Segmentectomy versus lobectomy in small-sized peripheral non-small-cell lung cancer (JCOG0802/WJOG4607L): a multicentre, open-label, phase 3, randomised, controlled, non-inferiority trial

Lobectomy is the standard of care for early-stage non-small-cell lung cancer (NSCLC). The survival and clinical benefits of segmentectomy have not been investigated in a randomised trial setting. We aimed to investigate if segmentectomy was non-inferior to lobectomy in patients with small-sized peri...

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Veröffentlicht in:The Lancet (British edition) Jg. 399; H. 10335; S. 1607 - 1617
Hauptverfasser: Saji, Hisashi, Okada, Morihito, Tsuboi, Masahiro, Nakajima, Ryu, Suzuki, Kenji, Aokage, Keiju, Aoki, Tadashi, Okami, Jiro, Yoshino, Ichiro, Ito, Hiroyuki, Okumura, Norihito, Yamaguchi, Masafumi, Ikeda, Norihiko, Wakabayashi, Masashi, Nakamura, Kenichi, Fukuda, Haruhiko, Nakamura, Shinichiro, Mitsudomi, Tetsuya, Watanabe, Shun-Ichi, Asamura, Hisao
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Sprache:Englisch
Veröffentlicht: England Elsevier Ltd 23.04.2022
Elsevier Limited
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ISSN:0140-6736, 1474-547X, 1474-547X
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Abstract Lobectomy is the standard of care for early-stage non-small-cell lung cancer (NSCLC). The survival and clinical benefits of segmentectomy have not been investigated in a randomised trial setting. We aimed to investigate if segmentectomy was non-inferior to lobectomy in patients with small-sized peripheral NSCLC. We conducted this randomised, controlled, non-inferiority trial at 70 institutions in Japan. Patients with clinical stage IA NSCLC (tumour diameter ≤2 cm; consolidation-to-tumour ratio >0·5) were randomly assigned 1:1 to receive either lobectomy or segmentectomy. Randomisation was done via the minimisation method, with balancing for the institution, histological type, sex, age, and thin-section CT findings. Treatment allocation was not concealed from investigators and patients. The primary endpoint was overall survival for all randomly assigned patients. The secondary endpoints were postoperative respiratory function (6 months and 12 months), relapse-free survival, proportion of local relapse, adverse events, proportion of segmentectomy completion, duration of hospital stay, duration of chest tube placement, duration of surgery, amount of blood loss, and the number of automatic surgical staples used. Overall survival was analysed on an intention-to-treat basis with a non-inferiority margin of 1·54 for the upper limit of the 95% CI of the hazard ratio (HR) and estimated using a stratified Cox regression model. This study is registered with UMIN Clinical Trials Registry, UMIN000002317. Between Aug, 10, 2009, and Oct 21, 2014, 1106 patients (intention-to-treat population) were enrolled to receive lobectomy (n=554) or segmentectomy (n=552). Patient baseline clinicopathological factors were well balanced between the groups. In the segmentectomy group, 22 patients were switched to lobectomies and one patient received wide wedge resection. At a median follow-up of 7·3 years (range 0·0–10·9), the 5-year overall survival was 94·3% (92·1–96·0) for segmentectomy and 91·1% for lobectomy (95% CI 88·4–93·2); superiority and non-inferiority in overall survival were confirmed using a stratified Cox regression model (HR 0·663; 95% CI 0·474–0·927; one-sided p<0·0001 for non-inferiority; p=0·0082 for superiority). Improved overall survival was observed consistently across all predefined subgroups in the segmentectomy group. At 1 year follow-up, the significant difference in the reduction of median forced expiratory volume in 1 sec between the two groups was 3·5% (p<0·0001), which did not reach the predefined threshold for clinical significance of 10%. The 5-year relapse-free survival was 88·0% (95% CI 85·0–90·4) for segmentectomy and 87·9% (84·8–90·3) for lobectomy (HR 0·998; 95% CI 0·753–1·323; p=0·9889). The proportions of patients with local relapse were 10·5% for segmentectomy and 5·4% for lobectomy (p=0·0018). 52 (63%) of 83 patients and 27 (47%) of 58 patients died of other diseases after lobectomy and segmentectomy, respectively. No 30-day or 90-day mortality was observed. One or more postoperative complications of grade 2 or worse occurred at similar frequencies in both groups (142 [26%] patients who received lobectomy, 148 [27%] who received segmentectomy). To our knowledge, this study was the first phase 3 trial to show the benefits of segmentectomy versus lobectomy in overall survival of patients with small-peripheral NSCLC. The findings suggest that segmentectomy should be the standard surgical procedure for this population of patients. National Cancer Center Research and the Ministry of Health, Labour, and Welfare of Japan.
