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Review article: Biomedical intelligence

Vol. 151 No. 0708 (2021)

Multimodal treatment strategies for colorectal liver metastases

DOI
https://doi.org/10.4414/smw.2021.20390
Cite this as:
Swiss Med Wkly. 2021;151:w20390
Published
15.02.2021

Summary

Colorectal cancer is the third most common cancer worldwide. Half of CRC patients develop liver metastases during the course of the disease, with a 5-year survival rate close to zero in the absence of therapy. Surgical resection remains the only possible curative option, and current guidelines recommend adjuvant chemotherapy, resulting in a 5-year survival rate exceeding 50%. Neoadjuvant systemic therapy is not indicated in cases with simple resection but should be offered to all patients with extensive bilobar disease. Personalised systemic treatment is essential to convert upfront non-resectable lesions to resectable ones. Anatomical resections, non-anatomical resections and two-stage hepatectomies can be performed though open or minimally invasive (laparoscopic or robotic) surgery.

The extent of a hepatic resection is limited by the risk of postoperative liver failure due to a too small liver remnant, inflow or outflow obstruction or insufficient biliary drainage. About 75% of patients are diagnosed with non-resectable liver metastases not amenable to a standard upfront resection. In recent years, effective therapeutic approaches have revolutionised liver surgery and new strategies have enabled the conversion of primarily non-resectable metastatic disease for resection. These strategies include oncological and surgical therapies, as well as combinations of the two. From an oncological perspective, colorectal liver metastases may be treated by systemic chemotherapy or immunotherapy, or selective intra-hepatic arterial infusion chemotherapy, depending on the extent of the disease and the mutational status. In surgery, we often apply two-stage strategies using portal vein occlusion, such as portal vein embolisation or ligation, or complex two-stage hepatectomy such as associating liver partition and portal vein ligation for staged hepatectomy. Other additive tools to reach curative resection are tumour ablations (electroporation, microwave or radiofrequency). The role of stereotactic radiation of liver metastases is not yet well defined. Modern radiation techniques, including image guidance, breath hold and gating, were only introduced for a larger patient population in recent years. Therefore, prospective studies with larger patient cohorts are still pending.

Over the last decade, liver transplantation has gained increasing attention in selective cases of non-resectable colorectal liver metastases, with promising cohort studies, but definitive recommendations must await the results of ongoing randomised controlled trials.

The optimal treatment of patients with colorectal liver metastases requires the timely association of various strategies, and all cases must be discussed at multidisciplinary team conferences. While colorectal liver metastases was a uniformly lethal condition a few decades ago, it has become amenable to curative therapies, with excellent quality of life in many scenarios. This review reports on up-to-date treatment modalities and their combinations in the treatment algorithm of colorectal liver metastases.

