Clinical Journal of Gastroenterology

, Volume 11, Issue 1, pp 53–61 | Cite as

Long-term survival after repeated resection of metachronous lung metastases from pStage IA pancreatic adenocarcinoma

  • Mamoru Miyasaka
  • Takehiro NojiEmail author
  • Kazuto Ohtaka
  • Ryohei Chiba
  • Shoki Sato
  • Yasuhito Shoji
  • Ryunosuke Hase
  • Tatsunosuke Ichimura
  • Satoshi Hirano
  • Naoto Senmaru
Case Report


Case report

A 70-year-old woman with pancreatic ductal adenocarcinoma was initially treated by distal pancreatectomy (DP). Thirty-five months later, another tumor appeared in the pancreatic head and was treated by pancreaticoduodenectomy. Histopathological findings identified both tumors as pancreatic ductal adenocarcinoma pStage IA. Computed tomography (CT) of the chest 16 months after the second pancreatectomy revealed a ground-glass opacity in segment 3 of the right lung. Chest CT 23 months after the second pancreatectomy revealed a nodular shadow in segment 1a of the right lung. Chest CT 39 months after the second pancreatectomy revealed a nodular shadow in segment 5 of the left lung. These lesions were treated by video-assisted thoracoscopic surgery partial resection. Histopathological and immunohistochemical features (positive for cytokeratin (CK)7 and CK20, negative for transcription factor-1) for these three lesions and the secondary pancreatic ductal adenocarcinoma were similar, indicating a diagnosis of lung metastasis from the second pancreatic ductal adenocarcinoma. The patient has remained alive and free of new metastases for 8 years after initial DP, 3 years after the last lung resection.


This patient has survived over the long term after undergoing three resections of lung metastases from resected pancreatic ductal adenocarcinoma.


Pancreatic ductal adenocarcinoma Lung metastasis Lung resection Long-term survival 


Compliance with ethical standards

Conflict of interest

Mamoru Miyasaka, Takehiro Noji, Kazuto Ohtaka, Ryohei Chiba, Shoki Sato, Yasuhito Shoji, Ryunosuke Hase, Tatsunosuke Ichimura, Satoshi Hirano, and Naoto Senmaru declares that they have no conflict of interest.

Human rights

All procedures followed have been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Informed consent

Informed consent was obtained from all patients for being included in the study.


