Abstract
The optimal surgical approach for elderly patients with early-stage non-small cell lung cancer (NSCLC) remains a topic of debate. A retrospective analysis was conducted on patients who underwent pulmonary resection for early-stage NSCLC at our single institution between January 2018 and December 2022. Propensity score matching was used to balance baseline characteristics between the sublobar resection and lobectomy groups. Perioperative outcomes, pulmonary function recovery, postoperative quality of life, and survival were compared between the two groups. A total of 151 patients were included, with 42 undergoing sublobar resection and 109 undergoing lobectomy. After propensity score matching, baseline characteristics were well-balanced between the two groups. Sublobar resection was associated with shorter operative time (125.83 ± 33.56 min vs. 161.14 ± 61.54 min, p = 0.048), less intraoperative blood loss [65 (30, 75) ml vs. 120 (70, 170) ml, p < 0.001], shorter drainage duration [3 (2, 5) days vs. 5 (3, 6) days, p < 0.001], shorter hospital stay [6 (4, 8) days vs. 10 (7, 13) days, p < 0.001], and fewer postoperative complications (11.9% vs. 47.6%, p < 0.001), compared to lobectomy. Moreover, sublobar resection led to better pulmonary function recovery and higher postoperative quality of life scores, with no significant difference in overall and disease-free survival between the groups. Sublobar resection in patients aged 80 and above with early-stage NSCLC offered comparable oncological outcomes to lobectomy while preserving more lung function and providing better postoperative recovery and long-term quality of life. These findings have important implications for treatment decision-making in elderly NSCLC patients.
Keywords: Elderly, Non-small cell lung cancer, Sublobar resection, The quality of life, Long-term survival
Background
Lobectomy with lymph node dissection or sampling is the standard surgical approach for non-small lung cancer (NSCLC) [1, 2]. However, recent findings from the multicenter randomized controlled trial, the Japan Clinical Oncology Group 0802/West Japan Oncology Group 4607L (JCOG0802/WJOG4607L) trial, suggested that for clinically stage Ia, tumor diameter ≤ 2 cm NSCLC, segmentectomy yielded comparable 5-year survival rates to standard lobectomy, indicating that segmentectomy should be considered the standard surgical procedure for this patient population [3]. Moreover, research by Takahiro Mimae et al. [4] indicated that patients with peripheral early-stage NSCLC tumors measuring 2–4 cm who are suitable for lobectomy may have equivalent overall survival (OS) outcomes with sublobar resection with adequate surgical margins. This suggests that a smaller extent of resection may achieve comparable long-term survival for early-stage lung cancer, a crucial consideration for elderly patients requiring preservation of pulmonary function [5].
Elderly patients with NSCLC, particularly those over the age of 80, often exhibit hesitancy and reluctance towards surgery. Firstly, there is a perception that surgery for lung cancer may not significantly increase life expectancy. Secondly, surgery may entail greater risks of complications due to age being a risk factor for postoperative complications even death [6, 7]. Thirdly, surgery may substantially impact the quality of life postoperatively. Therefore, when considering lobectomy in patients over 80 years of age, a careful and thorough assessment of patient tolerability is essential [8]. However, there is currently limited research on sublobar resection in lung cancer patients over 80 years, and the long-term survival and quality of life after sublobar resection remains unclear.
This study aimed to investigate the postoperative recovery, long-term quality of life, and prognosis of elderly patients over 80 years undergoing sublobar resection for early-stage NSCLC.
Materials and methods
Patient selection
Patients diagnosed with early-stage NSCLC who underwent lobectomy or sublobar resection at the Department of Thoracic Surgery, Daping Hospital, Army Medical University, between January 2018 and December 2022 were collected. Inclusion criteria were as follows: (I) age 80 years or older; (II) tumor diameter less than 3 cm (Fig. 1); (III) Video-assisted thoracoscopic surgery (VATS) lobectomy or sublobar resection; (IV) postoperative pathological diagnosis of NSCLC; (V) no prior treatment such as radiotherapy, chemotherapy, or ablation; (VI) surgical margin greater than 2 cm or tumor diameter; (VII) signed informed consent. Exclusion criteria were as follows: (I) poor cardiopulmonary function unable to tolerate surgery; (II) history of treatment for other malignancies within 5 years; (III) postoperative pathology indicating atypical adenomatous hyperplasia (AAH) or carcinoma in situ (AIS); (IV) small cell lung cancer; (V) conversion to open thoracotomy; (VI) refusal of follow-up. Ultimately, 151 patients were included in this study, as illustrated in Fig. 2.
Fig. 1.
Typical radiological images of the included cases. A Right upper pulmonary nodule located in the outer 1/3 of the lung. B Right upper pulmonary nodule located in the middle 1/3 of the lung. C Right upper pulmonary nodule located in the inner 1/3 of the lung. D Left upper pulmonary nodule located in the middle 1/3 of the lung. Wedge resection was done in case A. Segmentectomy was done in B. Lobectomy was done in C and D. Red arrows indicate pulmonary nodules
Fig. 2.
