Skip to main content
Top
Published in: Updates in Surgery 4/2014

01-12-2014 | Review Article

Lymphatic drainage of the liver and its implications in the management of colorectal cancer liver metastases

Authors: Renato Micelli Lupinacci, François Paye, Fabricio Ferreira Coelho, Jaime Arthur Pirolla Kruger, Paulo Herman

Published in: Updates in Surgery | Issue 4/2014

Login to get access

Abstract

The liver is the most common site of distant metastases in patients with colorectal cancer. Surgery represents the mainstream for curative treatment of colorectal cancer liver metastases (CRCLM) with long-term survival up to 58 and 36 % at 5 and 10 years, respectively. Despite advances on diagnosis, staging and surgical strategies, 60–70 % of patients will develop recurrence of the disease even after R0 resection of CRCLM. Tumor staging, prognosis, and therapeutic approaches for cancer are most often based on the extent of involvement of regional lymph nodes (LNs) and, to a lesser extent, on the invasion of regional lymphatic vessels draining the primary tumor. For CRCLM, the presence of intra hepatic lymphatic and blood vascular dissemination has been associated with an increased risk of intra hepatic recurrence, poorer disease-free and overall survival after liver resection. Also, several studies have reviewed the role of surgery in the patient with concomitant CRCLM and liver pedicle LN metastasis. Although pedicle LN involvement is related to worst survival rates, it does not differentiate patients that will relapse from those that will not. This review aims to briefly describe the anatomy of the liver’s lymphatic drainage, the incidence of intrahepatic lymphatic invasion and hilar lymph node involvement, as well as their clinical impact in CRCLM. A better understanding of the role of liver lymphatic metastasis might, in the near future, impact the strategy of systemic therapies after liver resection as for primary colorectal tumors.
Literature
1.
go back to reference Cummings LC, Payes JD, Cooper GS (2007) Survival after hepatic resection in metastatic colorectal cancer: a population-based study. Cancer 109(4):718–726PubMedCrossRef Cummings LC, Payes JD, Cooper GS (2007) Survival after hepatic resection in metastatic colorectal cancer: a population-based study. Cancer 109(4):718–726PubMedCrossRef
2.
go back to reference Rees M, Tekkis PP, Welsh FK, O’Rourke T, John TG (2008) Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg 247(1):125–135PubMedCrossRef Rees M, Tekkis PP, Welsh FK, O’Rourke T, John TG (2008) Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg 247(1):125–135PubMedCrossRef
3.
go back to reference Abdalla EK, Vauthey JN, Ellis LM, Ellis V, Pollock R, Broglio KR, Hess K, Curley SA (2004) Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 239(6):818–825PubMedCentralPubMedCrossRef Abdalla EK, Vauthey JN, Ellis LM, Ellis V, Pollock R, Broglio KR, Hess K, Curley SA (2004) Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 239(6):818–825PubMedCentralPubMedCrossRef
4.
go back to reference Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, Lillemoe KD, Yeo CJ, Cameron JL (2002) Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg 235(6):759–766PubMedCentralPubMedCrossRef Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, Lillemoe KD, Yeo CJ, Cameron JL (2002) Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg 235(6):759–766PubMedCentralPubMedCrossRef
5.
go back to reference Fernandez FG, Drebin JA, Linehan DC, Dehdashti F, Siegel BA, Strasberg SM (2004) Five-year survival after resection of hepatic metastases from colorectal cancer in patients screened by positron emission tomography with F-18 fluorodeoxyglucose (FDG-PET). Ann Surg 240(3):438–447PubMedCentralPubMedCrossRef Fernandez FG, Drebin JA, Linehan DC, Dehdashti F, Siegel BA, Strasberg SM (2004) Five-year survival after resection of hepatic metastases from colorectal cancer in patients screened by positron emission tomography with F-18 fluorodeoxyglucose (FDG-PET). Ann Surg 240(3):438–447PubMedCentralPubMedCrossRef
6.
go back to reference Pawlik TM, Scoggins CR, Zorzi D, Abdalla EK, Andres A, Eng C, Curley SA, Loyer EM, Muratore A, Mentha G, Capussotti L, Vauthey JN (2005) Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 241(5):715–722PubMedCentralPubMedCrossRef Pawlik TM, Scoggins CR, Zorzi D, Abdalla EK, Andres A, Eng C, Curley SA, Loyer EM, Muratore A, Mentha G, Capussotti L, Vauthey JN (2005) Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 241(5):715–722PubMedCentralPubMedCrossRef
7.
go back to reference Figueras J, Torras J, Valls C, Llado L, Ramos E, Marti-Ragué J, Serrano T, Fabregat J (2007) Surgical resection of colorectal liver metastases in patients with expanded indications: a single-center experience with 501 patients. Dis Colon Rectum 50(4):478–488PubMedCrossRef Figueras J, Torras J, Valls C, Llado L, Ramos E, Marti-Ragué J, Serrano T, Fabregat J (2007) Surgical resection of colorectal liver metastases in patients with expanded indications: a single-center experience with 501 patients. Dis Colon Rectum 50(4):478–488PubMedCrossRef
8.
