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Perioperative circulating tumor cells in surgical patients with non-small cell lung cancer: does surgical manipulation dislodge cancer cells thus allowing them to pass into the peripheral blood?

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Abstract

Purpose

We herein evaluated the status of circulating tumor cells (CTC) dislodged from the tumor during surgery in patients who underwent pulmonary resection for non-small cell lung cancer (NSCLC) to assess the clinical implications.

Methods

Tumor cells in the peripheral arterial blood before surgery (Before) and immediately after lung resection (After) and in the blood from the pulmonary vein of the resected lung were detected using a size selective method. The clinicopathological characteristics and the prognosis were then analyzed according to the CTC status: no tumor cells detected (N), single tumor cell or total number less than 4 cells (S), and existence of clustered cells (C).

Results

According to the CTC status, the patients were classified into the following three groups: Before-C and After-C, Group I (n = 6); Before-S or N and After-C, Group II (n = 9); and Before-S or N and After-S or N, Group III (n = 8). Group III showed a high rate of p-stage IA, smaller tumor size, lower CEA level, lower SUVmax level, and a higher relapse-free survival rate than the other groups.

Conclusions

CTCs were detected in patients after undergoing lung resection, some of which may have been dislodged by the surgical procedure. The presence of clustered CTCs after the operation indicated an unfavorable outcome.

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References

  1. Sawabata N, Miyaoka E, Asamura H, Nakanishi Y, Eguchi K, Mori M, et al. Japanese lung cancer registry study of 11,663 surgical cases in 2004: demographic and prognosis changes over decade. J Thorac Oncol. 2011;6:1229–35.

    Article  PubMed  Google Scholar 

  2. Desitter I, Guerrouahen BS, Benali-Furet N, Wechsler J, Jänne PA, Kuang Y, et al. A new device for rapid isolation by size and characterization of rare circulating tumor cells. Anticancer Res. 2011;31:427–41.

    PubMed  Google Scholar 

  3. Funaki S, Sawabata N, Nakagiri T, Shintani Y, Inoue M, Kadota Y, et al. Novel approach for detection of isolated tumor cells in pulmonary vein using negative selection method: morphological classification and clinical implications. Eur J Cardiothorac Surg. 2011;40:322–7.

    PubMed  Google Scholar 

  4. Funaki S, Sawabata N, Abulaiti A, Nakagiri T, Shintani Y, Inoue M, et al. Significance of tumour vessel invasion in determining the morphology of isolated tumour cells in the pulmonary vein in non-small-cell lung cancer. Eur J Cardiothorac Surg. 2013;43:1126–30.

    Article  PubMed  Google Scholar 

  5. Hansen E, Wolff N, Knuechel R, Ruschoff J, Hofstaedter F, Taeger K. Tumor cells in blood shed from the surgical field. Arch Surg. 1995;130:387–93.

    Article  CAS  PubMed  Google Scholar 

  6. Yamashita J, Matsuo A, Kurusu Y, Saishoji T, Hayashi N, Ogawa M. Preoperative evidence of circulating tumor cells by means of reverse transcriptase-polymerase chain reaction for carcinoembryonic antigen messenger RNA is an independent predictor of survival in non-small cell lung cancer: a prospective study. J Thorac Cardiovasc Surg. 2002;124:299–305.

    Article  CAS  PubMed  Google Scholar 

  7. Brown DC, Purushotham AD, Birnie GD, George WD. Detection of intraoperative tumor cell dissemination in patients with breast cancer by use of reverse transcription and polymerase chain reaction. Surgery. 1995;117:95–101.

    Article  CAS  PubMed  Google Scholar 

  8. Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC, Rao C, Tibbe AG, Uhr JW, Terstappen LW. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res. 2004;10:6897–904.

    Article  PubMed  Google Scholar 

  9. Pantel K, Brakenhoff RH, Brandt B. Detection, clinical relevance and specific biological properties of disseminating tumor cells. Nat Rev Cancer. 2008;8:329–40.

    Article  CAS  PubMed  Google Scholar 

  10. Sawabata N, Okumura M, Utsumi T, Inoue M, Shiono H, Minami M, et al. Circulating tumor cells in peripheral blood caused by surgical manipulation of non-small-cell lung cancer: pilot study using an immunocytology method. Gen Thorac Cardiovasc Surg. 2007;55:189–92.

    Article  PubMed  Google Scholar 

  11. Okumura Y, Tanaka F, Yoneda K, Hashimoto M, Takuwa T, Kondo N, et al. Circulating tumor cell in pulmonary venous blood of primary lung cancer patients. Ann Thorac Surg. 2009;87:1669–75.

    Article  PubMed  Google Scholar 

  12. Tanaka F, Yoneda K, Kondo N, Hashimoto M, Takuwa T, Matsumoto S, et al. Circulating tumor cell as a diagnostic marker in primary lung cancer. Clin Cancer Res. 2009;15:6980–6.

    Article  CAS  PubMed  Google Scholar 

  13. Hofman V, Bonnetaud C, Ilie MI, Vielh P, Vignaud JM, Fléjou JF, et al. Preoperative circulating tumor cell detection using the isolation by size of epithelial tumor cell method for patients with lung cancer is a new prognostic biomarker. Clin Cancer Res. 2011;17:827–35.

    Article  CAS  PubMed  Google Scholar 

  14. Yao X, Williamson C, Adalsteinsson VA, D’Agostino RS, Fitton T, Smaroff GG, et al. Tumor cells are dislodged into the pulmonary vein during lobectomy. J Thorac Cardiovasc Surg. 2014;148:3224–31.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Nakamura H, Takagi M. Clinical impact of the new IASLC/ATS/ERS lung adenocarcinoma classification for chest surgeons. Surg Today. 2015;45:1341–51.

    Article  PubMed  Google Scholar 

  16. Fukumoto K, Taniguchi T, Usami N, Kawaguchi K, Fukui T, Ishiguro F, Nakamura S, Yokoi K. Preoperative plasma d-dimer level is an independent prognostic factor in patients with completely resected non-small cell lung cancer. Surg Today. 2015;45:63–7.

    Article  CAS  PubMed  Google Scholar 

  17. Hou JM, Krebs M, Ward T, Sloane R, Priest L, Hughes A, et al. Circulating tumor cells as a window on metastasis biology in lung cancer. Am J Pathol. 2011;178:989–96.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Wang J, Wang K, Xu J, Huang J, Zhang T. Prognostic significance of circulating tumor cells in non-small-cell lung cancer patients: a meta-analysis. PLoS One. 2013;8:e78070.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Yu M, Bardia A, Wittner BS, Stott SL, Smas ME, Ting DT, et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science. 2013;339:580–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Aceto N, Bardia A, Miyamoto DT, Donaldson MC, Wittner BS, Spencer JA, et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell. 2014;158:1110–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors thank Dr. Hiroshi Maruyama and Dr. Minako Torii (Department of Pathology, Hoshigaoka Medical Center) for their contributions to the pathological diagnoses. This research was supported by a Grant-in-Aid for Scientific Research [(B) 25293301] from the Japan Ministry of Education, Science, Sports and Culture.

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Correspondence to Noriyoshi Sawabata.

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Sawabata, N., Funaki, S., Hyakutake, T. et al. Perioperative circulating tumor cells in surgical patients with non-small cell lung cancer: does surgical manipulation dislodge cancer cells thus allowing them to pass into the peripheral blood?. Surg Today 46, 1402–1409 (2016). https://doi.org/10.1007/s00595-016-1318-4

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  • DOI: https://doi.org/10.1007/s00595-016-1318-4

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