Flowchart summarizing the patient selection. VATS video-assisted thoracoscopic surgery, AAH atypical adenomatoid hyperplasia, AIS adenocarcinoma in situ, SCLC small cell lung cancer, NSCLC non-small cell lung cancer
Clinical and pathological data were collected, including age, gender, pulmonary function, BMI (Body mass index), preoperative comorbidity index (CCI), smoking history, tumor size, tumor location, surgical approach, operative duration, postoperative pathology, postoperative complications, drainage volume, drainage duration, and length of hospital stay. Postoperative pathological staging was determined according to the eighth edition of the AJCC TNM staging system. The age-adjusted Charlson comorbidity index (aCCI) was used to assess preoperative comorbidities and predict disease-related mortality [9, 10].
Surgical procedure
According to the NCCN guidelines [11] and the Chinese guidelines for the diagnosis and treatment of lung cancer [12], video-assisted thoracoscopic surgery (VATS) lung resection was performed. All patients underwent general anesthesia with double-lumen endotracheal intubation for single-lung ventilation in the lateral decubitus position. Surgery was performed through two or single ports, with incisions placed at the fourth or fifth intercostal space along the anterior axillary line, approximately 3–5 cm in length.
In the lobectomy group, lobectomy with hilar and mediastinal lymph node dissection was performed. In the sublobar resection group, segmentectomy, or wedge resection with hilar and mediastinal lymph node dissection was performed. Intraoperatively, the distance from the margin to the tumor edge was evaluated, and intraoperative frozen section analysis was performed if the distance was less than 20 mm. In cases where lymph node metastasis or positive margins were suspected, the procedure was converted to lobectomy. Finally, 9 cases were converted from sublobar resection to lobectomy (all excluded according to the exclusion criteria).
Postoperative management
Postoperatively, patients were managed according to standard thoracic surgery protocols and monitored in the thoracic surgery ward (patients were observed in the post-anesthesia care unit before being transferred to the thoracic surgery ward). Vital signs, 24-h drainage volume, urine output, and fluid replacement were closely monitored and recorded. Patients were encouraged to actively cough and expectorate to promote drainage and lung expansion, and early mobilization was encouraged. Chest X-rays, complete blood counts, and electrolyte tests were performed on the first postoperative day. Chest tubes were removed if there was no air leakage, drainage volume was less than 200 ml in 24 h, and chest X-ray showed no significant pneumothorax. Patients were discharged with regular follow-up appointments.
Follow-up
Patients were followed up regularly in the outpatient clinic after discharge. Typically, patients were followed up twice in the first 6 months, followed by biannual visits from 6 months to 3 years, and annual visits thereafter. Follow-up assessments included routine physical examination, laboratory tests (including complete blood count, hepatic and renal function, electrolytes, and tumor markers), and chest CT scans. PET-CT scans were performed based on clinical indications.
Outpatient records documented patient follow-up information and tumor recurrence. CT or PET-CT scans, along with pathological examinations (including biopsies and bronchoscopy), were used to confirm tumor recurrence. At the 1-year follow-up visit, patients completed the EORTC QLQ-C30 [13] and EORTC QLQ-LC13 [14] quality of life questionnaires, and pulmonary function tests were performed. Overall survival (OS) was defined as the time from primary tumor resection (date of surgery) to death. Disease-free survival (DFS) was defined as the time from primary tumor resection (date of surgery) to diagnosis of recurrence or metastasis.
Statistical analysis
Data were analyzed using SPSS 26.0 software (Statistical Package for the Social Sciences, Chicago, IL, USA), with p < 0.05 considered statistically significant. Propensity score (PS) analysis was carried out using logistic regression to create a propensity score for individual patients using demographic and clinical variables. Categorical variables were expressed as frequencies and percentages (%) and compared between groups using the chi-square test or Fisher’s exact test. Normally distributed continuous variables were presented as mean ± standard deviation and compared using independent sample t-tests. Non-normally distributed continuous variables were presented as median, 25th (Q1) percentile, and 75th (Q3) percentile and compared using the Wilcoxon rank-sum test. OS and DFS were estimated using Kaplan–Meier curves, and differences between the two groups were compared using univariable log-rank analyses.
Ethical approval
The study was conducted in accordance with the Declaration of Helsinki. It was approved by the Ethics Committee of the Army Medical Center of the Chinese People’s Liberation Army (Approval No.: Medical Research Ethics Review 2023(303)), while the need for informed consent was waived by the Ethics Committee of the Army Medical Center of the Chinese People’s Liberation Army for this retrospective analysis.
Results
Clinical characteristics
A total of 151 eligible cases were included, with 42 (42/151, 27.8%) in the sublobar resection group and 109 (109/151, 72.2%) in the lobectomy group. The baseline clinical characteristics of all cases are presented in Table 1. There were no significant differences between the two groups in terms of age, gender, BMI, and smoking history. However, compared to the lobectomy group, patients in the sublobar resection group had a higher aCCI (percentage of patients with a score of aCCI ≥ 5: 64.3% vs. 43.1%, p = 0.020), poorer performance status (p = 0.012), lower FVC (74.81 ± 9.35% vs. 83.86 ± 16.80%, p < 0.001), lower FEV1 (71.72 ± 10.03% vs. 79.06 ± 16.61%, p = 0.001), lower DLCO (75.83 ± 9.50% vs. 83.59 ± 16.11%, p = 0.004), and smaller tumor diameter (2.12 ± 0.49 cm vs. 2.42 ± 0.44 cm, p < 0.001).
