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  • Review Article
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Management of colorectal cancer presenting with synchronous liver metastases

Nature Reviews Clinical Oncology volume 11, pages 446–459 (2014)Cite this article

Subjects

Key Points

  • Up to a 20% of patients with colorectal cancer (CRC) present with synchronous hepatic metastases

  • In patients who present without intestinal obstruction or perforation, comprehensive whole-body imaging is required to exclude extrahepatic disease

  • Current evidence indicates a state of equipoise between several different management approaches for the treatment of CRC and synchronous liver metastatic disease, none of which has supportive randomized trial evidence

  • Neoadjuvant systemic chemotherapy is supported by current guidelines and can result in tumour downsizing, enabling some 'unresectable' liver metastases to be surgically removed

  • Surgery can take the form of the 'classic' approach (colorectal resection, then interval chemotherapy followed by liver resection), synchronous removal of liver and bowel tumours, or a liver-first approach

  • Clear superiority has not been demonstrated for any of these surgical interventions for CRC with synchronous liver metastases, although the mode of presentation can determine the approach used

Abstract

Up to a fifth of patients with colorectal cancer (CRC) present with synchronous hepatic metastases. In patients with CRC who present without intestinal obstruction or perforation and in whom comprehensive whole-body imaging confirms the absence of extrahepatic disease, evidence indicates a state of equipoise between several different management pathways, none of which has demonstrated superiority. Neoadjuvant systemic chemotherapy is advocated by current guidelines, but must be integrated with surgical management in order to remove the primary tumour and liver metastatic burden. Surgery for CRC with synchronous liver metastases can take a number of forms: the 'classic' approach, involving initial colorectal resection, interval chemotherapy and liver resection as the final step; simultaneous removal of the liver and bowel tumours with neoadjuvant or adjuvant chemotherapy; or a 'liver-first' approach (before or after systemic chemotherapy) with removal of the colorectal tumour as the final procedure. In patients with rectal primary tumours, the liver-first approach can potentially avoid rectal surgery in patients with a complete response to chemoradiotherapy. We overview the importance of precise nomenclature, the influence of clinical presentation on treatment options, and the need for accurate, up-to-date surgical terminology, staging tests and contemporary management options in CRC and synchronous hepatic metastatic disease, with an emphasis on multidisciplinary care.

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Figure 1: Segments of the human liver and current surgical nomenclature of liver sections.
Figure 2: Current terminology for major liver resections illustrating sections and segments removed at each procedure.
Figure 3: Flowchart outlining the management of CRC with synchronous liver metastases (modified based on ESMO guidelines).8

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References

  1. Department of Health and Human Services, Centers for Disease Control and Prevention, National Program of Cancer Registries (NPCR). United States Cancer Statistics (USCS): 1999–2010 Cancer Incidence and Mortality Data [online], (2014).

  2. Ferlay, J. et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur. J. Cancer 49, 1374–1403 (2013).

    CAS  PubMed  Google Scholar 

  3. Leporrier, J. et al. A population-based study of the incidence, management and prognosis of hepatic metastases from colorectal cancer. Br. J. Surg. 93, 465–474 (2006).

    Article  CAS  PubMed  Google Scholar 

  4. Manfredi, S. et al. Epidemiology and management of colorectal liver metastases. Ann. Surg. 244, 254–259 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Cancer Research UK. Statistics and outlook for bowel cancer [online], (2013).

  6. Tomlinson, J. S. et al. Actual 10-year survival after resection of colorectal liver metastases defines cure. J. Clin. Oncol. 25, 4575–4580 (2007).

    Article  PubMed  Google Scholar 

  7. Jain, V. K., Hawkes, E. A. & Cunningham, D. Integration of biologic agents with cytotoxic chemotherapy in metastatic colorectal cancer. Clin. Colorectal Cancer 10, 245–257 (2011).

    Article  CAS  PubMed  Google Scholar 

  8. Schmoll, H. J. et al. ESMO consensus guidelines for management of patients with colon and rectal cancer. A personalized approach to clinical decision making. Ann. Oncol. 23, 2479–2516 (2012).

    Article  CAS  PubMed  Google Scholar 

  9. Bismuth, H., Castaing, D. & Traynor, O. Surgery for synchronous hepatic metastases of colorectal cancer. Scand. J. Gastroenterol. 149, 144–149 (1988).

