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Abstract

Objective: To compare the risk of death, tumor recurrence, metastasis, and disease progression in early-stage non-small cell lung cancer (NSCLC) patients treated with thoracoscopic surgery and stereotactic body radiotherapy (SBRT). Methods: Patients who underwent radical surgery and SBRT for NSCLC between April 2010 and November 2021 were retrospectively analyzed. Continuous and categorical variables were compared using the Mann–Whitney U and Chi-square test, respectively. Kaplan–Meier curves were used to evaluate the survival outcomes of each patient group. Cox proportional hazard regression analyses were performed to estimate the risk of death, tumor recurrence, metastasis, and disease progression. Results: A total of 167 patients were enrolled, of whom 75 and 92 underwent SBRT and surgery, respectively. The median follow-up was 45 months (range, 4-105 months). SBRT patients were observed to be significantly older (median, 76.0 vs 67.0 years; P < .001), and associated with significantly higher mortality rate (42.7% vs 26.1%, P = .024). However, no significant difference in overall survival duration was seen between the SBRT and surgery groups (45.0 vs 41.0 months; P = .199). SBRT patients demonstrated significantly lower rates of metastasis (12.0% vs 30.4%, P = .004), and significantly longer metastasis-free survival (39.0 months vs 35.5 months, P = .020). The remaining outcomes, including tumor recurrence and disease progression rates, were similar between the groups. Compared to surgery, SBRT did not significantly associate with death, recurrence, or disease progression. Kaplan–Meier curves showed significant differences in overall, tumor recurrence-free, and disease progression-free survival between the groups (log-rank P < .05). Conclusions: SBRT demonstrated similar overall survival compared to radical surgery, and associated with significantly reduced risk of tumor metastasis. Our study thereby suggests SBRT as the best treatment option for patients with inoperable NSCLC.

Keywords

non-small cell lung cancer stereotactic body radiotherapy surgical treatment prognosis

Background

Lung cancer is currently the most common form of malignancy, and is the leading cause of cancer-related mortality.^1,2 Non-small cell lung cancer (NSCLC) accounts for approximately 80% of all lung cancers. Its therapeutic approach has been largely dependent on disease stage, with that for early-stage diseases often involving radical surgery, including lobectomy and segmentectomy, as well as adjuvant chemoradiotherapy.^3,4 Radical radiation treatment alone has demonstrated favorable outcomes among patients with early-stage NSCLC without lymph node involvement.⁵ However, radiotherapy is increasingly being considered a good treatment of choice for patients unfit for surgery, including the elderly, and those with comorbidities such as pulmonary insufficiency, coronary heart disease, and diabetes.

Stereotactic body radiotherapy (SBRT) involves the targeting of tumor cells with high-dose external radiation beams. It is not only non-invasive, but also high in precision owing to its respiratory gating techniques and its use of 4-dimensional imaging, which allow for the delivery of high radiation doses while sparing surrounding normal tissues.^6,7 Therefore, our study aimed to compare the outcomes of survival, recurrence and metastasis rates in patients with early-stage NSCLC who underwent SBRT and radical surgery over the past 10 years by conducting retrospective studies.

Methods

Patient Selection

Demographic and Clinical Characteristics Between the Groups

A total of 167 patients were included in our study, of whom 75 and 92 were classified as the SBRT and surgery group, respectively. A total of 75 patients with early-stage NSCLC who underwent CyberKnife SBRT at our hospital between April 9, 2010 and November 15, 2021 were retrospectively analyzed. Our study involved 2 patient groups—those who underwent CyberKnife SBRT (SBRT group), and those treated with radical surgery (surgery group). Among them, 52 and 23 were male and female, respectively, with a median age of 76 years (range, 54-92 years). There were 17 and 26 cases of squamous cell carcinoma and adenocarcinoma, respectively. Diagnosis was made based on positron emission tomography/computed tomography imaging alone (without biopsy) in 32 patients due to personal and physical reasons. A median radiation dose of 48 Gy (range, 36-64 Gy) was administered. A total of 92 patients were treated by radical surgery, of whom 65 and 27 were male and female, respectively. The median age was 67 years (range, 46-83 years). There were 27 cases of squamous cell carcinoma, 57 cases of adenocarcinoma, and 8 cases of other carcinoma types. All patient characteristics are summarized in Table 1. The reporting of this study conforms to STROBE guidelines.⁸

Table 1.

Patient Characteristics of the SBRT and Surgery Groups.

