World Journal of Surgery

, Volume 37, Issue 6, pp 1315–1321 | Cite as

Outcomes After Hepatic and Pulmonary Metastasectomies Compared With Pulmonary Metastasectomy Alone in Patients With Colorectal Cancer Metastasis to Liver and Lungs

  • Norifumi HattoriEmail author
  • Yukihide Kanemitsu
  • Koji Komori
  • Yasuhiro Shimizu
  • Tsuyoshi Sano
  • Yoshiki Senda
  • Tetsuya Mitsudomi
  • Takayuki Fukui



Surgical resection is the most effective treatment for colorectal cancer that has metastasized to the liver. Similarly, surgical resection improves survival for selected patients with pulmonary colorectal metastases. However, the indication for pulmonary metastasectomy is not clear in patients with both hepatic and pulmonary colorectal metastases. Therefore, we evaluated outcomes after pulmonary resection of colorectal metastases in patients with or without a history of curative hepatic metastasectomy.


We retrospectively analyzed 96 patients who underwent pulmonary metastasectomy from March 1999 to November 2009. Patients were grouped according to treatment: resection of pulmonary metastases alone (lung metastasectomy group) or resection of both hepatic and pulmonary metastases (liver and lung metastasectomy group). Overall survival (OS) and disease-free survival (DFS) were evaluated by Kaplan–Meier analysis. Survival curves were compared using the log-rank test.


The 5-year OS for all patients was 61.3 %, and the 5-year DFS was 26.7 %. Group comparisons showed that the 5-year OS of the lung metastasectomy group was significantly better than that of the liver and lung metastasectomy group (69 vs. 43 %; p = 0.030). However, the 5-year DFS rates of the lung metastasectomy group (25.8 %) and liver and lung metastasectomy group (28.0 %) did not differ significantly. Recurrence was higher after resection of both hepatic and pulmonary metastases than after pulmonary metastases alone (79 vs. 45 %; p = 0.025).


Resection of pulmonary colorectal metastases may increase survival. However, the combination of liver and lung metastasectomies had a worse prognosis than pulmonary metastasectomy alone. In selected patients, combined liver and lung metastasectomy can be beneficial and result in acceptable DFS.


Pulmonary Metastasis Pulmonary Resection Regional Lymph Node Metastasis Pulmonary Metastasectomy Colorectal Cancer Metastasis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Conflict of interest