    Article  CAS  Google Scholar 

  10. Fong, Y. et al. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann. Surg. 230, 309–318 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. National Institute for Health and Care Excellence. Colorectal Cancer: The diagnosis and management of colorectal cancer: NICE clinical guideline 131 [online], (2011).

  12. Brouquet, A. et al. Surgical strategies for synchronous colorectal liver metastases in 156 consecutive patients: classic, combined or reverse strategy? J. Am. Col. Surg. 210, 934–941 (2010).

    Article  Google Scholar 

  13. Adam, R., Lucidi, V. & Bismuth, H. Hepatic colorectal metastases: methods of improving resectability. Surg. Clin. North Am. 84, 659–671 (2004).

    Article  PubMed  Google Scholar 

  14. de Haas, R. J. et al. Comparison of simultaneous or delayed liver surgery for limited synchronous colorectal liver metastases. Br. J. Surg. 97, 1279–1289 (2010).

    Article  CAS  PubMed  Google Scholar 

  15. Hillingsø, J. G. & Wille-Jørgensen, P. Staged or simultaneous resection of synchronous liver metastases from colorectal cancer—a systematic review. Colorectal Dis. 11, 3–10 (2008).

    Article  PubMed  Google Scholar 

  16. Jegatheeswaran, S., Mason, J. M., Hancock, H. & Siriwardena, A. K. The liver-first approach to the management of colorectal cancer with synchronous hepatic metastases. JAMA Surg. 148, 385–391 (2013).

    Article  CAS  PubMed  Google Scholar 

  17. Mentha, G. et al. Neoadjuvant chemotherapy and resection of advanced synchronous liver metastases before the treatment of colorectal primary. Br. J. Surg. 93, 872–878 (2006).

    Article  CAS  PubMed  Google Scholar 

  18. Akilu, M. & Eng, C. The current landscape of locally advanced rectal cancer. Nat. Rev. Clin. Oncol. 8, 649–659 (2011).

    Article  CAS  Google Scholar 

  19. Sagar, J. Colorectal stents for the management of malignant colonic obstructions. Cochrane Database Systemic Reviews, Issue 11. Art. No.: CD007378 http://dx.doi.10.1002/14651858.CD007378.pub2 (2011).

    Google Scholar 

  20. de Jong, M. C. et al. The liver-first approach for synchronous colorectal liver metastasis: a 5-year single-centre experience. HPB (Oxford) 13, 745–752 (2011).

    Article  Google Scholar 

  21. O'Neill, B. D., Brown, G., Heald, R. J., Cunningham, D. & Tait, D. M. Non-operative treatment after neoadjuvant chemotherapy for rectal cancer. Lancet Oncol. 7, 625–633 (2007).

    Article  Google Scholar 

  22. Slesser, A. A. et al. A meta-analysis comparing simultaneous versus delayed resections in patients with synchronous colorectal liver metastases. Surg. Oncol. 22, 36–47 (2013).

    Article  CAS  PubMed  Google Scholar 

  23. Swan, P. J., Welsh, F. K., Chandrakumaran, K. & Rees, M. Long-term survival following delayed presentation and resection of colorectal liver metastases. Br. J. Surg. 98, 1309–1317 (2011).

    Article  CAS  PubMed  Google Scholar 

  24. Edge, S. B. et al. AJCC cancer staging manual 7th edn (Springer, 2010).

    Google Scholar 

  25. Mekenkamp, L. J. et al. Clinicopathological features and outcome in advanced colorectal cancer patients with synchronous vs. metachronous metastases. Br. J. Cancer 103, 159–164 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sethi, N. & Kang, Y. Unravelling the complexity of metastasis—molecular understanding and targeted therapies. Nat. Rev. Cancer 11, 735–748 (2011).

    Article  CAS  PubMed  Google Scholar 

  27. van der Wal, G. et al. Angiogenesis in synchronous and metachronous colorectal liver metastases. The liver as permissive soil. Ann. Surg. 255, 86–94 (2012).

    Article  PubMed  Google Scholar 

  28. Wikman, H., Vessella, R. & Pantel, K. Cancer micrometastasis and tumour dormancy. APMIS 116, 754–770 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. Chambers, A. F., Groom, A. C. & MacDonald, I. C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2, 563–572 (2002).

