Abstract

OBJECTIVES

The aim of this study was to compare the short-term and mid-term results of patients with centrally located lung cancer who underwent bronchial sleeve resection by robotic system or thoracotomy.

METHODS

From September 2014 to September 2015, 103 patients, including 17 robotic and 86 open cases, were included in our study. All the clinicopathological data, operative details and follow-up information were investigated.

RESULTS

There were no intraoperative deaths. The mean console time was 113.59 min. The operative time for robotic surgery (155.06 ± 44.75 min), even in our initial cases, was comparable to that for thoracotomy (150.30 ± 47.84 min, P = 0.71). The 30-day mortality rate in the robotic and thoracotomy groups was 1 (6%) patient and 2 (2%) patients, respectively, with no significant difference (P = 0.43). A total of 4 (24%) patients in the robotic group and 22 (26%) patients in the thoracotomy group experienced postoperative complications (P = 0.86). In multivariable analysis, tumour size and postoperative radiotherapy were significant predictors of relapse-free survival, whereas only the intensive care unit stay was a significant predictor of overall survival. There was no significant difference in relapse-free survival (log-rank P = 0.16) and overall survival (log-rank P = 0.59) between the 2 groups.

CONCLUSIONS

Robotic surgery for bronchial sleeve resection is safe and feasible and has similar oncological outcomes compared with open procedures. But long-term survival still needs to be investigated.

INTRODUCTION

Lung cancer is the main cause of death for cancer patients in terms of incidence and mortality [1]. Surgery remains the treatment of choice for resectable lung cancer. Pneumonectomy was widely adopted for patients with resectable, centrally located lung neoplasms in early days [2]. However, with the introduction of sleeve resection, many studies have demonstrated that, for the centrally located cases, sleeve resection could offer comparable oncological outcomes and reserve more lung parenchyma. Thus, it is a valid alternative to pneumonectomy [2–5].

Minimally invasive surgery has become an inevitable trend in thoracic surgery, especially for the resection of peripheral early-stage lung carcinoma. Video-assisted thoracoscopic surgery (VATS) provided perceptible benefits over thoracotomy in terms of reduced pain, shorter hospital stays and fewer postoperative complications [6]. When dealing with patients with central lung cancer, experienced surgeons have attempted VATS sleeve resection [7–10]. Nevertheless, the lack of depth perception and manoeuvrability makes bronchoplastic procedures technically demanding [11]. Therefore, the majority of sleeve resections are still performed by thoracotomy. The advent of a robotic surgical system with 3D vision and EndoWrist technology resulting in intuitive manipulation has overcome the deficiency of VATS and allowed surgeons to gain proficiency performing procedures with the robotic equipment [12]. Consequently, robotic surgery holds great promise for treating centrally located lung neoplasms. There had been only a few case reports of robotic sleeve resection [13–17] until Cerfolio [18] and Pan et al. [12] published their initial experiences with robotic sleeve resection and satisfactory perioperative outcomes in a group of patients. However, no study specifically addresses a comparative analysis of outcomes after bronchial sleeve resection by robotic system versus thoracotomy.

The aim of the study was to compare the short-term and mid-term results from patients with centrally located lung cancer who underwent bronchial sleeve resection by robotic system or thoracotomy.

MATERIALS AND METHODS

Study population

From September 2014 to September 2015, 151 patients with lung cancer had a bronchial sleeve resection in the Department of Thoracic Surgery, Shanghai Chest Hospital, including 21 (14%) robotic, 5 (3%) VATS and 125 (83%) open cases. The indications for a bronchial sleeve resection were (i) a tumour located at the origin of a lobar bronchus and (ii) positive N1 nodes invading the bronchus from the outside. The indications for robotic sleeve resection were (i) endobronchial lesions with limited invasion to adjacent lobe airway and (ii) small tumours (tumour size ≤ 5 cm), without surrounding structures or severe pulmonary artery invasion or severe calcification of peribronchial or perivascular lymph node. We excluded some patients to achieve better patient group homogeneity (Fig. 1). All the robotic operations in our hospital were performed using the da Vinci Surgical System SI (Intuitive Surgical, Sunnyvale, CA, USA).

Figure 1:

Inclusion and exclusion criteria. VATS: video-assisted thoracoscopic surgery.

All patients underwent a thorough preoperative examination, including a physical examination, serological examination, bronchoscopy, pulmonary function test, chest/brain computed tomography (CT), technetium bone scan and abdominal ultrasound. Endobronchial ultrasound-guided transbronchial needle aspiration or a positron emission tomography-CT scan was also an option for excluding mediastinal lymph node metastases.

