Long-Term Outcome and Cost-Effectiveness of Complete Versus Assisted Video-Assisted Thoracic Surgery for Non-Small Cell Lung Cancer
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1 2011;104: Long-Term Outcome and Cost-Effectiveness of Complete Versus Assisted Video-Assisted Thoracic Surgery for Non-Small Cell Lung Cancer JIANXING HE, MD, PhD, FACS, 1,2 * WENLONG SHAO, MD, 1,2,3 CHRISTOPHER CAO, MBBS, 4 TRISTAN YAN, MBBS, PhD, 4 DAOYUAN WANG, MD, 1,2 XIN-GUO XIONG, MD, 1,2 WEIQIANG YIN, MD, 1,2 XIN XU, MD, 1,2 HANZHANG CHEN, MD, 1,2 YUAN QIU, MD, 1,2 AND BAOLIANG ZHONG, MD 1,2 1 Department of Cardiothoracic Surgery, The First Affiliated Hospital of Guangzhou Medical College, Guangzhou, China 2 Guangzhou Institute of Respiratory Disease and China State Key Laboratory of Respiratory Disease, Guangzhou, China 3 Guangdong Cardiovascular Institute, Southern Medical University, Guangzhou, China 4 The Baird Institute for Applied Heart and Lung Surgical Research, University of Sydney, Sydney, NSW, Australia Background: To compare the outcomes and costs of two methods of video-assisted thoracoscopic surgery (VATS) major pulmonary resection in patients with clinically resectable non-small cell lung cancer (NSCLC). Methods: Between January 2000 and December 2007, 1,058 patients with proven stages I IIIA NSCLC underwent complete VATS (c-vats) or assisted VATS (a-vats) major pulmonary resection together with a systematic nodal dissection. Results: The study cohort consisted of 736 men and 322 women. Mean operative time was shorter for the a-vats cohort compared with the c-vats group (P ¼ 0.038). Overall survival (OS) at 5 years based on Kaplan Meier analysis was 55.3% (95%CI, %) for those who underwent c-vats and 47.7% (95%CI, %) for those who underwent a-vats (P ¼ 0.404). Gender, final pathology, TNM stage, and pt status were significant predictive factors for OS according to multivariate analysis. The total cost of a-vats lobectomy was lower than that of c-vats lobectomy. Conclusions: c-vats and a-vats yield similar results in patients with clinically resectable NSCLC. a-vats, however, may be less expensive and easier to adopt, making it a particularly attractive option for thoracic surgeons in developing countries. J. Surg. Oncol. 2011;104: ß 2011 Wiley-Liss, Inc. KEY WORDS: non-small cell lung cancer; video-assisted thoracoscopic surgery; long-term outcomes; cost-effectiveness INTRODUCTION Video-assisted thoracoscopic surgery (VATS) lobectomy is a minimally invasive technique of anatomic pulmonary resection, a procedure which remains the gold standard for the surgical management of non-small cell lung cancer (NSCLC). Meta-analyses [1,2], randomized trials [3 7], case control series [8,9], and large retrospective series [10,11] have all provided support for the safe and effective use of this minimally invasive technique. However, there are still discrepancies between the method of implementing VATS lobectomy in different centers [12]. Yim et al. [13] conducted a survey of minimally invasive thoracic surgeons in an effort to define their criteria for a VATS lobectomy. The results varied greatly: the numbers of incisions varied from three to five, the utility incision ranged from 4 to 10 cm, and the avoidance of rib spreading was not routine. A number of surgeons perform the procedure using direct visualization through the utility incision, using the thoracoscope merely as a light source, whilst others perform the procedure under total thoracoscopic visualization. Complete VATS (c-vats) has therefore been described as a purely endoscopic technique with 100% monitor visualization and without rib-spreading