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Primary Recurrence in the Lung is Related to Favorable Prognosis in Patients with Pancreatic Cancer and Postoperative Recurrence

World Journal of Surgery volume 41, pages 2858–2866 (2017)Cite this article

Abstract

Background

The pattern of recurrence affects the clinical outcome in tumor patients. However, the clinical significance of lung metastasis as the primary recurrence site after resection in patients with pancreatic cancer remains unclear. This study aimed to clarify the clinical significance of the primary recurrence site in patients with pancreatic cancer, in terms of prognosis and clinicopathological features.

Methods

This retrospective cohort study included 220 patients with postoperative recurrence after pancreatectomy for pancreatic cancer and classified by primary site of recurrence. We focused on patients with lung metastasis as the primary recurrence and investigated its correlation with prognosis and clinicopathological factors.

Results

Twenty-four (11%) patients had lung metastasis as the primary recurrence. This recurrence pattern had the best prognosis among all recurrence patterns, including liver metastasis and local recurrence. Patients with lung metastasis as the primary recurrence had favorable overall survival and survival from the date of recurrence compared with patients with other primary recurrence sites in both univariate (P = 0.0008 and P = 0.0005) and multivariate analyses (P = 0.0051 and P = 0.0068). In terms of clinicopathological features of resected pancreatic tumors, lung metastasis as the primary recurrence was associated with lower tumor stage and histologic grade, and less vascular invasion and residual tumor volume than liver metastasis.

Conclusions

Pancreatic cancer patients with lung metastasis as the primary recurrence after pancreatectomy have a better prognosis than those with other recurrence patterns.

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References

  1. Siegel RL, Miller KD, Jemal A (2015) Cancer statistics. CA Cancer J Clin 65:5–29

    Article  PubMed  Google Scholar 

  2. Vogelzang NJ, Benowitz SI, Adams SJ et al (2012) Clinical cancer advances 2011: annual report on progress against cancer from the American Society of Clinical Oncology. J Clin Oncol 30:88–109

    Article  PubMed  Google Scholar 

  3. Matsuno S, Egawa S, Fukuyama S et al (2004) Pancreatic cancer registry in Japan: 20 years of experience. Pancreas 28:219–230

    Article  PubMed  Google Scholar 

  4. Paulson AS, Tran Cao HS, Tempero MA et al (2013) Therapeutic advances in pancreatic cancer. Gastroenterology 144:1316–1326

    CAS  Article  PubMed  Google Scholar 

  5. Castellanos JA, Merchant NB (2014) Intensity of follow-up after pancreatic cancer resection. Ann Surg Oncol 21:747–751

    Article  PubMed  Google Scholar 

  6. Cameron JL, Riall TS, Coleman J et al (2006) One thousand consecutive pancreaticoduodenectomies. Ann Surg 244:10–15

    Article  PubMed  PubMed Central  Google Scholar 

  7. Richter A, Niedergethmann M, Sturm JW et al (2003) Long-term results of partial pancreaticoduodenectomy for ductal adenocarcinoma of the pancreatic head: 25-year experience. World J Surg 27:324–329. doi:10.1007/s00268-002-6659-z

    Article  PubMed  Google Scholar 

  8. Carpelan-Holmstrom M, Nordling S, Pukkala E et al (2005) Does anyone survive pancreatic ductal adenocarcinoma? A nationwide study re-evaluating the data of the Finnish Cancer Registry. Gut 54:385–387

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Wagner M, Redaelli C, Lietz M et al (2004) Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. Br J Surg 91:586–594

    CAS  Article  PubMed  Google Scholar 

  10. Suenaga M, Fujii T, Kanda M et al (2014) Pattern of first recurrent lesions in pancreatic cancer: hepatic relapse is associated with dismal prognosis and portal vein invasion. Hepatogastroenterology 61:1756–1761

    PubMed  Google Scholar 

  11. Hess KR, Varadhachary GR, Taylor SH et al (2006) Metastatic patterns in adenocarcinoma. Cancer 106:1624–1633

    Article  PubMed  Google Scholar 

  12. Kamisawa T, Isawa T, Koike M et al (1995) Hematogenous metastases of pancreatic ductal carcinoma. Pancreas 11:345–349

    CAS  Article  PubMed  Google Scholar 

  13. Goulart BH, Clark JW, Lauwers GY et al (2009) Long term survivors with metastatic pancreatic adenocarcinoma treated with gemcitabine: a retrospective analysis. J Hematol Oncol 2:13

    Article  PubMed  PubMed Central  Google Scholar 

  14. Gotfried JI, Kozuch PS (2011) Case report: long-term survival in patients with initial lung-only metastasis from pancreatic adenocarcinoma. J Gastrointest Cancer 43:50–55

    Article  Google Scholar 

  15. Kitasato Y, Nakayama M, Akasu G et al (2012) Metastatic pulmonary adenocarcinoma 13 years after curative resection for pancreatic cancer: report of a case and review of Japanese literature. JOP 13:296–300