Signed consent forms were provided by patients or their legal representatives. After obtaining the approval of the ethical review board, the medical records for all patients were reviewed. Corresponding clinicopathological data including age, gender, smoking history, comorbidities, pulmonary function, intraoperative information, postoperative complications and tumour staging (based on the seventh edition of the American Joint Committee on Cancer (AJCC) guidelines [19]) were investigated. The follow-up information was obtained during clinic visits or by telephone.

Surgical technique

After general anaesthesia with double-lumen tracheal intubation was successfully performed, the patients were placed in the lateral decubitus position. For the open cases, we usually used a posterolateral thoracotomy; the fifth intercostal space was selected to enter the chest cavity. For the robotic cases, the robot was docked at the posterior aspect of the patient with 30–45° between the vertebral column of the patient and the transverse axis of the cart. We commonly adopted a 3-arm robotic technique: a camera port (seventh interspace of the midaxillary line), 2 working ports (in the sixth interspace of the anterior axillary line and in the seventh interspace of the posterior axillary line, respectively) and an access incision (fourth interspace before the anterior axillary line). The specific information on our robotic technique was published previously [12, 16].

It is important to conduct the bronchial anastomosis with the proper tension. The management of the anastomosis should be the last step so as to reduce traction. Lymph node dissection could be performed before transection of bronchus. The pulmonary ligament should be freed to minimize the tension before accomplishing the bronchial anastomosis. Routinely, the bronchial margins were assessed by intraoperative frozen sections. While waiting, we usually continued to do the anastomosis. If the margin was positive, we would take it apart, perform a further resection and redo the anastomosis. In the open group, an end-to-end bronchial anastomosis was finished either via a continuous running suture (4-0 Prolene) or an interrupted suture (3-0 Vicryl). The stump was reinforcement according to the surgeon’s personal preference. In the robotic group, the anastomosis was finished via a continuous running suture (4-0 Prolene). A monofilament suture, which allowed smooth passage of sutures through the bronchus, helped us to slide and tie the knots. The anterior part was sewn up after suturing the posterior wall, and the sutures were tied together. In the robotic group, no muscle flap or any other autograft was used to wrap the anastomosis. Bronchoscopy was introduced before closing the chest to assess the integrity of the anastomosis. In addition, warm water was placed in the chest, and the anaesthetist was asked to deliver some small breaths to check for an air leak. Technical photographs are shown in Fig. 2.

Figure 2:

(A) Transection of bronchus intermedius with hook cautery; (B) transection of the right main bronchus; (C) end-to-end bronchial anastomosis by continuous running suture with 4-0 polypropylene; (D) check air leak. 1: robotic arm 1; 2: robotic arm 2.

Statistical analysis

Mean and standard deviations are used for continuous variables, whereas percentages are used for discrete characteristics. The Student’s t-test or the Fisher’s exact test was adopted, if appropriable, to compare demographics and outcomes between the 2 groups. The Kaplan–Meier method and the log-rank test were used for the distributions of relapse-free survival (RFS) and overall survival (OS) and their comparisons. Univariable and multivariable analyses were performed using Cox’s proportional hazards regression model. The end-point was recognized as event occurrence (relapse for RFS and death for OS). All the relevant clinical factors were combined in the univariable analysis in sequence, with the method ‘Enter’. Furthermore, all the relevant clinical factors were combined in the multivariable analysis when P < 0.05 in univariable analysis, also with the method ‘Enter’. A P-value <0.05 was considered statistically significant. The SPSS 19.0 software package (SPSS Inc., Chicago, IL, USA) and Prism 5 (Graph Pad Software Inc., La Jolla, CA, USA) were used for statistical analyses.

RESULTS

Clinicopathological factors

During the study period, 103 patients (17 robotic and 86 open cases) were enrolled in this study. Of the study cohort, 97 (94%) patients were men and 6 (6%) patients were women; they ranged in age from 40 years to 73 years (median 61.4 years). A majority of the patients (78.6%) were smokers. In addition, in 2 cases in the robotic arm and in 8 cases in the thoracotomy arm, the N1 node affected the resection margin from the outside. Five robotic cases and 15 open cases underwent a preoperative positron emission tomography-CT scan. The demographics of the patients are listed in Table 1.