Variables	Overall	Surgery group	SBRT group	P
n		92	75
Age^a	69.0 (65.0-76.0)	67.0 (63.0-72.5)	76.0 (69.0-78.0)	<.001
Male, n (%)		65 (70.7)	52 (69.3)	.853
Smoking index ≥ 400, n (%)	97 (58.1)	49 (53.3)	48 (64.0)	.162
Tumor size^a	2.5 (1.7-3.3)	2.0 (1.5-3.0)	3.0 (2.0-3.4)	.118
AJCC stage, n (%)				.131
First	129 (77.3)	67 (72.8)	62 (82.7)
Second	38 (22.7)	25 (27.2)	13 (17.3)
Tissue type, n (%) ^b				<.001
None	32 (19.2)	0	32 (42.7)
Squamous cell carcinoma	44 (26.4)	27 (29.4)	17 (22.7)
Adenocarcinoma	83 (49.7)	57 (62.0)	26 (34.7)
Other	8 (4.8)	8 (8.7)	0
KPS > 80, n (%)	38 (22.8)	21 (22.8)	17 (22.7)	.981
Complications, n (%)	93 (55.7)	49 (53.3)	44 (58.7)	.484
Therapeutic toxicity, n (%)	38 (22.8)	20 (21.7)	18 (24.0)	.729
Death, n (%)	56 (33.5)	24 (26.1)	32 (42.7)	.024
Overall survival^a	41.0 (27.0-64.0)	41.0 (26.0-60.5)	45.0 (30.0-72.0)	.199
Recurrence, n (%)	53 (31.7)	25 (27.2)	28 (37.3)	.161
Recurrence-free survival^a	38.0 (21.0-61.0)	36.5 (18.0-54.0)	38.0 (24.0-72.0)	.630
Metastasis, n (%)	37 (22.2)	28 (30.4)	9 (12.0)	.004
Metastasis-free survival^a	38.0 (22.0-60.0)	35.5 (17.5-52.5)	39.0 (28.0-72.0)	.020
Disease progression, n (%)	70 (41.9)	35 (38.0)	35 (46.7)	.261
Progression-free survival^a	36.0 (16.0-55.0)	32.0 (16.0-52.0)	37.0 (15.0-70.0)	.259

Abbreviations: AJCC, American Joint Committee on Cancer; KPS, Karnofsky Performance scale.

All continuous variables are expressed as median and interquartile range.

Assessed using the Fisher exact test.

Patients of the SBRT group were older than those of the surgery group (median, 76.0 years vs 67.0 years, P < .001). The SBRT group also consisted of significantly fewer cases of squamous cell carcinoma (22.7% vs 29.4%, P < .001) and adenocarcinoma (34.7% vs 62.0%, P < .001). The inclusion criteria included (1) age ≥ 18 years; (2) ECOG performance status score 0-1; (3) NSCLC confirmed on histopathology or imaging; and (4) NSCLC stages I and II. (5) Patient follow-up and evaluation data can be obtained through the case system or the hospital information system.

The exclusion criteria included (1) age < 18 years; (2) patients deemed unfit for treatment due to clinical reasons such as a history of myocardial infarction or cerebrovascular accident in the past 3 months, poor cardiac function (ejection fraction < 50%), and poor lung function (forced expiratory volume in 1 s [FEV1] < 50%); and (3) patients who refuse to cooperate.

SBRT Regime

All patients of the SBRT group underwent computed tomography imaging using a 16-row multidetector scanner (Phillips, The Netherlands). The scanning field range was defined as 15 cm from the superior and inferior borders of the lungs, while the scanning layer was set as 2 mm in thickness. All images were 3-dimensionally reconstructed. The gross tumor volume (GTV) was manually delineated by a radiation oncologist. The planned tumor volume (PTV) was set by expanding the GTV margins as follows: for upper and middle lung tumors, 5 mm in all directions; for lower lung tumors, 5 mm in the x and z axes, and 5 to 10 mm in the y axis. Organs at risk consisted of the bilateral lungs, trachea, bronchial tree, spinal cord, esophagus, and heart. The CyberKnife-Esplan4.0 planning system was used. CyberKnife SBRT uses a real-time image guidance system and a breath tracking system to perform low-fractionated, high-dose, dynamic irradiation. The restricted doses were defined in accordance with guidelines by the Radiation Therapy Oncology Group (RTOG),⁹ with average doses to the heart limited to ≤ 30 Gy, and maximum doses to the spinal cord restricted to < 45 Gy. Lung tissue limit V5 < 60% and V20 < 25%.

