Impact of Pulmonary Ligament Resection in Upper Lobectomies: A Multicenter Matched Cohort Study
Abstract
:1. Introduction
2. Materials and Methods
- perioperative results: operative time (min), pleural effusion (mL), complications (frequency and scores [9]), chest drainage removal (days) and length of stay, pleural space (defined as the presence of >20% pneumothorax or a 3 cm gap between visceral pleura and chest wall on a chest radiograph at the I postoperative day—POD [10]) and collapse rate (calculated on a chest X-ray by taking the difference between the preoperative baseline area and the actual postoperative area of the remaining lungs, dividing that difference by the preoperative area, and then multiplying the result by 100 to express it as a percentage).
- long-term results (after at least 3 months from the surgery): changes in the bronchial angle (defined as the convex angle formed between the axis of the trachea and the angles of the intermedius bronchus on the right side and the inferior bronchus on the left side), long-term complications, diaphragmatic paralysis (calculated quantitatively using the distance between the highest point of the diaphragm and the apex of the chest before and after surgery and defined as more than 30% [11] and qualitatively using ultrasound, fluoroscopy, or electrodiagnostic studies).
Statistical Analysis
3. Results
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations and Acronyms
ABPP | autologous blood patch pleurodesis |
AJCC | American Joint Committee on Cancer |
ARDS | acute respiratory distress syndrome |
BMI | body mass index |
CCI | Charlson Comorbidity Index |
ChT | chemotherapy |
CT | computed tomography |
ESTS | European Society of Thoracic Surgery |
FEV1 | Forced Expiratory Volume after 1 s |
FVC | forced vital capacity |
LOH | length of hospital stay |
ml | milliliters |
min | minutes |
MRI | magnetic resonance imaging |
NSCLC | non-small-cell lung cancer |
PAL | prolonged air leak |
PET | positron emission tomography |
POD | postoperative day |
PSM | propensity score matching |
pts | patients |
RLN | recurrent laryngeal nerve |
RT | radiotherapy |
SMD | standardized mean difference |
SSC | squamous cell carcinoma |
STROCSS | strengthening the reporting of cohort studies in surgery |
TNM | tumor, lymph node, metastasis |
VATS | Video-Assisted Thoracoscopic Surgery |
References
- Ettinger, D.S.; Wood, D.E.; Aisner, D.L.; Akerley, W.; Bauman, J.; Chirieac, L.R.; Hughes, M. Non-small cell lung cancer, version 5.2017, NCCN clinical practice guidelines in oncology. J. Natl. Compr. Canc. Netw. 2017, 15, 504–535. [Google Scholar] [CrossRef] [PubMed]