References

  1. https://www.bfs.admin.ch/bfs/de/home/statistiken/gesundheit/gesundheitszustand/krankheiten/krebs/spezifische.html July, 20th, 2020.
  2. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. Published online February 06, 2015. doi:.https://doi.org/10.3322/caac.21262
  3. Poston GJ, Adam R, Alberts S, Curley S, Figueras J, Haller D, et al. OncoSurge: a strategy for improving resectability with curative intent in metastatic colorectal cancer. J Clin Oncol. 2005;23(28):7125–34. Published online September 30, 2005. doi:.https://doi.org/10.1200/JCO.2005.08.722
  4. Slesser AA, Simillis C, Goldin R, Brown G, Mudan S, Tekkis PP. A meta-analysis comparing simultaneous versus delayed resections in patients with synchronous colorectal liver metastases. Surg Oncol. 2013;22(1):36–47. Published online December 21, 2012. doi:.https://doi.org/10.1016/j.suronc.2012.11.002
  5. Hackl C, Neumann P, Gerken M, Loss M, Klinkhammer-Schalke M, Schlitt HJ. Treatment of colorectal liver metastases in Germany: a ten-year population-based analysis of 5772 cases of primary colorectal adenocarcinoma. BMC Cancer. 2014;14(1):810. doi:.https://doi.org/10.1186/1471-2407-14-810
  6. Manfredi S, Lepage C, Hatem C, Coatmeur O, Faivre J, Bouvier AM. Epidemiology and management of liver metastases from colorectal cancer. Ann Surg. 2006;244(2):254–9. doi:.https://doi.org/10.1097/01.sla.0000217629.94941.cf
  7. Nordlinger B, Sorbye H, Glimelius B, Poston GJ, Schlag PM, Rougier P, et al.; EORTC Gastro-Intestinal Tract Cancer Group; Cancer Research UK; Arbeitsgruppe Lebermetastasen und-tumoren in der Chirurgischen Arbeitsgemeinschaft Onkologie (ALM-CAO); Australasian Gastro-Intestinal Trials Group (AGITG); Fédération Francophone de Cancérologie Digestive (FFCD). Perioperative chemotherapy with FOLFOX4 and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC Intergroup trial 40983): a randomised controlled trial. Lancet. 2008;371(9617):1007–16. doi:.https://doi.org/10.1016/S0140-6736(08)60455-9
  8. Wagner JS, Adson MA, Van Heerden JA, Adson MH, Ilstrup DM. The natural history of hepatic metastases from colorectal cancer. A comparison with resective treatment. Ann Surg. 1984;199(5):502–8. doi:.https://doi.org/10.1097/00000658-198405000-00002
  9. Lehmann K, Rickenbacher A, Weber A, Pestalozzi BC, Clavien PA. Chemotherapy before liver resection of colorectal metastases: friend or foe? Ann Surg. 2012;255(2):237–47. Published online November 02, 2011. doi:.https://doi.org/10.1097/SLA.0b013e3182356236
  10. Petrowsky H, Fritsch R, Guckenberger M, De Oliveira ML, Dutkowski P, Clavien PA. Modern therapeutic approaches for the treatment of malignant liver tumours. Nat Rev Gastroenterol Hepatol. 2020;17(12):755–72; Epub ahead of print. doi:.https://doi.org/10.1038/s41575-020-0314-8
  11. Nordlinger B, Sorbye H, Glimelius B, Poston GJ, Schlag PM, Rougier P, et al.; EORTC Gastro-Intestinal Tract Cancer Group; Cancer Research UK; Arbeitsgruppe Lebermetastasen und–tumoren in der Chirurgischen Arbeitsgemeinschaft Onkologie (ALM-CAO); Australasian Gastro-Intestinal Trials Group (AGITG); Fédération Francophone de Cancérologie Digestive (FFCD). Perioperative FOLFOX4 chemotherapy and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC 40983): long-term results of a randomised, controlled, phase 3 trial. Lancet Oncol. 2013;14(12):1208–15. doi:.https://doi.org/10.1016/S1470-2045(13)70447-9
  12. Van Cutsem E, Cervantes A, Adam R, Sobrero A, Van Krieken JH, Aderka D, et al. ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol. 2016;27(8):1386–422. Published online July 07, 2016. doi:.https://doi.org/10.1093/annonc/mdw235
  13. Niekel MC, Bipat S, Stoker J. Diagnostic imaging of colorectal liver metastases with CT, MR imaging, FDG PET, and/or FDG PET/CT: a meta-analysis of prospective studies including patients who have not previously undergone treatment. Radiology. 2010;257(3):674–84. Published online September 11, 2010. doi:.https://doi.org/10.1148/radiol.10100729