Table 1.
demographic and clinical characteristics of patients aged ≥ 80 years
| Variables | Before PSM | After PSM | ||||
|---|---|---|---|---|---|---|
| Sublobar resection (n = 42) | Lobectomy (n = 109) |
P Value | Sublobar resection (n = 42) | Lobectomy (n = 42) |
P value | |
| Age (years) | 83 (80–85) | 82 (80–84) | 0.564 | 83 (80–85) | 84 (81–86) | 0.773 |
| Gender (n [%]) | 0.676 | 0.208 | ||||
| Male | 13 (31.0%) | 30 (27.5%) | 13 (31.0%) | 8 (19.0%) | ||
| Female | 29 (69.0%) | 79 (72.5%) | 29 (69.0%) | 34 (81.0%) | ||
| BMI (kg/m2) | 24.22 ± 2.49 | 23.75 ± 3.11 | 0.385 | 24.22 ± 2.49 | 23.42 ± 2.81 | 0.171 |
| Smoking history | 0.543 | 0.178 | ||||
| Yes | 7 (16.7%) | 14 (12.8%) | 7 (16.7%) | 3 (7.1%) | ||
| No | 35 (83.3%) | 95 (87.2%) | 35 (83.3%) | 39 (92.9%) | ||
| aCCI | 0.020 | 0.125 | ||||
| < 5 | 15 (35.7%) | 62 (56.9%) | 15 (35.7%) | 23 (54.8%) | ||
| ≥ 5 | 27 (64.3%) | 47 (43.1%) | 27 (64.3%) | 19 (45.2%) | ||
| Performance status | 0.012 | 0.147 | ||||
| 0 | 11 (26.2%) | 61 (56.0%) | 11 (26.2%) | 20 (47.6%) | ||
| 1 | 27 (64.3%) | 43 (39.4%) | 27 (64.3%) | 21 (50.0%) | ||
| 2 | 4 (9.5%) | 5 (4.6%) | 4 (9.5%) | 1 (2.4%) | ||
| FVC% | 74.81 ± 9.35 | 83.86 ± 16.80 | < 0.001 | 74.81 ± 9.35 | 76.01 ± 11.74 | 0.654 |
| FEV1% | 71.72 ± 10.03 | 79.06 ± 16.61 | 0.001 | 71.72 ± 10.03 | 73.52 ± 14.29 | 0.506 |
| DLCO % | 75.83 ± 9.50 | 83.59 ± 16.11 | 0.004 | 75.83 ± 9.50 | 79.94 ± 9.83 | 0.117 |
| Tumor size (cm) | 2.12 ± 0.49 | 2.42 ± 0.44 | < 0.001 | 2.12 ± 0.49 | 2.26 ± 0.42 | 0.073 |
| Tumor location | 0.720 | 0.507 | ||||
| Right lung | 26 (61.9%) | 64 (58.7%) | 26 (61.9%) | 23 (54.8%) | ||
| Left lung | 16 (38.1%) | 45 (41.3%) | 16 (38.1%) | 19 (45.2%) | ||
PSM propensity score matching, CCI Charlson comorbidity index, FVC forced vital capacity, FEV1 forced expiratory volume at timed intervals of 1.0, DLCO diffusing capacity of the lungs for carbon monoxide. Matching with a 1:1 propensity score was used with a caliper value set = 0.1, and 42 pairs of samples were eventually matched
Propensity score matching
After 1:1 propensity score matching, 42 pairs of patients were selected (Table 1). Patients in both groups were well-balanced in terms of age, gender, body mass index, performance status, pulmonary function, preoperative comorbidity, tumor size, and tumor location. There were more female patients (69.0% and 81.0%, respectively), and more non-smokers (35/42, 83.3% vs. 39/42, 92.9%, respectively).
Perioperative outcomes
All cases in both groups achieved R0 resection. In the lobectomy group, one patient died of postoperative pulmonary embolism. After propensity score matching, compared to lobectomy, the sublobar resection group had shorter operative duration (125.83 ± 33.56 min vs. 161.14 ± 61.54 min, p = 0.048), less intraoperative blood loss [65 (30, 75) ml vs. 120 (70, 170) ml, p < 0.001], less total drainage volume [320 (210, 430) ml vs. 450 (360, 600) ml, p < 0.001], shorter drainage time [3 (2, 5) days vs. 5 (3, 6) days, p < 0.001], shorter hospital stay [6 (4, 8) days vs. 10 (7, 13) days, p < 0.001], fewer postoperative complications (11.9% vs. 47.6%, p < 0.001), but fewer lymph nodes removed [7 (4, 10) vs. 10 (8, 14), p < 0.001]. There was no significant difference in the rate of local recurrence between the sublobar group and lobectomy group [4 (9.5%) vs. 8 (7.3%), p = 0.657]. See Table 2.
Table 2.