- Lardinois, D.; De Leyn, P.; Van Schil, P.; Porta, R.R.; Waller, D.; Passlick, B.; Zielinski, M.; Junker, K.; Rendina, E.A.; Ris, H.B.; et al. ESTS guidelines for intraoperative lymph node staging in non-small cell lung cancer. Eur. J. Cardiothorac. Surg. 2006, 30, 787–792. [Google Scholar] [CrossRef] [PubMed]
- Bu, L.; Yang, A.-R.; Peng, H.; Xu, Z.-Y.; Wu, J.-Q.; Wang, P. Dividing inferior pulmonary ligament may change the bronchial angle. J. Surg. Res. 2015, 201, 208–212. [Google Scholar] [CrossRef] [PubMed]
- Moon, D.H.; Kim, H.R.; Lee, S.M.; Chae, E.J.; Choi, C.-M.; Choi, S.H.; Kim, Y.-H.; Kim, D.K.; Park, S.-I. Effect of inferior pulmonary ligament division on residual lung volume and function after a right upper lobectomy. Interact. Cardiovasc. Thorac. Surg. 2019, 28, 760–766. [Google Scholar] [CrossRef]
- Matsuoka, H.; Nakamura, H.; Nishio, W.; Sakamoto, T.; Harada, H.; Tsubota, N. Division of the Pulmonary Ligament After Upper Lobectomy is Less Effective for the Obliteration of Dead Space than Leaving It Intact. Surg. Today 2004, 34, 498–500. [Google Scholar] [CrossRef] [PubMed]
- Kuriyama, S.; Imai, K.; Saito, H.; Takashima, S.; Kurihara, N.; Demura, R.; Suzuki, H.; Harata, Y.; Sato, Y.; Nakayama, K.; et al. Inferior pulmonary ligament division during left upper lobectomy causes pulmonary dysfunction. Interdiscip. Cardiovasc. Thorac. Surg. 2023, 36. [Google Scholar] [CrossRef]
- Mathew, G.; Agha, R.; Albrecht, J.; Goel, P.; Mukherjee, I.; Pai, P.; D’Cruz, A.K.; Nixon, I.J.; Roberto, K.; Enam, S.A.; et al. STROCSS 2021: Strengthening the reporting of cohort, cross-sectional and case-control studies in surgery. Ann. Med. Surg. 2021, 72, 103026. [Google Scholar] [CrossRef] [PubMed]
- Adachi, H.; Sakamaki, K.; Nishii, T.; Yamamoto, T.; Nagashima, T.; Ishikawa, Y.; Ando, K.; Yamanaka, K.; Watanabe, K.; Kumakiri, Y.; et al. Lobe-Specific Lymph Node Dissection as a Standard Procedure in Surgery for Non–Small Cell Lung Cancer: A Propensity Score Matching Study. J. Thorac. Oncol. 2016, 12, 85–93. [Google Scholar] [CrossRef]
- Seely, A.J.; Ivanovic, J.; Threader, J.; Al-Hussaini, A.; Al-Shehab, D.; Ramsay, T.; Gilbert, S.; Maziak, D.E.; Shamji, F.M.; Sundaresan, R.S. Systematic Classification of Morbidity and Mortality After Thoracic Surgery. Ann. Thorac. Surg. 2010, 90, 936–942. [Google Scholar] [CrossRef]
- Solak, O.; Sayar, A.; Metin, M.; Turna, A.; Erdogu, V.; Pekçolaklar, A.; Gürses, A. Definition of postresectional residual pleural space. Can. J. Surg. 2007, 50, 39–42. [Google Scholar]
- Ventura, L.; Zhao, W.; Chen, T.; Wang, Z.; Feng, J.; Gu, Z.; Ji, C.; Fang, W. Significant diaphragm elevation suggestive of phrenic nerve injury after thoracoscopic lobectomy for lung cancer: An underestimated problem. Transl. Lung Cancer Res. 2020, 9, 1822–1830. [Google Scholar] [CrossRef]
- Amin, M.B. (Ed.) AJCC Cancer Staging Manual, 8th ed.; Springer: Chm, Switzerland, 2017; pp. 431–455. [Google Scholar]