go back to reference Hemming AW, Reed AI, Langham MR Jr, Fujita S, Howard RJ (2004) Combined resection of the liver and inferior vena cava for hepatic malignancy. Ann Surg 239:712–719PubMedCentralPubMedCrossRef Hemming AW, Reed AI, Langham MR Jr, Fujita S, Howard RJ (2004) Combined resection of the liver and inferior vena cava for hepatic malignancy. Ann Surg 239:712–719PubMedCentralPubMedCrossRef
9.
go back to reference Ferrero A, Polastri R, Muratore A, Zorzi D, Capussotti L (2004) Extensive resections for colorectal liver metastases. J Hepatobiliary Pancreat Surg 11:92–96PubMedCrossRef Ferrero A, Polastri R, Muratore A, Zorzi D, Capussotti L (2004) Extensive resections for colorectal liver metastases. J Hepatobiliary Pancreat Surg 11:92–96PubMedCrossRef
10.
go back to reference Elias D, Sideris L, Pocard M, Ouellet JF, Boige V, Lasser P, Pignon JP, Ducreux M (2004) Results of R0 resection for colorectal liver metastases associated with extra-hepatic disease. Ann Surg Oncol 11:274–280PubMedCrossRef Elias D, Sideris L, Pocard M, Ouellet JF, Boige V, Lasser P, Pignon JP, Ducreux M (2004) Results of R0 resection for colorectal liver metastases associated with extra-hepatic disease. Ann Surg Oncol 11:274–280PubMedCrossRef
11.
go back to reference Adam R, Delvart V, Pascal G, Valeanu A, Castaing D, Azoulay D, Giacchetti S, Paule B, Kunstlinger F, Ghémard O, Levi F, Bismuth H (2004) Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann Surg 240:644–657PubMedCentralPubMedCrossRef Adam R, Delvart V, Pascal G, Valeanu A, Castaing D, Azoulay D, Giacchetti S, Paule B, Kunstlinger F, Ghémard O, Levi F, Bismuth H (2004) Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann Surg 240:644–657PubMedCentralPubMedCrossRef
12.
go back to reference Tanaka K, Nojiri K, Kumamoto T, Takeda K, Endo I (2011) R1 resection for aggressive or advanced colorectal liver metastases is justified in combination with effective prehepatectomy chemotherapy. Eur J Surg Oncol 37:336–343PubMedCrossRef Tanaka K, Nojiri K, Kumamoto T, Takeda K, Endo I (2011) R1 resection for aggressive or advanced colorectal liver metastases is justified in combination with effective prehepatectomy chemotherapy. Eur J Surg Oncol 37:336–343PubMedCrossRef
13.
go back to reference Adam R, Bismuth H, Castaing D, Waechter F, Navarro F, Abascal A, Majno P, Engerran L (1997) Repeat hepatectomy for colorectal liver metastases. Ann Surg 225:51–62PubMedCentralPubMedCrossRef Adam R, Bismuth H, Castaing D, Waechter F, Navarro F, Abascal A, Majno P, Engerran L (1997) Repeat hepatectomy for colorectal liver metastases. Ann Surg 225:51–62PubMedCentralPubMedCrossRef
14.
go back to reference Homayounfar K, Bleckmann A, Conradi LC, Sprenger T, Beissbarth T, Lorf T, Niessner M, Sahlmann CO, Meller J, Becker H, Liersch T, Ghadimi BM (2012) Bilobar spreading of colorectal liver metastases does not significantly affect survival after R0 resection in the era of interdisciplinary multimodal treatment. Int J Colorectal Dis 27(10):1359–1367PubMedCentralPubMedCrossRef Homayounfar K, Bleckmann A, Conradi LC, Sprenger T, Beissbarth T, Lorf T, Niessner M, Sahlmann CO, Meller J, Becker H, Liersch T, Ghadimi BM (2012) Bilobar spreading of colorectal liver metastases does not significantly affect survival after R0 resection in the era of interdisciplinary multimodal treatment. Int J Colorectal Dis 27(10):1359–1367PubMedCentralPubMedCrossRef
15.
go back to reference Sasaki A, Iwashita Y, Shibata K, Matsumoto T, Ohta M, Kitano S (2005) Analysis of preoperative prognostic factors for long-term survival after hepatic resection of liver metastasis of colorectal carcinoma. J Gastrointest Surg 9:374–380PubMedCrossRef Sasaki A, Iwashita Y, Shibata K, Matsumoto T, Ohta M, Kitano S (2005) Analysis of preoperative prognostic factors for long-term survival after hepatic resection of liver metastasis of colorectal carcinoma. J Gastrointest Surg 9:374–380PubMedCrossRef
16.
go back to reference Scheele J, Stangl R, Altendorf-Hofmann A, Gall FP (1991) Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery 110:13–29PubMed Scheele J, Stangl R, Altendorf-Hofmann A, Gall FP (1991) Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery 110:13–29PubMed
17.
