Skip to main content

Advertisement

SpringerLink
Log in

Prognostic Analysis of Surgical Resection for Pulmonary Metastasis from Hepatocellular Carcinoma

  • Original Scientific Report
  • Published:
World Journal of Surgery Aims and scope Submit manuscript

Abstract

Introduction

Pulmonary metastases are the most common among extrahepatic recurrences from hepatocellular carcinoma (HCC). It causes high risk of HCC-related death, despite recent progress in therapeutic options. However, a role of pulmonary metastasectomy as well as prognostic factors after metastasectomy has not been well established. We aimed to investigate survival outcomes and prognostic factors after pulmonary resection for metastases from HCC.

Methods

A series of 93 patients who underwent pulmonary resections for metastases from HCC between June 1990 and July 2013 from multi-institutional database were retrospectively evaluated. Perioperative clinicopathological data and their association with prognosis were investigated.

Results

Of 93 patients, 77 had one pulmonary metastasis, and 16 had two or more. Recurrence after pulmonary resection was noted in 60 patients (64.5 %). The estimated 5-year overall survival rate was 41.4 % with median survival time after pulmonary metastatectomy of 39.0 months. Univariate prognostic analysis showed that disease-free interval of ≥12 months was significantly associated with favorable outcomes in both overall survival (5-year rate, 59.3 vs. 28.7 %, p = 0.026) and disease-specific survival (5-year rate, 62.5 vs. 36.2 %; p = 0.038) after pulmonary metastatectomy. A multivariate analysis revealed that disease-free interval was an independent prognostic factor (HR = 2.020, 95 % CI, 1.069–3.816, p = 0.030).

Conclusion

We have shown that a disease-free interval was an independent prognostic factor in patients who underwent pulmonary resection for metastasis from HCC. Also, pulmonary metastasectomy can be one of the therapeutic choices for select patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

HCC:

hepatocellular carcinoma

PM:

pulmonary metastases

CT:

computed tomography

OS:

overall survival

DSS:

disease-specific survival

DFI:

disease-free interval

IQR:

interquatile range

SD:

standard deviation

References

  1. Matsumata T, Kanematsu T, Takenaka K, Yoshida Y, Nishizaki T, Sugimachi K (1989) Patterns of intrahepatic recurrence after curative resection of hepatocellular carcinoma. Hepatology 9:457–460

    Article  CAS  PubMed  Google Scholar 

  2. Fan ST, Mau Lo C, Poon RT, Yeung C, Leung Liu C, Yuen WK, Ming Lam C, Ng KK, Ching Chan S (2011) Continuous improvement of survival outcomes of resection of hepatocellular carcinoma: a 20-year experience. Ann Surg 253:745–758

    Article  PubMed  Google Scholar 

  3. Hanazaki K, Kajikawa S, Shimozawa N, Mihara M, Shimada K, Hiraguri M, Koide N, Adachi W, Amano J (2000) Survival and recurrence after hepatic resection of 386 consecutive patients with hepatocellular carcinoma. J Am Coll Surg 191:381–388

    Article  CAS  PubMed  Google Scholar 

  4. Poon RTP, Fan ST, Wong J (2000) Risk factors, prevention and management of postoperative recurrence after resection of hepatocellular carcinoma. Ann Surg 232:10–24

    Article  Google Scholar 

  5. Leung U, Kuk D, D’Angelica MI, Kingham TP, Allen PJ, DeMatteo RP, Jarnagin WR, Fong Y (2015) Long-term outcomes following microwave ablation for liver malignancies. Br J Surg 102:85–91

    Article  CAS  PubMed  Google Scholar 

  6. Arii S, Monden K, Niwano M, Furutani M, Mori A, Mizumoto M, Imamura M (1998) Results of surgical treatment for recurrent hepatocellular carcinoma: comparison of outcome among patients with multicentric carcinogenesis, intrahepatic metastasis, and extrahepatic recurrence. J Hepatobiliary Pancreat Surg 5:86–92

    Article  CAS  PubMed  Google Scholar 

  7. Gwak GY, Jung JO, Sung SW, Lee HS (2004) Long-term survival after pulmonary metastatectomy of hepatocellular carcinoma; treatment outcome or natural history? Hepatogastroenterology 51:1428–1433

    PubMed  Google Scholar 

  8. Kow AW, Kwon CH, Song S, Kim JM, Joh JW (2015) Clinicopathological factors and long-term outcome comparing between lung and peritoneal metastasectomy after hepatectomy for hepatocellular carcinoma in a tertiary institution. Surgery 157:645–653