- Charlson, M.E.; Pompei, P.; Ales, K.L.; MacKenzie, C.R. A new method of classifying prognostic comorbidity in longitudinal studies: Development and validation. J. Chronic Dis. 1987, 40, 373–383. [Google Scholar] [CrossRef]
- Riquet, M.; Barthes, F.L.P.; Souilamas, R.; Hidden, G. Thoracic duct tributaries from intrathoracic organs. Ann. Thorac. Surg. 2002, 73, 892–898. [Google Scholar] [CrossRef] [PubMed]
- Yazgan, S.; Üçvet, A.; Türk, Y.; Gürsoy, S. The impact of dissection of station 9 on survival and the necessity of pulmonary ligament division during upper lobectomy for lung cancer. Acta Chir. Belg. 2023, 123, 148–155. [Google Scholar] [CrossRef] [PubMed]
- Lim, E.; Harris, R.A.; McKeon, H.E.; Batchelor, T.J.; Dunning, J.; Shackcloth, M.; Anikin, V.; Naidu, B.; Belcher, E.; Loubani, M.; et al. Impact of video-assisted thoracoscopic lobectomy versus open lobectomy for lung cancer on recovery assessed using self-reported physical function: VIOLET RCT. Health Technol. Assess. 2022, 26, 1–162. [Google Scholar] [CrossRef] [PubMed]
Before PSM | After PSM | |||||
---|---|---|---|---|---|---|
No Ligament Resection (n = 490) | Ligament Resection (n = 498) | p-Value | No Ligament Resection (n = 276) | Ligament Resection (n = 276) | p-Value | |
Age | 63.0 (56.0–71.0) | 69.0 (63.0–74.0) | <0.001 *a | 68.0 (61.0–72.75) | 68.0 (60.0–73.0) | 0.889 a |
Sex | 0.005 *b | 0.087 b | ||||
Male | 232 (47.3%) | 280 (56.2%) | 161 (58.3%) | 141 (51.1%) | ||
Female | 258 (52.7%) | 218 (43.8%) | 115 (41.7%) | 135 (48.9%) | ||
BMI | 23.96 (21.71–26.35) | 25.91 (23.12–28.41) | <0.001 *a | 25.125 (22.31–27.73) | 25.41 (22.95–28.38) | 0.214 a |
Smoking | <0.001 *b | 0.280 b | ||||
Current | 107 (21.8%) | 128 (25.7%) | 91 (33.0%) | 74 (26.8%) | ||
Never | 283 (57.8%) | 104 (20.9%) | 89 (32.2%) | 95 (34.4%) | ||
Previous | 100 (20.4%) | 266 (53.4%) | 96 (33.8%) | 107 (38.8%) | ||
FEV1 (%) | 95.76 (84.0–107.0) | 92.0 (77.0–106.25) | 0.001 *a | 98.21 ± 19.72 | 95.10 ± 21.25 | 0.313 c |
FVC (%) | 96.10 (86.2–108.0) | 98.0 (87.0–111.0) | 0.204 a | 98.10 (88.0–110.0) | 99.0 (88.0–112.0) | 0.622 a |
Comorbidities (pts) | 265 (54.1%) | 403 (80.9%) | <0.001 *b | 194 (70.3%) | 199 (72.1%) | 0.638 b |
Charlson Comorbidity Index | 3.0 (2.0–4.0) | 4.0 (3.0–5.0) | <0.001 *a | 4.0 (3.0–5.0) | 4.0 (3.0–5.0) | 0.564 a |
No Ligament Resection (n = 276) | Ligament Resection (n = 276) | p-Value | |
---|---|---|---|
Side | 0.861 b | ||
Right | 173 (62.7%) | 171 (62.0%) | |
Left | 103 (37.3%) | 105 (38.0%) | |
Surgery time (minutes) | 120.0 (100.0–151.50) | 140.0 (110.0–180.0) | <0.001 *a |
Estimated blood loss (mL) | 100.0 (50.0–100.0) | 100.0 (50.0–100.0) | 0.068 a |
Lymph node (number) | 10.0 (7.0–12.0) | 9.0 (7.0–12.0) | 0.657 a |
Lymph node station (number) | 5.0 (5.0–6.0) | 5.0 (4.0–6.0) | 0.945 a |