minithoracotomy, whereas assisted VATS (a-vats, also called hybrid VATS) involves performance of the main procedures via rib spreading (rigid or soft spreading) minithoracotomy (5 10 cm long) with both monitor and direct visualization [14,15]. It is not clear if the variability in VATS techniques has contributed to any confusion regarding its efficacy in the management of lung cancers [6,15]. The VATS lobectomy program at Guangzhou Medical College First Affiliated Hospital began in 1994 for selected patients with stage I primary lung cancers. After an initial learning-curve experience with the procedure, we adopted this approach (either c-vats or ß 2011 Wiley-Liss, Inc. a-vats lobectomy) routinely for the resection of NSCLC in all clinically resectable cases (stages I IIIA) [16,17], as well as for solitary fibrous tumors of the pleura [18]. In contrast to c-vats lobectomy, hand-suturing techniques, traditional instruments, and conventional approaches for anatomic dissection can be used conveniently during a-vats, which promotes a more rapid adoption of this minimally invasive approach, potentially reducing operating times, and minimizing the need for expensive disposable endoscopic products. Accurate financial analyses of new medical technologies are particularly important in today s cost-conscious health care environment [19]. The present study therefore compared not only the long-term survival outcomes of c-vats and a-vats lobectomy techniques, but also their economic impact on patients with NSCLC. Grant sponsor: National Natural Science Foundation of China; Grant number: ; Guangdong Province Science and Technology Planning Programme; Grant number: 2008A ; Guangdong Province Science and Technology Key Programme; Grant number: B Grant sponsor: Guangzhou City Science and Technology Planning Programme; Grant number: 2007Z3-E0261. *Correspondence to: Jianxing He, MD, PhD, FACS, Department of Cardiothoracic Surgery, The First Affiliated Hospital of Guangzhou Medical College, No. 151, Yanjiang Rd., Guangzhou , Guangdong Province, China. Fax: þ drjianxing.he@gmail.com Received 3 October 2010; Accepted 14 February 2011 DOI /jso Published online 8 March 2011 in Wiley Online Library (wileyonlinelibrary.com).
2 PATIENTS AND METHODS Patient Selection Between January 2000 and December 2007, 1,411 patients underwent operations for primary lung cancer by a single surgical team. Of the 1,411 patients, 1,268 patients were diagnosed histologically with NSCLC. In total, 1,058 patients met the inclusion criteria for this study of proven stages I IIIA NSCLC with complete removal of the primary tumor together with a systematic nodal dissection. The preoperative workup included thoracic computed tomography (CT) and upper abdominal and brain magnetic resonance imaging (MRI) to verify the absence of multiple pulmonary lesions and hepatic, adrenal, or brain metastases. Supplementary hepatic ultrasound and bone scintigraphic scans were ordered if clinically indicated. All patients underwent initial real-time video staging by thoracoscopy. Same individual surgeons performed both the c-vats and a- VATS procedures, and their experiences in these procedures were roughly equal. The indications for a-vats were: (1) tumor size >8 cm; (2) tumor location necessitating bronchial sleeve resection; (3) tumor invasion of the outer envelope of the lymphatic node or strong adhesions between the main vessels and tuberculous nodes, other inflammatory nodes, or adjacent tissue; (4) uncontrolled bleeding under video-vision; and (5) the patient s financial situation precluded the use of disposable endoscopic products. The most common operation performed for lung