The comparison of perioperative results between the sublobar resection group and the lobectomy group
| Variables | Before PSM | After PSM | ||||
|---|---|---|---|---|---|---|
| Sublobar resection (n = 42) | Lobectomy (n = 109) |
P Value | Sublobar resection (n = 42) | Lobectomy (n = 42) |
P Value | |
| Operative time (min) | 125.83 ± 33.56 | 158.47 ± 47.08 | 0.012 | 125.83 ± 33.56 | 161.14 ± 61.54 | 0.048 |
| Blood loss (mL) | 65 (30, 75) | 120 (70, 145) | < 0.001 | 65 (30, 75) | 120 (70, 170) | < 0.001 |
| Station of lymphadenectomy | 4 (3, 6) | 6 (4, 9) | < 0.001 | 4 (3, 6) | 6 (4, 8) | < 0.001 |
| Number of lymphadenectomy | 7 (4, 10) | 11 (8, 15) | < 0.001 | 7 (4, 10) | 10 (8, 14) | < 0.001 |
| Volume of drainage (ml) | 320 (210, 430) | 490 (350, 610) | < 0.001 | 320 (210, 430) | 450 (360, 600) | < 0.001 |
| Drainage duration (days) | 3 (2, 5) | 5 (3, 7) | < 0.001 | 3 (2, 5) | 5 (3, 6) | < 0.001 |
| Hospital stay (days) | 6 (4, 8) | 8 (5, 11) | < 0.001 | 6 (4, 8) | 10 (7, 13) | < 0.001 |
| Total complications | 5 (11.9%) | 33 (30.3%) | 0.020 | 5 (11.9%) | 20 (47.6%) | < 0.001 |
| Postoperative mortality | 0 | 1 | 0.320 | 0 | 1 | 0.320 |
| Histologic type | 0.303 | 0.560 | ||||
| Adenocarcinoma | 27 (64.3%) | 77 (70.6%) | 27 (64.3%) | 30 (71.4%) | ||
| Squamous | 9 (21.4%) | 25 (22.9%) | 9 (21.4%) | 9 (21.4%) | ||
| Others | 6 (14.3%) | 7 (6.4%) | 6 (14.3%) | 3 (7.2%) | ||
| Received adjuvant therapy | 14 (33.3%) | 61 (56.0%) | 0.013 | 14 (33.3%) | 16 (38.1%) | 0.649 |
| Local recurrence | 4 (9.5%) | 8 (7.3%) | 0.657 | 4 (9.5%) | 3 (7.1%) | 0.983 |
PSM propensity score matching. Sublobar resection, including wedge resection and segmentectomy
Pulmonary function and quality of life
One month post-surgery, the patient underwent a follow-up chest CT scan. Notably, a hyperdense strip was observed following sublobar resection but not in lobectomy. Furthermore, sublobar resection cases exhibited a smaller diaphragm elevation and a larger residual volume of the thoracic cavity compared to lobectomy cases (Fig. 3).
Fig. 3.
Typical pre- and postoperative radiographic images of the three surgical approaches. A and B, preoperative pulmonary nodule in case 1. C and D, horizontal and coronal CT after wedge resection. E and F, preoperative pulmonary nodule in case 2. G and H, horizontal and coronal CT after segmentectomy. I and J, preoperative pulmonary nodule in case 3. K and L, horizontal and coronal CT after lobectomy. Red arrows indicate the pulmonary nodules. Yellow arrows indicate the cut edge hyperdense areas left after surgery
To analyze the long-term pulmonary function and quality of life of patients postoperatively, pulmonary function tests were performed, and EORTC QLQ-C30 and EORTC QLQ-LC13 quality of life questionnaires were collected at the 1-year follow-up visit. The results showed that compared to the lobectomy group, the sublobar resection group had significantly higher postoperative pulmonary function indicators, including FVC: 2.05 ± 0.72 L vs. 1.51 ± 0.70 L, p = 0.006; FEV1: 1.85 ± 0.45 L vs. 1.51 ± 0.41 L, p = 0.001; DLCO: 6.38 ± 1.87 ml/mmHg.min vs. 4.98 ± 1.06 ml/mmHg min, p < 0.001; MVV: 71.05 ± 20.21 L/min vs. 57.24 ± 15.77 L/min, p = 0.022 (Table 3). This suggests that sublobar resection results in less loss of pulmonary function, preserving more lung parenchyma and function.
Table 3.
The comparison of pulmonary function 1 year postoperatively between the sublobar resection group and the lobectomy group
| Variables | Before PSM | After PSM | ||||
|---|---|---|---|---|---|---|
| Sublobar resection (n = 34) | Lobectomy (n = 97) |
P Value | Sublobar resection (n = 34) | Lobectomy (n = 34) |
P Value | |
| FVC (L) | 2.05 ± 0.72 | 1.66 ± 0.68 | 0.003 | 2.05 ± 0.72 | 1.51 ± 0.70 | 0.006 |
| Percentage of FVC (%) | 69.93 ± 15.95 | 67.25 ± 14.01 | 0.545 | 69.93 ± 15.95 | 57.85 ± 12.01 | 0.014 |
| FEV1 (L) | 1.85 ± 0.45 | 1.58 ± 0.46 | 0.002 | 1.85 ± 0.45 | 1.51 ± 0.41 | 0.001 |
| Percentage of FEV1 (%) | 75.66 ± 16.06 | 69.95 ± 14.83 | 0.047 | 75.66 ± 16.06 | 64.12 ± 13.87 | < 0.001 |
| DLCO (ml/(mmHg.min)) | 6.38 ± 1.87 | 5.74 ± 1.50 | 0.051 | 6.38 ± 1.87 | 4.98 ± 1.06 | < 0.001 |
| Percentage of DLCO (%) | 73.43 ± 20.85 | 70.40 ± 18.45 | 0.385 | 73.43 ± 20.85 | 61.76 ± 12.97 | 0.003 |
| MVV (L/min) | 71.05 ± 20.21 | 63.87 ± 18.81 | 0.189 | 71.05 ± 20.21 | 57.24 ± 15.77 | 0.022 |
| Percentage of MVV (%) | 73.62 ± 16.87 | 63.17 ± 18.70 | 0.053 | 73.62 ± 12.87 | 62.07 ± 11.56 | 0.002 |
Eight of the patients in the sublobar resection group and 12 of the patients in the lobectomy group died within 1 year without pulmonary function tests and quality of life scales being collected
PSM propensity score matching, FVC forced vital capacity. FEV1 forced expiratory volume at timed intervals of 1.0, DLCO diffusing capacity of the lungs for carbon monoxide, MVV maximum voluntary ventilation
The long-term (1-year postoperative) quality of life in the sublobar resection group, including global health status/QoL, physical function, dyspnea, and coughing scores, was significantly superior to that in the lobectomy group (Table 4). However, there were no significant differences between the two groups in terms of role, emotional, social, and cognitive functions. This indicates that patients undergoing sublobar resection have higher quality of life and fewer symptoms burden postoperatively.