AbstractList Lobectomy is the standard of care for early-stage non-small-cell lung cancer (NSCLC). The survival and clinical benefits of segmentectomy have not been investigated in a randomised trial setting. We aimed to investigate if segmentectomy was non-inferior to lobectomy in patients with small-sized peripheral NSCLC. We conducted this randomised, controlled, non-inferiority trial at 70 institutions in Japan. Patients with clinical stage IA NSCLC (tumour diameter ≤2 cm; consolidation-to-tumour ratio >0·5) were randomly assigned 1:1 to receive either lobectomy or segmentectomy. Randomisation was done via the minimisation method, with balancing for the institution, histological type, sex, age, and thin-section CT findings. Treatment allocation was not concealed from investigators and patients. The primary endpoint was overall survival for all randomly assigned patients. The secondary endpoints were postoperative respiratory function (6 months and 12 months), relapse-free survival, proportion of local relapse, adverse events, proportion of segmentectomy completion, duration of hospital stay, duration of chest tube placement, duration of surgery, amount of blood loss, and the number of automatic surgical staples used. Overall survival was analysed on an intention-to-treat basis with a non-inferiority margin of 1·54 for the upper limit of the 95% CI of the hazard ratio (HR) and estimated using a stratified Cox regression model. This study is registered with UMIN Clinical Trials Registry, UMIN000002317. Between Aug, 10, 2009, and Oct 21, 2014, 1106 patients (intention-to-treat population) were enrolled to receive lobectomy (n=554) or segmentectomy (n=552). Patient baseline clinicopathological factors were well balanced between the groups. In the segmentectomy group, 22 patients were switched to lobectomies and one patient received wide wedge resection. At a median follow-up of 7·3 years (range 0·0–10·9), the 5-year overall survival was 94·3% (92·1–96·0) for segmentectomy and 91·1% for lobectomy (95% CI 88·4–93·2); superiority and non-inferiority in overall survival were confirmed using a stratified Cox regression model (HR 0·663; 95% CI 0·474–0·927; one-sided p<0·0001 for non-inferiority; p=0·0082 for superiority). Improved overall survival was observed consistently across all predefined subgroups in the segmentectomy group. At 1 year follow-up, the significant difference in the reduction of median forced expiratory volume in 1 sec between the two groups was 3·5% (p<0·0001), which did not reach the predefined threshold for clinical significance of 10%. The 5-year relapse-free survival was 88·0% (95% CI 85·0–90·4) for segmentectomy and 87·9% (84·8–90·3) for lobectomy (HR 0·998; 95% CI 0·753–1·323; p=0·9889). The proportions of patients with local relapse were 10·5% for segmentectomy and 5·4% for lobectomy (p=0·0018). 52 (63%) of 83 patients and 27 (47%) of 58 patients died of other diseases after lobectomy and segmentectomy, respectively. No 30-day or 90-day mortality was observed. One or more postoperative complications of grade 2 or worse occurred at similar frequencies in both groups (142 [26%] patients who received lobectomy, 148 [27%] who received segmentectomy). To our knowledge, this study was the first phase 3 trial to show the benefits of segmentectomy versus lobectomy in overall survival of patients with small-peripheral NSCLC. The findings suggest that segmentectomy should be the standard surgical procedure for this population of patients. National Cancer Center Research and the Ministry of Health, Labour, and Welfare of Japan.