    Article  CAS  PubMed  Google Scholar 

  30. Hammoud, M. A., McCutcheon, I. E., Elsouki, R., Schoppa, D. & Patt, Y. Z. Colorectal carcinoma and brain metastases: distribution, treatment and survival. Ann. Surg. Oncol. 3, 453–463 (1996).

    Article  CAS  PubMed  Google Scholar 

  31. Karoui, M. et al. Stents for palliation of obstructive metastatic colon cancer. Arch. Surg. 142, 619–623 (2007).

    Article  PubMed  Google Scholar 

  32. Zhang, S., Gao, F., Luo, J. & Yang, J. Prognostic factors in survival of colorectal cancer patients with synchronous liver metastasis. Colorectal Dis. 12, 754–761 (2010).

    Article  CAS  PubMed  Google Scholar 

  33. Cirocchi, R. et al. Safety and efficacy of endoscopic colonic stenting as a bridge to surgery in the management of intestinal obstruction due to left colon and rectal cancer: a systematic review and meta-analysis. Surg. Oncol. 22, 14–21 (2013).

    Article  PubMed  Google Scholar 

  34. Amri, R., Bordeianou, L. G., Sylla, P. & Berger, D. L. Impact of screening colonoscopy on outcomes in colon cancer surgery. JAMA Surg. 148, 747–754 (2013).

    Article  PubMed  Google Scholar 

  35. Steele, R. J. et al. Results from the first three rounds of the Scottish demonstration pilot of FOBT screening for colorectal cancer. Gut 58, 530–535 (2009).

    Article  CAS  PubMed  Google Scholar 

  36. Logan, F. A. et al. Outcomes of the Bowel Cancer Screening Programme (BCSP) in England after the first 1 million tests. Gut 61, 1439–1446 (2012).

    Article  PubMed  Google Scholar 

  37. NICE, National Institute for Health and Clinical Excellence. NICE clinical guidelines 104: Metastatic malignant disease of unknown primary origin: Diagnosis and management of metastatic malignant disease of unknown primary origin [online], (2010).

  38. Hemminki, K., Riihimäki, M., Sundquist, K. & Hemminki, A. Site-specific survival rates for cancer of unknown primary according to location of metastases. Int. J. Cancer 133, 182–189 (2013).

    Article  CAS  PubMed  Google Scholar 

  39. Macmillan Cancer Support. About cancer of unknown primary [online], (2011).

  40. Collins, R. et al. Emergency Surgery: Standards for unscheduled care (Royal College of Surgeons of England, 2011).

    Google Scholar 

  41. Ghazi, S. et al. Clinicopathological analysis of colorectal cancer: a comparison between emergency and elective surgical cases. World J. Surg. Oncol. 11, 133–144 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Seah, D. W., Ibrahim, S. & Tay, K. H. Hartmann procedure: is it still relevant today? ANZ J. Surg. 75, 436–440 (2005).

    Article  PubMed  Google Scholar 

  43. Meyer, F. et al. Emergency operation in carcinomas of the left colon: value of Hartmann's procedure. Tech. Coloproctol. 8 (Suppl. 1), S226–S229 (2004).

    Article  PubMed  Google Scholar 

  44. Ansaloni, L. et al. Guidelines in the management of obstructing cancer of the left colon: consensus conference of the world society of emergency surgery (WSES) and peritoneum and surgery (PnS) society. World J. Emerg. Surg. 5, 29–39 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Tan, C. J., Dasari, B. V. & Gardiner, K. Systematic review and meta-analysis of randomized clinical trials of self-expanding metallic stents as a bridge to surgery versus emergency surgery for malignant left-sided large bowel obstruction. Br. J. Surg. 99, 469–476 (2012).

    Article  CAS  PubMed  Google Scholar 

  46. Hill, J. Stenting and colorectal cancer. Br. J. Surg. 95, 1195–1196 (2008).

    Article  CAS  PubMed  Google Scholar 

  47. Fowler, K. J., Linehan, D. C. & Menias, C. O. Colorectal liver metastases: state of the art imaging. Ann. Surg. Oncol. 20, 1185–1193 (2013).

    Article  PubMed  Google Scholar 

  48. National Comprehensive Cancer Network Oncologic Guidelines. Colon cancer [online], (2013).

  49. Berger-Kulemann, V. et al. Gadoxetic acid-enhanced 3.0T MR imaging versus multidetector-row CT in the detection of colorectal metastases in fatty liver using intraoperative ultrasound and histopathology as a standard of reference. Eur. J. Surg. Oncol. 38, 670–676 (2012).