cancer was lobectomy. A pneumonectomy was performed if a lobectomy would not have provided a complete resection and if the patient could physiologically tolerate the procedure. A segmentectomy was performed for metachronous T1N0 tumors and for patients who could not tolerate a lobectomy. Surgical-pathologic staging was carried out according to the seventh edition of the TNM Classification of Malignant Tumors by the IASLC [20]. Approval for the study was obtained from the Institutional Review Board, which waived the need for individual patient consent. Postoperative Management The length of postoperative stay, all major and minor complications, and mortality were recorded for each patient. Patients with stage IB disease were encouraged to undergo four cycles of platinum-based adjuvant third-generation chemotherapy. If no contraindications were encountered, patients with stages II IIIA disease underwent four to six cycles of platinum-based adjuvant third-generation chemotherapy. We did not recommend adjuvant radiotherapy routinely in patients with N2 disease if we had performed a complete mediastinal lymphadenectomy. These patients received radiotherapy, however, if an enlarged mediastinal lymph node was detected during postoperative follow-up. Follow-up data were obtained from records of post-discharge visits, interviews, tumor registry data, and regular radiographic follow-up. CT scans of the chest were generally obtained at 3, 6, 12, 18, and 24 months postoperatively and thereafter at yearly intervals. Cost Analysis The cost of performing a-vats and c-vats was evaluated for all patients included in the present study. Specifically, data on costs relating to the disposable equipment charges, theatre costs, high dependency unit costs, and cost of ward care were collected for each individual patient. Statistical Analysis Continuous variables were compared using Student s t-test. Categorical variables were compared using the Chi-square or Fischer s c-vats vs. a-vats For NSCLC 163 exact test where appropriate. Survival was calculated by the Kaplan Meier method, and differences in survival were determined by logrank analysis. Possible prognostic factors associated with survival probability at a significance level of 0.20 or less were considered in a multivariable Cox s proportional hazard regression analysis. The zero time was defined as the date of pulmonary resection, and the terminal event was defined as death attributable to cancer. To avoid controversy, we defined death as a cancer-related death when recurrence was evident before death or upon autopsy. All other deaths from unknown or non-cancer-related causes were treated as withdrawals, meaning that non-cancer-related deaths were censored. Significance was defined as P < RESULTS Patient characteristics and perioperative outcomes of c-vats and a-vats groups are summarized in Table I. The study cohort consisted of 736 men and 322 women with histologically confirmed NSCLC with a median age of 59 years (range years). There was a higher percentage of patients with stage I disease in the c- VATS group compared with the a-vats group (56.5% vs. 18.6%, P < 0.001). Despite a more frequent need for more complex procedures, mean operative time was shorter for the a-vats cohort compared with the c-vats group (P ¼ 0.038). Blood loss, chest tube duration, postoperative hospital stay, numbers of dissected lymph nodes, and dissected nodal stations were all similar for the two cohorts. There were no intraoperative deaths. Five patients (0.5%) died during the perioperative period, with causes that included respiratory failure (n ¼ 2), pulmonary embolus (n ¼ 2), and myocardial