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Preoperative biopsy and tumor recurrence of stage I adenocarcinoma of the lung

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Abstract

Purpose

To evaluate whether preoperative biopsy affects the outcomes of patients undergoing at least lobectomy for stage I lung adenocarcinoma.

Methods

We reviewed the medical records of patients who underwent surgery for stage I lung adenocarcinoma between 2006 and 2013. Tumor recurrence and survival were compared between patients who underwent preoperative biopsy, including computed tomographic-guided needle biopsy and transbronchial biopsy, and those who underwent intraoperative frozen section.

Results

Among 509 patients, 229 patients (44.9%) underwent preoperative biopsy and 280 patients had lung adenocarcinoma diagnosed by intraoperative frozen section (reference group). Recurrence developed in 65 (12.8%) patients within a median follow-up period of 54.4 months. Multivariate analysis demonstrated that preoperative biopsy (OR 1.97, p = 0.045), radiological solid appearance (OR 5.43, p < 0.001), and angiolymphatic invasion (OR 2.48, p = 0.010) were independent predictors of recurrence. In the overall cohort, preoperative biopsy appeared to worsen 5-year disease-free and overall survival significantly (76.6% vs. 93.0%, p < 0.001; and 83.8% vs. 94.5%, p = 0.002, respectively) compared with the reference group. After propensity matching, multivariable logistic regression still identified preoperative biopsy as an independent predictor of overall recurrence (OR 2.21, p = 0.048) after adjusting for tumor characteristics.

Conclusion

Preoperative biopsy might be considered a prognosticator of recurrence of stage I adenocarcinoma of the lungs in patients who undergo at least anatomic lobectomy without postoperative adjuvant chemotherapy.

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Abbreviations

CTGNB:

Computed tomographic-guided needle biopsy

TBB:

Trans-bronchial biopsy

ALI:

Angiolymphatic invasion

LRPD:

Local recurrence with pleural disseminations

OR:

Odds ratio

HR:

Hazard ratio

DFS:

Disease-free survival

NSCLC:

Non-small cell lung cancer

VATS:

Video-assisted thoracic surgery

CEA:

Carcinoembryonic antigen

TDR:

Tumor shadow disappearance rate

GGN:

Pure ground glass nodule

PET:

Positron emission tomography

VPI:

Visceral pleural invasion

IASLC:

International association for the study of lung cancer

References

  1. Wu CC, Maher MM, Shepard JA. Complications of ct-guided percutaneous needle biopsy of the chest: Prevention and management. AJR Am J Roentgenol. 2011;196:W678–W682682.

    Article  Google Scholar 

  2. Choo JY, Park CM, Lee NK, Lee SM, Lee HJ, Goo JM. Percutaneous transthoracic needle biopsy of small (≤ 1 cm) lung nodules under c-arm cone-beam CT virtual navigation guidance. Eur Radiol. 2013;23:712–9.

    Article  Google Scholar 

  3. Tam AL, Kim ES, Lee JJ, Ensor JE, Hicks ME, Tang X, et al. Feasibility of image-guided transthoracic core-needle biopsy in the battle lung trial. J Thorac Oncol. 2013;8:436–42.

    Article  Google Scholar 

  4. Kohman LJ, Gu L, Altorki N, Scalzetti E, Veit LJ, Wallen JM, et al. Biopsy first: lessons learned from cancer and leukemia group b (CALGB) 140503. J Thorac Cardiovasc Surg. 2017;153:1592–7.

    Article  Google Scholar 

  5. Huang KY, Ko PZ, Yao CW, Hsu CN, Fang HY, Tu CY, et al. Inaccuracy of lung adenocarcino***ma subtyping using preoperative biopsy specimens. J Thorac Cardiovasc Surg. 2017;154:332 9 e1.

    Google Scholar 

  6. Ofiara LM, Navasakulpong A, Ezer N, Gonzalez AV. The importance of a satisfactory biopsy for the diagnosis of lung cancer in the era of personalized treatment. Curr Oncol. 2012;19:S16–S23.

    Article  CAS  Google Scholar 

  7. Nakajima J. Preoperative pathological diagnosis of lung cancer: Is it always necessary? Ann Thorac Cardiovasc Surg. 2012;18:183–5.