    Article  CAS  PubMed  Google Scholar 

  50. Kulemann, V. et al. Preoperative detection of colorectal liver metastases in fatty liver: MDCT or MRI? Eur. J. Radiol. 79, e1–e6 (2011).

    Article  PubMed  Google Scholar 

  51. Kong, G. et al. The use of 18F-FDG PET/CT in colorectal liver metastases-comparison with CT and liver MRI. Eur. J. Nucl. Med. Mol. Imaging 35, 1323–1329 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. Scharitzer, M. et al. Preoperative evaluation of colorectal liver metastases: comparison between gadoxetic acid-enhanced 3.0-T MRI and contrast-enhanced MDCT with histopathological correlation. Eur. Radiol. 23, 2187–2196 (2013).

    Article  CAS  PubMed  Google Scholar 

  53. Akay, S., Kocaoglu, M., Emer, O., Battal, B. & Arslan, N. Diagnostic accuracy of whole-body diffusion-weighted magnetic resonance imaging with 3.0T in detection of primary and metastatic neoplasms. J. Med. Imaging Radiat. Oncol. 57, 274–282 (2013).

    Article  PubMed  Google Scholar 

  54. Marckmann, P. et al. Nephrogenic systemic fibrosis: suspected causative role of gadodiamide used for contrast-enhanced magnetic resonance imaging. J. Am. Soc. Nephrol. 17, 2359–2362 (2006).

    Article  PubMed  Google Scholar 

  55. Royal College of Radiologists. Evidence-based indications for the use of PET-CT in the United Kingdom 2012 [online], (2012).

  56. Pawlik, T. et al. Trends in nontherapeutic laparotomy rates in patients undergoing surgical therapy for hepatic colorectal metastases. Ann. Surg. Oncol. 16, 371–378 (2009).

    Article  PubMed  Google Scholar 

  57. Adams, R. B. et al. Selection for hepatic resection of colorectal liver metastases: expert consensus statement. HPB (Oxford) 15, 91–103 (2013).

    Article  PubMed Central  Google Scholar 

  58. The Royal College of Radiologists. Ultrasound training recommendations for medical and surgical specialties 2nd edn [online], (2012).

  59. Westwood, M. et al. Contrast-enhanced ultrasound using SonoVue® (sulphur hexafluoride microbubbles) compared with contrast-enhanced computed tomography and contrast-enhanced magnetic resonance imaging for the characterisation of focal liver lesions and detection of liver metastases: a systematic review and cost-effectiveness analysis. Health Technol. Assess. 17, 1–243 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Gozzetti, G., Mazziotti, A. & Jovine, E. Intraoperative ultrasound—diagnostic aspects in liver surgery in Surgery of the Liver and Biliary Tract 2nd edn (ed. Blumgart, L. H.) 451–458 (Churchill Livingstone, 1994).

    Google Scholar 

  61. Mazzoni, G. et al. Intra-operative ultrasound for detection of liver metastases from colorectal cancer. Liver Int. 1, 88–94 (2008).

    Google Scholar 

  62. Garden, O. J. et al. Guidelines for resection of colorectal cancer liver metastases. Gut 55 (Suppl. 3), iii1–iii8 (2006).

    PubMed  PubMed Central  Google Scholar 

  63. Sorbye, H. et al. Predictive factors for the benefit of perioperative FOLFOX for resectable liver metastasis in colorectal cancer patients (EORTC Intergroup Trial 40983). Ann. Surg. 255, 534–539 (2012).

    Article  PubMed  Google Scholar 

  64. Garcea, G. et al. Improving the diagnostic yield from staging laparoscopy for periampullary malignancies: the value of preoperative inflammatory markers and radiological tumor size. Pancreas 41, 233–237 (2012).

    Article  PubMed  Google Scholar 

  65. Coburn, N. et al. Optimal management of gastric cancer: results from an international RAND/UCLA expert panel. Ann. Surg. 259, 102–108 (2014).

    Article  PubMed  Google Scholar 

  66. Dunne, D. F. et al. Routine staging laparoscopy has no place in the management of colorectal liver metastases. Eur. J. Surg. Oncol. 39, 721–725 (2013).