go back to reference Homayounfar K, Bleckmann A, Conradi LC, Sprenger T, Lorf T, Niessner M, Sahlmann CO, Meller J, Liersch T, Ghadimi BM (2013) Metastatic recurrence after complete resection of colorectal liver metastases: impact of surgery and chemotherapy on survival. Int J Colorectal Dis 28(7):1009–1017PubMedCentralPubMedCrossRef Homayounfar K, Bleckmann A, Conradi LC, Sprenger T, Lorf T, Niessner M, Sahlmann CO, Meller J, Liersch T, Ghadimi BM (2013) Metastatic recurrence after complete resection of colorectal liver metastases: impact of surgery and chemotherapy on survival. Int J Colorectal Dis 28(7):1009–1017PubMedCentralPubMedCrossRef
18.
go back to reference Butte JM, Gonen M, Ding P, Goodman KA, Allen PJ, Nash GM, Guillem J, Paty PB, Saltz LB, Kemeny NE, Dematteo RP, Fong Y, Jarnagin WR, Weiser MR, D’Angelica MI (2012) Patterns of failure in patients with early onset (synchronous) resectable liver metastases from rectal cancer. Cancer 118(21):5414–5423PubMedCrossRef Butte JM, Gonen M, Ding P, Goodman KA, Allen PJ, Nash GM, Guillem J, Paty PB, Saltz LB, Kemeny NE, Dematteo RP, Fong Y, Jarnagin WR, Weiser MR, D’Angelica MI (2012) Patterns of failure in patients with early onset (synchronous) resectable liver metastases from rectal cancer. Cancer 118(21):5414–5423PubMedCrossRef
19.
go back to reference Witte MH, Dellinger MT, McDonald DM, Nathanson SD, Boccardo FM, Campisi CC, Sleeman JP, Gershenwald JE (2011) Lymphangiogenesis and hemangiogenesis: potential targets for therapy. J Surg Oncol 103(6):489–500PubMedCrossRef Witte MH, Dellinger MT, McDonald DM, Nathanson SD, Boccardo FM, Campisi CC, Sleeman JP, Gershenwald JE (2011) Lymphangiogenesis and hemangiogenesis: potential targets for therapy. J Surg Oncol 103(6):489–500PubMedCrossRef
20.
go back to reference Mohammed RA, Martin SG, Gill MS, Green AR, Paish EC, Ellis IO (2007) Improved methods of detection of lymphovascular invasion demonstrate that it is the predominant method of vascular invasion in breast cancer and has important clinical consequences. Am J Surg Pathol 31(12):1825–1833PubMedCrossRef Mohammed RA, Martin SG, Gill MS, Green AR, Paish EC, Ellis IO (2007) Improved methods of detection of lymphovascular invasion demonstrate that it is the predominant method of vascular invasion in breast cancer and has important clinical consequences. Am J Surg Pathol 31(12):1825–1833PubMedCrossRef
21.
go back to reference Nathanson SD, Kwon D, Kapke A, Alford SH, Chitale D (2009) The role of lymph node metastasis in the systemic dissemination of breast cancer. Ann Surg Oncol 16(12):3396–3405PubMedCrossRef Nathanson SD, Kwon D, Kapke A, Alford SH, Chitale D (2009) The role of lymph node metastasis in the systemic dissemination of breast cancer. Ann Surg Oncol 16(12):3396–3405PubMedCrossRef
22.
go back to reference Ercolani G, Grazi GL, Ravaioli M, Grigioni WF, Cescon M, Gardini A, Del Gaudio M, Cavallari A (2004) The role of lymphadenectomy for liver tumors: further considerations on the appropriateness of treatment strategy. Ann Surg 239:202–209PubMedCentralPubMedCrossRef Ercolani G, Grazi GL, Ravaioli M, Grigioni WF, Cescon M, Gardini A, Del Gaudio M, Cavallari A (2004) The role of lymphadenectomy for liver tumors: further considerations on the appropriateness of treatment strategy. Ann Surg 239:202–209PubMedCentralPubMedCrossRef
23.
go back to reference Moszkowicz D, Cauchy F, Dokmak S, Belghiti J (2012) Routine pedicular lymphadenectomy for colorectal liver metastases. J Am Coll Surg 214(6):e39–e45PubMedCrossRef Moszkowicz D, Cauchy F, Dokmak S, Belghiti J (2012) Routine pedicular lymphadenectomy for colorectal liver metastases. J Am Coll Surg 214(6):e39–e45PubMedCrossRef
24.
go back to reference Ohtani O, Ohtani Y (2008) Lymph circulation in the liver. Anat Rec 291:643–652CrossRef Ohtani O, Ohtani Y (2008) Lymph circulation in the liver. Anat Rec 291:643–652CrossRef
25.
go back to reference August DA, Sugarbaker PH, Schneider PD (1985) Lymphatic dissemination of hepatic metastases. Implications for the follow-up and treatment of patients with colorectal cancer. Cancer 55:1490–1494PubMedCrossRef August DA, Sugarbaker PH, Schneider PD (1985) Lymphatic dissemination of hepatic metastases. Implications for the follow-up and treatment of patients with colorectal cancer. Cancer 55:1490–1494PubMedCrossRef
26.