infarct (n ¼ 1). There were one or more complications in 101 patients (9.5%), as shown in Table II. The prevalence of all complications was similar for the two cohorts. The 30-day mortality of c-vats and a-vats were 2.6% and 2.8%, respectively (P > 0.05). The 90-day mortality of c-vats and a-vats were 4.0% and 4.2%, respectively (P > 0.05). The 5-year overall survival (OS) rates for both groups combined into stages I, II, and IIIA patients were 71.9% (95%CI, %), 46.2% (95%CI, %), and 40.6% (95%CI, %), respectively (Fig. 1A). Univariate analysis by log-rank test indicated that gender, final pathology, TNM stage, and pt status each had a statistically significant impact on OS (P ¼ 0.004, P < 0.001, P < 0.001, and P < 0.001, respectively) (Table III). When pt was divided into pt 2 cm, pt >2 cm but 3 cm, pt >3 cm but 5 cm, pt >5 cmbut7 cm, and pt >7 cm, the respective 5-year survival rates were 66.8, 62.5, 51.7, 30.9, and 36.8%, respectively (P < 0.001). There was no difference in OS between the c-vats and a-vats groups. Kaplan Meier survival at 5 years was 55.3% (95%CI, %) for those who underwent c-vats and 47.7% (95%CI, %) for those who underwent a-vats (P ¼ 0.404) (Table III). Subgroup analyses did not discern a statistically significant difference between the c-vats group and a-vats group in either stage I or II. However, in stage IIIA patients, there was a statistically significant difference favoring the a-vats cohort (P ¼ 0.010) (Fig. 2). Gender, final pathology, TNM stage, and pt status were significant predictive factors for OS according to multivariate analysis. The disposable equipment charge, hospital charge, and the total cost were all lower for patients who underwent a-vats lobectomy when compared to c-vats lobectomy, as summarized in Table IV. DISCUSSION Interestingly, results of the present study found no difference in OS between the c-vats group and the a-vats group for patients with stage I or II disease. However, for patients with stage IIIA
3 164 He et al. TABLE I. Patient Characteristics and Operative Data (n ¼ 1,058) Types of VATS Characteristic No. of patients (%) c-vats (n ¼ 627) a-vats (n ¼ 431) P Gender Male 736 (69.6) Female 322 (30.4) Age (years) (65.2) > (34.8) Forced expiratory volume in 1 sec FEV1 (L) FEV1 (% predicted) Smoking status Non-smoker 255 (24.1) Smoker 803 (75.9) ECOG performance status (65.2) (34.8) TNM stage <0.001 I IA 239 (22.6) IB 195 (18.4) II IIA 177 (16.7) IIB 120 (11.3) IIIA 327 (30.9) pt status < (16.7) >2to3 248 (23.4) >3to5 353 (33.4) >5to7 180 (17.0) >7 100 (9.5) pn status <0.001 N0 555 (52.5) N1/N2 503 (47.5) Lymphovascular invasion <0.001 Lymphovascular invasion 509 (48.1) Without lymphovascular invasion 549 (51.9) Type of resection Lobectomy 861 (81.4) Right upper lobectomy 251 (23.7) Right middle lobectomy 59 (5.6) Right lower lobectomy 141 (13.3) Right middle and lower bilobectomy 50 (4.7) Right upper and middle bilobectomy 21 (2.0) 12 9 Left upper lobectomy 140 (13.2) Left lower lobectomy 199 (18.8) Pneumonectomy 46 (4.3) Left 29 (2.7) Right 17 (1.6) 6 11 Segmentectomy 49 (4.6) Sleeve lobectomy 102 (9.6) Final pathology <0.001 Adenocarcinoma 579 (54.7) Squamous cell 300 (28.4) Bronchioalveolar carcinoma 85 (8.1) Adenocarcinoma squamous cell carcinoma 43 (4.1) Large cell 27 (2.6) Others 24 (2.3) Operative time a (min) Blood loss (ml) Chest tube duration a (days) Postoperative hospital stay a, days Dissected lymph nodes a Dissected nodal stations a VATS, video-assisted thoracic surgery; c-vats, complete VATS; a-vats, assisted VATS; ECOG, Eastern Cooperative Oncology Group; TNM, tumornode-metastasis. a Values are expressed as mean standard deviation.