Table 4.
The comparison of quality of life 1 year postoperatively between the sublobar resection group and the lobectomy group
| Variables | Sublobar resection (n = 34) | Lobectomy (n = 97) |
Statistical value | P Value |
|---|---|---|---|---|
| EORTC QLQ-C30 | ||||
| Global health status/QoL | 70.9 (47.9–77.1) | 58.3 (41.7–75.0) | 3.090 | 0.002 |
| Physical function | 73.3 (66.7–93.3) | 75.0 (53.3–80.0) | 2.501 | 0.012 |
| Role function | 75.0 (33.3–83.3) | 66.7 (33.3–83.3) | 1.096 | 0.273 |
| Emotional function | 75.0 (41.7–91.7) | 66.7 (41.7–83.3) | 0.161 | 0.872 |
| Cognitive function | 66.7 (66.7–83.3) | 66.7 (50.0–83.3) | 0.800 | 0.424 |
| Social function | 83.3 (66.7–100) | 83.3 (66.7–83.3) | 0.534 | 0.593 |
| Fatigue | 33.3 (22.2–55.6) | 33.3 (11.1–50.0) | 1.539 | 0.124 |
| Nausea/vomiting | 16.7 (0–33.3) | 16.7 (0–33.3) | 0.712 | 0.476 |
| Pain | 33.3 (16.7–33.3) | 16.7 (16.7–33.3) | 1.058 | 0.290 |
| Dyspnea | 0 (0–33.3) | 33.3 (0–66.7) | 2.601 | 0.009 |
| Insomnia | 0 (0–33.3) | 0 (0–33.3) | 0.878 | 0.380 |
| Appetite loss | 0 (0–33.3) | 0 (0–33.3) | 0.156 | 0.876 |
| Constipation | 33.3 (0–66.7) | 33.3 (0–33.3) | 0.381 | 0.703 |
| Diarrhea | 0 (0–33.3) | 0 (0–33.3) | 0.770 | 0.441 |
| Financial problem | 16.7 (0–33.3) | 33.3 (0–33.3) | 0.157 | 0.876 |
| EORTC QLQ-LC13 | ||||
| Dyspnea | 11.1 (0–33.3) | 44.4 (11.1–55.6) | 4.686 | < 0.001 |
| Coughing | 0 (0–33.3) | 33.3 (0–66.7) | 2.795 | 0.005 |
| Hemoptysis | 0 (0–33.3) | 0 (0–33.3) | 0.566 | 0.572 |
| Sore mouth | 33.3 (0–66.7) | 33.3 (0–66.7) | 0.195 | 0.845 |
| Dysphagia | 0 (0–33.3) | 0 (0–33.3) | 0.890 | 0.374 |
| Peripheral neuropathy | 0 (0–33.3) | 0 (0–33.3) | 1.113 | 0.266 |
| Alopecia | 0 (0–33.3) | 33.3 (0–33.3) | 2.096 | 0.036 |
| Overall pain* | 11.1 (0–33.3) | 22.2 (0–33.3) | 0.989 | 0.323 |
Eight of the patients in the sublobar resection group and 12 of the patients in the lobectomy group died within 1 year without pulmonary function tests and quality of life scales being collected
QLQ quality of life questionnaire, EORTC European Organisation for the Research and Treatment of Cancer
*This entry is a combination of three pain-related items including pain in chest, pain in arm or shoulder and pain in other parts
Survival analysis
The last follow-up was in October 2023, with a median follow-up time of 46 months overall. The median follow-up time in the sublobar resection group was 37 months (4–66 months), with 1-year survival rate of 90.2%, 3-year survival rate of 56.6%, and 5-year survival rate of 48.1%. In the lobectomy group, the median follow-up time was 49 months (1–75 months), with 1-year survival rate of 97.2%, 3-year survival rate of 72.0%, and 5-year survival rate of 51.1%. There were no significant differences in DFS and OS between the two groups (Fig. 4). After propensity score matching, there were still no significant differences in 5-year DFS (43.8% vs. 45.4%, p = 0.423) and 5-year OS (48.1% vs. 51.1%, p = 0.612) between the two surgical approaches (Fig. 4).
Fig. 4.