go back to reference Ito M, Mishima Y, Sato T (1991) An anatomical study of the lymphatic drainage of the gallbladder. Surg Radiol Anat 13(2):89–104PubMedCrossRef Ito M, Mishima Y, Sato T (1991) An anatomical study of the lymphatic drainage of the gallbladder. Surg Radiol Anat 13(2):89–104PubMedCrossRef
27.
go back to reference Santos C, López-Doriga A, Navarro M, Mateo J, Biondo S, Martínez Villacampa M, Soler G, Sanjuan X, Paules MJ, Laquente B, Guinó E, Kreisler E, Frago R, Germà JR, Moreno V, Salazar R (2013) Clinicopathological risk factors of stage II colon cancer: results of a prospective study. Colorectal Dis 15(4):414–422PubMedCrossRef Santos C, López-Doriga A, Navarro M, Mateo J, Biondo S, Martínez Villacampa M, Soler G, Sanjuan X, Paules MJ, Laquente B, Guinó E, Kreisler E, Frago R, Germà JR, Moreno V, Salazar R (2013) Clinicopathological risk factors of stage II colon cancer: results of a prospective study. Colorectal Dis 15(4):414–422PubMedCrossRef
28.
go back to reference Lee JH, Jang HS, Kim JG, Cho HM, Shim BY, Oh ST, Yoon SC, Kim YS, Choi BO, Kim SH (2012) Lymphovascular invasion is a significant prognosticator in rectal cancer patients who receive preoperative chemoradiotherapy followed by total mesorectal excision. Ann Surg Oncol 19(4):1213–1221PubMedCrossRef Lee JH, Jang HS, Kim JG, Cho HM, Shim BY, Oh ST, Yoon SC, Kim YS, Choi BO, Kim SH (2012) Lymphovascular invasion is a significant prognosticator in rectal cancer patients who receive preoperative chemoradiotherapy followed by total mesorectal excision. Ann Surg Oncol 19(4):1213–1221PubMedCrossRef
30.
go back to reference Sasaki A, Aramaki M, Kawano K, Yasuda K, Inomata M, Kitano S (2002) Prognostic significance of intrahepatic lymphatic invasion in patients with hepatic resection due to metastases from colorectal carcinoma. Cancer 95(1):105–111PubMedCrossRef Sasaki A, Aramaki M, Kawano K, Yasuda K, Inomata M, Kitano S (2002) Prognostic significance of intrahepatic lymphatic invasion in patients with hepatic resection due to metastases from colorectal carcinoma. Cancer 95(1):105–111PubMedCrossRef
31.
go back to reference Bockhorn M, Sotiropoulos G, Neuhaus J, Sgourakis G, Sheu SY, Molmenti E, Fingas C, Trarbach T, Frilling A, Broelsch CE (2009) Prognostic impact of intrahepatic lymphatic and microvascular involvement in cases of colorectal liver metastases. Int J Colorectal Dis 24(7):845–850PubMedCrossRef Bockhorn M, Sotiropoulos G, Neuhaus J, Sgourakis G, Sheu SY, Molmenti E, Fingas C, Trarbach T, Frilling A, Broelsch CE (2009) Prognostic impact of intrahepatic lymphatic and microvascular involvement in cases of colorectal liver metastases. Int J Colorectal Dis 24(7):845–850PubMedCrossRef
32.
go back to reference Korita PV, Wakai T, Shirai Y, Sakata J, Takizawa K, Cruz PV, Ajioka Y, Hatakeyama K (2007) Intrahepatic lymphatic invasion independently predicts poor survival and recurrences after hepatectomy in patients with colorectal carcinoma liver metastases. Ann Surg Oncol 14(12):3472–3480PubMedCrossRef Korita PV, Wakai T, Shirai Y, Sakata J, Takizawa K, Cruz PV, Ajioka Y, Hatakeyama K (2007) Intrahepatic lymphatic invasion independently predicts poor survival and recurrences after hepatectomy in patients with colorectal carcinoma liver metastases. Ann Surg Oncol 14(12):3472–3480PubMedCrossRef
33.
go back to reference Yokoyama N, Shirai Y, Ajioka Y, Nagakura S, Suda T, Hatakeyama K (2002) Immunohistochemically detected hepatic micrometastases predict a high risk of intrahepatic recurrence after resection of colorectal carcinoma liver metastases. Cancer 94(6):1642–1647PubMedCrossRef Yokoyama N, Shirai Y, Ajioka Y, Nagakura S, Suda T, Hatakeyama K (2002) Immunohistochemically detected hepatic micrometastases predict a high risk of intrahepatic recurrence after resection of colorectal carcinoma liver metastases. Cancer 94(6):1642–1647PubMedCrossRef
34.
go back to reference Wakai T, Shirai Y, Sakata J, Kameyama H, Nogami H, Iiai T, Ajioka Y, Hatakeyama K (2012) Histologic evaluation of intrahepatic micrometastases in patients treated with or without neoadjuvant chemotherapy for colorectal carcinoma liver metastasis. Int J Clin Exp Pathol 5(4):308–314PubMedCentralPubMed Wakai T, Shirai Y, Sakata J, Kameyama H, Nogami H, Iiai T, Ajioka Y, Hatakeyama K (2012) Histologic evaluation of intrahepatic micrometastases in patients treated with or without neoadjuvant chemotherapy for colorectal carcinoma liver metastasis. Int J Clin Exp Pathol 5(4):308–314PubMedCentralPubMed
35.