Radical Surgery Regime

All patients of the surgery group underwent thoracoscopic segmentectomy and precise positioning through visual precision lung expansion technology using the lung expansion technique. High-frequency jet ventilation was used to generate a clear inter-segment plane between expanded and collapsed lung tissues, which allowed for accurate identification of the affected bronchi. Small lung nodules were managed by thoracoscopic segmentectomy and undergone thoracoscopic segmentectomy.

Follow-up and Evaluation Criteria

All evaluation and follow-up data were obtained from the clinical database or from the hospital information system. All patients were followed up every 3 months within the first year of treatment, and every 6 months thereafter until disease progression or death. The deadline for follow-up of surviving patients in this study is the end of March 2022, and the follow-up of deceased patients ends time of death follow-up 4 to 105 months; the median value is 45 months. Among them, the shortest follow-up time is 4 months after treatment, the patient died because of sudden bleeding.

Treatment efficacy was evaluated according to the Response Evaluation Criteria in Solid Tumours (RECIST) 1.1 guideline, while radiation-induced injury was evaluated according to standards of the RTOG.

Measured Outcomes

Survival was assessed from the date of treatment intervention to that of death by any cause. Tumor recurrence was defined as follows: in the SBRT group, tumor reappearance locally or in the hilar and mediastinal lymph nodes; in the surgery group, tumor reappearance in the mediastinal and hilar lymph nodes in any patient, within the same lobe among wedge or segment resection patients, or in the surgical stump among lobectomy patients. Metastasis was defined as tumor recurrence at any location other than the locoregion. Disease progression was defined as the development of metastasis at any site or death by any cause. Adverse outcomes were defined as tumor recurrence, metastasis, disease progression, or death.

Statistical Analysis

Normality was assessed using the Shapiro–Wilk test. All continuous variables were found to be non-normally distributed, and are thus expressed as median and interquartile range, and were compared using the Mann–Whitney U-test. Categorical variables are expressed as frequency (percentage), and were compared using the Chi-square test. Survival was assessed in terms of the Kaplan–Meier survival curve. Cox proportional hazard regression models were used to estimate the risk of death, tumor recurrence, metastasis, and disease progression in terms of hazard ratio (HR) and 95% confidence interval (CI). The multicollinearity of independent variables in each model was tested using the tolerance and variance expansion factor (Appendix 1, Supplemental Table 1). The equiproportional hypothesis of the Cox regression model was validated using the Kolmogorov type supremum test based on 1000 simulations (Appendix 2, Supplemental Table 2). When the equal-scale assumption was not met, the risk of occurrence of outcomes was estimated using time-dependent Cox regression models. Ten of our patients were found to have died from causes other than lung cancer. To account for the competitive risk of death, Cox regression was repeated following omission of these patients. Results were subsequently verified using a competitive risk model.

Due to the small number of outcome events, with metastasis being the least frequent event (n = 37), 4 independent variables were included in each multivariate model according to the 10 Events Per Variable principle. The following models were eventually generated to account for potential confounders: Model 1, unadjusted; Model 2, adjusted for age, gender and smoking status; Model 3, adjusted for tumor size, American Joint Committee on Cancer (AJCC) stage, and tissue type; and Model 4, adjusted for Karnofsky Performance Score (KPS), comorbidities, and therapeutic toxicity. All analyses were performed using the SAS software (Version 9.4; SAS Institute Inc., Cary, NC). Statistical significance was considered as 2-sided P-values < .05.

Results

The median follow-up period was 45 months (range, 4-105 months). The SBRT group associated with significantly higher rates of death (42.7% vs 26.1%, P = .024). However, no significant difference in overall survival between the SBRT and surgery groups were observed (45.0 [30.0-72.0] months versus 41.0 [26.0-60.5] months, respectively; P = .199). The rate of metastasis was significantly lower in the SBRT group (12.0% vs 30.4%, P = .004), with significantly longer survival without metastasis (39.0 [28.0-72.0] months versus 35.5 [17.5-52.5] months, P = .020). No significant differences were observed in the remaining variables, including recurrence and disease progression.

