Abstract
Background
Hepatic pedicle clamping is often used during liver resection. While its use reduces blood loss and transfusion requirements, the long-term effect on survival and recurrence has been debated. This study evaluates the effect of hepatic pedicle clamping [i.e., Pringle maneuver (PM)] on survival and recurrence following hepatic resection for colorectal liver metastasis (CRLM).
Methods
Patients who underwent R0 resection for CRLM from 1991 to 2004 were identified from a prospectively maintained database. Operative, perioperative, and clinicopathological variables were analyzed. The primary outcomes were disease-free survival (DFS) and liver recurrence (LR). Disease extent was categorized using a well-defined clinical risk score (CRS). Subgroup analysis was performed for patients given preoperative systemic chemotherapy and postoperative pump chemotherapy.
Results
This study included 928 consecutive patients with median follow-up of 8.9 years. PM was utilized in 874 (94 %) patients, with median time of 35 min (range 1–181 min). On univariate analysis, only resection type (p < 0.001) and tumor number (p = 0.002) were associated with use of PM. Younger age (p = 0.006), longer operative time (p < 0.001), and multiple tumors (p = 0.006) were associated with prolonged PM (>60 min). There was no association between DFS, overall survival (OS) or LR and Pringle time. Neither the CRS nor use of neoadjuvant therapy stratified disease-related outcome with respect to use of PM.
Conclusions
PM was used in most patients undergoing resection for CRLM and did not adversely influence intrahepatic recurrence, DFS, or OS.
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References
Tomlinson JS, Jarnagin WR, DeMatteo RP, et al. Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol. 2007;25(29):4575–80.
Abdalla EK, Vauthey JN, Ellis LM, et al. Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg. 2004;239(6):818–25; discussion 825–817.
Nordlinger B, Guiguet M, Vaillant JC, et al. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Association Francaise de Chirurgie. Cancer. 1996;77(7):1254–62.
Zakaria S, Donohue JH, Que FG, et al. Hepatic resection for colorectal metastases: value for risk scoring systems? Ann Surg. 2007;246(2):183–91.
Farid SG, Aldouri A, Morris-Stiff G, et al. Correlation between postoperative infective complications and long-term outcomes after hepatic resection for colorectal liver metastasis. Ann Surg. 2010;251(1):91–100.
Are C, Gonen M, Zazzali K, et al. The impact of margins on outcome after hepatic resection for colorectal metastasis. Ann Surg. 2007;246(2):295–300.
Shirabe K, Takenaka K, Gion T, et al. Analysis of prognostic risk factors in hepatic resection for metastatic colorectal carcinoma with special reference to the surgical margin. Br J Surg. 1997;84(8):1077–80.
Ito H, Are C, Gonen M, et al. Effect of postoperative morbidity on long-term survival after hepatic resection for metastatic colorectal cancer. Ann Surg. 2008;247(6):994–1002.
Pringle JH. V. Notes on the Arrest of Hepatic Hemorrhage Due to Trauma. Ann Surg. 1908;48(4):541–9.
Lesurtel M, Selzner M, Petrowsky H, McCormack L, Clavien PA. How should transection of the liver be performed?: a prospective randomized study in 100 consecutive patients: comparing four different transection strategies. Ann Surg. 2005;242(6):814–22, discussion 822–813.
Man K, Fan ST, Ng IO, Lo CM, Liu CL, Wong J. Prospective evaluation of Pringle maneuver in hepatectomy for liver tumors by a randomized study. Ann Surg. 1997;226(6):704–11; discussion 711–703.
Ezaki T, Seo Y, Tomoda H, Furusawa M, Kanematsu T, Sugimachi K. Partial hepatic resection under intermittent hepatic inflow occlusion in patients with chronic liver disease. Br J Surg. 1992;79(3):224–6.
Huguet C, Gavelli A, Bona S. Hepatic resection with ischemia of the liver exceeding one hour. J Am Coll Surg. 1994;178(5):454–8.
Makuuchi M, Mori T, Gunven P, Yamazaki S, Hasegawa H. Safety of hemihepatic vascular occlusion during resection of the liver. Surg Gynecol Obstet. 1987;164(2):155–8.
van der Bilt JD, Kranenburg O, Nijkamp MW, et al. Ischemia/reperfusion accelerates the outgrowth of hepatic micrometastases in a highly standardized murine model. Hepatology. 2005;42(1):165–75.