    Article  CAS  PubMed  Google Scholar 

  67. Bipat, S. et al. Evidence-base guideline on management of colorectal liver metastases in the Netherlands. Neth. J. Med. 65, 5–14 (2007).

    CAS  PubMed  Google Scholar 

  68. Czoski-Murray, C. et al. What is the value of routinely testing full blood count, electrolytes and urea, and pulmonary function tests before elective surgery in patients with no apparent clinical indication and in subgroups of patients with common comorbidities: a systematic review of the clinical and cost-effective literature? Health Technol. Assess. 50, 1–159 (2012).

    Google Scholar 

  69. Pannell, L. M., Reyes, E. M. & Underwood, S. R. Cardiac risk assessment before non-cardiac surgery. Eur. Heart J. Cardiovasc. Imaging 4, 316–322 (2013).

    Article  Google Scholar 

  70. Asli, I. et al. The utility and prognostic value of dipyridamole technetium-99m sestamibi myocardial perfusion imaging SPECT in predicting perioperative cardiac events following non-cardiac surgery. Perfusion 4, 333–339 (2013).

    Article  Google Scholar 

  71. Junejo, M. et al. Cardiopulmonary exercise testing for preoperative risk assessment before hepatic resection. Br. J. Surg. 99, 1097–1104 (2012).

    Article  CAS  PubMed  Google Scholar 

  72. Vauthey, J. N. et al. Chemotherapy regimen predicts steatohepatitis and an increase in 90-day mortality after surgery for hepatic colorectal metastases. J. Clin. Oncol. 13, 2065–2072 (2006).

    Article  CAS  Google Scholar 

  73. Zorzi, D. et al. Chemotherapy-associated hepatotoxicity and surgery for colorectal liver metastases. Br. J. Surg. 3, 274–286 (2007).

    Article  CAS  Google Scholar 

  74. Schwarz, R. E., Abdalla, E. K., Aloia, T. A. & Vauthey, J. N. AHPBA/SSO/SSAT sponsored consensus conference on the multidisciplinary treatment of colorectal cancer metastases. HPB (Oxford) 2, 89–90 (2013).

    Article  Google Scholar 

  75. Belghiti, J. et al. The Brisbane 2000 terminology of liver anatomy and resections. HPB (Oxford) 2, 333–339 (2000).

    Article  Google Scholar 

  76. Sigurdsson, H. K. et al. Palliative surgery for rectal cancer in a national cohort. Colorectal Dis. 4, 336–343 (2008).

    Article  Google Scholar 

  77. Kobayashi, H. et al. Clinical benefit of surgery for stage IV colorectal cancer with synchronous peritoneal metastases. J. Gastroenterol. 49, 646–654 (2014).

    Article  PubMed  Google Scholar 

  78. Elias, D. M. & Ouellet, J. F. Incidence, distribution and significance of hilar lymph node metastases in hepatic colorectal metastases. Surg. Oncol. Clin. N. Am. 1, 221–229 (2003).

    Article  Google Scholar 

  79. Treasure, T. & Utley, M. Surgical removal of asymptomatic pulmonary metastases: time for better evidence. BMJ 346, 824 (2013).

    Article  Google Scholar 

  80. Limmer, S. et al. Sequential surgical resection of hepatic and pulmonary metastases from colorectal cancer. Langenbecks Arch. Surg. 395, 1128–1138 (2010).

    Article  Google Scholar 

  81. Embún, R. et al. Pulmonary metastasectomy in colorectal cancer: a prospective study of demography and clinical characteristics of 543 patients in the Spanish colorectal metastasectomy registry (GECMP-CCR). BMJ Open 3, 1–12 (2013).

    Article  Google Scholar 

  82. Jegatheeswaran, S., Satyadas, T., Sheen, A. J., Treasure, T. & Siriwardena, A. K. Thoracic surgical management of colorectal lung metastases: a questionnaire survey of members of the Society for Cardiothoracic Surgery in Great Britain and Ireland. Ann. R. Coll. Surg. Engl. 95, 140–143 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Treasure, T., Fallowfield, L., Lees, B. & Farewell, V. Pulmonary metastasectomy in colorectal cancer. Thorax 67, 185–187 (2012).

    Article  PubMed  Google Scholar 

  84. Pathak, S., Sarno, G., Nunes, Q. & Poston, G. J. Synchronous resection for colorectal liver metastases: the future. Eur. J. Surg. Oncol. 11, 1044–1046 (2010).

