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Decreasing Prevalence of Benign Etiology in Resected Lung Nodules Suspicious for Lung Cancer over the Last Decade

  • Author Footnotes
    1 Zelin Ma, Yang Zhang and Qingyuan Huang contributed equally to this work.
    ,
    Author Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Zelin Ma
    Footnotes
    1 Zelin Ma, Yang Zhang and Qingyuan Huang contributed equally to this work.
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Affiliations
    Department of Thoracic Surgery and State Key Laboratory of Genetic Engineering, Fudan University Shanghai Cancer Center, Shanghai, China

    Institution of Thoracic Oncology, Fudan University, Shanghai, China

    Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    1 Zelin Ma, Yang Zhang and Qingyuan Huang contributed equally to this work.
    ,
    Author Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Yang Zhang
    Footnotes
    1 Zelin Ma, Yang Zhang and Qingyuan Huang contributed equally to this work.
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Affiliations
    Department of Thoracic Surgery and State Key Laboratory of Genetic Engineering, Fudan University Shanghai Cancer Center, Shanghai, China

    Institution of Thoracic Oncology, Fudan University, Shanghai, China

    Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    1 Zelin Ma, Yang Zhang and Qingyuan Huang contributed equally to this work.
    ,
    Author Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Qingyuan Huang
    Footnotes
    1 Zelin Ma, Yang Zhang and Qingyuan Huang contributed equally to this work.
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Affiliations
    Department of Thoracic Surgery and State Key Laboratory of Genetic Engineering, Fudan University Shanghai Cancer Center, Shanghai, China

    Institution of Thoracic Oncology, Fudan University, Shanghai, China

    Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Fangqiu Fu
    Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Affiliations
    Department of Thoracic Surgery and State Key Laboratory of Genetic Engineering, Fudan University Shanghai Cancer Center, Shanghai, China

    Institution of Thoracic Oncology, Fudan University, Shanghai, China

    Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Chaoqiang Deng
    Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Affiliations
    Department of Thoracic Surgery and State Key Laboratory of Genetic Engineering, Fudan University Shanghai Cancer Center, Shanghai, China

    Institution of Thoracic Oncology, Fudan University, Shanghai, China

    Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    3 Shengping Wang is a radiologist and Yuan Li is a pathologist.
    Shengping Wang
    Footnotes
    3 Shengping Wang is a radiologist and Yuan Li is a pathologist.
    Affiliations
    Institution of Thoracic Oncology, Fudan University, Shanghai, China

    Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China

    Department of Radiology, Fudan University Shanghai Cancer Center, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    3 Shengping Wang is a radiologist and Yuan Li is a pathologist.
    Yuan Li
    Footnotes
    3 Shengping Wang is a radiologist and Yuan Li is a pathologist.
    Affiliations
    Institution of Thoracic Oncology, Fudan University, Shanghai, China

    Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China

    Department of Pathology, Fudan University Shanghai Cancer Center, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Haiquan Chen
    Correspondence
    Address reprint requests to Haiquan Chen, MD, PhD, Department of Thoracic Surgery, Fudan University Shanghai Cancer Center, 270 Dong-An Road, Shanghai 200032, China.
    Footnotes
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    Affiliations
    Department of Thoracic Surgery and State Key Laboratory of Genetic Engineering, Fudan University Shanghai Cancer Center, Shanghai, China

    Institution of Thoracic Oncology, Fudan University, Shanghai, China

    Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
    Search for articles by this author
  • Author Footnotes
    1 Zelin Ma, Yang Zhang and Qingyuan Huang contributed equally to this work.
    2 Zelin Ma, Yang Zhang, Qingyuan Huang, Fangqiu Fu, Chaoqiang Deng and Haquan Chen are thoracic surgeons.
    3 Shengping Wang is a radiologist and Yuan Li is a pathologist.
      This study investigated treatment strategy for suspicious lung cancer with postoperatively proven benign etiology. In this retrospective study, we collected patients who underwent pulmonary resection for radiologically suspected lung cancer from 2010 to 2019 at Department of Thoracic Surgery, Fudan University Shanghai Cancer Center (FUSCC). Radiological features, preoperative follow-up time, preoperative pathology and postoperative pathology of these patients were documented. We classified resected benign lesions based on paraffin section and compared the therapy management performed on indeterminate lung nodules of 2 time periods (2010–2014 vs 2015–2019). 17,188 patients were included in this cohort and 1,381 (8.03%) cases were postoperatively proved to be benign lesions. Resected benign lesions proportion significantly decreased by years, from 14.5–6.2%. The respective resected benign lesions proportions for pure GGO nodules, part solid nodules and solid nodules were 5.3%, 3.0% and 11.7%. The resected benign lesions rate for patients with longer preoperative follow-up time was much lower (p < 0.001). Among the benign lesions, 14.2% were benign tumors, 25.7% were granulomatous, 30.2% were pneumonia, 18.0% were fibrosis and 11.9% were other types. If we consider that resections for granulomatous and pneumonia radiologically featured as solid nodules exceeding 2 cm, benign tumor and inflammatory pseudotumor are therapeutic, the nontherapeutic pulmonary resection rate is 4.26%. For patients with GGO nodules, the median preoperative follow-up time increased with the time being and the resected benign rate in period 2 (2015–2019) was significantly lower than that in period 1 (2010–2014). Wedge resection was the most common surgery strategy especially for small nodules and no matter for small or large nodules, the frequency of sublobar resection in period 2 was higher than that in period 1. The resected benign lesions rate at our department was relatively low and decreasing over the last decade. Meanwhile, our follow-up and surgical strategy improved over time. For patients with GGO nodules, 4-6months preoperative follow-up is recommended to avoid surgical intervention for benign lesions. For solid nodules with inconclusive diagnosis, limited resection should be first considered to maintain the balance between reducing the risk of cancer progressing and minimizing the resection for benign lesions.