Lymph node station#9 harvested (yes) | 0 (0.0%) | 127 (46.0%) | <0.001 * |
Pleural space (yes) | 30 (10.9%) | 19 (6.9%) | 0.100 b |
Pleural space (mm) | 40.0 (34.75–55.5) | 35.0 (30.0–44.0) | 0.096 a |
Collapse rate (%) | 7.0 (4.0-10.0) | 7.0 (5.0–10.0) | 0.361 a |
POD1 effusion (mL) | 250.0 (250.0–257.50) | 250.0 (200.0–357.50) | 0.155 a |
POD2 effusion (mL) | 150.0 (150.0–250.0) | 150.0 (100.0–300.0) | 0.620 a |
POD3 effusion (mL) | 150.0 (150.0–168.75) | 150.0 (100.0–200.0) | 0.520 a |
Chest drainage duration (days) | 3.0 (2.0–4.0) | 3.0 (2.0–5.0) | 0.133 a |
Discharge with drainage | 0 (0.0%) | 0 (0.0%) | - |
Postoperative bronchoscopy abnormalities (yes) | 1 (0.4%) | 0 (0.0%) | 0.317 b |
Bronchial kinking | 0 (0.0%) | 1 (0.4%) | 0.317 b |
LOH (days) | 5.0 (4.0–7.0) | 5.0 (3.0–7.0) | 0.203 a |
In-hospital mortality | 0 (0.0%) | 1 (0.4%) | 0.317 b |
30-day mortality | 0 (0.0%) | 2 (0.7%) | 0.157 b |
90-day mortality | 0 (0.0%) | 3 (1.1%) | 0.082 b |
No Ligament Resection (n = 276) | Ligament Resection (n = 276) | p-Value | |
---|---|---|---|
Early complications (pts) | 38 (13.8%) | 52 (18.8%) | 0.107 a |
Number of complications | 0.272 a | ||
one | 33 (12.0%) | 45 (16.3%) | |
two | 5 (1.8%) | 7 (2.5%) | |
Early complications (type) | 0.379 a | ||
Pneumonia | 8 (2.9%) | 3 (1.1%) | |
ARDS | 0 (0.0%) | 2 (0.7%) | |
Atrial fibrillation | 14 (5.1%) | 24 (8.4%) | |
PAL | 13 (4.7%) | 12 (4.3%) | |
Pneumothorax | 0 (0.0%) | 1 (0.4%) | |
Atelectasis | 1 (0.4%) | 2 (0.7%) | |
Anemia | 0 (0.0%) | 2 (0.7%) | |
Lung hemorrhage | 0 (0.0%) | 1 (0.4%) | |
Delirium | 0 (0.0%) | 1 (0.4%) | |
Kidney failure | 0 (0.0%) | 1 (0.4%) | |
Bleeding | 1 (0.4%) | 1 (0.4%) | |
RLN paralysis | 2 (0.7%) | 3 (1.1%) | |
Pulmonary infarction | 0 (0.0%) | 1 (0.4%) | |
Diaphragmatic elevation | 4 (1.4%) | 4 (1.4%) | |
Esophageal injury | 0 (0.0%) | 1 (0.4%) | |
Treatment of early complication | 0.556 a | ||
Observation | 4 (1.4%) | 3 (1.1%) | |
Medical therapy | 18 (6.5%) | 20 (7.2%) | |
Chest drainage insertion | 0 (0.0%) | 1 (0.4%) | |
Completion pneumonectomy | 0 (0.0%) | 1 (0.4%) | |
Endoscopic approach | 1 (0.4%) | 3 (1.1%) | |
Reoperation | 1 (0.4%) | 1 (0.4%) | |
ABPP for PAL | 14 (5.1%) | 23 (8.3%) | |
PAL (pts) | 14 (5.1%) | 24 (8.7%) | 0.093 a |
Diaphragmatic elevation (yes) | 4 (1.4%) | 4 (1.4%) | 1.000 b |
Chest drainage reinsertion (yes) | 0 (0.0%) | 1 (0.4%) | 1.000 b |
Clavien–Dindo Classification | 0.311 a | ||
Grade 1 | 6 (2.2%) | 6 (2.2%) | |
Grade 2 | 30 (10.9%) | 36 (13.0%) | |
Grade 3A | 1 (0.4%) | 4 (1.4%) | |
Grade 3B | 1 (0.4%) | 2 (0.7%) | |
Grade IVA | 0 (0.0%) | 3 (0.7%) | |
Grade IVB | 0 (0.0%) | 0 (0.0%) | |
Grade V | 0 (0.0%) | 1 (0.4%) | |
Late complications (pts) | 26 (9.4%) | 27 (9.8%) | 0.885 a |
Late bronchial kinking | 0 (0.0%) | 0 (0.0%) | - |