Table 1:

Demographics in patients having sleeve resection

CharacteristicsRobotic (n = 17)Open (n = 86)P-value
Age (years), mean ± SD62.00 ± 7.8661.14 ± 8.440.69
Gender, n (%)0.013
 Male17 (100)80 (93)
 Female0 (0)6 (7)
Smoking history, n (%)<0.001
 Never11 (65)11 (13)
 Ever6 (35)75 (87)
BMI (kg/m2), mean ± SD23.29 ± 2.8023.46 ± 2.950.83
Comorbidities, n (%)0.69
 Hypertension1 (6)11 (13)
 Coronary heart disease1 (6)2 (2)
 Diabetes mellitus2 (12)7 (8)
ASA score, n (%)0.54
 11 (6)7 (8)
 212 (71)64 (74)
 34 (24)15 (17)
Pulmonary function, mean ± SD
 FEV1%74.88 ± 11.5680.86 ± 13.390.11
 DLCO%83.69 ± 14.5985.00 ± 17.550.79
CharacteristicsRobotic (n = 17)Open (n = 86)P-value
Age (years), mean ± SD62.00 ± 7.8661.14 ± 8.440.69
Gender, n (%)0.013
 Male17 (100)80 (93)
 Female0 (0)6 (7)
Smoking history, n (%)<0.001
 Never11 (65)11 (13)
 Ever6 (35)75 (87)
BMI (kg/m2), mean ± SD23.29 ± 2.8023.46 ± 2.950.83
Comorbidities, n (%)0.69
 Hypertension1 (6)11 (13)
 Coronary heart disease1 (6)2 (2)
 Diabetes mellitus2 (12)7 (8)
ASA score, n (%)0.54
 11 (6)7 (8)
 212 (71)64 (74)
 34 (24)15 (17)
Pulmonary function, mean ± SD
 FEV1%74.88 ± 11.5680.86 ± 13.390.11
 DLCO%83.69 ± 14.5985.00 ± 17.550.79

ASA: American Society of Anesthesiologists; BMI: body mass index; DLCO: carbon monoxide diffusing capacity; FEV1: forced expiratory volume in 1 s; SD: standard deviation.

Table 1:

Demographics in patients having sleeve resection

CharacteristicsRobotic (n = 17)Open (n = 86)P-value
Age (years), mean ± SD62.00 ± 7.8661.14 ± 8.440.69
Gender, n (%)0.013
 Male17 (100)80 (93)
 Female0 (0)6 (7)
Smoking history, n (%)<0.001
 Never11 (65)11 (13)
 Ever6 (35)75 (87)
BMI (kg/m2), mean ± SD23.29 ± 2.8023.46 ± 2.950.83
Comorbidities, n (%)0.69
 Hypertension1 (6)11 (13)
 Coronary heart disease1 (6)2 (2)
 Diabetes mellitus2 (12)7 (8)
ASA score, n (%)0.54
 11 (6)7 (8)
 212 (71)64 (74)
 34 (24)15 (17)
Pulmonary function, mean ± SD
 FEV1%74.88 ± 11.5680.86 ± 13.390.11
 DLCO%83.69 ± 14.5985.00 ± 17.550.79
CharacteristicsRobotic (n = 17)Open (n = 86)P-value
Age (years), mean ± SD62.00 ± 7.8661.14 ± 8.440.69
Gender, n (%)0.013
 Male17 (100)80 (93)
 Female0 (0)6 (7)
Smoking history, n (%)<0.001
 Never11 (65)11 (13)
 Ever6 (35)75 (87)
BMI (kg/m2), mean ± SD23.29 ± 2.8023.46 ± 2.950.83
Comorbidities, n (%)0.69
 Hypertension1 (6)11 (13)
 Coronary heart disease1 (6)2 (2)
 Diabetes mellitus2 (12)7 (8)
ASA score, n (%)0.54
 11 (6)7 (8)
 212 (71)64 (74)
 34 (24)15 (17)
Pulmonary function, mean ± SD
 FEV1%74.88 ± 11.5680.86 ± 13.390.11
 DLCO%83.69 ± 14.5985.00 ± 17.550.79

ASA: American Society of Anesthesiologists; BMI: body mass index; DLCO: carbon monoxide diffusing capacity; FEV1: forced expiratory volume in 1 s; SD: standard deviation.

Perioperative management, tumour characteristics and operative details are listed in Table 2. We usually obtained the results of frozen sections about 30 min after sending the tumour tissues for analysis, and the waiting time was not excluded from the operative time. The operative time of robotic surgery (155.06 ± 44.75 min), even in our initial cases, was comparable to that with a thoracotomy (150.30 ± 47.84 min, P = 0.71). No statistically significant difference was found in terms of mean intraoperative blood loss (P = 0.19), neoadjuvant chemotherapy (P = 0.35), postoperative radiotherapy (P = 0.301), tumour stage (P = 0.42), differentiation (P = 0.28) and the distribution of histological findings (P = 0.31). More open group patients required postoperative chemotherapy (P = 0.028). Squamous cell carcinoma was identified as the most common histological type of tumour in both groups. One patient in the robotic group was converted to thoracotomy because of severe calcification of the lymph nodes.