Risk of Death, Tumor Recurrence, Metastasis, and Disease Progression

The risks for death, tumor recurrence, metastasis, and disease progression are shown in Table 2, while the Kaplan–Meier curves for adverse outcome-free survival are shown in Figure 1. The risk of metastasis was significantly lower in the SBRT group compared to the surgery group, and significance remained following adjustments for all potential confounders in Model 2 (HR, 0.25; 95% CI, 0.12-0.55), Model 3 (HR, 0.43; 95% CI, 0.19-0.94), and Model 4 (HR, 0.32; 95% CI, 0.15-0.69). Kaplan–Meier survival curve demonstrated a log-rank of P = .002 for metastasis-free survival (Figure 1). In contrast, the risk of death, tumor recurrence, and disease progression were similar between both groups, with log-rank values of P < .05 observed for overall, recurrence-free, and disease progression-free survival.

Figure 1.

Kaplan–Meier curves for overall, tumor recurrence-free, metastasis-free, and disease progression-free survival in all patients.

Table 2.

Cox Regression Analysis for the Risk of Death, Tumor Recurrence, Metastasis, and Disease Progression in all Patients.

	HR (95% CI)
	Surgery group	SBRT group
Death
Model 1	Reference	1.49 (0.87-2.55)
Model 2	Reference	1.16 (0.66-2.03)*
Model 3	Reference	1.69 (0.95-3.03)*
Model 4	Reference	1.55 (0.90-2.66)
Tumor recurrence
Model 1	Reference	1.15 (0.66-1.99)
Model 2	Reference	0.94 (0.52-1.70)
Model 3	Reference	1.10 (0.59-2.02)
Model 4	Reference	1.18 (0.68-2.06)
Metastasis
Model 1	Reference	0.32 (0.15-0.68)
Model 2	Reference	0.25 (0.12-0.55)
Model 3	Reference	0.43 (0.19-0.94)
Model 4	Reference	0.32 (0.15-0.69)
Disease progression
Model 1	Reference	1.14 (0.71-1.83)
Model 2	Reference	0.99 (0.60-1.64)
Model 3	Reference	1.32 (0.78-2.22)
Model 4	Reference	1.16 (0.72-1.86)

Model 1: unadjusted; Model 2: adjusted for age, sex, and smoking index; Model 3: adjusted for tumor size, AJCC stage, and tissue type; Model 4: adjusted for KPS, complications, and toxicity.

Abbreviations: HR, hazard ratio; CI, confidence interval. *Time-dependent Cox regression model was used.

Analysis was repeated following omission of the 10 patients with NSCLC-unrelated death, as shown in Table 3 and Figure 2. The SBRT group remained significantly associated with a decreased risk of metastasis, even after adjusting for confounders in Model 2 (HR, 0.30; 95% CI, 0.14-0.66), and Model 4 (HR, 0.38; 95% CI, 0.17-0.79). However, no significance was observed in Model 3 (HR, 0.47; 95% CI, 0.21-1.04). Nevertheless, a log-rank of P = .007 for metastasis-free survival was observed. The association of SBRT with decreased risk of metastasis in all models was verified using competitive risk models (Supplemental Table 3). The association of SBRT with death, tumor recurrence, and disease progression remained insignificantly different, and a similar log-rank values of P < .05 were shown for overall, tumor recurrence-, and disease progression-free survival.

Figure 2.

Kaplan–Meier curves for overall, tumor recurrence-free, metastasis-free, and disease progression-free in patients who died from lung cancer.

Table 3.

Cox Regression Analysis for the Risk of Death, Tumor Recurrence, Metastasis, and Disease Progression in Patients With NSCLC-Related Death.

	HR (95% CI)
	Surgery group	SBRT group
Death
Model 1	Reference	1.30 (0.72-2.34)
Model 2	Reference	1.07 (0.58-1.97)*
Model 3	Reference	1.40 (0.74-2.65)*
Model 4	Reference	1.36 (0.75-2.45)
Tumor recurrence
Model 1	Reference	1.25 (0.70-2.22)
Model 2	Reference	1.05 (0.56-1.95)
Model 3	Reference	1.12 (0.59-2.14)
Model 4	Reference	1.27 (0.71-2.26)
Metastasis
Model 1	Reference	0.37 (0.17-0.79)
Model 2	Reference	0.30 (0.14-0.66)
Model 3	Reference	0.47 (0.21-1.04)
Model 4	Reference	0.38 (0.17-0.79)
Disease progression
Model 1	Reference	1.25 (0.77-2.05)
Model 2	Reference	1.11 (0.66-1.86)
Model 3	Reference	1.27 (0.78-2.08)
Model 4	Reference	1.38 (0.81-2.37)

Model 1: unadjusted; Model 2: adjusted for age, sex, and smoking index; Model 3: adjusted for tumor size, AJCC stage, and tissue type; Model 4: adjusted for KPS, complications, and toxicity.