go back to reference Lupinacci RM, Mello ES, Pinheiro RS, Marques G, Coelho FF, Kruger JA, Perini MV, Cecconello I, Herman P (2014) Intrahepatic lymphatic invasion but not vascular invasion is a major prognostic factor after resection of colorectal cancer liver metastases. World J Surg 38(8):2089–2096PubMedCrossRef Lupinacci RM, Mello ES, Pinheiro RS, Marques G, Coelho FF, Kruger JA, Perini MV, Cecconello I, Herman P (2014) Intrahepatic lymphatic invasion but not vascular invasion is a major prognostic factor after resection of colorectal cancer liver metastases. World J Surg 38(8):2089–2096PubMedCrossRef
36.
go back to reference Hadj AK, Malcontenti-Wilson C, Nikfarjam M, Christophi C (2012) Lymphatic patterns of colorectal liver metastases. J Surg Res 173(2):292–298PubMedCrossRef Hadj AK, Malcontenti-Wilson C, Nikfarjam M, Christophi C (2012) Lymphatic patterns of colorectal liver metastases. J Surg Res 173(2):292–298PubMedCrossRef
37.
go back to reference Gurusamy KS, Imber C, Davidson BR (2008) Management of the hepatic lymph nodes during resection of liver metastases from colorectal cancer: a systematic review. HPB Surg 2008:684150PubMedCentralPubMedCrossRef Gurusamy KS, Imber C, Davidson BR (2008) Management of the hepatic lymph nodes during resection of liver metastases from colorectal cancer: a systematic review. HPB Surg 2008:684150PubMedCentralPubMedCrossRef
39.
go back to reference Nakamura S, Yokoi Y, Suzuki S, Baba S, Muro H (1992) Results of extensive surgery for liver metastases in colorectal carcinoma. Br J Surg 79:35–38PubMedCrossRef Nakamura S, Yokoi Y, Suzuki S, Baba S, Muro H (1992) Results of extensive surgery for liver metastases in colorectal carcinoma. Br J Surg 79:35–38PubMedCrossRef
40.
go back to reference Beckurts KTE, Hölscher AH, Thorban S, Bollschweiler E, Siewert JR (1997) Significance of lymph node involvement at the hepatic hilum in the resection of colorectal liver metastases. Br J Surg 84:1081–1084PubMedCrossRef Beckurts KTE, Hölscher AH, Thorban S, Bollschweiler E, Siewert JR (1997) Significance of lymph node involvement at the hepatic hilum in the resection of colorectal liver metastases. Br J Surg 84:1081–1084PubMedCrossRef
41.
go back to reference Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH (1999) Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 230:309–318PubMedCentralPubMedCrossRef Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH (1999) Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 230:309–318PubMedCentralPubMedCrossRef
42.
go back to reference Gibbs JF, Weber TK, Rodriguez-Bigas MA, Driscoll DL, Petrelli NJ (1998) Intraoperative determinants of unresectability for patients with colorectal hepatic metastases. Cancer 82:1244–1249PubMedCrossRef Gibbs JF, Weber TK, Rodriguez-Bigas MA, Driscoll DL, Petrelli NJ (1998) Intraoperative determinants of unresectability for patients with colorectal hepatic metastases. Cancer 82:1244–1249PubMedCrossRef
43.
go back to reference Minagawa M, Makuuchi M, Torzilli G, Takayama T, Kawasaki S, Kosuge T, Yamamoto J, Imamura H (2000) Extension of the frontiers of surgical indications in the treatment of liver metastasis from colorectal cancer: long term results. Ann Surg 231:487–499PubMedCentralPubMedCrossRef Minagawa M, Makuuchi M, Torzilli G, Takayama T, Kawasaki S, Kosuge T, Yamamoto J, Imamura H (2000) Extension of the frontiers of surgical indications in the treatment of liver metastasis from colorectal cancer: long term results. Ann Surg 231:487–499PubMedCentralPubMedCrossRef
44.
go back to reference Laurent C, Sa Cunha A, Rullier E, Smith D, Rullier A, Saric J (2004) Impact of microscopic hepatic lymph node involvement on survival after resection of colorectal liver metastasis. J Am Coll Surg 198:884–891PubMedCrossRef Laurent C, Sa Cunha A, Rullier E, Smith D, Rullier A, Saric J (2004) Impact of microscopic hepatic lymph node involvement on survival after resection of colorectal liver metastasis. J Am Coll Surg 198:884–891PubMedCrossRef
45.