Lobectomy is the standard of care for early-stage non-small-cell lung cancer (NSCLC). The survival and clinical benefits of segmentectomy have not been investigated in a randomised trial setting. We aimed to investigate if segmentectomy was non-inferior to lobectomy in patients with small-sized peripheral NSCLC.BACKGROUNDLobectomy is the standard of care for early-stage non-small-cell lung cancer (NSCLC). The survival and clinical benefits of segmentectomy have not been investigated in a randomised trial setting. We aimed to investigate if segmentectomy was non-inferior to lobectomy in patients with small-sized peripheral NSCLC.We conducted this randomised, controlled, non-inferiority trial at 70 institutions in Japan. Patients with clinical stage IA NSCLC (tumour diameter ≤2 cm; consolidation-to-tumour ratio >0·5) were randomly assigned 1:1 to receive either lobectomy or segmentectomy. Randomisation was done via the minimisation method, with balancing for the institution, histological type, sex, age, and thin-section CT findings. Treatment allocation was not concealed from investigators and patients. The primary endpoint was overall survival for all randomly assigned patients. The secondary endpoints were postoperative respiratory function (6 months and 12 months), relapse-free survival, proportion of local relapse, adverse events, proportion of segmentectomy completion, duration of hospital stay, duration of chest tube placement, duration of surgery, amount of blood loss, and the number of automatic surgical staples used. Overall survival was analysed on an intention-to-treat basis with a non-inferiority margin of 1·54 for the upper limit of the 95% CI of the hazard ratio (HR) and estimated using a stratified Cox regression model. This study is registered with UMIN Clinical Trials Registry, UMIN000002317.METHODSWe conducted this randomised, controlled, non-inferiority trial at 70 institutions in Japan. Patients with clinical stage IA NSCLC (tumour diameter ≤2 cm; consolidation-to-tumour ratio >0·5) were randomly assigned 1:1 to receive either lobectomy or segmentectomy. Randomisation was done via the minimisation method, with balancing for the institution, histological type, sex, age, and thin-section CT findings. Treatment allocation was not concealed from investigators and patients. The primary endpoint was overall survival for all randomly assigned patients. The secondary endpoints were postoperative respiratory function (6 months and 12 months), relapse-free survival, proportion of local relapse, adverse events, proportion of segmentectomy completion, duration of hospital stay, duration of chest tube placement, duration of surgery, amount of blood loss, and the number of automatic surgical staples used. Overall survival was analysed on an intention-to-treat basis with a non-inferiority margin of 1·54 for the upper limit of the 95% CI of the hazard ratio (HR) and estimated using a stratified Cox regression model. This study is registered with UMIN Clinical Trials Registry, UMIN000002317.Between Aug, 10, 2009, and Oct 21, 2014, 1106 patients (intention-to-treat population) were enrolled to receive lobectomy (n=554) or segmentectomy (n=552). Patient baseline clinicopathological factors were well balanced between the groups. In the segmentectomy group, 22 patients were switched to lobectomies and one patient received wide wedge resection. At a median follow-up of 7·3 years (range 0·0-10·9), the 5-year overall survival was 94·3% (92·1-96·0) for segmentectomy and 91·1% for lobectomy (95% CI 88·4-93·2); superiority and non-inferiority in overall survival were confirmed using a stratified Cox regression model (HR 0·663; 95% CI 0·474-0·927; one-sided p<0·0001 for non-inferiority; p=0·0082 for superiority). Improved overall survival was observed consistently across all predefined subgroups in the segmentectomy group. At 1 year follow-up, the significant difference in the reduction of median forced expiratory volume in 1 sec between the two groups was 3·5% (p<0·0001), which did not reach the predefined threshold for clinical significance of 10%. The 5-year relapse-free survival was 88·0% (95% CI 85·0-90·4) for segmentectomy and 87·9% (84·8-90·3) for lobectomy (HR 0·998; 95% CI 0·753-1·323; p=0·9889). The proportions of patients with local relapse were 10·5% for segmentectomy and 5·4% for lobectomy (p=0·0018). 