4 c-vats vs. a-vats For NSCLC 165 TABLE II. Complications After VATS for NSCLC (n ¼ 1,058) Types of VATS Complication a No. of patients (%) c-vats (n ¼ 627) a-vats (n ¼ 431) P None 957 (90.5) Air leak (lasting 7 days) 42 (4.0) Symptomatic atrial fibrillation 26 (2.5) Serous drainage (requiring drainage 7 days) 16 (1.5) Pneumonia 11 (1.0) Subcutaneous air (requiring reinsertion of chest tube or 9 (0.9) subcutaneous catheter) Myocardial infarction 6 (0.6) Empyema 2 (0.2) 1 1 Atelectasis 2 (0.2) 1 1 Anastomotic fistula 2 (0.2) 1 1 VATS, video-assisted thoracic surgery; NSCLC, non-small cell lung cancer; c-vats, complete VATS; a-vats, assisted VATS. a Most patients (90.5%) had no complications; some patients had more than one. disease, there was a statistically significant difference in OS favoring the a-vats cohort that was independent of other variables (P ¼ 0.010) (Fig. 2). Shigemura et al. [6] suggested that different VATS lobectomy techniques may yield different perioperative outcomes, with better results in the early postoperative period for c- VATS compared to a-vats, including less intraoperative bleeding, faster recovery, and shorter hospitalization, which may be attributed to minimization of immune disturbance and preservation of host immunity at the time of resection. These data may support the use of complete endoscopic surgery for patients with stage IA lung cancer. However, similar to our findings, Shigemura et al. [15] found there was no difference in 5-year survival between the c-vats group and a-vats group. Both c- and a-vats lobectomy procedures are regarded as popular surgical treatment modalities for lung cancer in China, where a 2008 survey showed that 86% of Chinese surgeons considered a- VATS to be an acceptable minimally invasive thoracic procedure [21]. In the same study, over 85% of surgeons did not believe that there was any significant difference in postoperative pain or loss of organ function between the c- and a-vats approaches. Complex procedures such as sleeve resection, however, can be more easily performed using the minimal rib spreading of the a-vats approach [22]. In the current study, a-vats was significantly less expensive than c- VATS, possibly because traditional hand-suturing and dissection techniques saved significant amounts of operating time and disposable product charges. This may partially explain why a-vats procedures were preferred by 86% of thoracic surgeons in China. In developing countries, a patient s financial situation is an important consideration in choosing the type of operation, and the a-vats technique has potential for expansion in those countries. Additionally, the majority of the world s population receives healthcare based on a fee-for-service model, and in the age of universal contraction of Fig. 1. Cumulative Kaplan Meier survival curves for patients with NSCLC, stratified according to TNM stage (A, P < 0.001) and pt status (B, P < 0.001).
5 166 He et al. TABLE III. Univariate and Multivariate Analysis of Overall Survival in Patients With NSCLC (n ¼ 1,058) Characteristic Five-year survival rates % (95%CI) Univariate analysis, P-value a Multivariate analysis HR (95%CI) P-Value b Gender Male 50.3 (45.8, 54.8) Reference group Female 57.0 (49.9, 64.1) (0.504, 0.877) Age (years) (47.8, 57.6) > (47.3, 59.5) Smoking status Non-smoker 53.0 (45.8, 60.3) Smoker 52.4 (47.9, 56.9) ECOG performance status (50.6, 64.4) Reference group (46.7, 55.7) (0.511, 1.785) Type of VATS approach c-vats 55.3 (50.6, 60.0) a-vats 47.7 (41.2, 54.2) Final pathology <0.001 Non-squamous cell 50.2 (45.7, 54.7) Reference group Squamous cell 58.5 (51.6, 65.4) (1.344, 2.179) TNM stage <0.001 <0.001 I 71.9 (66.6, 77.2) Reference group II 46.2 (39.0, 53.5) (1.197, 2.716) IIIA 40.6 (24.9, 56.3) (1.712, 4.802) pt status <0.001 < (58.0, 75.6) Reference group >2 to (54.9, 70.1) (0.573, 1.170) >3 to (45.2, 58.2) (0.910, 1.751) >5 to (21.3, 40.5) (1.591, 3.558) > (24.7, 49.0) (1.774, 4.633) pn status < N (62.6, 72.4) Reference group N1/N (28.7, 39.7) (0.490, 3.413) Lymphovascular invasion < No 67.9 (63.0, 72.8) Reference group Yes 34.2 (28.7, 39.7) (0.400, 2.963) Type of resection Non-lobectomy 47.2 (38.6, 55.8) Lobectomy 53.7 (49.4, 58.0) NSCLC, non-small cell lung cancer; CI, confidence interval; HR, hazard ratio; ECOG, Eastern Cooperative Oncology Group; VATS, video-assisted thoracoscopic surgery; c-vats, complete VATS; a-vats, assisted VATS; Non-lobectomy, pneumonectomy, segmentectomy, or sleeve lobectomy. a Log-rank test. b Using Cox proportional hazards regression model. Fig. 2. Cumulative Kaplan Meier survival curves for patients with NSCLC stratified according to the type of VATS approach in stage I (A, P ¼ 0.306), stage II (B, P ¼ 0.058), and sage IIIA (C, P ¼ 0.010). VATS, video-assisted thoracoscopic surgery; c-vats, complete VATS; a- VATS, assisted VATS.