    Article  Google Scholar 

  85. Spampinato, M. G., Mandalá, L., Quarta, G., Del Medico, P. & Baldazzi, G. One-stage, totally laparoscopic major hepatectomy and colectomy for colorectal neoplasm with synchronous liver metastasis: safety, feasibility and outcome. Surgery 6, 861–865 (2013).

    Article  Google Scholar 

  86. Nordlinger, B. et al. 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 371, 1007–1016 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Nordlinger, B. et al. 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. 14, 1208–1215 (2013).

    Article  CAS  PubMed  Google Scholar 

  88. Chua, T. C., Saxena, A., Liauw, W., Kokandi, A. & Morris, D. L. Systematic review of randomized and nonrandomized trials of the clinical response and outcomes of neoadjuvant systemic chemotherapy for resectable colorectal liver metastases. Ann. Surg. Oncol. 2, 492–501 (2010).

    Article  Google Scholar 

  89. Primrose, J. N. et al. A randomized clinical trial of chemotherapy compared to chemotherapy in combination with cetuximab in k-RAS wild-type patients with operable metastases from colorectal cancer [abstract]. J. Clin. Oncol. 31 (Suppl.), a3504 (2013).

    Google Scholar 

  90. Van Cutsem, E. et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N. Engl. J. Med. 360, 1408–1417 (2009).

    Article  CAS  PubMed  Google Scholar 

  91. Normanno, N. et al. Implications for KRAS status and EGFR-targeted therapies in metastatic CRC. Nat. Rev. Clin. Oncol. 9, 519–527 (2009).

    Article  CAS  Google Scholar 

  92. Adam, R. et al. Rescue surgery for unresectable colorectal liver metastases downstaged by chemotherapy: a model to predict long-term survival. Ann. Surg. 4, 644–657 (2004).

    Google Scholar 

  93. Petrelli, F. et al. FOLFIRI-bevacizumab as first-line chemotherapy in 3,500 patients with advanced colorectal cancer: a pooled analysis of 29 published trials. Clin. Colorectal Cancer 12, 145–151 (2013).

    Article  CAS  PubMed  Google Scholar 

  94. Kishi, Y. et al. Extended preoperative chemotherapy does not improve pathologic response and increases postoperative liver insufficiency after hepatic resection for colorectal liver metastases. Ann. Surg. Oncol. 11, 2870–2876 (2010).

    Article  Google Scholar 

  95. Folprecht, G. et al. Tumour response and secondary resectability of colorectal liver metastases following neoadjuvant chemotherapy with cetuximab: the CELIM randomised phase 2 trial. Lancet Oncol. 11, 38–47 (2010).

    Article  CAS  PubMed  Google Scholar 

  96. Bischof, D. A., Clary, B. M., Maithel, S. K. & Pawlik, T. M. Surgical management of disappearing colorectal liver metastases. Br. J. Surg. 100, 1414–1420 (2013).

    Article  CAS  PubMed  Google Scholar 

  97. Hamady, Z. Z. et al. One-millimeter cancer-free margin is curative for colorectal liver metastases: a propensity score case-match approach. Ann. Surg. 259, 543–548 (2014).

    Article  PubMed  Google Scholar 

  98. Sarpel, U. et al. Does anatomic versus nonanatomic resection affect recurrence and survival in patients undergoing surgery for colorectal liver metastasis? Ann. Surg. Oncol. 2, 379–384 (2009).

    Article  Google Scholar 

  99. Kulik, U., Bektas, H., Klempnauer, J. & Lehner, E. Repeat liver resection for colorectal metastases. Br. J. Surg. 7, 926–932 (2013).

    Article  Google Scholar 

  100. Morris-Stiff, G., Gomez, D. & Prasad, R. Quantitative assessment of hepatic function and its relevance to the liver surgeon. J. Gastrointest. Surg. 2, 374–385 (2009).

    Article  Google Scholar 

  101. Fung, J. et al. Use of liver stiffness measurement for liver resection surgery: correlation with indocyanine green clearance testing and post-operative outcome. PLoS ONE 28, e72306 (2013).

    Article  CAS  Google Scholar 

  102. Wakiya, T. et al. Evaluation of the usefulness of the indocyanine green clearance test for chemotherapy-associated liver injury in patients with colorectal cancer liver metastasis. Ann. Surg. Oncol. 21, 167–172 (2014).