Abbreviations: HR, hazard ratio; CI, confidence interval. *Time-dependent Cox regression model was used.

Discussion

NSCLC accounts for approximately 80% of lung cancers. Radical surgery is indicated for most patients with early-stage diseases, with lobectomy considered the accepted standard of care for NSCLC.⁹ However, this is often challenging for patients who are frail and comorbid. CyberKnife SBRT, characterized by its use of real-time image guidance and breath tracking systems for the delivery of low-fractionated, high-dose, and dynamic irradiation, has recently found its role in the management of early NSCLC.¹⁰ Moreover, it has been shown to achieve comparable treatment efficacy compared to surgical resection even among surgically fit patients.^11–14 Current guidelines by the American Society of Radiation Oncology and the American Society of Clinical Oncology advocate its use among high surgical risk patients,¹⁵ particularly those with predicted FEV1 < 50%, predicted carbon monoxide diffusing capacity < 50%, or a combination of age, impaired lung function, pulmonary hypertension, and poor left ventricular function.

Treatment of early NSCLC with SBRT has resulted in a complete response rates of 33% to 61%, local control rates as high as 85% to 98%, median survival time of 34 to 45 months, and 3-year overall survival rates of 48% to 65%.¹⁶ Our study found no significant differences demonstrated in the overall survival probability of SBRT and surgical patients, with no significant differences observed in overall survival as well (45.0 vs 41.0 months, respectively). Furthermore, SBRT associated with significantly lower rates of metastasis, significantly longer metastasis-free survival (39.0 vs 35.5 months, respectively), and significantly reduced risk of metastasis. No significant differences were observed in tumor recurrence or disease progression. On exclusion of patients with NSCLC-unrelated death, SBRT remained unassociated with death, disease recurrence, and progression. Two prospective Phase II clinical trials (JCOG 0403 and RTOG 0618) evaluated the use of SBRT in operable Phase I NSCLC, and showed 3-year overall survival rates of 76% to 85%, which were similar to those observed with surgery.^17,18 In line with this, Dong et al.¹⁹ found no significant differences in overall survival rates between SBRT and surgery, and supported SBRT as a favorable treatment option for NSCLC patients of ≥ 70 years.

However, the clinical benefits of SBRT in relation to surgery remain controversial, as several retrospective studies have shown significant inferiority of SBRT in terms of survival outcomes compared to video-assisted thoracoscopic surgery.^20–24 Nonetheless, such survival benefits observed with surgery may be due to the routine administration of adjuvant chemotherapy in the presence of systemic mediastinal lymph node dissection. In addition, the clinical demographic of patients indicated for SBRT may have further skewed the results for overall survival.

Our study had several limitations. While a preference match analysis was performed, our study was retrospective in design, and certain unidentified factors, such as subsequent treatment modalities, may have confounded our results.

Conclusion

SBRT as a treatment for early NSCLC demonstrated comparable overall survival outcomes compared to radical surgery. SBRT further associated with significantly lower metastasis rate and significantly longer metastasis-free survival. SBRT may be a safe and effective treatment modality for elderly and inoperable patients with NSCLC.

Supplemental Material

sj-pdf-1-tct-10.1177_15330338231219369 - Supplemental material for Comparison of Treatment Outcomes Between Thoracoscopic Surgery and Stereotactic Body Radiotherapy for Early-Stage Non-Small Cell Lung Cancer

Supplemental material, sj-pdf-1-tct-10.1177_15330338231219369 for Comparison of Treatment Outcomes Between Thoracoscopic Surgery and Stereotactic Body Radiotherapy for Early-Stage Non-Small Cell Lung Cancer by Qin Tian, Xinxin Zhao, Cong Zhang, Nannan Tian and Hongchun Bian in Technology in Cancer Research & Treatment

Footnotes

Acknowledgments

The author(s) thank all patients for their support during this study.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Ethics Approval and Consent Statement

This retrospective study was approved by the Ethics Committee of the 960th Hospital of the People's Liberation Army (Approval number: (2023) Scientific Research Ethics Review No. 059). Informed consent was obtained from the patients before they underwent radiotherapy and surgery, and the consent included the possibility of treatment and post-treatment follow up.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Qin Tian

Supplemental Material

Supplemental material for this article is available online.

Abbreviations

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Supplementary Material

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