    Article  Google Scholar 

  8. Inoue M, Honda O, Tomiyama N, Minami M, Sawabata N, Kadota Y, et al. Risk of pleural recurrence after computed tomographic-guided percutaneous needle biopsy in stage I lung cancer patients. Ann Thorac Surg. 2011;91:1066–71.

    Article  Google Scholar 

  9. Matsuguma H, Nakahara R, Kondo T, Kamiyama Y, Mori K, Yokoi K. Risk of pleural recurrence after needle biopsy in patients with resected early stage lung cancer. Ann Thorac Surg. 2005;80:2026–31.

    Article  Google Scholar 

  10. Sawabata N, Ohta M, Maeda H. Fine-needle aspiration cytologic technique for lung cancer has a high potential of malignant cell spread through the tract. Chest. 2000;118:936–9.

    Article  CAS  Google Scholar 

  11. Kara M, Alver G, Sak SD, Kavukcu S. Implantation metastasis caused by fine needle aspiration biopsy following curative resection of stage IB non-small cell lung cancer. Eur J Cardiothorac Surg. 2001;20:868–70.

    Article  CAS  Google Scholar 

  12. NCCN. NCCN guidelines version 3 2018, non-small cell lung cancer; 2018. https://www.nccn.org/professinals/physician_fls/f_guidelinesasp#nscl.

  13. Takamochi K, Nagai K, Yoshida J, Suzuki K, Ohde Y, Nishimura M, et al. Pathologic N0 status in pulmonary adenocarcinoma is predictable by combining serum carcinoembryonic antigen level and computed tomographic findings. J Thorac Cardiovasc Surg. 2001;122:325–30.

    Article  CAS  Google Scholar 

  14. Edge SB, Compton CC. The American joint committee on cancer: the 7th of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17:1471–4.

    Article  Google Scholar 

  15. Travis WD, Brambilla E, Rami-Porta R, Vallieres E, Tsuboi M, Rusch V, et al. Visceral pleural invasion: pathologic criteria and use of elastic stains: proposal for the 7th of the TNM classification for lung cancer. J Thorac Oncol. 2008;3:1384–90.

    Article  Google Scholar 

  16. Hung JJ, Jeng WJ, Hsu WH, Chou TY, Lin SF, Wu YC. Prognostic significance of the extent of visceral pleural invasion in completely resected node-negative non-small cell lung cancer. Chest. 2012;142:141–50.

    Article  Google Scholar 

  17. Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, et al. International association for the study of lung cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011;6:244–85.

    Article  Google Scholar 

  18. Yoshizawa A, Motoi N, Riely GJ, Sima CS, Gerald WL, Kris MG, et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases. Mod Pathol. 2011;24:653–64.

    Article  CAS  Google Scholar 

  19. Yu YC, Hsu PK, Yeh YC, Huang CS, Hsieh CC, Chou TY, et al. Surgical results of synchronous multiple primary lung cancers: similar to the stage-matched solitary primary lung cancers? Ann Thorac Surg. 2013;96:1966–74.

    Article  Google Scholar 

  20. Dietel M, Bubendorf L, Dingemans AM, Dooms C, Elmberger G, Garcia RC, et al. Diagnostic procedures for non-small-cell lung cancer (NSCLC): recommendations of the European Expert Group. Thorax. 2016;71:177–84.

    Article  Google Scholar 

  21. Iida T, Shiba M, Yoshino I, Miyaoka E, Asamura H, Date H, et al. Surgical intervention for non-small-cell lung cancer patients with pleural carcinomatosis: results from the Japanese Lung Cancer Registry in 2004. J Thorac Oncol. 2015;10:1076–82.

    Article  Google Scholar 

  22. Okamoto T, Iwata T, Mizobuchi T, Hoshino H, Moriya Y, Yoshida S, et al. Pulmonary resection for lung cancer with malignant pleural disease first detected at thoracotomy. Eur J Cardiothorac Surg. 2012;41:25–30.

    Article  Google Scholar 

  23. Asakura K, Izumi Y, Yamauchi Y, Nakatsuka S, Inoue M, Yashiro H, et al. Incidence of pleural recurrence after computed tomography-guided needle biopsy in stage I lung cancer. PLoS ONE. 2012;7:e42043.