    PubMed  Google Scholar 

  16. Deeb A, Haque SU, Olowokure O (2015) Pulmonary metastases in pancreatic cancer, is there a survival influence? J Gastrointest Oncol 6:E48–E51

    PubMed  PubMed Central  Google Scholar 

  17. Kruger S, Haas M, Burger PJ et al (2016) Isolated pulmonary metastases define a favorable subgroup in metastatic pancreatic cancer. Pancreatology 2016(16):593–598

    Article  Google Scholar 

  18. Edge SB, Byrd DR, Compton CC et al. (2010) Exocrine and endocrine pancreas. In: Edge SB (ed) AJCC cancer staging manual, 7th edn. Springer, New York, pp 241–248

    Google Scholar 

  19. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674

    CAS  Article  PubMed  Google Scholar 

  20. Riihimaki M, Thomsen H, Hemminki A et al (2013) Comparison of survival of patients with metastases from known versus unknown primaries: survival in metastatic cancer. BMC Cancer 13:36

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hemminki K, Riihimaki M, Sundquist K et al (2013) Site-specific survival rates for cancer of unknown primary according to location of metastases. Int J Cancer 133:182–189

    CAS  Article  PubMed  Google Scholar 

  22. Thomas RM, Truty MJ, Nogueras-Gonzalez GM et al (2012) Selective reoperation for locally recurrent or metastatic pancreatic ductal adenocarcinoma following primary pancreatic resection. J Gastrointest Surg 16:1696–1704

    Article  PubMed  Google Scholar 

  23. Boone BA, Zeh HJ, Mock BK et al (2014) Resection of isolated local and metastatic recurrence in periampullary adenocarcinoma. HPB (Oxford) 16:197–203

    Article  Google Scholar 

  24. Brieau B, Barret M, Rouquette A et al (2015) Resection of late pulmonary metastases from pancreatic adenocarcinoma: is surgery an option? Cancer Investig 33:522–525

    CAS  Article  Google Scholar 

  25. Arnaoutakis GJ, Rangachari D, Laheru DA et al (2011) Pulmonary resection for isolated pancreatic adenocarcinoma metastasis: an analysis of outcomes and survival. J Gastrointest Surg 15:1611–1617

    Article  PubMed  PubMed Central  Google Scholar 

  26. Weiss L (1985) Mechanisms of metastatic patterns. In: Weiss L (ed) Principles of metastasis. Academic PressInc-Verlag, Orlando, pp 200–256

    Google Scholar 

  27. Tan KK, Lopes Gde L Jr., Sim R (2009) How uncommon are isolated lung metastases in colorectal cancer? A review from database of 754 patients over 4 years. J Gastrointest Surg 13:642–648

    Article  PubMed  Google Scholar 

  28. Pihl E, Hughes ES, McDermott FT et al (1987) Lung recurrence after curative surgery for colorectal cancer. Dis Colon Rectum 30:417–419

    CAS  Article  PubMed  Google Scholar 

  29. Lisa JR, Trinidad S, Rosenblatt MB (1964) Pulmonary manifestations of carcinoma of the pancreas. Cancer 17:395–401

    CAS  Article  PubMed  Google Scholar 

  30. Merrie AE, Phillips LV, Yun K et al (2001) Skip metastases in colon cancer: assessment by lymph node mapping using molecular detection. Surgery 129:684–691

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

This work was funded by a Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grant Numbers: 26293305, 25293285), Scientific Research on Innovative Areas (Grant Number: 26108010), and Heilongjiang Postdoctoral Science Foundation funded project (Grant Number: LBH-Z16157).

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Affiliations

  1. Department of Hepatobiliary and Pancreatic Surgery, Harbin Medical University Cancer Hospital, Harbin, People’s Republic of China

    Biao Zheng

  2. Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Fukuoka, 812-8582, Japan

    Biao Zheng, Kenoki Ohuchida, Zilong Yan, Takashi Okumura, Takao Ohtsuka & Masafumi Nakamura

  3. Advanced Medical Initiatives, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan

    Kenoki Ohuchida

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  1. Biao Zheng
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  2. Kenoki Ohuchida
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  3. Zilong Yan
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  4. Takashi Okumura
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  5. Takao Ohtsuka
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  6. Masafumi Nakamura
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Corresponding authors

Correspondence to Kenoki Ohuchida or Masafumi Nakamura.

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The authors declare no conflicts of interest.

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Zheng, B., Ohuchida, K., Yan, Z. et al. Primary Recurrence in the Lung is Related to Favorable Prognosis in Patients with Pancreatic Cancer and Postoperative Recurrence. World J Surg 41, 2858–2866 (2017). https://doi.org/10.1007/s00268-017-4068-6

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  • DOI: https://doi.org/10.1007/s00268-017-4068-6