asbun H, O’Rourke N, Tanabe M, Koffron AJ, Tsung A, Soubrane O, Machado MA, Gayet B, Troisi RI, Pessaux P, Van Dam RM, Scatton O, Abu Hilal M, Belli G, Kwon CH, Edwin B, Choi GH, Aldrighetti LA, Cai X, Cleary S, Chen KH, Schon MR, Sugioka A, Tang CN, Herman P, Pekolj J, Chen XP, Dagher I, Jarnagin W, Yamamoto M, Strong R, Jagannath P, Lo CM, Clavien PA, Kokudo N, Barkun J, Strasberg SM (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261:619–629

    PubMed  Google Scholar 

  36. Abu Hilal M, Underwood T, Taylor MG, Hamdan K, Elberm H, Pearce NW (2010) Bleeding and hemostasis in laparoscopic liver surgery. Surg Endosc 24:572–577

    Article  PubMed  Google Scholar 

  37. Storz P, Buess GF, Kunert W, Kirschniak A (2012) 3D HD versus 2D HD: surgical task efficiency in standardised phantom tasks. Surg Endosc 26:1454–1460

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank Dr. Nobutaka Tanaka, Dr. Yukihiro Nomura, and Dr. Motoki Nagai at Asahi General Hospital for helping with acquisition of data and providing useful insights.

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Correspondence to Yoshikuni Kawaguchi or Brice Gayet.

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Disclosures

Yoshikuni Kawaguchi, Takeo Nomi, David Fuks, Frederic Mal, Norihiro Kokudo, and Brice Gayet have no conflict of interest or financial ties to disclose.

Electronic supplementary material

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Supplementary video 1

Inflow occlusion technique (Pringle maneuver). A tape is placed around the hepatoduodenal ligament, along which a tube is introduced to allow occlusion of hepatic inflow. Parenchymal transection close to the surface does not cause bleeding without applying the Pringle maneuver as in this case. The tube is repositioned when it interferes with the transection. The inflow occlusion technique is performed to address persistent bleeding deep within the liver, after which parenchymal transection is subsequently performed using standard techniques on the cut surface. (MPG 61220 kb)

Supplementary video 2

Removal of bipolar forceps while continuing to apply current. Bipolar forceps are used for bleeding control. The postcoagulation tissue is removed with the tips as the forceps are withdrawn, causing re-bleeding at the same point on removal. To avoid re-bleeding under these circumstances, bipolar forceps should be removed from the point of bleeding with the current still applied. (MPG 37272 kb)

Supplementary video 3

Replacement of bipolar forceps. Bipolar forceps are replaced with a clean set to prevent inefficient coagulation and adherence to the liver parenchyma due to excessive burnt tissue on the tips after coagulation. (MPG 17586 kb)

Supplementary video 4

Preservation of intra-abdominal pressure. Bleeding is first controlled by compression with forceps. Subsequently, a suction catheter is used cautiously so as not to decrease the intra-abdominal pressure while accommodating bipolar coagulation. (MPG 16208 kb)

Supplementary video 5

Bipolar coagulation with simultaneous compression of the liver parenchyma. During bleeding control using bipolar coagulation, the liver parenchyma is compressed by a suction catheter to reduce hepatic venous pressure with interest and optimize contact between the device tips and the bleeding point. (MPG 9108 kb)

Supplementary video 6

Bipolar coagulation and placement of fibrillar oxidized cellulose. Whenever bleeding persists after an attempt at bleeding control with bipolar coagulation, a small amount of fibrillar oxidized cellulose is placed on the point of subsequent oozing, providing short-term local compression. (MPG 22612 kb)

Supplementary video 7

Bleeding of peripheral portal pedicle. Massive bleeding is encountered from the stump of a peripheral portal pedicle during transection of the liver. Such massive bleeding can be controlled by a combination of the techniques previously described, including compression of the liver parenchyma by forceps and preservation of the intra-abdominal pressure. (MPG 36558 kb)

Supplementary video 8

Bleeding directly from the hepatic vein: instantaneous (single shot) bipolar coagulation. Bleeding from small holes on the hepatic vein is controlled using instantaneous (single shot) coagulation with bipolar forceps. (MPG 13522 kb)

Supplementary video 9

Introduction of a gauze through a hand-assisted system at the beginning of the procedure. A gauze is introduced through a hand-assisted system before parenchymal transection if there is judged to be a high risk of massive bleeding. The gauze is placed on the bleeding point using the surgeon’s hand when bleeding control is difficult. The point of bleeding was controlled 5 minutes after manual compression with the gauze. Subsequent transection was performed with the gauze still on the cut surface to suppress oozing. (MPG 55348 kb)

Supplementary video 10

Conversion to an open approach. During extended left lateral sectionectomy including segment 4a, bleeding is encountered when parenchymal transection is performed on the liver surface, where risk of bleeding is generally considered to be lower than that deep within the liver. Bleeding control has been attempted laparoscopically, but conversion to an open approach is needed due to persistent bleeding from the parenchyma close to the surface. (MPG 43238 kb)

Supplementary video 11

Bleeding control using a monopolar electrode with saline irrigation. Bleeding from the hepatic vein and the cut surface of the liver is controlled using a monopolar electrode with saline irrigation. This device delivers less intense coagulation to the cut surface while avoiding carbonization of the tissue. (MPG 23088 kb)

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Kawaguchi, Y., Nomi, T., Fuks, D. et al. Hemorrhage control for laparoscopic hepatectomy: technical details and predictive factors for intraoperative blood loss. Surg Endosc 30, 2543–2551 (2016). https://doi.org/10.1007/s00464-015-4520-3

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  • DOI: https://doi.org/10.1007/s00464-015-4520-3

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