    Article  PubMed  Google Scholar 

  103. Ulla, M. et al. New surgical strategy to induce liver hypertrophy: role of MDCT-volumetry to monitor and predict liver growth. Hepatogastroenterology 122, 337–342 (2013).

    Google Scholar 

  104. Broquet, A., Andreou, A., Shindo, J. & Vauthey, J. N. Methods to improve resectability in hepatocellular carcinoma. Recent Results Cancer Res. 190, 57–67 (2013).

    Article  Google Scholar 

  105. Jamdar, S., Sheen, A. J. & Siriwardena, A. K. Colorectal liver metastases in Contemporary Coloproctology (eds Brown S. R. et al.) 201–213 (Springer-Verlag, 2012).

    Chapter  Google Scholar 

  106. Shindoh, J. et al. Kinetic growth rate after portal vein embolization predicts posthepatectomy outcomes: towards zero liver-related mortality in patients with colorectal liver metastases and small future liver remnant. J. Am. Coll. Surg. 2, 201–209 (2013).

    Article  Google Scholar 

  107. Hoekstra, L. T. et al. Tumor progression after preoperative portal vein embolization. Ann. Surg. 5, 812–817 (2012).

    Article  Google Scholar 

  108. Schnitzbauer, A. A. et al. Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling two-staged extended right hepatic resection in small-for-size settings. Ann. Surg. 255, 405–414 (2012).

    Article  PubMed  Google Scholar 

  109. Lam, V. W. et al. A systematic review of two-stage hepatectomy in patients with initially unresectable colorectal liver metastases. HPB (Oxford) 7, 483–491 (2013).

    Article  Google Scholar 

  110. Karoui, M. et al. Combined first-stage hepatectomy and colorectal resection in a two-stage hepatectomy strategy for bilobar synchronous liver metastases. Br. J. Surg. 97, 1354–1362 (2010).

    Article  CAS  PubMed  Google Scholar 

  111. Abdalla, E. K. et al. Locoregional surgical and interventional therapies for advanced colorectal cancer liver metastases: expert consensus statements. HPB (Oxford) 15, 119–130 (2013).

    Article  Google Scholar 

  112. Decadt, B. & Siriwardena, A. K. Radiofrequency ablation of liver tumours: a systematic review. Lancet Oncol. 5, 550–560 (2004).

    Article  PubMed  Google Scholar 

  113. Lloyd, D. M. et al. International multicentre prospective study on microwave ablation of liver tumours: preliminary results. HPB (Oxford) 13, 579–585 (2011).

    Article  Google Scholar 

  114. Aksoy, E. et al. Clinical scenarios associated with local recurrence after laparoscopic radiofrequency thermal ablation of colorectal liver metastases. Surgery 154, 748–752 (2013).

    Article  PubMed  Google Scholar 

  115. Scheele, J., Stangl, R., Altendorf-Hofmann, A. & Gall, F. P. Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery 110, 13–29 (1991).

    CAS  PubMed  Google Scholar 

  116. Elias, D., Detroz, B., Lasser, P., Plaud, B. & Jerbi, G. Is simultaneous hepatectomy and intestinal anastomosis safe? Am. J. Surg. 169, 254–260 (1995).

    Article  CAS  PubMed  Google Scholar 

  117. Nordlinger, B. et al. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1,568 patients. Association Française de Chirurgie. Cancer 77, 1254–1262 (1996).

    Article  CAS  PubMed  Google Scholar 

  118. Martin, R. et al. Simultaneous liver and colorectal resections are safe for synchronous colorectal liver metastasis. J. Am. Coll. Surg. 197, 233–242 (2003).

    Article  PubMed  Google Scholar 

  119. Weber, J. C., Bachellier, P., Oussoultzoglou, E. & Jaeck, D. Simultaneous resection of colorectal primary tumour and synchronous liver metastases. Br. J. Surg. 90, 956–962 (2003).

    Article  CAS  PubMed  Google Scholar 

  120. Chua, H. K. et al. Concurrent vs. staged colectomy and hepatectomy for primary colorectal cancer with synchronous hepatic metastases. Dis. Colon Rectum 47, 1310–1316 (2004).