  1. 1.
    Sadahiro S, Suzuki T, Ishikawa K et al (2003) Recurrence patterns after curative resection of colorectal cancer in patients followed for a minimum of ten years. Hepatogastroenterology 50:1362–1366PubMedGoogle Scholar
  2. 2.
    Sugihara K, Hojo K, Moriya Y et al (1993) Pattern of recurrence after hepatic resection for colorectal metastases. Br J Surg 80:1032–1035PubMedCrossRefGoogle Scholar
  3. 3.
    Scheele J, Strangl R, Altendorf-Hoffman A (1990) Hepatic metastases from colorectal carcinoma: impact of surgical resection on the natural history. Br J Surg 77:1241–1246PubMedCrossRefGoogle Scholar
  4. 4.
    Goya T, Miyazawa N, Kondo H et al (1989) Surgical resection of pulmonary metastases from colorectal cancer: 10-year follow-up. Cancer 64:1418–1421PubMedCrossRefGoogle Scholar
  5. 5.
    McCormack PM, Burt ME, Bains MS et al (1992) Lung resection for colorectal metastases: 10-year results. Arch Surg 127:1403–1406PubMedCrossRefGoogle Scholar
  6. 6.
    Abdalla EK, Vauthey JN, Ellis LM et al (2004) Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 239:818–825PubMedCrossRefGoogle Scholar
  7. 7.
    Bradley AL, Chapman WC, Wright JK et al (1999) Surgical experience with hepatic colorectal metastasis. Am Surg 65:560–566PubMedGoogle Scholar
  8. 8.
    Doci R, Gennari L, Bignami P et al (1991) One hundred patients with hepatic metastases from colorectal cancer treated by resection: analysis of prognostic determinants. Br J Surg 78:797–801PubMedCrossRefGoogle Scholar
  9. 9.
    Fong Y, Fortner J, Sun RL et al (1999) Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 230:309–318PubMedCrossRefGoogle Scholar
  10. 10.
    Ohlsson B, Stenram U, Tranberg KG (1998) Resection of colorectal liver metastases: 25-year experience. World J Surg 22:268–276. doi: 10.1007/s002689900381 PubMedCrossRefGoogle Scholar
  11. 11.
    McAfee MK, Allen MS, Trastek VF et al (1992) Colorectal lung metastases: results of surgical excision. Ann Thorac Surg 53:780–785PubMedCrossRefGoogle Scholar
  12. 12.
    Saito Y, Omiya H, Kohno K et al (2002) Pulmonary metastatectomy for 165 patients with colorectal carcinoma: a prognostic assessment. J Thorac Cardiovasc Surg 124:1007–1013PubMedCrossRefGoogle Scholar
  13. 13.
    Pfannschmidt J, Muley T, Hoffmann H et al (2003) Prognostic factors and survival after complete resection of pulmonary metastases from colorectal carcinoma: experience in 167 patients. J Thorac Cardiovasc Surg 126:732–739PubMedCrossRefGoogle Scholar
  14. 14.
    Kanemitsu Y, Kato T, Hirai T et al (2004) Preoperative probability model for predicting overall survival after resection of pulmonary metastases from colorectal cancer. Br J Surg 91:112–120PubMedCrossRefGoogle Scholar
  15. 15.
    Iizasa T, Suzuki M, Yoshida S et al (2006) Prediction of prognosis and surgical indications for pulmonary metastasectomy from colorectal cancer. Ann Thorac Surg 82:254–260PubMedCrossRefGoogle Scholar
  16. 16.
    Rama N, Monteiro A, Bernardo JE et al (2009) Lung metastases from colorectal cancer: surgical resection and prognostic factors. Eur J Cardiothorac Surg 35:444–449PubMedCrossRefGoogle Scholar
  17. 17.
    Kanemitsu Y, Kato T, Komori K et al (2010) Validation of a nomogram for predicting overall survival after resection of pulmonary metastases from colorectal cancer at a single center. World J Surg 34:2973–2978. doi: 10.1007/s00268-010-0745-4 PubMedCrossRefGoogle Scholar
  18. 18.
    Ambiru S, Miyazaki M, Ito H et al (1998) Resection of hepatic and pulmonary metastases in patients with colorectal carcinoma. Cancer 82:274–278PubMedCrossRefGoogle Scholar
  19. 19.
    Shah SA, Haddad R, Al-Sukhni W et al (2006) Surgical resection of hepatic and pulmonary metastases from colorectal carcinoma. J Am Coll Surg 202:468–475PubMedCrossRefGoogle Scholar
  20. 20.
    Ike H, Shimada H, Togo S et al (2002) Sequential resection of lung metastasis following partial hepatectomy for colorectal cancer. Br J Surg 89:1164–1168PubMedCrossRefGoogle Scholar
  21. 21.
    Shimizu Y, Yasui K, Sano T et al (2008) Validity of observation interval for synchronous hepatic metastases of colorectal cancer: changes in hepatic and extrahepatic metastatic foci. Langenbecks Arch Surg 393:181–184PubMedCrossRefGoogle Scholar