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      REFERENCES

        • Callister M.E.
        • Baldwin D.R.
        How should pulmonary nodules be optimally investigated and managed?.
        Lung Cancer. 2016; 91: 48-55
        • Wood D.E.
        • Kazerooni E.A.
        • Baum S.L.
        • et al.
        Lung cancer screening, version 3.2018, NCCN clinical practice guidelines in oncology.
        J Natl Compr Canc Netw. 2018; 16: 412-441
        • Zhang Y.
        • Jheon S.
        • Li H.
        • et al.
        Results of low-dose computed tomography as a regular health examination among Chinese hospital employees.
        J Thorac Cardiovasc Surg. 2019; 160: 824-831
        • Team N.L.S.T.R.
        • Aberle D.R.
        • Adams A.M.
        • et al.
        Reduced lung-cancer mortality with low-dose computed tomographic screening.
        N. Engl. J. Med. 2011; 365: 395-409
        • Smith M.A.
        • Battafarano R.J.
        • Meyers B.F.
        • et al.
        Prevalence of benign disease in patients undergoing resection for suspected lung cancer.
        Ann Thorac Surg. 2006; 81 (discussion 1828-9): 1824-1828
        • Grogan E.L.
        • Weinstein J.J.
        • Deppen S.A.
        • et al.
        Thoracic operations for pulmonary nodules are frequently not futile in patients with benign disease.
        J Thorac Oncol. 2011; 6: 1720-1725
        • Andalib A.
        • Ramana-Kumar A.V.
        • Bartlett G.
        • et al.
        Influence of postoperative infectious complications on long-term survival of lung cancer patients: a population-based cohort study.
        J Thorac Oncol. 2013; 8: 554-561
        • Rosen J.E.
        • Hancock J.G.
        • Kim A.W.
        • et al.
        Predictors of mortality after surgical management of lung cancer in the National Cancer Database.
        Ann Thorac Surg. 2014; 98: 1953-1960
        • Altorki N.K.
        • Wang X.
        • Wigle D.
        • et al.
        Perioperative mortality and morbidity after sublobar versus lobar resection for early-stage non-small-cell lung cancer: post-hoc analysis of an international, randomised, phase 3 trial (CALGB/Alliance 140503).
        Lancet Respir Med. 2018; 6: 915-924
        • Patz Jr., E.F.
        • Pinsky P.
        • Gatsonis C.
        • et al.
        Overdiagnosis in low-dose computed tomography screening for lung cancer.
        JAMA Intern Med. 2014; 174: 269-274
        • Bach P.B.
        • Mirkin J.N.
        • Oliver T.K.
        • et al.
        Benefits and harms of CT screening for lung cancer: a systematic review.
        Jama. 2012; 307: 2418-2429
        • Ten Haaf K.
        • de Koning H.J.
        Overdiagnosis in lung cancer screening: why modelling is essential.
        J Epidemiol Community Health. 2015; 69: 1035-1039
        • Lien Y.C.
        • Hsu H.S.
        • Li W.Y.
        • et al.
        Pulmonary hamartoma.
        J Chin Med Assoc. 2004; 67: 21-26
        • Matsuda E.
        • Okabe K.
        • Kobayashi S.
        • et al.
        Pulmonary hamartoma associated with lung cancer.
        Kyobu Geka. 2010; 63: 875-878
        • Hirai S.
        • Katayama T.
        • Chatani N.
        • et al.
        Inflammatory pseudotumor suspected of lung cancer treated by thoracoscopic resection.
        Ann Thorac Cardiovasc Surg. 2011; 17: 48-52
        • Fabre D.
        • Fadel E.
        • Singhal S.
        • et al.
        Complete resection of pulmonary inflammatory pseudotumors has excellent long-term prognosis.
        J Thorac Cardiovasc Surg. 2009; 137: 435-440
        • Travis W.D.
        • Brambilla E.
        • Nicholson A.G.
        • et al.
        The 2015 world health organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classification.
        J Thorac Oncol. 2015; 10: 1243-1260
        • Hsu L.
        • Achkar J.M.
        • Keller S.M.
        • et al.
        National trends in benign pulmonary resections: association with CT and PET imaging.
        Chest. 2015; 147: e61-e62
        • Kuo E.
        • Bharat A.
        • Bontumasi N.
        • et al.
        Impact of video-assisted thoracoscopic surgery on benign resections for solitary pulmonary nodules.
        Ann Thorac Surg. 2012; 93 (discussion 272-3): 266-272
        • Field J.K.
        • Smith R.A.
        • Aberle D.R.
        • et al.
        International association for the study of lung cancer computed tomography screening workshop 2011 report.
        J Thorac Oncol. 2012; 7: 10-19
        • Lee H.Y.
        • Lee K.S.
        Ground-glass opacity nodules: histopathology, imaging evaluation, and clinical implications.
        J Thorac Imaging. 2011; 26: 106-118
        • Ye T.
        • Deng L.
        • Wang S.
        • et al.
        Lung adenocarcinomas manifesting as radiological part-solid nodules define a special clinical subtype.
        J Thorac Oncol. 2019; 14: 617-627
        • Fu F.
        • Zhang Y.
        • Wen Z.
        • et al.
        Distinct prognostic factors in patients with stage I Non–small cell lung cancer with radiologic part-solid or solid lesions.
        J Thorac Oncol. 2019; 14: 2133-2142
        • Zhang Y.
        • Fu F.
        • Chen H.
        Management of ground-glass opacities in the lung cancer spectrum.
        Ann Thorac Surg. 2020; 110: 1796-1804
        • Zhang J.
        • Gold K.A.
        • Lin H.Y.
        • et al.
        Relationship between tumor size and survival in non-small-cell lung cancer (NSCLC): an analysis of the surveillance, epidemiology, and end results (SEER) registry.
        J Thorac Oncol. 2015; 10: 682-690
        • Choi E.K.
        • Park H.L.
        • Yoo I.R.
        • et al.
        The clinical value of F-18 FDG PET/CT in differentiating malignant from benign lesions in pneumoconiosis patients.
        Eur Radiol. 2020; 30: 442-451
      1. Kagimoto A., Tsutani Y., Handa Y., et al: Patient selection of sublobar resection using visual evaluation of positron-emission tomography (PET) for early-stage lung adenocarcinoma. 2020