go back to reference Elias D, Saric J, Jaeck D, Arnaud JP, Gayet B, Rivoire M, Lorimier G, Carles J, Lasser P (1996) Prospective study of microscopic lymph node involvement of the hepatic pedicle during curative hepatectomy for colorectal metastases. Br J Surg 83:942–945PubMedCrossRef Elias D, Saric J, Jaeck D, Arnaud JP, Gayet B, Rivoire M, Lorimier G, Carles J, Lasser P (1996) Prospective study of microscopic lymph node involvement of the hepatic pedicle during curative hepatectomy for colorectal metastases. Br J Surg 83:942–945PubMedCrossRef
46.
go back to reference Kokudo N, Sato T, Seki M, Ohta H, Azekura K, Ueno M, Matsubara T, Yanagisawa A, Kato Y, Takahashi T (1999) Hepatic lymph node involvement in resected cases of liver metastases from colorectal cancer. Dis Colon Rectum 42:1285–1290PubMedCrossRef Kokudo N, Sato T, Seki M, Ohta H, Azekura K, Ueno M, Matsubara T, Yanagisawa A, Kato Y, Takahashi T (1999) Hepatic lymph node involvement in resected cases of liver metastases from colorectal cancer. Dis Colon Rectum 42:1285–1290PubMedCrossRef
47.
go back to reference Sanchez-Cespedes M, Esteller M, Hibi K, Cope FO, Westra WH, Piantadosi S, Herman JG, Jen J, Sidransky D (1999) Molecular detection of neoplastic cells in lymph nodes of metastatic colorectal cancer patients predicts recurrence. Clin Cancer Res 5:2450–2454PubMed Sanchez-Cespedes M, Esteller M, Hibi K, Cope FO, Westra WH, Piantadosi S, Herman JG, Jen J, Sidransky D (1999) Molecular detection of neoplastic cells in lymph nodes of metastatic colorectal cancer patients predicts recurrence. Clin Cancer Res 5:2450–2454PubMed
48.
go back to reference Rodgers MS, McCall JL (2000) Surgery for colorectal liver metastases with hepatic lymph node involvement: a systematic review. Br J Surg 87:1142–1155PubMedCrossRef Rodgers MS, McCall JL (2000) Surgery for colorectal liver metastases with hepatic lymph node involvement: a systematic review. Br J Surg 87:1142–1155PubMedCrossRef
49.
go back to reference Jaeck D, Nakano H, Bachellier P, Inoue K, Weber JC, Oussoultzoglou E, Wolf P, Chenard-Neu MP (2002) Significance of hepatic pedicle lymph node involvement in patients with colorectal liver metastases: a prospective study. Ann Surg Oncol 9:430–438PubMedCrossRef Jaeck D, Nakano H, Bachellier P, Inoue K, Weber JC, Oussoultzoglou E, Wolf P, Chenard-Neu MP (2002) Significance of hepatic pedicle lymph node involvement in patients with colorectal liver metastases: a prospective study. Ann Surg Oncol 9:430–438PubMedCrossRef
50.
go back to reference Grobmyer SR, Wang L, Gonen M, Fong Y, Klimstra D, D’Angelica M, DeMatteo RP, Schwartz L, Blumgart LH, Jarnagin WR (2006) Perihepatic lymph node assessment in patients undergoing partial hepatectomy for malignancy. Ann Surg 244(2):260–264PubMedCentralPubMedCrossRef Grobmyer SR, Wang L, Gonen M, Fong Y, Klimstra D, D’Angelica M, DeMatteo RP, Schwartz L, Blumgart LH, Jarnagin WR (2006) Perihepatic lymph node assessment in patients undergoing partial hepatectomy for malignancy. Ann Surg 244(2):260–264PubMedCentralPubMedCrossRef
51.
go back to reference Rau C, Blanc B, Ronot M, Dokmak S, Aussilhou B, Faivre S, Vilgrain V, Paradis V, Belghiti J (2012) Neither preoperative computed tomography nor intra-operative examination can predict metastatic lymph node in the hepatic pedicle in patients with colorectal liver metastasis. Ann Surg Oncol 19(1):163–168PubMedCrossRef Rau C, Blanc B, Ronot M, Dokmak S, Aussilhou B, Faivre S, Vilgrain V, Paradis V, Belghiti J (2012) Neither preoperative computed tomography nor intra-operative examination can predict metastatic lymph node in the hepatic pedicle in patients with colorectal liver metastasis. Ann Surg Oncol 19(1):163–168PubMedCrossRef
52.
go back to reference Viana EF, Herman P, Siqueira SC, Taka T, Carvalho P, Coelho FF, Pugliese V, Saad WA, D’Albuquerque LA (2009) Lymphadenectomy in colorectal cancer liver metastases resection: incidence of hilar lymph nodes micrometastasis. J Surg Oncol 100:534–537PubMedCrossRef Viana EF, Herman P, Siqueira SC, Taka T, Carvalho P, Coelho FF, Pugliese V, Saad WA, D’Albuquerque LA (2009) Lymphadenectomy in colorectal cancer liver metastases resection: incidence of hilar lymph nodes micrometastasis. J Surg Oncol 100:534–537PubMedCrossRef
53.
go back to reference Fortner JG (1988) Recurrence of colorectal cancer after hepatic resection. Am J Surg 155(3):378–382PubMedCrossRef Fortner JG (1988) Recurrence of colorectal cancer after hepatic resection. Am J Surg 155(3):378–382PubMedCrossRef
54.