  14. Chu QD, Volmer CM, Zibari GB, Orloff SL, Williams M, Gimenez ME, eds. Hepato-Pancreato-Biliary and Transplant Surgery: Practical Management of Dilemmas. AHPBA: Beaux Books; 2018.
  15. Moulton CA, Gu CS, Law CH, Tandan VR, Hart R, Quan D, et al. Effect of PET before liver resection on surgical management for colorectal adenocarcinoma metastases: a randomized clinical trial. JAMA. 2014;311(18):1863–9. Published online May 16, 2014. doi:.https://doi.org/10.1001/jama.2014.3740
  16. Pugh RN, Murray-Lyon IM, Dawson JL, Pietroni MC, Williams R. Transection of the oesophagus for bleeding oesophageal varices. Br J Surg. 1973;60(8):646–9. Published online August 01, 1973. doi:.https://doi.org/10.1002/bjs.1800600817
  17. Child CG (ed.) The Liver and Portal Hypertension. Philadelphia and London: W. B. Saunders Co. Ltd; 1964.
  18. Zipprich A, Kuss O, Rogowski S, Kleber G, Lotterer E, Seufferlein T, et al. Incorporating indocyanin green clearance into the Model for End Stage Liver Disease (MELD-ICG) improves prognostic accuracy in intermediate to advanced cirrhosis. Gut. 2010;59(7):963–8. Published online June 29, 2010. doi:.https://doi.org/10.1136/gut.2010.208595
  19. Stauber RE, Wagner D, Stadlbauer V, Palma S, Gurakuqi G, Kniepeiss D, et al. Evaluation of indocyanine green clearance and model for end-stage liver disease for estimation of short-term prognosis in decompensated cirrhosis. Liver Int. 2009;29(10):1516–20. doi:.https://doi.org/10.1111/j.1478-3231.2009.02104.x
  20. Lisotti A, Azzaroli F, Buonfiglioli F, Montagnani M, Cecinato P, Turco L, et al. Indocyanine green retention test as a noninvasive marker of portal hypertension and esophageal varices in compensated liver cirrhosis. Hepatology. 2014;59(2):643–50. Published online September 17, 2013. doi:.https://doi.org/10.1002/hep.26700
  21. de Liguori Carino N, O’Reilly DA, Dajani K, Ghaneh P, Poston GJ, Wu AV. Perioperative use of the LiMON method of indocyanine green elimination measurement for the prediction and early detection of post-hepatectomy liver failure. Eur J Surg Oncol. 2009;35(9):957–62. doi:.https://doi.org/10.1016/j.ejso.2009.02.003
  22. Ray S, Mehta NN, Golhar A, Nundy S. Post hepatectomy liver failure - A comprehensive review of current concepts and controversies. Ann Med Surg (Lond). 2018;34(34):4–10. doi:.https://doi.org/10.1016/j.amsu.2018.08.012
  23. Ge PL, Du SD, Mao YL. Advances in preoperative assessment of liver function. Hepatobiliary Pancreat Dis Int. 2014;13(4):361–70. Published online August 08, 2014. doi:.https://doi.org/10.1016/S1499-3872(14)60267-8
  24. Hoekstra LT, de Graaf W, Nibourg GA, Heger M, Bennink RJ, Stieger B, et al. Physiological and biochemical basis of clinical liver function tests: a review. Ann Surg. 2013;257(1):27–36. Published online July 28, 2012. doi:.https://doi.org/10.1097/SLA.0b013e31825d5d47
  25. Mizuguchi T, Kawamoto M, Meguro M, Hui TT, Hirata K. Preoperative liver function assessments to estimate the prognosis and safety of liver resections. Surg Today. 2014;44(1):1–10. Published online March 12, 2013. doi:.https://doi.org/10.1007/s00595-013-0534-4
  26. Du ZG, Li B, Wei YG, Yin J, Feng X, Chen X. A new scoring system for assessment of liver function after successful hepatectomy in patients with hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int. 2011;10(3):265–9. Published online June 15, 2011. doi:.https://doi.org/10.1016/S1499-3872(11)60044-1
  27. Lock JF, Westphal T, Rubin T, Malinowski M, Schulz A, Jara M, et al. LiMAx Test Improves Diagnosis of Chemotherapy-Associated Liver Injury Before Resection of Colorectal Liver Metastases. Ann Surg Oncol. 2017;24(9):2447–55. Published online May 19, 2017. doi:.https://doi.org/10.1245/s10434-017-5887-2
  28. Bennink RJ, Dinant S, Erdogan D, Heijnen BH, Straatsburg IH, van Vliet AK, et al. Preoperative assessment of postoperative remnant liver function using hepatobiliary scintigraphy. J Nucl Med. 2004;45(6):965–71.