    Article  PubMed  Google Scholar 

  121. Capussotti, L. et al. Major liver resections synchronous with colorectal surgery. Ann. Surg. Oncol. 14, 195–201 (2006).

    Article  Google Scholar 

  122. Reddy, S. K. et al. Simultaneous resections of colorectal cancer and synchronous liver metastases: a multi-institutional analysis. Ann. Surg. Oncol. 14, 3481–3491 (2007).

    Article  PubMed  Google Scholar 

  123. Vassiliou, I. et al. Surgical approaches of resectable synchronous colorectal liver metastases: timing considerations. World J. Gastroenterol. 13, 1431–1434 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Thelen, A. et al. Simultaneous versus staged liver resection of synchronous liver metastases from colorectal cancer. Int. J. Colorectal Dis. 22, 1269–1276 (2007).

    Article  PubMed  Google Scholar 

  125. Turrini, O. et al. Strategies for the treatment of synchronous liver metastasis. Eur. J. Surg. Oncol. 33, 735–740 (2007).

    Article  CAS  PubMed  Google Scholar 

  126. Yan, T. D., Chu, F., Black, D., King, D. W. & Morris, D. L. Synchronous resection of colorectal primary cancer and liver metastases. World J. Surg. 31, 1496–1501 (2007).

    Article  PubMed  Google Scholar 

  127. Slupski, M., Wlodarczyk, Z., Jasinski, M., Masztalerz, M. & Tujakowsk, I. J. Outcomes of simultaneous and delayed resections of synchronous colorectal liver metastases. Can. J. Surg. 52, E241–E244 (2009).

    PubMed  PubMed Central  Google Scholar 

  128. Luo, Y. et al. Simultaneous liver and colorectal resections are safe for synchronous colorectal liver metastases. J. Gastrointest. Surg. 14, 1974–1980 (2010).

    Article  PubMed  Google Scholar 

  129. Kaibori, M. et al. Timing of resection for synchronous liver metastases from colorectal cancer. Dig. Dis. Sci. 55, 3262–3270 (2010).

    Article  PubMed  Google Scholar 

  130. Broquet, A. et al. Surgical strategies for synchronous colorectal liver metastases in 156 consecutive patients: classic, combined or reverse strategy? J. Am. Coll. Surg. 210, 934–941 (2010).

    Article  Google Scholar 

  131. Mentha, G. et al. 'Liver first' approach in the treatment of colorectal cancer with synchronous liver metastases. Dig. Surg. 25, 430–435 (2008).

    Article  PubMed  Google Scholar 

  132. Mentha, G. et al. Treatment strategies for the management of advanced colorectal liver metastases detected synchronously with the primary tumour. Eur. J. Surg. Oncol. 33, S76–S83 (2007).

    Article  PubMed  Google Scholar 

  133. Adam, R. et al. The oncosurgery approach to managing liver metastases from colorectal cancer: a multidisciplinary international consensus. Oncologist 17, 1225–1239 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Hepatobiliary Surgery Unit, Manchester Biomedical Research Centre and NIHR Greater Manchester Research Network, Manchester Royal Infirmary, Oxford Road, Manchester, M13 9WL, UK

    Ajith K. Siriwardena & Santhalingam Jegatheeswaran

  2. Durham Clinical Trials Unit, School of Medicine, Pharmacy and Health, Wolfson Research Institute, Durham University Queen's Campus, University Boulevard, Stockton-on-Tees, TS17 6BH, UK

    James M. Mason & Helen C. Hancock

  3. Department of Medical Oncology, Christie Hospital, Wilmslow Road, Manchester, M20 4BX, UK

    Saifee Mullamitha

Authors
  1. Ajith K. Siriwardena
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  2. James M. Mason
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  3. Saifee Mullamitha
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  4. Helen C. Hancock
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  5. Santhalingam Jegatheeswaran
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Contributions

A.K.S. and S.J. researched the data for the article, and A.K.S., J.M.M., S.M. and S.J. substantially contributed to discussion of content. A.K.S., J.M.M., S.M. and H.C.H. wrote the article, and all authors reviewed/edited the manuscript before submission.

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Correspondence to Ajith K. Siriwardena.

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Siriwardena, A., Mason, J., Mullamitha, S. et al. Management of colorectal cancer presenting with synchronous liver metastases. Nat Rev Clin Oncol 11, 446–459 (2014). https://doi.org/10.1038/nrclinonc.2014.90

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