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Published in: Annals of Surgical Oncology 6/2020

01-06-2020 | Gallbladder Cancer | Hepatobiliary Tumors

Proposed Definition for Oligometastatic Recurrence in Biliary Tract Cancer Based on Results of Locoregional Treatment: A Propensity-Score-Stratified Analysis

Authors: Koshiro Morino, MD, Satoru Seo, MD, PhD, Tomoaki Yoh, MD, PhD, Ken Fukumitsu, MD, PhD, Takamichi Ishii, MD, PhD, Kojiro Taura, MD, PhD, Satoshi Morita, PhD, Toshimi Kaido, MD, PhD, Shinji Uemoto, MD, PhD

Published in: Annals of Surgical Oncology | Issue 6/2020

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Abstract

Background

Oligometastatic recurrence involves relapsed tumors for which locoregional treatment (LT) may yield a survival benefit. However, there are no clear criteria for selecting patients for LT or determining the effects of LT in recurrent biliary tract cancer (BTC). The aim of this retrospective study is to assess the effects of LT on survival outcomes and to identify potential criteria for selecting LT in recurrent BTC.

Patients and Methods

In the present work, 232 consecutive patients with recurrent BTC who initially underwent curative surgery between 1996 and 2015 were evaluated. The primary outcome was length of survival after recurrence (SAR). Propensity score stratification with various tumor-related factors was used to identify patients who would likely benefit from LT.

Results

Among the cohort, 60 (25.9%) patients underwent LT, whereas 172 (74.1%) patients did not. The multivariate Cox model identified carbohydrate antigen 19-9 levels of > 50 U/mL, multiorgan recurrence, tumor number > 3, tumor size > 30 mm, and early recurrence (≤ 1 year) as independent predictors of poor SAR (P < 0.001 for each factor). In the propensity-score-stratified analysis, LT was associated with survival benefits for patients representing single-organ recurrence with at most three tumors and late-onset recurrence (> 1 year) (median SAR: 48.6 vs. 14.2 months, n = 33 vs. n = 34, hazard ratio: 0.10, 95% confidence interval: 0.04–0.20, P < 0.001).