  29. Clavien PA, Petrowsky H, DeOliveira ML, Graf R. Strategies for safer liver surgery and partial liver transplantation. N Engl J Med. 2007;356(15):1545–59. Published online April 13, 2007. doi:.https://doi.org/10.1056/NEJMra065156
  30. Nordlinger B, Guiguet M, Vaillant JC, Balladur P, Boudjema K, Bachellier P, et al.; Association Française de Chirurgie. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Cancer. 1996;77(7):1254–62. Published online April 01, 1996. doi:.https://doi.org/10.1002/(SICI)1097-0142(19960401)77:7<1254::AID-CNCR5>3.0.CO;2-I
  31. Mitry E, Fields AL, Bleiberg H, Labianca R, Portier G, Tu D, et al. Adjuvant chemotherapy after potentially curative resection of metastases from colorectal cancer: a pooled analysis of two randomized trials. J Clin Oncol. 2008;26(30):4906–11. Published online September 17, 2008. doi:.https://doi.org/10.1200/JCO.2008.17.3781
  32. Baltatzis M, Chan AK, Jegatheeswaran S, Mason JM, Siriwardena AK. Colorectal cancer with synchronous hepatic metastases: Systematic review of reports comparing synchronous surgery with sequential bowel-first or liver-first approaches. Eur J Surg Oncol. 2016;42(2):159–65. doi:.https://doi.org/10.1016/j.ejso.2015.11.002
  33. de Haas RJ, Adam R, Wicherts DA, Azoulay D, Bismuth H, Vibert E, et al. Comparison of simultaneous or delayed liver surgery for limited synchronous colorectal metastases. Br J Surg. 2010;97(8):1279–89. Published online June 26, 2010. doi:.https://doi.org/10.1002/bjs.7106
  34. Mentha G, Majno PE, Andres A, Rubbia-Brandt L, Morel P, Roth AD. Neoadjuvant chemotherapy and resection of advanced synchronous liver metastases before treatment of the colorectal primary. Br J Surg. 2006;93(7):872–8. Published online May 04, 2006. doi:.https://doi.org/10.1002/bjs.5346
  35. Zorzi D, Mullen JT, Abdalla EK, Pawlik TM, Andres A, Muratore A, et al. Comparison between hepatic wedge resection and anatomic resection for colorectal liver metastases. J Gastrointest Surg. 2006;10(1):86–94. Published online December 22, 2005. doi:.https://doi.org/10.1016/j.gassur.2005.07.022
  36. Hamady ZZ, Lodge JP, Welsh FK, Toogood GJ, White A, John T, et al. One-millimeter cancer-free margin is curative for colorectal liver metastases: a propensity score case-match approach. Ann Surg. 2014;259(3):543–8. Published online June 05, 2013. doi:.https://doi.org/10.1097/SLA.0b013e3182902b6e
  37. Hammond JS, Muirhead W, Zaitoun AM, Cameron IC, Lobo DN. Comparison of liver parenchymal ablation and tissue necrosis in a cadaveric bovine model using the Harmonic Scalpel, the LigaSure, the Cavitron Ultrasonic Surgical Aspirator and the Aquamantys devices. HPB (Oxford). 2012;14(12):828–32. doi:.https://doi.org/10.1111/j.1477-2574.2012.00547.x
  38. Eshmuminov D, Raptis DA, Linecker M, Wirsching A, Lesurtel M, Clavien PA. Meta-analysis of associating liver partition with portal vein ligation and portal vein occlusion for two-stage hepatectomy. Br J Surg. 2016;103(13):1768–82. Published online September 17, 2016. doi:.https://doi.org/10.1002/bjs.10290
  39. de Santibañes E, Clavien PA. Playing Play-Doh to prevent postoperative liver failure: the “ALPPS” approach. Ann Surg. 2012;255(3):415–7. Published online February 15, 2012. doi:.https://doi.org/10.1097/SLA.0b013e318248577d
  40. Langiewicz M, Schlegel A, Saponara E, Linecker M, Borger P, Graf R, et al. Hedgehog pathway mediates early acceleration of liver regeneration induced by a novel two-staged hepatectomy in mice. J Hepatol. 2017;66(3):560–70. Published online October 25, 2016. doi:.https://doi.org/10.1016/j.jhep.2016.10.014
  41. Petrowsky H, Györi G, de Oliveira M, Lesurtel M, Clavien PA. Is partial-ALPPS safer than ALPPS? A single-center experience. Ann Surg. 2015;261(4):e90–2. Published online February 24, 2015. doi:.https://doi.org/10.1097/SLA.0000000000001087
  42. Moris D, Ronnekleiv-Kelly S, Kostakis ID, Tsilimigras DI, Beal EW, Papalampros A, et al. Operative Results and Oncologic Outcomes of Associating Liver Partition and Portal Vein Ligation for Staged Hepatectomy (ALPPS) Versus Two-Stage Hepatectomy (TSH) in Patients with Unresectable Colorectal Liver Metastases: A Systematic Review and Meta-Analysis. World J Surg. 2018;42(3):806–15. Published online August 12, 2017. doi:.https://doi.org/10.1007/s00268-017-4181-6
