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      A standard for hilar and intrapulmonary lymph node dissection and pathological examination in early non-small cell lung cancer

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          Abstract

          Background

          There is considerable variation in the staging of lymph nodes (LNs) as part of tumor, node, metastasis (TNM) staging of non-small cell lung cancer (NSCLC). A new dissection and pathological examination standard for hilar and intrapulmonary LNs needs to be established for patients with early-stage T1–3N0M0 NSCLC.

          Methods

          This study involved 3,002 patients with T1–3N0M0 NSCLC who underwent radical lobectomy or total pneumonectomy in the thoracic departments of 11 Chinese institutions between January 1999 and October 2013. The Cox model was applied for univariate and multivariate analyses in the examination of station 10, 11 LN and station 12, 13, 14 LN. A hilar and intrapulmonary standard (HI standard) was then established based on univariate and multiple-factor analyses conducted using the Cox model.

          Results

          Among the 3,002 patients enrolled in the study, 2,609 underwent at least one examination of station 10, 11 LN (A1), while 393 did not undergo examination of station 10, 11 LN (A0). The A0 and A1 groups had 5-year survival rates of 76% and 80%, respectively (P=0.018). Further, 1,764 patients underwent at least one examination of station 12, 13, 14 LN (B1), while 1,238 patients did not (B0). The B0 and B1 groups had 5-year survival rates of 77% and 82%, respectively (P=0.008). In total, 1,269 patients attained the HI standard (C1), and 1,733 did not (C0). The C0 and C1 groups had 5-year survival rates of 77% and 83%, respectively (P<0.001).

          Conclusions

          The HI standard can improve both the prognosis and survival rates of patients with T1–3N0M0 NSCLC. This will provide important guidance for pulmonary LN dissection and pathological examination in NSCLC cases.

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          Most cited references20

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          Revised ESTS guidelines for preoperative mediastinal lymph node staging for non-small-cell lung cancer.

          Accurate preoperative staging and restaging of mediastinal lymph nodes in patients with potentially resectable non-small-cell lung cancer (NSCLC) is of paramount importance. In 2007, the European Society of Thoracic Surgeons (ESTS) published an algorithm on preoperative mediastinal staging integrating imaging, endoscopic and surgical techniques. In 2009, the International Association for the Study of Lung Cancer (IASLC) introduced a new lymph node map. Some changes in this map have an important impact on mediastinal staging. Moreover, more evidence of the different mediastinal staging technique has become available. Therefore, a revision of the ESTS guidelines was needed. In case of computed tomography (CT)-enlarged or positron emission tomography (PET)-positive mediastinal lymph nodes, tissue confirmation is indicated. Endosonography [endobronchial ultrasonography (EBUS)/esophageal ultrasonography (EUS)] with fine-needle aspiration (FNA) is the first choice (when available), since it is minimally invasive and has a high sensitivity to rule in mediastinal nodal disease. If negative, surgical staging with nodal dissection or biopsy is indicated. Video-assisted mediastinoscopy is preferred to mediastinoscopy. The combined use of endoscopic staging and surgical staging results in the highest accuracy. When there are no enlarged lymph nodes on CT and when there is no uptake in lymph nodes on PET or PET-CT, direct surgical resection with systematic nodal dissection is indicated for tumours ≤ 3 cm located in the outer third of the lung. In central tumours or N1 nodes, preoperative mediastinal staging is indicated. The choice between endoscopic staging with EBUS/EUS and FNA or video-assisted mediastinoscopy depends on local expertise to adhere to minimal requirements for staging. For tumours >3 cm, preoperative mediastinal staging is advised, mainly in adenocarcinoma with high standardized uptake value. For restaging, invasive techniques providing histological information are advisable. Both endoscopic techniques and surgical procedures are available, but their negative predictive value is lower compared with the results obtained in baseline staging. An integrated strategy using endoscopic staging techniques to prove mediastinal nodal disease and mediastinoscopy to assess nodal response after induction therapy needs further study.
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            ERS/ESTS clinical guidelines on fitness for radical therapy in lung cancer patients (surgery and chemo-radiotherapy).