Kaplan–Meier curves for survival before and after propensity score matching between sublobar resection and lobectomy. A DFS between sublobar resection and lobectomy before PSM. B DFS between sublobar resection and lobectomy after PSM. C OS between sublobar resection and lobectomy before PSM. D OS between sublobar resection and lobectomy after PSM. DFS disease free survival, OS overall survival, PSM propensity score matching
Discussion
This study demonstrated that sublobar resection, including wedge resection and segmentectomy, yields comparable DFS and OS outcomes to lobectomy in patients aged 80 and above with early-stage NSCLC. Moreover, sublobar resection presented lower perioperative risks in the short term and offered superior long-term recovery of pulmonary function and postoperative quality of life. These findings have significant implications for treatment strategies in elderly NSCLC patients.
It is well-known that patients undergoing lobectomy typically have higher cardiopulmonary demands compared to those undergoing sublobar resection [15]. Lobectomy demands a higher level of cardiopulmonary reserve due to the extensive nature of the procedure, including the removal of an entire lobe of the lung, which can significantly impact postoperative pulmonary function. In contrast, patients undergoing sublobar resection, such as segmentectomy or wedge resection, may have compromised baseline cardiopulmonary function, often associated with advanced age or comorbidities. In our study, this made the direct comparison of data between the two groups challenging. Therefore, through propensity score matching, we were able to balance the baseline data between the two groups, enabling a more rigorous statistical analysis and discussion of the study [16].
Previous studies have indicated that compared to lobectomy, sublobar resection is associated with shorter operative times, less intraoperative blood loss, and lower rates of complications [17, 18]. Although our study focused on patients aged 80 and above, similar conclusions can be drawn [19]. Shorter operative times and less intraoperative blood loss are generally believed to result in faster and better postoperative recovery, which is particularly crucial for elderly patients aged 80 and above. Prolonged operative times significantly reduce the tolerance of elderly patients to surgery, leading to delayed extubation and removal of drainage tubes [20, 21]. Similarly, increased intraoperative blood loss can slow down the postoperative recovery process, reduce mobility, and increase the risk of thrombosis [22, 23]. Especially after propensity score matching, there were no statistically significant differences in the impact of the two surgical approaches on patient prognosis.
Sublobar resection has a smaller resection range than lobectomy, preserving more lung parenchyma and thus having less impact on lung function compared to lobectomy [24]. This is more beneficial for postoperative pulmonary function recovery. In our study, at the 1-year postoperative follow-up, pulmonary function indicators in the sublobar resection group were superior to those in the lobectomy group. Particularly for patients aged 80 and above, preserving more pulmonary function allows for better management of lung-related diseases postoperatively. Furthermore, better pulmonary function implies better quality of life and greater self-care ability. However, there were no significant differences between the two groups in terms of role, emotional, social, and cognitive functions. One potential explanation could be attributed to the resilience and adaptability of elderly patients, in coping with the challenges posed by lung cancer surgery [25]. Additionally, the comprehensive multidisciplinary care provided to elderly patients undergoing lung cancer surgery, including preoperative assessments, perioperative support, and postoperative rehabilitation, may contribute to the preservation of functional status and quality of life across both surgical groups. In summary, compared to lobectomy, sublobar resection may result in superior postoperative long-term quality of life for elderly patients [26, 27].
Our study showed that the overall DFS and OS in the sublobar resection group were lower than those in the lobectomy group among elderly patients. However, there was no statistically significant difference between the two groups. Similar to some previous studies, although the range of sublobar resection was smaller than that of lobectomy, and the number of lymph node dissections was lower in the sublobar resection group, the overall survival rate was not inferior to that of standard lobectomy [28, 29]. The emergence of these statistical results may be because the expected lifespan of elderly patients is much lower than that of younger patients. Regardless of whether lobectomy or sublobar resection is performed, there is a certain degree of decrease in overall quality of life postoperatively for elderly patients. The decrease in quality of life is more pronounced in the lobectomy group than in the sublobar resection group. Adapting to the postoperative state requires a longer time and more human and material resources to help elderly patients adapt to their new life situations. However, the adaptability of patients aged 80 and above is often lower, and some may even be unable to adapt, resulting in no difference in postoperative survival rates among these patients [30–32]. Additionally, these patients have a greater fear of disease progression than younger patients. Due to a certain degree of bias in their understanding of the disease, it is difficult for them to obtain correct disease knowledge through scientific channels. This has an impact on the recovery process and quality of life postoperatively, which may, in turn, have a certain impact on the overall prognosis [19, 33, 34].
Our study has some limitations. It is a retrospective analysis that requires more systematic and in-depth statistical analysis. However, this study also provides effective evidence for future research. Additionally, the sample size of this study is small, and more multicenter, large-sample studies and data are needed to support the results of this study. Although some elderly patients choose to undergo surgery, there are still many patients aged 80 and above who do not undergo surgery for various reasons such as economic reasons, underlying diseases, or surgical risks. Especially with the emergence of genetic testing and targeted therapy, it provides another treatment option for elderly patients [35]. We will continue to work on this study to provide more powerful evidence.
In conclusion, sublobar resection in patients aged 80 and above preserves more pulmonary function, achieves a better quality of life and has a similar prognosis compared to lobectomy, making it a safe, reliable, and practical surgical approach.