Late complications (type) | 0.958 a | ||
Arrhythmia | 18 (6.5%) | 18 (6.5%) | |
RLN palsy | 2 (0.7%) | 3 (1.1%) | |
Diaphragmatic paralysis | 4 (1.4%) | 5 (1.8%) | |
Chronic cough | 2 (0.7%) | 1 (0.4%) | |
Treatment of late complications | 0.710 a | ||
Observation | 4 (1.4%) | 5 (1.8%) | |
Medical therapy | 20 (7.2%) | 19 (6.9%) | |
Logopedic therapy | 1 (0.4%) | 3 (1.1%) | |
Thyroplasty | 1 (0.4%) | 0 (0.0%) | |
Bronchial angle (°) | 135.5 (122.25–148.0) | 124.0 (107.0–145.0) | <0.001 *c |
Diaphragmatic paralysis (yes) | 4 (1.4%) | 5 (1.8%) | 1.000 b |
Histology | 0.740 a | ||
adenocarcinoma | 220 (79.7%) | 222 (80.4%) | |
SSC | 38 (13.8%) | 34 (12.3%) | |
Large cell carcinoma | 8 (2.9%) | 12 (4.3%) | |
Adenosquamous | 10 (3.6%) | 8 (2.9%) | |
Tumor size (cm) | 2.58 ± 1.23 | 2.77 ± 1.35 | 0.074 c |
Tumor status | 0.254 a | ||
pT1a | 13 (4.7%) | 16 (5.8%) | |
pT1b | 88 (31.9%) | 90 (32.6%) | |
pT1c | 78 (28.3%) | 55 (19.9%) | |
pT2a | 67 (24.3%) | 69 (25.0%) | |
pT2b | 14 (5.1%) | 23 (8.3%) | |
pT3 | 14 (5.1%) | 20 (7.2%) | |
pT4 | 2 (0.7%) | 3 (1.1%) | |
Lymph node status | 0.311 a | ||
N0 | 250 (90.6%) | 240 (87.0%) | |
N1 | 14 (5.1%) | 16 (5.8%) | |
N2 | 12 (4.3%) | 20 (7.2%) | |
Lymph node station #9 positive | 0 (0.0%) | 2 (0.7%) | 0.499 b |
TNM staging (8th edition) | 0.116 a | ||
IA | 176 (63.8%) | 149 (54.0%) | |
IB | 52 (18.8%) | 56 (20.3%) | |
IIA | 11 (4.0%) | 19 (6.9%) | |
IIB | 19 (6.9%) | 27 (9.8%) | |
IIIA | 17 (6.2%) | 20 (7.2%) | |
IIIB | 1 (0.4%) | 5 (1.8%) | |
1-year survival | 274 (99.3%) | 270 (97.8%) | 0.154 a |
No Ligament Resection Right (n = 169) Left (n = 103) | Ligament Resection Right (n = 167) Left (n = 105) | p-Value | |
---|---|---|---|
Surgery time (minutes) | |||
Right | 120.0 (99.50–145.0) | 140.0 (110.0–180.0) | <0.001 *a |
Left | 136.94 ± 44.68 | 142.28 ± 48.64 | 0.411 b |
Pleural space (yes) | |||
Right | 23 (13.3%) | 11 (6.4%) | 0.033 *c |
Left | 7 (6.8%) | 8 (7.6%) | 0.819 c |
Pleural space (mm) | |||
Right | 43.0 (38.0–61.0) | 35.0 (30.0–45.0) | 0.077 a |
Left | 35.71 ± 4.23 | 37.62 ± 5.78 | 0.484 b |
Collapse rate (%) | |||
Right | 7.0 (4.0–10.0) | 7.0 (5.0–11.0) | 0.437 a |
Left | 7.0 (4.0–10.0) | 7.0 (5.0–10.0) | 0.639 a |
POD1 effusion (mL) | |||
Right | 250.0 (250.0–250.0) | 250.0 (200.0–400.0) | 0.072 a |
Left | 250.0 (160.0–300.0) | 250.0 (150.0–350.0) | 0.915 a |
POD2 effusion (mL) | |||
Right | 150.0 (150.0–240.0) | 150.0 (100.0–300.0) | 0.598 a |
Left | 150.0 (100.0–275.0) | 170.0 (100.0–300.0) | 0.177 a |
POD3 effusion (mL) | |||
Right | 150.0 (150.0–162.50) | 150.0 (100.0–200.0) | 0.241 a |
Left | 150.0 (50.0–200.0) | 150.0 (100.0–200.0) | 0.700 a |
Chest drainage duration (days) | |||
Right | 3.0 (2.0–4.5) | 3.0 (2.0–5.0) | 0.416 a |
Left | 3.0 (2.0–4.0) | 3.0 (2.0–5.0) | 0.154 a |
Early complications (pts) | |||