            A collaboration of multidisciplinary experts on the functional evaluation of lung cancer patients has been facilitated by the European Respiratory Society (ERS) and the European Society of Thoracic Surgery (ESTS), in order to draw up recommendations and provide clinicians with clear, up-to-date guidelines on fitness for surgery and chemo-radiotherapy. The subject was divided into different topics, which were then assigned to at least two experts. The authors searched the literature according to their own strategies, with no central literature review being performed. The draft reports written by the experts on each topic were reviewed, discussed and voted on by the entire expert panel. The evidence supporting each recommendation was summarised, and graded as described by the Scottish Intercollegiate Guidelines Network Grading Review Group. Clinical practice guidelines were generated and finalized in a functional algorithm for risk stratification of the lung resection candidates, emphasising cardiological evaluation, forced expiratory volume in 1 s, systematic carbon monoxide lung diffusion capacity and exercise testing. Contrary to lung resection, for which the scientific evidences are more robust, we were unable to recommend any specific test, cut-off value, or algorithm before chemo-radiotherapy due to the lack of data. We recommend that lung cancer patients should be managed in specialised settings by multidisciplinary teams.
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              Association of Pathologic Nodal Staging Quality With Survival Among Patients With Non–Small Cell Lung Cancer After Resection With Curative Intent

              This study determines whether survival was affected by more stringent definitions of pathologic nodal staging quality in a cohort of patients with non–small cell lung cancer who underwent resection with curative intent. Question Does the thoroughness of pathologic nodal examination affect the prognostic value of pN classification in resectable non–small cell lung cancer? Findings In this study of 2047 patients with non–small cell lung cancer, sequential improvement in survival of pN0 and pN1 cohorts with increasing stringency was found. The pN1 cohorts with examination of 3 or more mediastinal nodal stations had the greatest survival improvements. Meaning The prognostic value of pN stratification depends on the thoroughness of examination, potentially accounting for a large proportion of the intercontinental differences in lung cancer survival; more thorough nodal examination practice must be disseminated to improve the prognostic value of the TNM staging system. Importance Pathologic nodal stage is the most significant prognostic factor in resectable non–small cell lung cancer (NSCLC). The International Association for the Study of Lung Cancer NSCLC staging project revealed intercontinental differences in N category–stratified survival. These differences may indicate differences not only in cancer biology but also in the thoroughness of the nodal examination. Objective To determine whether survival was affected by sequentially more stringent definitions of pN staging quality in a cohort of patients with NSCLC after resection with curative intent. Design This observational study used the Mid-South Quality of Surgical Resection cohort, a population-based database of lung cancer resections with curative intent. A total of 2047 consecutive patients who underwent surgical resection at 11 hospitals with at least 5 annual lung cancer resections in 4 contiguous US Dartmouth hospital referral regions in northern Mississippi, eastern Arkansas, and western Tennessee (>90% of the eligible population) were included. Resections were performed from January 1, 2009, through January 25, 2016. Survival was evaluated with the Kaplan-Meier method and Cox proportional hazards models. Exposures Eight sequentially more stringent pN staging quality strata included the following: all patients (group 1); those with complete resections only (group 2); those with examination of at least 1 mediastinal lymph node (group 3); those with examination of at least 10 lymph nodes (group 4); those with examination of at least 3 hilar or intrapulmonary and at least 3 mediastinal lymph nodes (group 5); those with examination of at least 10 lymph nodes, including at least 1 mediastinal lymph node (group 6); those with examination of at least 1 hilar or intrapulmonary and at least 3 mediastinal nodal stations (group 7); and those with examination of at least 1 hilar or intrapulmonary lymph node, at least 10 total lymph nodes, and at least 3 mediastinal nodal stations (group 8). Main Outcomes and Measures N category–stratified overall survival. Results Of the total 2047 patients (1046 men [51.1%] and 1001 women [48.9%]; mean [SD] age, 67.0 [9.6] years) included in the analysis, the eligible analysis population ranged from 541 to 2047, depending on stringency. Sequential improvement in the N category–stratified 5-year survival of pN0 and pN1 tumors was found from the least stringent group (0.63 [95% CI, 0.59-0.66] for pN0 vs 0.46 [95% CI, 0.38-0.54] for pN1) to the most stringent group (0.71 [95% CI, 0.60-0.79] for pN0 vs 0.60 [95% CI, 0.43-0.73] for pN1). The pN1 cohorts with 3 or more mediastinal nodal stations examined had the most striking survival improvements. More stringently defined mediastinal nodal examination was associated with better separation in survival curves between patients with pN1 and pN2 tumors. Conclusions and Relevance The prognostic value of pN stratification depends on the thoroughness of examination. Differences in thoroughness of nodal staging may explain a large proportion of intercontinental survival differences. More thorough nodal examination practice must be disseminated to improve the prognostic value of the TNM staging system. Future updates of the TNM staging system should incorporate more quality restraints.
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                Author and article information