        • Wahidi M.M.
        • Govert J.A.
        • Goudar R.K.
        • et al.
        Evidence for the treatment of patients with pulmonary nodules: when is it lung cancer?: ACCP evidence-based clinical practice guidelines (2nd edition).
        Chest. 2007; 132: 94s-107s
        • Rui Y.
        • Han M.
        • Zhou W.
        • et al.
        Non-malignant pathological results on transthoracic CT guided core-needle biopsy: when is benign really benign?.
        Clin Radiol. 2018; 73 (757.e1-757.e7)
        • Fontaine-Delaruelle C.
        • Souquet P.J.
        • Gamondes D.
        • et al.
        Negative predictive value of transthoracic core-needle biopsy: A multicenter study.
        Chest. 2015; 148: 472-480
        • Gelbman B.D.
        • Cham M.D.
        • Kim W.
        • et al.
        Radiographic and clinical characterization of false negative results from CT-guided needle biopsies of lung nodules.
        J Thorac Oncol. 2012; 7: 815-820
      2. National Comprehensive Cancer Network Guidelines in Oncology. Non-Small Cell Lung Cancer (Version 8.2020). https://www.nccn.org/professionals/physician_gls/pdf/nscl.pdf. Accessed September 15,2020.

        • Sakakibara Y.
        • Suzuki Y.
        • Fujie T.
        • et al.
        Radiopathological features and identification of mycobacterial infections in granulomatous nodules resected from the lung.
        Respiration. 2017; 93: 264-270

      Linked Article

      • Commentary: Reducing Resection of Benign Pulmonary Nodules – A Laudable Goal, but How and at What Cost?
        Seminars in Thoracic and Cardiovascular SurgeryVol. 34Issue 3
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          The most recent United States Preventive Services Task Force Recommendations have expanded lung cancer screening with annual low dose computed tomography (CT) scan to adults from 50 to 80 years old with a 20 pack-year smoking history within the past 15 years.1 These guidelines are based on the National Lung Screening Trial and the Dutch-Belgian lung cancer screening trial (Nederlands-Leuvens Longkanker Screenings Onderzoek), performed within the last decade.2,3 To standardize the interpretation of these screening CT scans, the American College of Radiology developed the Lung Imaging Reporting and Data System (Lung-RADS) to classify lung nodules and determine the need for further imaging or intervention.
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