    Article  CAS  Google Scholar 

  24. Peters-Engl C, Konstantiniuk P, Tausch C, Haid A, Hoffmann B, Jagoutz-Herzlinger M, et al. The impact of preoperative breast biopsy on the risk of sentinel lymph node metastases: analysis of 2502 cases from the Austrian Sentinel Node Biopsy Study Group. Br J Cancer. 2004;91:1782–6.

    Article  CAS  Google Scholar 

  25. Martin RC 2nd, Scoggins CR, Ross MI, Reintgen DS, Noyes RD, Edwards MJ, McMasters KM. Is incisional biopsy of melanoma harmful? Am J Surg. 2005;190:913–7.

    PubMed  Google Scholar 

  26. Matsuoka T, Sonobe M, Date H. Intraoperative fine-needle aspiration biopsy (FNA) for lung cancer: diagnostic value and risk of pleural dissemination. Surg Today. 2015;45:695–9.

    Article  Google Scholar 

  27. Gould MK, Donington J, Lynch WR, Mazzone PJ, Midthun DE, Naidich DP, et al. Evaluation of individuals with pulmonary nodules: when is it lung cancer? Diagnosis and management of lung cancer, 3rd ed: American college of chest physicians evidence-based clinical practice guidelines. Chest. 2013;143:e93S–e120S.

    Article  Google Scholar 

  28. Broderick SR, Meyers BF. Pet staging of mediastinal lymph nodes in thoracic oncology. Thorac Surg Clin. 2012;22:161–6.

    Article  Google Scholar 

  29. Tsutani Y, Miyata Y, Nakayama H, Okumura S, Adachi S, Yoshimura M, et al. Prediction of pathologic node-negative clinical stage Ia lung adenocarcinoma for optimal candidates undergoing sublobar resection. J Thorac Cardiovasc Surg. 2012;144:1365–71.

    Article  Google Scholar 

  30. Quarterman RL, McMillan A, Ratcliffe MB, Block MI. Effect of preoperative delay on prognosis for patients with early stage non-small cell lung cancer. J Thorac Cardiovasc Surg. 2003;125:108–13 (discussion 13–4).

  31. Yanagawa N, Shiono S, Abiko M, Ogata SY, Sato T, Tamura G. New IASLC/ATS/ERS classification and invasive tumor size are predictive of disease recurrence in stage I lung adenocarcinoma. J Thorac Oncol. 2013;8:612–8.

    Article  Google Scholar 

  32. National Lung Screening Trial Research Trial, Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365:395–409.

  33. Grogan EL, Weinstein JJ, Deppen SA, Putnam JB Jr, Nesbitt JC, Lambright ES, et al. Thoracic operations for pulmonary nodules are frequently not futile in patients with benign disease. J Thorac Oncol. 2011;6:1720–5.

    Article  Google Scholar 

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Funding

Taipei Veterans General Hospital-National Yang-Ming University Excellent Physician Scientists Cultivation Program, No. 105-V-B-035.

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Authors and Affiliations

  1. Division of Thoracic Surgery, Department of Surgery, Taipei Veterans General Hospital, 201, Section 2, Shih-Pai Road, Taipei, Taiwan

    Chien-Sheng Huang, Po-Kuei Hsu, Wen-Hu Hsu & Biing-Shiun Huang

  2. Division of Cardiovascular Surgery, Department of Surgery, Taipei Veterans General Hospital, Taipei, Taiwan

    Chun-Che Shih

  3. Department of Radiology, Taipei Veterans General Hospital, Taipei, Taiwan

    Chun-Ku Chen & Mei-Han Wu

  4. Department of Pathology, Taipei Veterans General Hospital, Taipei, Taiwan

    Yi-Chen Yeh & Teh-Ying Chou

  5. Institute of Clinical Medicine, School of Medicine, National Yang-Ming University, Taipei, Taiwan

    Chien-Sheng Huang & Chun-Che Shih

  6. Institute of Health and Welfare Policy, National Yang-Ming University, Taipei, Taiwan

    Hui-Shan Chen

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  1. Chien-Sheng Huang
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Correspondence to Chien-Sheng Huang.

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Huang, CS., Hsu, PK., Chen, CK. et al. Preoperative biopsy and tumor recurrence of stage I adenocarcinoma of the lung. Surg Today 50, 673–684 (2020). https://doi.org/10.1007/s00595-019-01941-3

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  • DOI: https://doi.org/10.1007/s00595-019-01941-3

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