  1. 1.
    Goldstein D, El-Maraghi RH, Hammel P, Heinemann V, Kunzmann V, Sastre J, et al. nab-Paclitaxel plus gemcitabine for metastatic pancreatic cancer: long-term survival from a phase III trial. J Natl Cancer Inst. 2015;107:dju413.CrossRefPubMedGoogle Scholar
  2. 2.
    Conroy T, Desseigne F, Ychou M, Bouché O, Guimbaud R, Bécouarn Y, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364:1817–25.CrossRefPubMedGoogle Scholar
  3. 3.
    Kleeff J, Reiser C, Hinz U, Bachmann J, Debus J, Jaeger D, et al. Surgery for recurrent pancreatic ductal adenocarcinoma. Ann Surg. 2007;245:566–72.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Sperti C, Pasquali C, Piccoli A, Pedrazzoli S. Recurrence after resection for ductal adenocarcinoma of the pancreas. World J Surg. 1997;21:195–200.CrossRefPubMedGoogle Scholar
  5. 5.
    Van den Broeck A, Sergeant G, Ectors N, Van Steenbergen W, Aerts R, Topal B. Patterns of recurrence after curative resection of pancreatic ductal adenocarcinoma. Eur J Surg Oncol. 2009;35:600–4.CrossRefPubMedGoogle Scholar
  6. 6.
    Nakajima M, Ueno T, Suzuki N, Matsui H, Shindo Y, Sakamoto K, et al. Novel indications for surgical resection of metachronous lung metastases from pancreatic cancer after curative resection. J Clin Gastroenterol. 2017;51:e34–38.CrossRefGoogle Scholar
  7. 7.
    Robinson LA, Tanvetyanon T, Springett G, Fontaine J, Toloza E, Hodul P, et al. Pulmonary metastasectomy for suspected pancreaticbiliary cancer. J Thorac Cardiovasc Surg. 2016;152:175–82.CrossRefGoogle Scholar
  8. 8.
    Brieau B, Barret M, Rouquette A, Dreanic J, Brezault C, Regnard JF, et al. Resection of late pulmonary metastases from pancreatic adenocarcinoma: is surgery an option? Cancer Invest. 2015;33:522–5.CrossRefPubMedGoogle Scholar
  9. 9.
    Evans DB, Rich TA, Byrd DR, Cleary KR, Connelly JH, Levin B, et al. Preoperative chemoradiation and pancreaticoduodenectomy for adenocarcinoma of the pancreas. Arch Surg. 1992;127:1335–9.CrossRefPubMedGoogle Scholar
  10. 10.
    Sugiura T, Uesaka K, Mihara K, Sasaki K, Kanemoto H, Mizuno T, et al. Margin status, recurrence pattern, and prognosis after resection of pancreatic cancer. Surgery. 2013;154:1078–86.CrossRefPubMedGoogle Scholar
  11. 11.
    Papavasiliou P, Hoffman JP, Cohen SJ, Meyer JE, Watson JC, Chun YS. Impact of preoperative therapy on patterns of recurrence in pancreatic cancer. HPB (Oxford). 2014;16:34–9.CrossRefGoogle Scholar
  12. 12.
    Wangjam T, Zhang Z, Zhou XC, Lyer L, Faisal F, Soares KC, et al. Resected pancreatic ductal adenocarcinomas with recurrence limited in lung have a significantly better prognosis than those with other recurrence patterns. Oncotarget. 2015;6:36903–10.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Yamashita K, Miyamoto A, Hama N, Asaoka T, Maeda S, Omiya H, et al. Survival impact of pulmonary metastasis as recurrence of pancreatic ductal adenocarcinoma. Dig Surg. 2015;32:464–71.CrossRefPubMedGoogle Scholar
  14. 14.
    Weitz J, Blumgart LH, Fong Y, Jarnagin WR, D’Angelica M, Harrison LE, et al. Partial hepatectomy for metastases from noncolorectal, nonneuroendocrine carcinoma. Ann Surg. 2005;241:269–76.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Yamada H, Hirano S, Tanaka E, Shichinohe T, Kondo S. Surgical treatment of liver metastases from pancreatic cancer. HPB (Oxford). 2006;8:85–8.CrossRefGoogle Scholar
  16. 16.
    Detry O, Warzee F, Polus M, De Roover A, Meurisse M, Honore P. Liver resection for noncolorectal, nonneuroendocrine metastases. Acta Chir Belg. 2003;103:458–62.CrossRefPubMedGoogle Scholar
  17. 17.
    Kruger S, Haas M, Burger PJ, Ormanns S, Modest DP, Westphalen CB, et al. Isolated pulmonary metastases define a favorable subgroup in metastatic pancreatic cancer. Pancreatology. 2016;16:593–8.CrossRefPubMedGoogle Scholar
  18. 18.
    Downs-Canner S, Zenati M, Boone BA, Varley PR, Steve J, Hogg ME, et al. The indolent nature of pulmonary metastases from ductal adenocarcinoma of the pancreas. J Surg Oncol. 2015;112:80–5.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Nakada T, Koshiishi H, Imaizumi K, Murata T, Tokura M, Hoshino M, et al. A case of resectable lung metastasis one year six months after surgery for pancreatic cancer. Jpn J Cancer Chemother. 2014;41:2160–2.Google Scholar