  22. 22.
    Scheithauer W, Rosen H, Kornek GV et al (1993) Randomised comparison of combination chemotherapy plus supportive care with supportive care alone in patients with metastatic colorectal cancer. BMJ 306:752–755PubMedCrossRefGoogle Scholar
  23. 23.
    Murata S, Moriya Y, Akasu T et al (1998) Resection of both hepatic and pulmonary metastases in patients with colorectal cancer. Cancer 83:1086–1093PubMedCrossRefGoogle Scholar
  24. 24.
    Nordlinger B, Guiget M, Vaillant JC et al (1996) Surgical resection of colorectal carcinoma metastases to the liver: a prognostic scoring system to improve case selection, based on 1568 patients. Cancer 77:1254–1262PubMedCrossRefGoogle Scholar
  25. 25.
    Taylor M, Forster J, Langer B et al (1997) A study of prognostic factors for hepatic resection for colorectal metastases. Am J Surg 173:467–471PubMedCrossRefGoogle Scholar
  26. 26.
    Choti MA, Sitzmann JV, Tiburi MF et al (2002) Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg 235:759–766PubMedCrossRefGoogle Scholar
  27. 27.
    Turk PS, Wanebo HJ (1993) Results of surgical treatment of nonhepatic recurrence of colorectal carcinoma. Cancer 71:4267–4277PubMedCrossRefGoogle Scholar
  28. 28.
    Okumura S, Kondo H, Tsuboi M et al (1996) Pulmonary resection for metastatic colorectal cancer: experiences with 159 patients. J Thorac Cardiovasc Surg 112:867–874PubMedCrossRefGoogle Scholar
  29. 29.
    Koga R, Yamamoto J, Saiura A et al (2006) Surgical resection of pulmonary metastases from colorectal cancer: four favourable prognostic factors. Jpn J Clin Oncol 36:643–648PubMedCrossRefGoogle Scholar
  30. 30.
    Regnard JF, Grunenwald D, Spaggiari L et al (1998) Surgical treatment for hepatic and pulmonary metastases from colorectal cancers. Ann Thorac Surg 66:214–218PubMedCrossRefGoogle Scholar
  31. 31.
    Kobayashi K, Kawamura M, Ishihara T (1999) Surgical treatment for both pulmonary and hepatic metastases from colorectal cancer. J Thorac Cardiovasc Surg 118:1090–1096PubMedCrossRefGoogle Scholar
  32. 32.
    Nagakura S, Shirai Y, Yamamoto Y et al (2001) Simultaneous detection of colorectal carcinoma liver and lung metastases does not warrant resection. J Am Coll Surg 193:153–160PubMedCrossRefGoogle Scholar
  33. 33.
    Brouquet A, Vauthey JN, Contreras CM et al (2011) Improved survival after resection of liver and lung colorectal metastases compared with liver-only metastases: a study of 112 patients with limited lung metastatic disease. J Am Coll Surg 213:62–69PubMedCrossRefGoogle Scholar
  34. 34.
    Gonzalez M, Robert JH, Halkic N et al (2012) Survival after lung metastasectomy in colorectal cancer patients with previously resected liver metastases. World J Surg 36:386–391. doi: 10.1007/s00268-011-1381-3 PubMedCrossRefGoogle Scholar
  35. 35.
    Sakamoto Y, Sakaguchi Y, Oki E et al (2012) Surgical outcomes after resection of both hepatic and pulmonary metastases from colorectal cancer. World J Surg 36:2708–2713. doi: 10.1007/s00268-012-1708-8 PubMedCrossRefGoogle Scholar
  36. 36.
    Rena O, Casadio C, Viano F et al (2002) Pulmonary resection for metastases from colorectal cancer: factors influencing prognosis—twenty-year experience. Eur J Cardiothorac Surg 21:906–912PubMedCrossRefGoogle Scholar
  37. 37.
    Higashiyama M, Kodama K, Higaki N et al (2003) Surgery for pulmonary metastases from colorectal cancer: the importance of prethoracotomy serum carcinoembryonic antigen as an indicator of prognosis. Jpn J Thorac Cardiovasc Surg 51:289–296PubMedCrossRefGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2013

Authors and Affiliations

  • Norifumi Hattori
    • 1
    Email author
  • Yukihide Kanemitsu
    • 1
  • Koji Komori
    • 1
  • Yasuhiro Shimizu
    • 1
  • Tsuyoshi Sano
    • 1
  • Yoshiki Senda
    • 1
  • Tetsuya Mitsudomi
    • 2
  • Takayuki Fukui
    • 2
  1. 1.Department of Gastroenterological SurgeryAichi Cancer CenterNagoyaJapan
  2. 2.Department of Thoracic SurgeryAichi Cancer CenterNagoyaJapan

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