Table 2:

Intraoperative information, perioperative management and tumour characteristics of patients having sleeve resections

CharacteristicsRobotic (n = 17)Open (n = 86)P-value
Intraoperative information
 Average operative time (min), mean ± SD155.06 ± 44.75150.30 ± 47.840.71
 Average console time (min), mean ± SD113.59 ± 36.61
 Blood loss during operation (ml), mean ± SD164.71 ± 105.72233.73 ± 208.520.19
 Conversion to thoracotomy, n (%)1 (6)
 Surgical procedures, n (%)0.22
  Right upper lobe8 (47)44 (51)
  Right lower lobe07 (8)
  Right upper lobe + middle lobe01 (1)
  Right upper lobe + S601 (1)
  Right middle lobe + lower lobe04 (5)
  Left upper lobe2 (12)18 (21)
  Left lower lobe5 (29)10 (12)
  Left lower lobe + S4 + 52 (12)1 (1)
 LN stations dissected, mean ± SD7.24 ± 1.487.16 ± 1.750.87
 Total LNs removed, mean ± SD15.82 ± 5.0015.81 ± 6.030.99
Perioperative management, n (%)
 Neoadjuvant chemotherapy4 (24)11 (13)0.35
 Postoperative chemotherapy6 (35)55 (64)0.028
 Postoperative radiotherapy6 (35)20 (23)0.301
Tumour characteristics
 Laterality, n (%)0.14
  Left9 (53)29 (34)
  Right8 (47)57 (66)
 Histological status, n (%)0.31
  Adenocarcinoma09 (11)
  Squamous cell carcinoma13 (76)62 (72)
  Small cell lung cancer1 (6)4 (5)
  Others3 (18)11 (13)
 Stump, n (%)0.56
  R016 (94)77 (90)
  R11 (6)9 (10)
 Stage, n (%)0.42
  Ia + Ib6 (35)36 (42)
  IIa + IIb5 (30)29 (34)
  IIIa6 (35)21 (24)
 T size, mean ± SD3.48 ± 1.273.58 ± 1.690.82
 T stage, n (%)0.11
  1a + 1b5 (29)33 (39)
  2a + 2b9 (53)51 (59)
  33 (18)2 (2)
 N stage, n (%)0.79
  N07 (42)36 (42)
  N15 (29)29 (34)
  N25 (29)21 (24)
 Grade, n (%)0.28
  Well differentiated11 (66)11 (13)
  Moderately differentiated1 (6)19 (22)
  Poorly differentiated3 (18)29 (34)
  Unknown2 (12)27 (31)
CharacteristicsRobotic (n = 17)Open (n = 86)P-value
Intraoperative information
 Average operative time (min), mean ± SD155.06 ± 44.75150.30 ± 47.840.71
 Average console time (min), mean ± SD113.59 ± 36.61
 Blood loss during operation (ml), mean ± SD164.71 ± 105.72233.73 ± 208.520.19
 Conversion to thoracotomy, n (%)1 (6)
 Surgical procedures, n (%)0.22
  Right upper lobe8 (47)44 (51)
  Right lower lobe07 (8)
  Right upper lobe + middle lobe01 (1)
  Right upper lobe + S601 (1)
  Right middle lobe + lower lobe04 (5)
  Left upper lobe2 (12)18 (21)
  Left lower lobe5 (29)10 (12)
  Left lower lobe + S4 + 52 (12)1 (1)
 LN stations dissected, mean ± SD7.24 ± 1.487.16 ± 1.750.87
 Total LNs removed, mean ± SD15.82 ± 5.0015.81 ± 6.030.99
Perioperative management, n (%)
 Neoadjuvant chemotherapy4 (24)11 (13)0.35
 Postoperative chemotherapy6 (35)55 (64)0.028
 Postoperative radiotherapy6 (35)20 (23)0.301
Tumour characteristics
 Laterality, n (%)0.14
  Left9 (53)29 (34)
  Right8 (47)57 (66)
 Histological status, n (%)0.31
  Adenocarcinoma09 (11)
  Squamous cell carcinoma13 (76)62 (72)
  Small cell lung cancer1 (6)4 (5)
  Others3 (18)11 (13)
 Stump, n (%)0.56
  R016 (94)77 (90)
  R11 (6)9 (10)
 Stage, n (%)0.42
  Ia + Ib6 (35)36 (42)
  IIa + IIb5 (30)29 (34)
  IIIa6 (35)21 (24)
 T size, mean ± SD3.48 ± 1.273.58 ± 1.690.82
 T stage, n (%)0.11
  1a + 1b5 (29)33 (39)
  2a + 2b9 (53)51 (59)
  33 (18)2 (2)
 N stage, n (%)0.79
  N07 (42)36 (42)
  N15 (29)29 (34)
  N25 (29)21 (24)
 Grade, n (%)0.28
  Well differentiated11 (66)11 (13)
  Moderately differentiated1 (6)19 (22)
  Poorly differentiated3 (18)29 (34)
  Unknown2 (12)27 (31)