Conclusions

Patients with recurrent BTC may benefit from LT if they have single-organ recurrence with at most three tumors and late-onset recurrence. We propose that these patients may have clinically relevant “oligometastatic recurrence” of BTC.
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Literature
1.
go back to reference Katanoda K, Matsuda T, Matsuda A, et al. An updated report of the trends in cancer incidence and mortality in Japan. Jpn J Clin Oncol. 2013;43:492–507.CrossRef Katanoda K, Matsuda T, Matsuda A, et al. An updated report of the trends in cancer incidence and mortality in Japan. Jpn J Clin Oncol. 2013;43:492–507.CrossRef
2.
go back to reference Primrose JN, Fox RP, Palmer DH, et al. Capecitabine compared with observation in resected biliary tract cancer (BILCAP): a randomised, controlled, multicentre, phase 3 study. Lancet Oncol. 2019;20:663–73.CrossRef Primrose JN, Fox RP, Palmer DH, et al. Capecitabine compared with observation in resected biliary tract cancer (BILCAP): a randomised, controlled, multicentre, phase 3 study. Lancet Oncol. 2019;20:663–73.CrossRef
3.
go back to reference Sulpice L, Rayar M, Boucher E, et al. Treatment of recurrent intrahepatic cholangiocarcinoma. Br J Surg. 2012;99:1711–7.CrossRef Sulpice L, Rayar M, Boucher E, et al. Treatment of recurrent intrahepatic cholangiocarcinoma. Br J Surg. 2012;99:1711–7.CrossRef
4.
go back to reference Takahashi Y, Ebata T, Yokoyama Y, et al. Surgery for recurrent biliary tract cancer: a single-center experience with 74 consecutive resections. Ann Surg. 2015;262:121–9.CrossRef Takahashi Y, Ebata T, Yokoyama Y, et al. Surgery for recurrent biliary tract cancer: a single-center experience with 74 consecutive resections. Ann Surg. 2015;262:121–9.CrossRef
5.
go back to reference Miyazaki Y, Kokudo T, Amikura K, et al. Survival of surgery for recurrent biliary tract cancer: a single-center experience and systematic review of literature. Jpn J Clin Oncol. 2017;47:206–12.CrossRef Miyazaki Y, Kokudo T, Amikura K, et al. Survival of surgery for recurrent biliary tract cancer: a single-center experience and systematic review of literature. Jpn J Clin Oncol. 2017;47:206–12.CrossRef
6.
go back to reference Park HM, Yun SP, Lee EC, et al. Outcomes for patients with recurrent intrahepatic cholangiocarcinoma after surgery. Ann Surg Oncol. 2016;23(13):4392–400.CrossRef Park HM, Yun SP, Lee EC, et al. Outcomes for patients with recurrent intrahepatic cholangiocarcinoma after surgery. Ann Surg Oncol. 2016;23(13):4392–400.CrossRef
7.
go back to reference Yoh T, Hatano E, Seo S, et al. Long-term survival of recurrent intrahepatic cholangiocarcinoma: the impact and selection of repeat surgery. World J Surg. 2018;42:1848–56.CrossRef Yoh T, Hatano E, Seo S, et al. Long-term survival of recurrent intrahepatic cholangiocarcinoma: the impact and selection of repeat surgery. World J Surg. 2018;42:1848–56.CrossRef
8.
go back to reference Kim E, Kim YJ, Kim K, et al. Salvage radiotherapy for locoregionally recurrent extrahepatic bile duct cancer after radical surgery. Br J Radiol. 2017;90:20170308.CrossRef Kim E, Kim YJ, Kim K, et al. Salvage radiotherapy for locoregionally recurrent extrahepatic bile duct cancer after radical surgery. Br J Radiol. 2017;90:20170308.CrossRef
9.
go back to reference Kim SW, Lim DH, Park HC, et al. Salvage radiation therapy for isolated local recurrence of extrahepatic cholangiocarcinoma after radical surgery: a retrospective study. Ann Surg Oncol. 2015;22:1308–14.CrossRef Kim SW, Lim DH, Park HC, et al. Salvage radiation therapy for isolated local recurrence of extrahepatic cholangiocarcinoma after radical surgery: a retrospective study. Ann Surg Oncol. 2015;22:1308–14.CrossRef
10.
go back to reference Ercolani G, Vetrone G, Grazi GL, et al. Intrahepatic cholangiocarcinoma: primary liver resection and aggressive multimodal treatment of recurrence significantly prolong survival. Ann Surg. 2010;252:107–14.CrossRef Ercolani G, Vetrone G, Grazi GL, et al. Intrahepatic cholangiocarcinoma: primary liver resection and aggressive multimodal treatment of recurrence significantly prolong survival. Ann Surg. 2010;252:107–14.CrossRef
11.