    Article  PubMed  Google Scholar 

  9. Thomford NR, Woolner LB, Clagett OT (1965) The surgical treatment of metastatic tumors in the lungs. J Thorac Cardiovasc Surg 49:357–363

    CAS  PubMed  Google Scholar 

  10. Kawamura M, Nakajima J, Matsuguma H, Horio H, Miyoshi S, Nakagawa K, Fujisawa T, Kobayashi K, Metastatic Lung Tumor Study Group of Japan (2008) Surgical outcomes for pulmonary metastases from hepatocellular carcinoma. Eur J Cardiothorac Surg 34:196–199

    Article  PubMed  Google Scholar 

  11. Shirabe K, Takeishi K, Taketomi A, Uchiyama H, Kayashima H, Maehara Y (2011) Improvement of long-term outcomes in hepatitis C virus antibody-positive patients with hepatocellular carcinoma after hepatectomy in the modern era. World J Surg 35:1072–1084. doi:10.1007/s00268-011-1013-y

    Article  PubMed  Google Scholar 

  12. Nakagawa T, Kamiyama T, Nakanishi K, Yokoo H, Kamachi H, Matsushita M, Todo S (2006) Pulmonary resection for metastases from hepatocellular carcinoma: factors influencing prognosis. J Thorac Cardiovasc Surg 131:1248–1254

    Article  PubMed  Google Scholar 

  13. Kuo SW, Chang YL, Huang PM, Hsu HH, Chen JS, Lee JM, Lee PH, Lee YC (2007) Prognostic factors for pulmonary metastasectomy in hepatocellular carcinoma. Ann Surg Oncol 14:992–1997

    Article  PubMed  Google Scholar 

  14. Cho S, Ryu KM, Hwang YJ, Lee EB (2010) Prognostic factors for pulmonary metastasectomy in the treatment of hepatocellular carcinoma. J Thorac Oncol 5:1251–1254

    Article  PubMed  Google Scholar 

  15. Kitano K, Murayama T, Sakamoto M, Nagayama K, Ueno K, Murakawa T, Nakajima J (2012) Outcome and survival analysis of pulmonary metastasectomy for hepatocellular carcinoma. Eur J Cardiothorac Surg 41:376–382

    Article  PubMed  Google Scholar 

  16. Yoon YS, Kim HK, Kim J, Choi YS, Shim YM, Paik SW, Kim K (2010) Long-term survival and prognostic factors after pulmonary metastasectomy in hepatocellularcarcinoma. Ann Surg Oncol 17:2795–2801

    Article  PubMed  Google Scholar 

  17. Hwang S, Kim YH, Kim DK, Ahn CS, Moon DB, Kim KH, Ha TY, Song GW, Jung DH, Kim HR, Park GC, Namgoong JM, Yoon SY, Jung SW, Park SI, Lee SG (2012) Resection of pulmonary metastases from hepatocellular carcinoma following liver transplantation. World J Surg 36:1592–1602. doi:10.1007/s00268-012-1533-0

    Article  PubMed  Google Scholar 

  18. Katyal S, Oliver JH 3rd, Peterson MS, Ferris JV, Carr BS, Baron RL (2000) Extrahepatic metastases of hepatocellular carcinoma. Radiology 216:698–703

    Article  CAS  PubMed  Google Scholar 

  19. Lin DY, Lin SM, Liaw YF (1997) Non-surgical treatment of hepatocellular carcinoma. J Gastroenterol Hepatol 12:S319–S328

    Article  CAS  PubMed  Google Scholar 

  20. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, Bolondi L, Greten TF, Galle PR, Seitz JF, Borbath I, Häussinger D, Giannaris T, Shan M, Moscovici M, Voliotis D, Bruix J, SHARP Investigators Study Group (2008) Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359:378–390

    Article  CAS  PubMed  Google Scholar 

  21. Tomimaru Y, Sasaki Y, Yamada T, Eguchi H, Takami K, Ohigashi H, Higashiyama M, Ishikawa O, Kodama K, Imaoka S (2006) The significance of surgical resection for pulmonary metastasis from hepatocellular carcinoma. Am J Surg 192:46–51

    Article  PubMed  Google Scholar 

  22. Han KN, Kim YT, Yoon JH, Suh KS, Song JY, Kang CH, Sung SW, Kim JH (2010) Role of surgical resection for pulmonary metastasis of hepatocellular carcinoma. Lung Cancer 70:295–300

    Article  PubMed  Google Scholar 

  23. Lam CM, Lo CM, Yuen WK, Liu CL, Fan ST (1998) Prolonged survival in selected patients following surgical resection for pulmonary metastasis from hepatocellular carcinoma. Br J Surg 85:1198–1200