  43. Lau WY, Lai EC. Modifications of ALPPS - from complex to more complex or from complex to less complex operations. Hepatobiliary Pancreat Dis Int. 2017;16(4):346–52. Published online August 22, 2017. doi:.https://doi.org/10.1016/S1499-3872(17)60034-1
  44. Linecker M, Stavrou GA, Oldhafer KJ, Jenner RM, Seifert B, Lurje G, et al. The ALPPS Risk Score: Avoiding Futile Use of ALPPS. Ann Surg. 2016;264(5):763–71. Published online October 18, 2016. doi:.https://doi.org/10.1097/SLA.0000000000001914
  45. Eshmuminov D, Tschuor C, Raptis DA, Boss A, Wurnig MC, Sergeant G, et al. Rapid liver volume increase induced by associating liver partition with portal vein ligation for staged hepatectomy (ALPPS): Is it edema, steatosis, or true proliferation? Surgery. 2017;161(6):1549–52. Published online April 16, 2017. doi:.https://doi.org/10.1016/j.surg.2017.01.005
  46. Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg. 2015;261(4):619–29. Published online March 06, 2015. doi:.https://doi.org/10.1097/sla.0000000000001184
  47. Fretland AA, Dagenborg VJ, Bjørnelv GMW, Kazaryan AM, Kristiansen R, Fagerland MW, et al. Laparoscopic Versus Open Resection for Colorectal Liver Metastases: The OSLO-COMET Randomized Controlled Trial. Ann Surg. 2018;267(2):199–207. Published online June 29, 2017. doi:.https://doi.org/10.1097/SLA.0000000000002353
  48. Aghayan DL, Fretland AA, Kazaryan AM, Sahakyan MA, Dagenborg VJ, Bjørnbeth BA, et al. Laparoscopic versus open liver resection in the posterosuperior segments: a sub-group analysis from the OSLO-COMET randomized controlled trial. HPB (Oxford). 2019;21(11):1485–90. Published online April 10, 2019. doi:.https://doi.org/10.1016/j.hpb.2019.03.358
  49. Clavien PA, Barkun J. Consensus conference on laparoscopic liver resection: a jury-based evaluation. Ann Surg. 2015;261(4):630–1. Published online March 06, 2015. doi:.https://doi.org/10.1097/SLA.0000000000001183
  50. Abu Hilal M, Aldrighetti L, Dagher I, Edwin B, Troisi RI, Alikhanov R, et al. The Southampton Consensus Guidelines for Laparoscopic Liver Surgery: From Indication to Implementation. Ann Surg. 2018;268(1):11–8. Published online October 25, 2017. doi:.https://doi.org/10.1097/SLA.0000000000002524
  51. Fruscione M, Pickens R, Baker EH, Cochran A, Khan A, Ocuin L, et al. Robotic-assisted versus laparoscopic major liver resection: analysis of outcomes from a single center. HPB (Oxford). 2019;21(7):906–11. Published online January 09, 2019. doi:.https://doi.org/10.1016/j.hpb.2018.11.011
  52. Seror O. Ablative therapies: Advantages and disadvantages of radiofrequency, cryotherapy, microwave and electroporation methods, or how to choose the right method for an individual patient? Diagn Interv Imaging. 2015;96(6):617–24. Published online May 20, 2015. doi:.https://doi.org/10.1016/j.diii.2015.04.007
  53. Loveman E, Jones J, Clegg AJ, Picot J, Colquitt JL, Mendes D, et al. The clinical effectiveness and cost-effectiveness of ablative therapies in the management of liver metastases: systematic review and economic evaluation. Health Technol Assess. 2014;18(7):vii–viii, 1–283. doi:.https://doi.org/10.3310/hta18070
  54. Coletti L, Battaglia V, De Simone P, Turturici L, Bartolozzi C, Filipponi F. Safety and feasibility of electrochemotherapy in patients with unresectable colorectal liver metastases: A pilot study. Int J Surg. 2017;44:26–32. doi:.https://doi.org/10.1016/j.ijsu.2017.06.033
  55. Dawson LA, Normolle D, Balter JM, McGinn CJ, Lawrence TS, Ten Haken RK. Analysis of radiation-induced liver disease using the Lyman NTCP model. Int J Radiat Oncol Biol Phys. 2002;53(4):810–21. Published online July 04, 2002. doi:.https://doi.org/10.1016/S0360-3016(02)02846-8