go back to reference Zhang SJ, Hu P, Wang N, et al. Thermal ablation versus repeated hepatic resection for recurrent intrahepatic cholangiocarcinoma. Ann Surg Oncol 2013;20(11):3596–602.CrossRef Zhang SJ, Hu P, Wang N, et al. Thermal ablation versus repeated hepatic resection for recurrent intrahepatic cholangiocarcinoma. Ann Surg Oncol 2013;20(11):3596–602.CrossRef
12.
go back to reference Park SY, Kim JH, Won HJ, et al. Radiofrequency ablation of hepatic metastases after curative resection of extrahepatic cholangiocarcinoma. AJR Am J Roentgenol. 2011;197:W1129–34.CrossRef Park SY, Kim JH, Won HJ, et al. Radiofrequency ablation of hepatic metastases after curative resection of extrahepatic cholangiocarcinoma. AJR Am J Roentgenol. 2011;197:W1129–34.CrossRef
13.
go back to reference Spolverato G, Kim Y, Alexandrescu S, et al. Management and outcomes of patients with recurrent intrahepatic cholangiocarcinoma following previous curative-intent surgical resection. Ann Surg Oncol. 2016;23:235–43.CrossRef Spolverato G, Kim Y, Alexandrescu S, et al. Management and outcomes of patients with recurrent intrahepatic cholangiocarcinoma following previous curative-intent surgical resection. Ann Surg Oncol. 2016;23:235–43.CrossRef
14.
go back to reference Miyazaki M, Shimizu H, Yoshitomi H, et al. Clinical implication of surgical resection for recurrent biliary tract cancer: does it work or not? Ann Gastroenterol Surg. 2017;1:164–70.CrossRef Miyazaki M, Shimizu H, Yoshitomi H, et al. Clinical implication of surgical resection for recurrent biliary tract cancer: does it work or not? Ann Gastroenterol Surg. 2017;1:164–70.CrossRef
15.
go back to reference Keane FK, Zhu AX, Hong TS. Radiotherapy for biliary tract cancers. Semin Radiat Oncol. 2018;28:342–50.CrossRef Keane FK, Zhu AX, Hong TS. Radiotherapy for biliary tract cancers. Semin Radiat Oncol. 2018;28:342–50.CrossRef
16.
17.
go back to reference Niibe Y, Hayakawa K. Oligometastases and oligo-recurrence: the new era of cancer therapy. Jpn J Clin Oncol. 2010;40:107–11.CrossRef Niibe Y, Hayakawa K. Oligometastases and oligo-recurrence: the new era of cancer therapy. Jpn J Clin Oncol. 2010;40:107–11.CrossRef
18.
go back to reference Tait CR, Waterworth A, Loncaster J, et al. The oligometastatic state in breast cancer: hypothesis or reality. Breast. 2005;14:87–93.CrossRef Tait CR, Waterworth A, Loncaster J, et al. The oligometastatic state in breast cancer: hypothesis or reality. Breast. 2005;14:87–93.CrossRef
19.
go back to reference Dethy S, Piccart MJ, Paesmans M, et al. History of brain and epidural metastases from breast cancer in relation with the disease evolution outside the central nervous system. Eur Neurol. 1995;35:38–42.CrossRef Dethy S, Piccart MJ, Paesmans M, et al. History of brain and epidural metastases from breast cancer in relation with the disease evolution outside the central nervous system. Eur Neurol. 1995;35:38–42.CrossRef
20.
go back to reference Oh Y, Taylor S, Bekele BN, et al. Number of metastatic sites is a strong predictor of survival in patients with nonsmall cell lung cancer with or without brain metastases. Cancer. 2009;115:2930–38.CrossRef Oh Y, Taylor S, Bekele BN, et al. Number of metastatic sites is a strong predictor of survival in patients with nonsmall cell lung cancer with or without brain metastases. Cancer. 2009;115:2930–38.CrossRef
21.
go back to reference Foster CC, Weichselbaum RR, Pitroda SP. Oligometastatic prostate cancer: reality or figment of imagination? Cancer. 2019;125:340–52.CrossRef Foster CC, Weichselbaum RR, Pitroda SP. Oligometastatic prostate cancer: reality or figment of imagination? Cancer. 2019;125:340–52.CrossRef
22.
go back to reference Ost P, Reynders D, Decaestecker K, et al. Surveillance or metastasis-directed therapy for oligometastatic prostate cancer recurrence: a prospective, randomized, multicenter phase II trial. J Clin Oncol. 2018;36:446–53.CrossRef Ost P, Reynders D, Decaestecker K, et al. Surveillance or metastasis-directed therapy for oligometastatic prostate cancer recurrence: a prospective, randomized, multicenter phase II trial. J Clin Oncol. 2018;36:446–53.CrossRef
23.