52 (63%) of 83 patients and 27 (47%) of 58 patients died of other diseases after lobectomy and segmentectomy, respectively. No 30-day or 90-day mortality was observed. One or more postoperative complications of grade 2 or worse occurred at similar frequencies in both groups (142 [26%] patients who received lobectomy, 148 [27%] who received segmentectomy).FINDINGSBetween Aug, 10, 2009, and Oct 21, 2014, 1106 patients (intention-to-treat population) were enrolled to receive lobectomy (n=554) or segmentectomy (n=552). Patient baseline clinicopathological factors were well balanced between the groups. In the segmentectomy group, 22 patients were switched to lobectomies and one patient received wide wedge resection. At a median follow-up of 7·3 years (range 0·0-10·9), the 5-year overall survival was 94·3% (92·1-96·0) for segmentectomy and 91·1% for lobectomy (95% CI 88·4-93·2); superiority and non-inferiority in overall survival were confirmed using a stratified Cox regression model (HR 0·663; 95% CI 0·474-0·927; one-sided p<0·0001 for non-inferiority; p=0·0082 for superiority). Improved overall survival was observed consistently across all predefined subgroups in the segmentectomy group. At 1 year follow-up, the significant difference in the reduction of median forced expiratory volume in 1 sec between the two groups was 3·5% (p<0·0001), which did not reach the predefined threshold for clinical significance of 10%. The 5-year relapse-free survival was 88·0% (95% CI 85·0-90·4) for segmentectomy and 87·9% (84·8-90·3) for lobectomy (HR 0·998; 95% CI 0·753-1·323; p=0·9889). The proportions of patients with local relapse were 10·5% for segmentectomy and 5·4% for lobectomy (p=0·0018). 52 (63%) of 83 patients and 27 (47%) of 58 patients died of other diseases after lobectomy and segmentectomy, respectively. No 30-day or 90-day mortality was observed. One or more postoperative complications of grade 2 or worse occurred at similar frequencies in both groups (142 [26%] patients who received lobectomy, 148 [27%] who received segmentectomy).To our knowledge, this study was the first phase 3 trial to show the benefits of segmentectomy versus lobectomy in overall survival of patients with small-peripheral NSCLC. The findings suggest that segmentectomy should be the standard surgical procedure for this population of patients.INTERPRETATIONTo our knowledge, this study was the first phase 3 trial to show the benefits of segmentectomy versus lobectomy in overall survival of patients with small-peripheral NSCLC. The findings suggest that segmentectomy should be the standard surgical procedure for this population of patients.National Cancer Center Research and the Ministry of Health, Labour, and Welfare of Japan.FUNDINGNational Cancer Center Research and the Ministry of Health, Labour, and Welfare of Japan.
Summary Background Lobectomy is the standard of care for early-stage non-small-cell lung cancer (NSCLC). The survival and clinical benefits of segmentectomy have not been investigated in a randomised trial setting. We aimed to investigate if segmentectomy was non-inferior to lobectomy in patients with small-sized peripheral NSCLC. Methods We conducted this randomised, controlled, non-inferiority trial at 70 institutions in Japan. Patients with clinical stage IA NSCLC (tumour diameter ≤2 cm; consolidation-to-tumour ratio >0·5) were randomly assigned 1:1 to receive either lobectomy or segmentectomy. Randomisation was done via the minimisation method, with balancing for the institution, histological type, sex, age, and thin-section CT findings. Treatment allocation was not concealed from investigators and patients. The primary endpoint was overall survival for all randomly assigned patients. The secondary endpoints were postoperative respiratory function (6 months and 12 months), relapse-free survival, proportion