Author contributions
JL and HZ were responsible for data collection and writing the first draft; NL, WZ and FD were responsible for data collection, collation, and analysis; HZ, FD, XW and XW were responsible for perioperative management and follow-up and assisted in data collection and collation; XW and XW was responsible for topic selection, design, paper review and revision.
Data Availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Declarations
Ethics approval and consent to participate
The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Competing interests
No conflict of interest exists in the submission of this manuscript, and the manuscript is approved by all authors for publication.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Jianfeng Li and Hongjie Zhu contributed equally to this work.
Contributor Information
Xintian Wang, Email: wxt000926@163.com.
Xiaoli Wu, Email: ffx5201212@163.com.
References
- 1.Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg. 1995;60(3):615–22 (discussion 622–613). [DOI] [PubMed] [Google Scholar]
- 2.Darling GE, Allen MS, Decker PA, Ballman K, Malthaner RA, Inculet RI, Jones DR, McKenna RJ, Landreneau RJ, Rusch VW, et al. Randomized trial of mediastinal lymph node sampling versus complete lymphadenectomy during pulmonary resection in the patient with N0 or N1 (less than hilar) non-small cell carcinoma: results of the American College of Surgery Oncology Group Z0030 Trial. J Thorac Cardiovasc Surg. 2011;141(3):662–70. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Hattori A, Suzuki K, Takamochi K, Wakabayashi M, Sekino Y, Tsutani Y, Nakajima R, Aokage K, Saji H, Tsuboi M, et al. Segmentectomy versus lobectomy in small-sized peripheral non-small-cell lung cancer with radiologically pure-solid appearance in Japan (JCOG0802/WJOG4607L): a post-hoc supplemental analysis of a multicentre, open-label, phase 3 trial. Lancet Respir Med. 2024;12(2):105–16. [DOI] [PubMed] [Google Scholar]
- 4.Aokage K, Suzuki K, Saji H, Wakabayashi M, Kataoka T, Sekino Y, Fukuda H, Endo M, Hattori A, Mimae T, et al. Segmentectomy for ground-glass-dominant lung cancer with a tumour diameter of 3 cm or less including ground-glass opacity (JCOG1211): a multicentre, single-arm, confirmatory, phase 3 trial. Lancet Respir Med. 2023;11(6):540–9. [DOI] [PubMed] [Google Scholar]
- 5.Park B, Lee G, Kim HK, Choi YS, Zo JI, Shim YM, Kim J. A retrospective comparative analysis of elderly and younger patients undergoing pulmonary resection for stage I non-small cell lung cancer. World J Surg Oncol. 2016;14(1):13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Okami J, Shintani Y, Okumura M, Ito H, Ohtsuka T, Toyooka S, Mori T, Watanabe SI, Date H, Yokoi K, et al. Demographics, safety and quality, and prognostic information in both the seventh and eighth editions of the tnm classification in 18,973 surgical cases of the Japanese Joint Committee of Lung Cancer Registry Database in 2010. J Thorac Oncol. 2019;14(2):212–22. [DOI] [PubMed] [Google Scholar]
- 7.Okami J, Higashiyama M, Asamura H, Goya T, Koshiishi Y, Sohara Y, Eguchi K, Mori M, Nakanishi Y, Tsuchiya R, et al. Pulmonary resection in patients aged 80 years or over with clinical stage I non-small cell lung cancer: prognostic factors for overall survival and risk factors for postoperative complications. J Thorac Oncol. 2009;4(10):1247–53. [DOI] [PubMed] [Google Scholar]
- 8.Saji H, Ueno T, Nakamura H. Prospective observational cohort study of postoperative risk and prognosis scoring for elderly patients with medically operable lung cancer (JACS1303). Gen Thorac Cardiovasc Surg. 2016;64(10):634–5. [DOI] [PubMed] [Google Scholar]
- 9.Charlson M, Szatrowski TP, Peterson J, Gold J. Validation of a combined comorbidity index. J Clin Epidemiol. 1994;47(11):1245–51. [DOI] [PubMed] [Google Scholar]
- 10.Koppie TM, Serio AM, Vickers AJ, Vora K, Dalbagni G, Donat SM, Herr HW, Bochner BH. Age-adjusted Charlson comorbidity score is associated with treatment decisions and clinical outcomes for patients undergoing radical cystectomy for bladder cancer. Cancer. 2008;112(11):2384–92. [DOI] [PubMed] [Google Scholar]
- 11.Ettinger DS, Wood DE, Aisner DL, Akerley W, Bauman JR, Bharat A, Bruno DS, Chang JY, Chirieac LR, D’Amico TA, et al. Non-small cell lung cancer, version 3.2022, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2022;20(5):497–530. [DOI] [PubMed] [Google Scholar]
- 12.Chinese guidelines for diagnosis and treatment of primary lung cancer 2018 (English version). Chin J Cancer Res Chung-kuo yen cheng yen chiu. 2019;31(1):1–28. [DOI] [PMC free article] [PubMed]
- 13.Knobel H, Loge JH, Brenne E, Fayers P, Hjermstad MJ, Kaasa S. The validity of EORTC QLQ-C30 fatigue scale in advanced cancer patients and cancer survivors. Palliat Med. 2003;17(8):664–72. [DOI] [PubMed] [Google Scholar]