6 c-vats vs. a-vats For NSCLC 167 TABLE IV. Summary of Mean Costs Stratified by Surgical Approach Types of VATS c-vats a-vats P Disposable equipment charges (US $) a 3, <0.001 Hospital charges (US $) Theatre cost a 4, , <0.001 High dependency unit a Ward stay cost a <0.001 Total (US $) a 5, , <0.001 VATS, video-assisted thoracoscopic surgery; c-vats, complete VATS; a-vats, assisted VATS. a Values are expressed as mean standard deviation. health budgets, the substantial savings of a-vats may have wider implications beyond developing countries. Previous studies that have investigated the effect of gender on the surgical outcomes of lung cancers have suggested that female gender confers a survival advantage [23 25]. Results of the present study is consistent with those findings, as women were shown to have better survival outcomes than men. The reasons for this survival advantage have not been fully elucidated, but are most likely due to a variety of factors. Exogenous or endogenous estrogens [26] and genetic and emotional factors may play important roles in the development of lung cancer and survival in women [27]. Many investigators have reported the effects of tumor size on staging and patient survival [28 30]. Under the 2009 system, current T1 tumors would be divided into T1a (2 cm in greatest dimension) and T1b (>2 cmbut 3 cm) tumors. Results from the IASLC Lung Cancer Staging Project also show that T2 tumors can be divided into three subgroups (tumors >3 cm but 5 cm; tumors >5 cm but 7 cm; and tumors >7 cm). In the present study, we analyzed survival characteristics according to pt status and found that there were prognostic differences amongst the new T classifications. The present study design was limited to a retrospective investigation, and a prospective randomized controlled study on a larger scale is required to reach definitive conclusions regarding the efficacy of c-vats relative to a-vats lobectomy in patients with NSCLC. In particular, our criteria for assigning patients to a-vats versus c-vats tended to place patients with more complex procedures and higher risk factors into the former group. Despite these differences, a-vats was found to have a similar survival outcome when compared to c-vats, and in fact may be associated with a survival advantage in patients with more advanced disease. In conclusion, our data suggest that in experienced hands, c- or a- VATS may be considered equivalent alternatives to achieve a minimally invasive surgical therapy for selected patients with clinically resectable NSCLC. Assisted-VATS may be more easily adopted in surgical centers in developing countries, however, given a reduced need for specialized training, encouraging long-term outcomes, and lower cost compared to c-vats. ACKNOWLEDGMENTS This study was supported in part by National Natural Science Foundation of China (no ), Guangdong Province Science and Technology Planning Programme (no. 2008A ), Guangdong Province Science and Technology Key Programme (no. 2007B ), and Guangzhou City Science and Technology Planning Programme (no. 2007Z3-E0261). The authors are grateful to Dr. Michael J. Mann, MD, Department of Cardiothoracic Surgery, UCSF Helen Diller Comprehensive Cancer Center, for help editing this paper. REFERENCES 1. Whitson BA, Groth SS, Duval SJ, et al.: Surgery for early stage non-small cell lung cancer: A systematic review of the videoassisted thoracoscopic surgery versus thoracotomy approaches to lobectomy. Ann Thorac Surg 2008;86: Yan TD, Black D, Bannon PG, et al.: Systematic review and meta-analysis of randomized and non-randomized trials on safety and efficacy of video-assisted thoracic surgery lobectomy for early-stage non-small-call lung cancer. 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