of local relapse, adverse events, proportion of segmentectomy completion, duration of hospital stay, duration of chest tube placement, duration of surgery, amount of blood loss, and the number of automatic surgical staples used. Overall survival was analysed on an intention-to-treat basis with a non-inferiority margin of 1·54 for the upper limit of the 95% CI of the hazard ratio (HR) and estimated using a stratified Cox regression model. This study is registered with UMIN Clinical Trials Registry, UMIN000002317. Findings Between Aug, 10, 2009, and Oct 21, 2014, 1106 patients (intention-to-treat population) were enrolled to receive lobectomy (n=554) or segmentectomy (n=552). Patient baseline clinicopathological factors were well balanced between the groups. In the segmentectomy group, 22 patients were switched to lobectomies and one patient received wide wedge resection. At a median follow-up of 7·3 years (range 0·0–10·9), the 5-year overall survival was 94·3% (92·1–96·0) for segmentectomy and 91·1% for lobectomy (95% CI 88·4–93·2); superiority and non-inferiority in overall survival were confirmed using a stratified Cox regression model (HR 0·663; 95% CI 0·474–0·927; one-sided p<0·0001 for non-inferiority; p=0·0082 for superiority). Improved overall survival was observed consistently across all predefined subgroups in the segmentectomy group. At 1 year follow-up, the significant difference in the reduction of median forced expiratory volume in 1 sec between the two groups was 3·5% (p<0·0001), which did not reach the predefined threshold for clinical significance of 10%. The 5-year relapse-free survival was 88·0% (95% CI 85·0–90·4) for segmentectomy and 87·9% (84·8–90·3) for lobectomy (HR 0·998; 95% CI 0·753–1·323; p=0·9889). The proportions of patients with local relapse were 10·5% for segmentectomy and 5·4% for lobectomy (p=0·0018). 52 (63%) of 83 patients and 27 (47%) of 58 patients died of other diseases after lobectomy and segmentectomy, respectively. No 30-day or 90-day mortality was observed. One or more postoperative complications of grade 2 or worse occurred at similar frequencies in both groups (142 [26%] patients who received lobectomy, 148 [27%] who received segmentectomy). Interpretation To our knowledge, this study was the first phase 3 trial to show the benefits of segmentectomy versus lobectomy in overall survival of patients with small-peripheral NSCLC. The findings suggest that segmentectomy should be the standard surgical procedure for this population of patients. Funding National Cancer Center Research and the Ministry of Health, Labour, and Welfare of Japan.
Author Aoki, Tadashi
Ito, Hiroyuki
Okumura, Norihito
Suzuki, Kenji
Tsuboi, Masahiro
Asamura, Hisao
Okami, Jiro
Wakabayashi, Masashi
Saji, Hisashi
Nakamura, Shinichiro
Ikeda, Norihiko
Watanabe, Shun-Ichi
Aokage, Keiju
Mitsudomi, Tetsuya
Yamaguchi, Masafumi
Yoshino, Ichiro
Nakamura, Kenichi
Okada, Morihito
Nakajima, Ryu
Fukuda, Haruhiko
Author_xml – sequence: 1
  givenname: Hisashi
  surname: Saji
  fullname: Saji, Hisashi
  email: hsaji@marianna-u.ac.jp
  organization: Department of Chest Surgery, St Marianna University School of Medicine, Kawasaki, Japan
– sequence: 2
  givenname: Morihito
  surname: Okada
  fullname: Okada, Morihito
  organization: Department of Surgical Oncology, Research Institute for Radiation Biology and Medicine, Hiroshima University, Hiroshima, Japan
– sequence: 3
  givenname: Masahiro
  surname: Tsuboi
  fullname: Tsuboi, Masahiro
  organization: Department of Thoracic Surgery, National Cancer Center Hospital East, Kashiwa, Japan
– sequence: 4
  givenname: Ryu
  surname: Nakajima
  fullname: Nakajima, Ryu
  organization: Department of Thoracic Surgery, Osaka City General Hospital, Osaka, Japan
– sequence: 5
  givenname: Kenji
  surname: Suzuki
  fullname: Suzuki, Kenji
  organization: Department of General Thoracic Surgery, Juntendo University School of Medicine, Tokyo, Japan
– sequence: 6
  givenname: Keiju
  surname: Aokage
  fullname: Aokage, Keiju
  organization: Department of Thoracic Surgery, National Cancer Center Hospital East, Kashiwa, Japan