Right | 25 (14.5%) | 31 (18.1%) | 0.356 c |
Left | 13 (12.6%) | 21 (20.0%) | 0.150 c |
PAL (pts) | |||
Right | 12 (6.9%) | 16 (9.4%) | 0.412 c |
Left | 2 (1.9%) | 8 (7.6%) | 0.056 c |
Diaphragmatic elevation (yes) | |||
Right | 4 (2.3%) | 3 (1.8%) | 1.000 d |
Left | 0 (0.0%) | 1 (1.0%) | 1.000 d |
Bronchial angle (°) | |||
Right | 135.37 ± 24.67 | 126.84 ± 23.67 | 0.001 *b |
Left | 133.11 ± 16.08 | 126.49 ± 22.64 | 0.016 *b |
Diaphragmatic paralysis (yes) | |||
Right | 4 (2.3%) | 4 (2.3%) | 1.000 d |
Left | 0 (0.0%) | 1 (1.0%) | 1.000 d |
Univariable Analysis | Multivariable Analysis | |||
---|---|---|---|---|
Variable | p-Value | HR | 95% CI | p-Value |
Gender | 0.684 | - | - | - |
Age | 0.010 | 1.020 | 0.990–1.052 | 0.191 |
BMI | 0.789 | - | - | - |
Smoking habits | 0.978 | - | - | - |
CCI | 0.003 | 1.140 | 0.952–1.365 | 0.154 |
Side upper lobectomy | 0.984 | - | - | - |
Surgery time (min) | 0.001 | 1.007 | 1.002–1.011 | 0.005 * |
Univariable Analysis | Multivariable Analysis | |||
---|---|---|---|---|
Variable | p-Value | HR | 95% CI | p-Value |
Gender | 0.338 | - | - | - |
Age | 0.290 | - | - | - |
BMI | 0.044 | 1.049 | 0.986–1.115 | 0.128 |
Smoking habits | 0.242 | - | - | - |
CCI | 0.232 | - | - | - |
Side upper lobectomy | 0.286 | - | - | - |
Surgery time (min) | 0.188 | 1.003 | 0.997–1.008 | 0.356 |
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Share and Cite
Campisi, A.; Dell’Amore, A.; Fang, W.; Roca, G.; Silvestrin, S.; Nicotra, S.; Chen, Y.; Gabryel, P.; Sielewicz, M.; Piwkowski, C.; et al. Impact of Pulmonary Ligament Resection in Upper Lobectomies: A Multicenter Matched Cohort Study. J. Clin. Med. 2024, 13, 6950. https://doi.org/10.3390/jcm13226950
Campisi A, Dell’Amore A, Fang W, Roca G, Silvestrin S, Nicotra S, Chen Y, Gabryel P, Sielewicz M, Piwkowski C, et al. Impact of Pulmonary Ligament Resection in Upper Lobectomies: A Multicenter Matched Cohort Study. Journal of Clinical Medicine. 2024; 13(22):6950. https://doi.org/10.3390/jcm13226950
Chicago/Turabian StyleCampisi, Alessio, Andrea Dell’Amore, Wentao Fang, Gabriella Roca, Stefano Silvestrin, Samuele Nicotra, Yang Chen, Piotr Gabryel, Magdalena Sielewicz, Cezary Piwkowski, and et al. 2024. "Impact of Pulmonary Ligament Resection in Upper Lobectomies: A Multicenter Matched Cohort Study" Journal of Clinical Medicine 13, no. 22: 6950. https://doi.org/10.3390/jcm13226950
APA StyleCampisi, A., Dell’Amore, A., Fang, W., Roca, G., Silvestrin, S., Nicotra, S., Chen, Y., Gabryel, P., Sielewicz, M., Piwkowski, C., Rocca, E. L., Patirelis, A., Ambrogi, V., Giovannetti, R., Rea, F., & Infante, M. (2024). Impact of Pulmonary Ligament Resection in Upper Lobectomies: A Multicenter Matched Cohort Study. Journal of Clinical Medicine, 13(22), 6950. https://doi.org/10.3390/jcm13226950