  56. Petrelli F, Comito T, Barni S, Pancera G, Scorsetti M, Ghidini A ; SBRT for CRC liver metastases. Stereotactic body radiotherapy for colorectal cancer liver metastases: A systematic review. Radiother Oncol. 2018;129(3):427–34. Published online July 13, 2018. doi:.https://doi.org/10.1016/j.radonc.2018.06.035
  57. Lee J, Shin IS, Yoon WS, Koom WS, Rim CH. Comparisons between radiofrequency ablation and stereotactic body radiotherapy for liver malignancies: Meta-analyses and a systematic review. Radiother Oncol. 2020;145:63–70. Published online January 11, 2020. doi:.https://doi.org/10.1016/j.radonc.2019.12.004
  58. Jackson WC, Tao Y, Mendiratta-Lala M, Bazzi L, Wahl DR, Schipper MJ, et al. Comparison of Stereotactic Body Radiation Therapy and Radiofrequency Ablation in the Treatment of Intrahepatic Metastases. Int J Radiat Oncol Biol Phys. 2018;100(4):950–8. doi:.https://doi.org/10.1016/j.ijrobp.2017.12.014
  59. Witt JS, Rosenberg SA, Bassetti MF. MRI-guided adaptive radiotherapy for liver tumours: visualising the future. Lancet Oncol. 2020;21(2):e74–82. Published online February 03, 2020. doi:.https://doi.org/10.1016/S1470-2045(20)30034-6
  60. Vilgrain V, Pereira H, Assenat E, Guiu B, Ilonca AD, Pageaux GP, et al.; SARAH Trial Group. Efficacy and safety of selective internal radiotherapy with yttrium-90 resin microspheres compared with sorafenib in locally advanced and inoperable hepatocellular carcinoma (SARAH): an open-label randomised controlled phase 3 trial. Lancet Oncol. 2017;18(12):1624–36. Published online November 07, 2017. doi:.https://doi.org/10.1016/S1470-2045(17)30683-6
  61. Morse MA, Hanks BA, Suhocki P, Doan PL, Liu EA, Frost P, et al. Improved time to progression for transarterial chemoembolization compared with transarterial embolization for patients with unresectable hepatocellular carcinoma. Clin Colorectal Cancer. 2012;11(3):185–90. Published online January 28, 2012. doi:.https://doi.org/10.1016/j.clcc.2011.11.003
  62. Wasan HS, Gibbs P, Sharma NK, Taieb J, Heinemann V, Ricke J, et al.; FOXFIRE trial investigators; SIRFLOX trial investigators; FOXFIRE-Global trial investigators. First-line selective internal radiotherapy plus chemotherapy versus chemotherapy alone in patients with liver metastases from colorectal cancer (FOXFIRE, SIRFLOX, and FOXFIRE-Global): a combined analysis of three multicentre, randomised, phase 3 trials. Lancet Oncol. 2017;18(9):1159–71. doi:.https://doi.org/10.1016/S1470-2045(17)30457-6
  63. Dutkowski P, De Rougemont O, Müllhaupt B, Clavien PA. Current and future trends in liver transplantation in Europe. Gastroenterology. 2010;138(3):802–9.e4. doi:.https://doi.org/10.1053/j.gastro.2010.01.030
  64. Starzl TE. The saga of liver replacement, with particular reference to the reciprocal influence of liver and kidney transplantation (1955-1967). J Am Coll Surg. 2002;195(5):587–610. doi:.https://doi.org/10.1016/S1072-7515(02)01498-9
  65. Gores GJ. Liver transplantation for malignant disease. Gastroenterol Clin North Am. 1993;22(2):285–99. Published online June 01, 1993.
  66. Penn I. Hepatic transplantation for primary and metastatic cancers of the liver. Surgery. 1991;110(4):726–34, discussion 734–5. Published online October 01, 1991.
  67. Moris D, Tsilimigras DI, Chakedis J, Beal EW, Felekouras E, Vernadakis S, et al. Liver transplantation for unresectable colorectal liver metastases: A systematic review. J Surg Oncol. 2017;116(3):288–97. doi:.https://doi.org/10.1002/jso.24671
  68. Hagness M, Foss A, Line PD, Scholz T, Jørgensen PF, Fosby B, et al. Liver transplantation for nonresectable liver metastases from colorectal cancer. Ann Surg. 2013;257(5):800–6. Published online January 31, 2013. doi:.https://doi.org/10.1097/SLA.0b013e3182823957
  69. Toso C, Pinto Marques H, Andres A, Castro Sousa F, Adam R, Kalil A, et al.; Compagnons Hépato-Biliaires Group. Liver transplantation for colorectal liver metastasis: Survival without recurrence can be achieved. Liver Transpl. 2017;23(8):1073–6. doi:.https://doi.org/10.1002/lt.24791

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