go back to reference Ekberg H, Tranberg KG, Andersson R, Lundstedt C, Hägerstrand I, Ranstam J, Bengmark S (1987) Pattern of recurrence in liver resection for colorectal secondaries. World J Surg 11(4):541–547PubMedCrossRef Ekberg H, Tranberg KG, Andersson R, Lundstedt C, Hägerstrand I, Ranstam J, Bengmark S (1987) Pattern of recurrence in liver resection for colorectal secondaries. World J Surg 11(4):541–547PubMedCrossRef
55.
go back to reference Hughes KS, Simon R, Songhorabodi S, Adson MA, Ilstrup DM, Fortner JG, Maclean BJ, Foster JH, Daly JM, Fitzherbert D (1986) Resection of the liver for colorectal carcinoma metastases: a multi-institutional study of patterns of recurrence. Surgery 100(2):278–284PubMed Hughes KS, Simon R, Songhorabodi S, Adson MA, Ilstrup DM, Fortner JG, Maclean BJ, Foster JH, Daly JM, Fitzherbert D (1986) Resection of the liver for colorectal carcinoma metastases: a multi-institutional study of patterns of recurrence. Surgery 100(2):278–284PubMed
56.
go back to reference Bennett JJ, Schmidt CR, Klimstra DS, Grobmyer SR, Ishill NM, D’Angelica M, DeMatteo RP, Fong Y, Blumgart LH, Jarnagin WR (2008) Perihepatic lymph node micrometastases impact outcome after partial hepatectomy for colorectal metastases. Ann Surg Oncol 15:1130–1136PubMedCrossRef Bennett JJ, Schmidt CR, Klimstra DS, Grobmyer SR, Ishill NM, D’Angelica M, DeMatteo RP, Fong Y, Blumgart LH, Jarnagin WR (2008) Perihepatic lymph node micrometastases impact outcome after partial hepatectomy for colorectal metastases. Ann Surg Oncol 15:1130–1136PubMedCrossRef
57.
go back to reference Kane JM 3rd, Kahlenberg MS, Rodriguez-Bigas MA, Gibbs JF, Petrelli NJ (2002) Intraoperative hepatic lymphatic mapping in patients with liver metastases from colorectal carcinoma. Am Surg 68(9):745–750PubMed Kane JM 3rd, Kahlenberg MS, Rodriguez-Bigas MA, Gibbs JF, Petrelli NJ (2002) Intraoperative hepatic lymphatic mapping in patients with liver metastases from colorectal carcinoma. Am Surg 68(9):745–750PubMed
58.
go back to reference Maharaj R, Shukla PJ, Naraynsingh V, Dan D, Hariharan S (2011) Sentinel lymph node biopsy in gastrointestinal malignancies-where do we stand? Indian J Cancer 48(3):345–350PubMedCrossRef Maharaj R, Shukla PJ, Naraynsingh V, Dan D, Hariharan S (2011) Sentinel lymph node biopsy in gastrointestinal malignancies-where do we stand? Indian J Cancer 48(3):345–350PubMedCrossRef
59.
go back to reference Carpizo DR, D´Angelica M (2009) Liver resection for metastatic colorectal cancer in the presence of extrahepatic disease. Ann Surg Oncol 16:2411–2421PubMedCrossRef Carpizo DR, D´Angelica M (2009) Liver resection for metastatic colorectal cancer in the presence of extrahepatic disease. Ann Surg Oncol 16:2411–2421PubMedCrossRef
60.
go back to reference Ishibashi K, Ohsawa T, Yokohama M, Ishizuka N, Miyazaki T, Nakada H, Gonda T, Ishida H (2006) Hepatic lymph node involvement in patients with synchronous multiple liver metastases of colorectal cancer. Gan To Kagaku Ryoho 33:1834–1837PubMed Ishibashi K, Ohsawa T, Yokohama M, Ishizuka N, Miyazaki T, Nakada H, Gonda T, Ishida H (2006) Hepatic lymph node involvement in patients with synchronous multiple liver metastases of colorectal cancer. Gan To Kagaku Ryoho 33:1834–1837PubMed
61.
go back to reference Nakamura S, Yokoi Y, Suzuki S, Baba S, Muro H (1992) Results of extensive surgery for liver metastases in colorectal carcinoma. Br J Surg 79:35–38PubMedCrossRef Nakamura S, Yokoi Y, Suzuki S, Baba S, Muro H (1992) Results of extensive surgery for liver metastases in colorectal carcinoma. Br J Surg 79:35–38PubMedCrossRef
62.
go back to reference Elias DD, Ouellet JJF, Bellon NN, Pignon JJP, Pocard MM, Lasser PP (2003) Extrahepatic disease does not contraindicate hepatectomy for colorectal liver metastases. Br J Surg 90(5):567–574PubMedCrossRef Elias DD, Ouellet JJF, Bellon NN, Pignon JJP, Pocard MM, Lasser PP (2003) Extrahepatic disease does not contraindicate hepatectomy for colorectal liver metastases. Br J Surg 90(5):567–574PubMedCrossRef
63.