Doi K, Horiuchi T, Uchinami M, et al. Hepatic ischemia-reperfusion promotes liver metastasis of colon cancer. J Surg Res. 2002;105(2):243–7.
Nicoud IB, Jones CM, Pierce JM, et al. Warm hepatic ischemia-reperfusion promotes growth of colorectal carcinoma micrometastases in mouse liver via matrix metalloproteinase-9 induction. Cancer Res. 2007;67(6):2720–8.
Ishizuka M, Kubota K, Kita J, Shimoda M, Kato M, Sawada T. Duration of hepatic vascular inflow clamping and survival after liver resection for hepatocellular carcinoma. Br J Surg. 2011;98(9):1284–90.
Giuliante F, Ardito F, Pulitano C, et al. Does hepatic pedicle clamping affect disease-free survival following liver resection for colorectal metastases? Ann Surg. 2010;252(6):1020–6.
Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg. 1999;230(3):309–18; discussion 318–321.
Jarnagin WR, Gonen M, Fong Y, et al. Improvement in perioperative outcome after hepatic resection: analysis of 1,803 consecutive cases over the past decade. Ann Surg. 2002;236(4):397–406; discussion 406–397.
Kemeny N, Huang Y, Cohen AM, et al. Hepatic arterial infusion of chemotherapy after resection of hepatic metastases from colorectal cancer. N Engl J Med. 1999;341(27):2039–48.
Jarnagin WR, Conlon K, Bodniewicz J, et al. A clinical scoring system predicts the yield of diagnostic laparoscopy in patients with potentially resectable hepatic colorectal metastases. Cancer. 2001;91(6):1121–8.
Melendez JA, Arslan V, Fischer ME, et al. Perioperative outcomes of major hepatic resections under low central venous pressure anesthesia: blood loss, blood transfusion, and the risk of postoperative renal dysfunction. J Am Coll Surg. 1998;187(6):620–5.
Paugam-Burtz C, Janny S, Delefosse D, et al. Prospective validation of the “fifty–fifty” criteria as an early and accurate predictor of death after liver resection in intensive care unit patients. Ann Surg. 2009;249(1):124–8.
House MG, Ito H, Gonen M, et al. Survival after hepatic resection for metastatic colorectal cancer: trends in outcomes for 1,600 patients during two decades at a single institution. J Am Coll Surg. 2010;210(5):744–52, 752–745.
Ishizaki Y, Yoshimoto J, Miwa K, Sugo H, Kawasaki S. Safety of prolonged intermittent Pringle maneuver during hepatic resection. Arch Surg. 2006;141(7):649–53; discussion 654.
Hannoun L, Borie D, Delva E, et al. Liver resection with normothermic ischaemia exceeding 1 h. Br J Surg. 1993;80(9):1161–5.
Elias D, Desruennes E, Lasser P. Prolonged intermittent clamping of the portal triad during hepatectomy. Br J Surg. 1991;78(1):42–4.
Kim YI, Nakashima K, Tada I, Kawano K, Kobayashi M. Prolonged normothermic ischaemia of human cirrhotic liver during hepatectomy: a preliminary report. Br J Surg. 1993;80(12):1566–70.
Torzilli G, Procopio F, Donadon M, Del Fabbro D, Cimino M, Montorsi M. Safety of intermittent Pringle maneuver cumulative time exceeding 120 minutes in liver resection: a further step in favor of the “radical but conservative” policy. Ann Surg. 2012;55(2):270–80. doi:10.1097/SLA.1090b1013e318232b318375.
Narita M, Oussoultzoglou E, Fuchshuber P, et al. Prolonged portal triad clamping increases postoperative sepsis after major hepatectomy in patients with sinusoidal obstruction syndrome and/or steatohepatitis. World J Surg. 2012;36(8):1848–57.
Clavien PA, Yadav S, Sindram D, Bentley RC. Protective effects of ischemic preconditioning for liver resection performed under inflow occlusion in humans. Ann Surg. 2000;232(2):155–62.
Clavien PA, Selzner M, Rudiger HA, et al. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg. 2003;238(6):843–50; discussion 851–842.
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Weiss, M.J., Ito, H., Araujo, R.L.C. et al. Hepatic Pedicle Clamping During Hepatic Resection for Colorectal Liver Metastases: No Impact on Survival or Hepatic Recurrence. Ann Surg Oncol 20, 285–294 (2013). https://doi.org/10.1245/s10434-012-2583-0
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DOI: https://doi.org/10.1245/s10434-012-2583-0