  20. 20.
    Thomas RM, Truty MJ, Noguearas-Gonzalez GM, Fleming JB, Vauthey JN, Pisters PWT, et al. Selective reoperation for locally recurrent or metastatic pancreatic ductal adenocarcinoma following primary pancreatic resection. J Gastrointet Surg. 2012;16:1696–704.CrossRefGoogle Scholar
  21. 21.
    Kitasato Y, Nakayama M, Akasu G, Yoshitomi M, Mikagi K, Maruyama Y, et al. Metastatic pulmonary adenocarcinoma 13 years after curative resection for pancreatic cancer: report of a case and review of Japanese literature. JOP. 2012;13:296–300.PubMedGoogle Scholar
  22. 22.
    Arnaoutakis GJ, Rangachari D, Laheru DA, Lacobuzio-Donahue CA, Hruban RH, Herman JM, et al. Pulmonary resection for isolated pancreatic adenocarcinoma metastasis: an analysis of outcomes and survival. J Gastrointest Surg. 2011;15:1611–7.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Zheng B, Ohuchida K, Yan Z, Okumura T, Ohtsuka T, Nakamura M. Primary recurrence in the lung is related to faborable prognosis in patients with pancreatic cancer and postoperative recurrence. World J Surg. 2017. doi: 10.1007/s00268-017-4068-6.PubMedGoogle Scholar
  24. 24.
    Takano K, Kurosaki I, Minagawa M, Kitami C, Date K, Hatakeyama K, et al. Clinicopathological features of delayed isolated lung metastases after radical pancreatectomy for pancreatic cancer. Jpn J Gastroenterol Surg. 2010;43:1270–5.CrossRefGoogle Scholar
  25. 25.
    Katz MH, Wang H, Fleming JB, Sun CC, Hwang RF, Wolff RA, et al. Long-term survival after multidisciplinary management of resected pancreatic adenocarcinoma. Ann Surg Oncol. 2009;16:836–47.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Matoso A, Singh K, Jacob R, Greaves WO, Tavares R, Noble L, et al. Comparison of thyroid transcription factor-1 expression by 2 monoclonal antibodies in pulmonary and nonpulmonary primary tumors. Appl Immunohistochem Mol Morphol. 2010;18:142–9.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Park SY, Kim BH, Kim JH, Lee S, Kang GH. Panels of immunohistochemical markers help determine primary sites of metastatic adenocarcinoma. Arch Pathol Lab Med. 2007;131:1561–7.PubMedGoogle Scholar
  28. 28.
    Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, et al. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Scl USA. 2001;98:10356–61.CrossRefGoogle Scholar
  29. 29.
    Masugi Y, Yamazaki K, Hibi T, Aiura K, Kitagawa Y, Sakamoto M. Solitary cell infiltration is a novel indicator of poor prognosis and epithelial-mesenchymal transition in pancreatic cancer. Hum Pathol. 2010;41:1061–8.CrossRefPubMedGoogle Scholar
  30. 30.
    Karamitopoulou E, Zlobec I, Born D, Kondi-Pafiti A, Lykoudis P, Mellou A, et al. Tumor budding is a strong and independent prognostic factor in pancreatic cancer. Eur J Cacncer. 2013;49:1032–9.CrossRefGoogle Scholar
  31. 31.
    Weiser MR, Downey RJ, Leung DH, Brennan MF. Repeat resection of pulmonary metastases in patients with soft-tissue sarcoma. J Am Coll Surg. 2000;191:184–90.CrossRefPubMedGoogle Scholar
  32. 32.
    Welter S, Jacobs J, Krbek T, Krebs B, Stamatis G. Long-term survival after repeated resection of pulmonary metastases from colorectal cancer. Ann Thorac Surg. 2007;84:203–10.CrossRefPubMedGoogle Scholar
  33. 33.
    Hachimaru A, Maeda R, Suda T, Takagi Y. Repeat pulmonary resection for recurrent lung metastases from colorectal cancer: an analysis of prognostic factors. Interact Cardiovasc Thorac Surg. 2016;22:826–30.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Japanese Society of Gastroenterology 2017

Authors and Affiliations

  • Mamoru Miyasaka
    • 1
    • 2
  • Takehiro Noji
    • 2
    Email author
  • Kazuto Ohtaka
    • 1
  • Ryohei Chiba
    • 1
  • Shoki Sato
    • 1
  • Yasuhito Shoji
    • 1
  • Ryunosuke Hase
    • 1
  • Tatsunosuke Ichimura
    • 1
  • Satoshi Hirano
    • 2
  • Naoto Senmaru
    • 1
  1. 1.Department of SurgerySteel Memorial Muroran HospitalMuroranJapan
  2. 2.Gastroenterological Surgery IIHokkaido University Graduate School of MedicineSapporoJapan

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