go back to reference Wakai T, Shirai Y, Sakata J, Nagahashi M, Kaneko K, Hatakeyama K (2009) Hepatic lymph node dissection provides a survival benefit for patients with nodal disease of colorectal carcinoma liver metastases. Hepatogastroenterology 56:186–190PubMed Wakai T, Shirai Y, Sakata J, Nagahashi M, Kaneko K, Hatakeyama K (2009) Hepatic lymph node dissection provides a survival benefit for patients with nodal disease of colorectal carcinoma liver metastases. Hepatogastroenterology 56:186–190PubMed
64.
go back to reference Adam R, de Haas RJ, Wicherts DA, Aloia TA, Delvart V, Azoulay D, Bismuth H, Castaing D (2008) Is hepatic resection justified after chemotherapy in patients with colorectal liver metastases and lymph node involvement? J Clin Oncol 26:3672–3680PubMedCrossRef Adam R, de Haas RJ, Wicherts DA, Aloia TA, Delvart V, Azoulay D, Bismuth H, Castaing D (2008) Is hepatic resection justified after chemotherapy in patients with colorectal liver metastases and lymph node involvement? J Clin Oncol 26:3672–3680PubMedCrossRef
65.
go back to reference Elias DD, Liberale GG, Vernerey DD, Pocard M, Ducreux M, Boige V, Malka D, Pignon JP, Lasser P (2005) Hepatic and extrahepatic colorectal metastases: when resectable, their localization does not matter, but their total number has a prognostic effect. Ann Surg Oncol 12(11):900–909PubMedCrossRef Elias DD, Liberale GG, Vernerey DD, Pocard M, Ducreux M, Boige V, Malka D, Pignon JP, Lasser P (2005) Hepatic and extrahepatic colorectal metastases: when resectable, their localization does not matter, but their total number has a prognostic effect. Ann Surg Oncol 12(11):900–909PubMedCrossRef
66.
go back to reference Giuliano AE, Jones RC, Brennan M, Statman R (1997) Sentinel lymphadenectomy in breast cancer. J Clin Oncol 15:2345–2350PubMed Giuliano AE, Jones RC, Brennan M, Statman R (1997) Sentinel lymphadenectomy in breast cancer. J Clin Oncol 15:2345–2350PubMed
67.
68.
go back to reference Maehara Y, Baba H, Ohno S, Sugimachi K (1995) Cytokeratin staining reveals micrometastases in lymph nodes of early gastric cancer. Surgery 117:480PubMedCrossRef Maehara Y, Baba H, Ohno S, Sugimachi K (1995) Cytokeratin staining reveals micrometastases in lymph nodes of early gastric cancer. Surgery 117:480PubMedCrossRef
69.
go back to reference Noura S, Yamamoto H, Miyake Y, Bn Kim, Takayama O, Seshimo I, Ikenaga M, Ikeda M, Sekimoto M, Matsuura N, Monden M (2002) Immunohistochemical assessment of localization and frequency of micrometastases in lymph nodes of colorectal cancer. Clin Cancer Res 8:759–767PubMed Noura S, Yamamoto H, Miyake Y, Bn Kim, Takayama O, Seshimo I, Ikenaga M, Ikeda M, Sekimoto M, Matsuura N, Monden M (2002) Immunohistochemical assessment of localization and frequency of micrometastases in lymph nodes of colorectal cancer. Clin Cancer Res 8:759–767PubMed
70.
go back to reference Lupinacci RM, Herman P, Coelho FC, Viana EF, D’Albuquerque LA, Cecconello I (2013) Diagnosis and impact of hilar lymph node micrometastases on the outcome of resected colorectal liver metastasis. Hepatogastroenterology 60(122):333–336PubMed Lupinacci RM, Herman P, Coelho FC, Viana EF, D’Albuquerque LA, Cecconello I (2013) Diagnosis and impact of hilar lymph node micrometastases on the outcome of resected colorectal liver metastasis. Hepatogastroenterology 60(122):333–336PubMed
71.
go back to reference Tschmelittsch J, Klimstra DS, Cohen AM (2000) Lymph node micrometastases do not predict relapse in stage II colon cancer. Ann Surg Oncol 7:601–608CrossRef Tschmelittsch J, Klimstra DS, Cohen AM (2000) Lymph node micrometastases do not predict relapse in stage II colon cancer. Ann Surg Oncol 7:601–608CrossRef
Metadata
Title
Lymphatic drainage of the liver and its implications in the management of colorectal cancer liver metastases
Authors
Renato Micelli Lupinacci
François Paye
Fabricio Ferreira Coelho
Jaime Arthur Pirolla Kruger
Paulo Herman
Publication date
01-12-2014
Publisher
Springer Milan
Published in
Updates in Surgery / Issue 4/2014
Print ISSN: 2038-131X
Electronic ISSN: 2038-3312
DOI
https://doi.org/10.1007/s13304-014-0265-0

Other articles of this Issue 4/2014

Updates in Surgery 4/2014 Go to the issue