                Journal
                Transl Lung Cancer Res
                Transl Lung Cancer Res
                TLCR
                Translational Lung Cancer Research
                AME Publishing Company
                2218-6751
                2226-4477
                December 2021
                December 2021
                : 10
                : 12
                : 4587-4599
                Affiliations
                [1 ]Department of Thoracic Surgery, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China , deptCollaborative Innovation Center for Cancer Medicine , Guangzhou, China;
                [2 ]Department of Medical Oncology, Cancer Hospital of University of Chinese Academy of Sciences , deptZhejiang Cancer Hospital , Hangzhou, China;
                [3 ]deptDepartment of Thoracic Surgery , Affiliated Hospital of Qingdao University , Qingdao, China;
                [4 ]deptDepartment of Breast Surgery , Affiliated Tumor Hospital of Guangxi Medical University , Nanning, China;
                [5 ]Medical College of Nanchang University , Nanchang, China;
                [6 ]deptDepartment of Clinic Medicine, School of Queen Mary , Nanchang University , Nanchang, China;
                [7 ]Department of Thoracic Surgery, Nantong Third People’s Hospital Nantong University, Nantong , China;
                [8 ]deptDepartment of Thoracic Surgery , Ningbo First Hospital of Zhejiang University , Ningbo, China;
                [9 ]Department of Thoracic Surgery, Affiliated Jiangyin Hospital of Southeast University, Jiangyin , China;
                [10 ]deptDepartment of Pathology , The Second Hospital of Jilin University , Changchun, China;
                [11 ]deptDepartment of Thoracic Surgery, The Second Affiliated Hospital of Medical College , Xi’an Jiaotong University , Xi’an, China;
                [12 ]deptDepartment of Thoracic Surgery, Taizhou Hospital of Zhejiang Province , Wenzhou Medical University , Taizhou, China;
                [13 ]Department of Respiratory Medicine,, Affiliated Jinling Hospital, Medical School of Nanjing University , Nanjing, China;
                [14 ]deptDivision of Thoracic Surgery, Faculty of Medicine , University of Ottawa , Ottawa, ON, Canada;
                [15 ]deptDepartments of Outcomes Research and General Anesthesia, Anesthesiology Institute , Cleveland Clinic , Cleveland, OH, USA;
                [16 ]deptSection of Thoracic Surgery, Department of Surgery, Miller School of Medicine , University of Miami , Miami, FL, USA;
                [17 ]deptDepartment of Statistics , Southern Medical University , Guangzhou, China;
                [18 ]deptDepartment of Interventional Oncology, The First Affiliated Hospital , Sun Yat-sen University , Guangzhou, China
                Author notes

                Contributions: (I) Conception and design: W Yao, Z Zhu, H Yang; (II) Administrative support: Z Song, W Jiao, C Xu, Q Huang, C An, J Shi, G Yu, P Sun, Y Zhang, J Shen; (III) Provision of study materials or patients: Q Huang, C An, J Shi, G Yu, P Sun, Y Zhang, J Shen, Z Zhu; (IV) Collection and assembly of data: W Mei, L Zhu; (V) Data analysis and interpretation: J Qian, L Zhu; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

                [#]

                These authors contributed equally to this work.

                Correspondence to: Chunwei Xu, MD, PhD. Department of Respiratory Medicine, Affiliated Jinling Hospital, Medical School of Nanjing University, 305 Zhongshan Road, Nanjing 210002, China. Email: xuchunweibbb@ 123456163.com ; Jun Qian, PhD. Department of Statistics, Southern Medical University, 1023 Shatainan Road, Guangzhou 510515, China. Email: qianjun_gz@ 123456126.com ; Dr. Wang Yao, MD. Department of Interventional Oncology, The First Affiliated Hospital, Sun Yat-sen University, 58 Zhongshan Second Road, Guangzhou 510060, China. Email: yaow7@ 123456mail.sysu.edu.cn ; Dr. Han Yang, MD, PhD. Department of Thoracic Surgery, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, 651 Dongfeng Road East, Guangzhou 510060, China. Email: yanghan@ 123456sysucc.org.cn .
                Article
                tlcr-10-12-4587
                10.21037/tlcr-21-959
                8743510
                35070763
                660eca73-3844-4b5b-8e82-05ff614ed697
                2021 Translational Lung Cancer Research. All rights reserved.

                Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0.

                History
                : 27 October 2021
                : 23 December 2021
                Categories
                Original Article

                non-small cell lung cancer (nsclc),lymph node dissection (ln dissection),early stage,pathological examination standard

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