- 14.Coon CD, Schlichting M, Zhang X. Interpreting within-patient changes on the EORTC QLQ-C30 and EORTC QLQ-LC13. Patient. 2022;15(6):691–702. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Abbas AE. Surgical management of lung cancer: history, evolution, and modern advances. Curr Oncol Rep. 2018;20(12):98. [DOI] [PubMed] [Google Scholar]
- 16.Austin PC. An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivar Behav Res. 2011;46(3):399–424. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Qiu B, Ji Y, Zhang F, Bai G, Xue Q, Polaczek M, Tosi D, Koike T, Gao S, He J. Outcomes and experience of anatomical partial lobectomy. J Thorac Cardiovasc Surg. 2022;164(3):637-647.e631. [DOI] [PubMed] [Google Scholar]
- 18.Yang SM, Hsu HH, Chen JS. Recent advances in surgical management of early lung cancer. J Formosan Med Assoc Taiwan yi zhi. 2017;116(12):917–23. [DOI] [PubMed] [Google Scholar]
- 19.Horák P, Kengbaeva M, Doležal J, Harciníková N, Fanta J, Vobořil R. Is high age a contraindication to pulmonary resection? Rozhledy v Chirurgii Mesicnik Ceskoslovenske Chirurgicke Spolecnosti. 2021;100(10):484–9. [DOI] [PubMed] [Google Scholar]
- 20.Afonso M, Branco C, Alfaro TM. Sublobar resection in the treatment of elderly patients with early-stage non-small cell lung cancer. J Brasil Pneumol. 2020;46(4): e20190145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Smelt J, Lovejoy CA, Thakker R, Hunt I, Martin F, Tan C. Elective lung resections in the elderly: where do we draw the line? Thorac Cardiovasc Surg. 2021;69(1):109–12. [DOI] [PubMed] [Google Scholar]
- 22.Bravo-Iñiguez C, Perez Martinez M, Armstrong KW, Jaklitsch MT. Surgical resection of lung cancer in the elderly. Thorac Surg Clin. 2014;24(4):371–81. [DOI] [PubMed] [Google Scholar]
- 23.Barta JA, Zinner RG, Unger M. Lung cancer in the older patient. Clin Geriatr Med. 2017;33(4):563–77. [DOI] [PubMed] [Google Scholar]
- 24.Patella M, Tessitore A, Cianfarani A, Minerva EM, Cafarotti S. Early outcome of anatomical lung resection for non-small cell lung cancer in the elderly. Eur Rev Med Pharmacol Sci. 2021;25(16):5129–36. [DOI] [PubMed] [Google Scholar]
- 25.Lima GS, Figueira ALG, Carvalho EC, Kusumota L, Caldeira S. Resilience in older people: a concept analysis. Healthcare (Basel). 2023;11(18):2491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Panagopoulos N, Grapatsas K, Leivaditis V, Galanis M, Dougenis D. Are extensive open lung resections for elderly patients with lung cancer justified? Curr Oncol. 2023;30(6):5470–84. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Blanco R, Maestu I, de la Torre MG, Cassinello A, Nuñez I. A review of the management of elderly patients with non-small-cell lung cancer. Ann Oncol. 2015;26(3):451–63. [DOI] [PubMed] [Google Scholar]
- 28.Rivera C, Falcoz PE, Rami-Porta R, Velly JF, Begueret H, Roques X, Dahan M, Jougon J. Mediastinal lymphadenectomy in elderly patients with non-small-cell lung cancer. Eur J Cardiothorac Surg. 2013;44(1):88–92. [DOI] [PubMed] [Google Scholar]
- 29.Ramos R, Girard P, Masuet C, Validire P, Gossot D. Mediastinal lymph node dissection in early-stage non-small cell lung cancer: totally thoracoscopic vs thoracotomy. Eur J Cardiothorac Surg. 2012;41(6):1342–8 (discussion 1348). [DOI] [PubMed] [Google Scholar]
- 30.Fabrikant MS, Wisnivesky JP, Marron T, Taioli E, Veluswamy RR. Benefits and challenges of lung cancer screening in older adults. Clin Ther. 2018;40(4):526–34. [DOI] [PubMed] [Google Scholar]
- 31.Thomas PA, Couderc AL, Boulate D, Greillier L, Charvet A, Brioude G, Trousse D, D’Journo XB, Barlesi F, Loundou A. Early-stage non-small cell lung cancer beyond life expectancy: still not too old for surgery? Lung Cancer (Amsterdam, Netherlands). 2021;152:86–93. [DOI] [PubMed] [Google Scholar]
- 32.Tutic-Horn M, Gambazzi F, Rocco G, Mosimann M, Schneiter D, Opitz I, Martucci N, Hillinger S, Weder W, Jungraithmayr W. Curative resection for lung cancer in octogenarians is justified. J Thorac Dis. 2017;9(2):296–302. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Detillon D, Veen EJ. Postoperative outcome after pulmonary surgery for non-small cell lung cancer in elderly patients. Ann Thorac Surg. 2018;105(1):287–93. [DOI] [PubMed] [Google Scholar]
- 34.Suh WN, Kong KA, Han Y, Kim SJ, Lee SH, Ryu YJ, Lee JH, Shim SS, Kim Y, Chang JH. Risk factors associated with treatment refusal in lung cancer. Thorac Cancer. 2017;8(5):443–50. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Losanno T, Gridelli C. Recent advances in targeted advanced lung cancer therapy in the elderly. Expert Rev Anticancer Ther. 2017;17(9):787–97. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.