go back to reference Jingu K, Matsushita H, Yamamoto T, et al. Stereotactic radiotherapy for pulmonary oligometastases from colorectal cancer: a systematic review and meta-analysis. Technol Cancer Res Treat. 2018;17:1533033818794936.CrossRef Jingu K, Matsushita H, Yamamoto T, et al. Stereotactic radiotherapy for pulmonary oligometastases from colorectal cancer: a systematic review and meta-analysis. Technol Cancer Res Treat. 2018;17:1533033818794936.CrossRef
24.
go back to reference Chiapponi C, Berlth F, Plum PS, et al. Oligometastatic disease in upper gastrointestinal cancer—how to proceed? Visc Med. 2017;33:31–4.CrossRef Chiapponi C, Berlth F, Plum PS, et al. Oligometastatic disease in upper gastrointestinal cancer—how to proceed? Visc Med. 2017;33:31–4.CrossRef
25.
go back to reference Hellman S. Karnofsky memorial lecture. Natural history of small breast cancers. J Clin Oncol. 1994;12:2229–34.CrossRef Hellman S. Karnofsky memorial lecture. Natural history of small breast cancers. J Clin Oncol. 1994;12:2229–34.CrossRef
26.
go back to reference Valle J, Wasan H, Palmer DH, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362:1273–81.CrossRef Valle J, Wasan H, Palmer DH, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362:1273–81.CrossRef
27.
go back to reference Okusaka T, Nakachi K, Fukutomi A, et al. Gemcitabine alone or in combination with cisplatin in patients with biliary tract cancer: a comparative multicentre study in Japan. Br J Cancer. 2010;103:469–74.CrossRef Okusaka T, Nakachi K, Fukutomi A, et al. Gemcitabine alone or in combination with cisplatin in patients with biliary tract cancer: a comparative multicentre study in Japan. Br J Cancer. 2010;103:469–74.CrossRef
28.
go back to reference Sobin LH, Gospodarowicz MK, Wittekind C, editors. TNM classification of malignant tumors, 7th ed. New York: Wiley; 2009. Sobin LH, Gospodarowicz MK, Wittekind C, editors. TNM classification of malignant tumors, 7th ed. New York: Wiley; 2009.
29.
go back to reference Brookhart MA, Schneeweiss S, Rothman KJ, et al. Variable selection for propensity score models. Am J Epidemiol. 2006;163:1149–56.CrossRef Brookhart MA, Schneeweiss S, Rothman KJ, et al. Variable selection for propensity score models. Am J Epidemiol. 2006;163:1149–56.CrossRef
30.
go back to reference Stenestrand U, Wallentin L. Early revascularisation and 1-year survival in 14-day survivors of acute myocardial infarction: a prospective cohort study. Lancet. 2002;359:1805–11.CrossRef Stenestrand U, Wallentin L. Early revascularisation and 1-year survival in 14-day survivors of acute myocardial infarction: a prospective cohort study. Lancet. 2002;359:1805–11.CrossRef
31.
go back to reference Austin PC. An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivariate Behav Res. 2011;46:399–424.CrossRef Austin PC. An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivariate Behav Res. 2011;46:399–424.CrossRef
32.
go back to reference Zhang XF, Beal EW, Chakedis J, et al. Defining early recurrence of hilar cholangiocarcinoma after curative-intent surgery: a multi-institutional study from the US extrahepatic biliary malignancy consortium. World J Surg. 2018;42:2919–29.CrossRef Zhang XF, Beal EW, Chakedis J, et al. Defining early recurrence of hilar cholangiocarcinoma after curative-intent surgery: a multi-institutional study from the US extrahepatic biliary malignancy consortium. World J Surg. 2018;42:2919–29.CrossRef
33.
go back to reference Ercolani G, Dazzi A, Giovinazzo F, et al. Intrahepatic, peri-hilar and distal cholangiocarcinoma: three different locations of the same tumor or three different tumors? Eur J Surg Oncol. 2015;41:1162–9.CrossRef Ercolani G, Dazzi A, Giovinazzo F, et al. Intrahepatic, peri-hilar and distal cholangiocarcinoma: three different locations of the same tumor or three different tumors? Eur J Surg Oncol. 2015;41:1162–9.CrossRef
Metadata
Title
Proposed Definition for Oligometastatic Recurrence in Biliary Tract Cancer Based on Results of Locoregional Treatment: A Propensity-Score-Stratified Analysis
Authors
Koshiro Morino, MD
Satoru Seo, MD, PhD
Tomoaki Yoh, MD, PhD
Ken Fukumitsu, MD, PhD
Takamichi Ishii, MD, PhD
Kojiro Taura, MD, PhD
Satoshi Morita, PhD
Toshimi Kaido, MD, PhD
Shinji Uemoto, MD, PhD
Publication date
01-06-2020
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 6/2020
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-020-08207-0

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