    Article  CAS  PubMed  Google Scholar 

  24. Nakajima J, Tanaka M, Matsumoto J, Takeuchi E, Fukami T, Takamoto S (2005) Appraisal of surgical treatment for pulmonary metastasis from hepatocellular carcinoma. World J Surg 29:715–718. doi:10.1007/s00268-005-7687-2

    Article  PubMed  Google Scholar 

  25. Kanzaki R, Higashiyama M, Fujiwara A, Tokunaga T, Maeda J, Okami J, Nishimura K, Kodama K (2010) Outcome of surgical resection of pulmonary metastasis from urinary tract transitional cell carcinoma. Interact CardioVasc Thorac Surg 11:60–64

    Article  PubMed  Google Scholar 

  26. Suemitsu R, Takeo S, Kusumoto E, Hamatake M, Ikejiri K, Saitsu H (2010) Results of a pulmonary metastasectomy in patients with colorectal cancer. Surg Today 41:54–59

    Article  PubMed  Google Scholar 

  27. Yang Y, Nagano H, Ota H, Morimoto O, Nakamura M, Wada H, Noda T, Damdinsuren B, Marubashi S, Miyamoto A, Takeda Y, Dono K, Umeshita K, Nakamori S, Wakasa K, Sakon M, Monden M (2007) Patterns and clinicopathologic features of extrahepatic recurrence of hepatocellular carcinoma after curative resection. Surgery 141:196–202

    Article  PubMed  Google Scholar 

  28. Taketomi A, Toshima T, Kitagawa D, Motomura T, Takeishi K, Mano Y, Kayashima H, Sugimachi K, Aishima S, Yamashita Y, Ikegami T, Gion T, Uchiyama H, Soejima Y, Maeda T, Shirabe K, Maehara Y (2010) Predictors of extrahepatic recurrence after curative hepatectomy for hepatocellular carcinoma. Ann Surg Oncol 17:2740–2746

    Article  PubMed  Google Scholar 

  29. Hirokawa F, Hayashi M, Miyamoto Y, Asakuma M, Shimizu T, Komeda K, Inoue Y, Uchiyama K (2014) Surgical treatment of extrahepatic recurrence of hepatocellular carcinoma. Langenbecks Arch Surg 399:1057–1064

    Article  PubMed  Google Scholar 

  30. Aberg T (1997) Selection mechanisms as major determinants of survival after pulmonary metastasectomy. Ann Thorac Surg 63:611–612

    Article  CAS  PubMed  Google Scholar 

  31. Fiorentino F, Treasure T (2015) Pulmonary metastasectomy: a call for better data collection, presentation and analysis. Future Oncol 11(2 Suppl):19–23

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Ms. Ai Yamakawa for the great efforts for the management of the database of our study group. The authors also appreciate the helping hand of Dr. Boris Hristov, MD, in editing this manuscript.

Author information

Authors and Affiliations

  1. Department of Surgery, Teikyo University School of Medicine, Tokyo, Japan

    Yusuke Takahashi & Masafunmi Kawamura

  2. Department of Surgery, Tokyo Medical University, Tokyo, Japan

    Norihiko Ikeda

  3. Department of Thoracic Surgery, The University of Tokyo Graduate School of Medicine, Tokyo, Japan

    Jun Nakajima

  4. Osaka University Graduate School of Medicine, Suita Osaka, Japan

    Noriyoshi Sawabata

  5. Department of General Thoracic Surgery, Dokkyo Medical University, Tochigi, Japan

    Masayuki Chida

  6. Department of Thoracic Surgery, Tokyo Metropolitan Cancer and Infectious Diseases Center Komagome Hospital, Tokyo, Japan

    Hirotoshi Horio

  7. Department of Chest Surgery, Cancer Institute Hospital, Tokyo, Japan

    Sakae Okumura

Authors
  1. Yusuke Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Norihiko Ikeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Nakajima
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Noriyoshi Sawabata
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masayuki Chida
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hirotoshi Horio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sakae Okumura
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Masafunmi Kawamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

The Metastatic Lung Tumor Study Group of Japan

Corresponding author

Correspondence to Yusuke Takahashi.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TIFF 118 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takahashi, Y., Ikeda, N., Nakajima, J. et al. Prognostic Analysis of Surgical Resection for Pulmonary Metastasis from Hepatocellular Carcinoma. World J Surg 40, 2178–2185 (2016). https://doi.org/10.1007/s00268-016-3580-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00268-016-3580-4

Keywords

Search

Navigation