– sequence: 7
  givenname: Tadashi
  surname: Aoki
  fullname: Aoki, Tadashi
  organization: Department of Thoracic Surgery, Niigata Cancer Center Hospital, Niigata, Japan
– sequence: 8
  givenname: Jiro
  surname: Okami
  fullname: Okami, Jiro
  organization: Department of General Thoracic Surgery, Osaka International Cancer Institute, Osaka, Japan
– sequence: 9
  givenname: Ichiro
  surname: Yoshino
  fullname: Yoshino, Ichiro
  organization: Department of General Thoracic Surgery, Chiba University Graduate School of Medicine, Chiba, Japan
– sequence: 10
  givenname: Hiroyuki
  surname: Ito
  fullname: Ito, Hiroyuki
  organization: Department of Thoracic Surgery, Kanagawa Cancer Center, Yokohama, Japan
– sequence: 11
  givenname: Norihito
  surname: Okumura
  fullname: Okumura, Norihito
  organization: Department of Thoracic Surgery, Kurashiki Central Hospital, Kurashiki, Japan
– sequence: 12
  givenname: Masafumi
  surname: Yamaguchi
  fullname: Yamaguchi, Masafumi
  organization: Department of Thoracic Oncology, National Hospital Organization Kyushu Cancer Center, Fukuoka, Japan
– sequence: 13
  givenname: Norihiko
  surname: Ikeda
  fullname: Ikeda, Norihiko
  organization: Department of Surgery, Tokyo Medical University, Tokyo, Japan
– sequence: 14
  givenname: Masashi
  surname: Wakabayashi
  fullname: Wakabayashi, Masashi
  organization: Japan Clinical Oncology Group Data Center/Operations Office, National Cancer Center Hospital, Tokyo, Japan
– sequence: 15
  givenname: Kenichi
  surname: Nakamura
  fullname: Nakamura, Kenichi
  organization: Japan Clinical Oncology Group Data Center/Operations Office, National Cancer Center Hospital, Tokyo, Japan
– sequence: 16
  givenname: Haruhiko
  surname: Fukuda
  fullname: Fukuda, Haruhiko
  organization: Japan Clinical Oncology Group Data Center/Operations Office, National Cancer Center Hospital, Tokyo, Japan
– sequence: 17
  givenname: Shinichiro
  surname: Nakamura
  fullname: Nakamura, Shinichiro
  organization: West Japan Oncology Group Data Center, Osaka, Japan
– sequence: 18
  givenname: Tetsuya
  surname: Mitsudomi
  fullname: Mitsudomi, Tetsuya
  organization: Department of Thoracic Surgery, Kindai University Faculty of Medicine, Osaka-Sayama, Japan
– sequence: 19
  givenname: Shun-Ichi
  surname: Watanabe
  fullname: Watanabe, Shun-Ichi
  organization: Department of Thoracic Surgery, National Cancer Center Hospital, Tokyo, Japan
– sequence: 20
  givenname: Hisao
  surname: Asamura
  fullname: Asamura, Hisao
  organization: Division of Thoracic Surgery, Keio University School of Medicine, Tokyo, Japan
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35461558$$D View this record in MEDLINE/PubMed
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Snippet Lobectomy is the standard of care for early-stage non-small-cell lung cancer (NSCLC). The survival and clinical benefits of segmentectomy have not been...
Summary Background Lobectomy is the standard of care for early-stage non-small-cell lung cancer (NSCLC). The survival and clinical benefits of segmentectomy...
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SubjectTerms Carcinoma, Non-Small-Cell Lung
Clinical trials
Complications
Disease
Fatalities
Humans
Lung cancer
Lung Neoplasms
Lymphatic system
Mastectomy, Segmental
Medical prognosis
Metastasis
Neoplasm Recurrence, Local - pathology
Neoplasm Staging
Non-small cell lung carcinoma
Oncology
Ostomy
Patients
Pneumonectomy
Postoperative
Randomization
Registration
Regression models
Respiratory function
Small cell lung carcinoma
Staples
Subgroups
Surgery
Survival
Tumors
Title Segmentectomy versus lobectomy in small-sized peripheral non-small-cell lung cancer (JCOG0802/WJOG4607L): a multicentre, open-label, phase 3, randomised, controlled, non-inferiority trial
URI https://www.clinicalkey.com/#!/content/1-s2.0-S0140673621023333
https://dx.doi.org/10.1016/S0140-6736(21)02333-3
https://www.ncbi.nlm.nih.gov/pubmed/35461558
https://www.proquest.com/docview/2653247913
https://www.proquest.com/docview/2655106457
Volume 399
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