LN: lymph node; N: node; S: segment; SD: standard deviation; T: tumour.

Table 2:

Intraoperative information, perioperative management and tumour characteristics of patients having sleeve resections

CharacteristicsRobotic (n = 17)Open (n = 86)P-value
Intraoperative information
 Average operative time (min), mean ± SD155.06 ± 44.75150.30 ± 47.840.71
 Average console time (min), mean ± SD113.59 ± 36.61
 Blood loss during operation (ml), mean ± SD164.71 ± 105.72233.73 ± 208.520.19
 Conversion to thoracotomy, n (%)1 (6)
 Surgical procedures, n (%)0.22
  Right upper lobe8 (47)44 (51)
  Right lower lobe07 (8)
  Right upper lobe + middle lobe01 (1)
  Right upper lobe + S601 (1)
  Right middle lobe + lower lobe04 (5)
  Left upper lobe2 (12)18 (21)
  Left lower lobe5 (29)10 (12)
  Left lower lobe + S4 + 52 (12)1 (1)
 LN stations dissected, mean ± SD7.24 ± 1.487.16 ± 1.750.87
 Total LNs removed, mean ± SD15.82 ± 5.0015.81 ± 6.030.99
Perioperative management, n (%)
 Neoadjuvant chemotherapy4 (24)11 (13)0.35
 Postoperative chemotherapy6 (35)55 (64)0.028
 Postoperative radiotherapy6 (35)20 (23)0.301
Tumour characteristics
 Laterality, n (%)0.14
  Left9 (53)29 (34)
  Right8 (47)57 (66)
 Histological status, n (%)0.31
  Adenocarcinoma09 (11)
  Squamous cell carcinoma13 (76)62 (72)
  Small cell lung cancer1 (6)4 (5)
  Others3 (18)11 (13)
 Stump, n (%)0.56
  R016 (94)77 (90)
  R11 (6)9 (10)
 Stage, n (%)0.42
  Ia + Ib6 (35)36 (42)
  IIa + IIb5 (30)29 (34)
  IIIa6 (35)21 (24)
 T size, mean ± SD3.48 ± 1.273.58 ± 1.690.82
 T stage, n (%)0.11
  1a + 1b5 (29)33 (39)
  2a + 2b9 (53)51 (59)
  33 (18)2 (2)
 N stage, n (%)0.79
  N07 (42)36 (42)
  N15 (29)29 (34)
  N25 (29)21 (24)
 Grade, n (%)0.28
  Well differentiated11 (66)11 (13)
  Moderately differentiated1 (6)19 (22)
  Poorly differentiated3 (18)29 (34)
  Unknown2 (12)27 (31)
CharacteristicsRobotic (n = 17)Open (n = 86)P-value
Intraoperative information
 Average operative time (min), mean ± SD155.06 ± 44.75150.30 ± 47.840.71
 Average console time (min), mean ± SD113.59 ± 36.61
 Blood loss during operation (ml), mean ± SD164.71 ± 105.72233.73 ± 208.520.19
 Conversion to thoracotomy, n (%)1 (6)
 Surgical procedures, n (%)0.22
  Right upper lobe8 (47)44 (51)
  Right lower lobe07 (8)
  Right upper lobe + middle lobe01 (1)
  Right upper lobe + S601 (1)
  Right middle lobe + lower lobe04 (5)
  Left upper lobe2 (12)18 (21)
  Left lower lobe5 (29)10 (12)
  Left lower lobe + S4 + 52 (12)1 (1)
 LN stations dissected, mean ± SD7.24 ± 1.487.16 ± 1.750.87
 Total LNs removed, mean ± SD15.82 ± 5.0015.81 ± 6.030.99
Perioperative management, n (%)
 Neoadjuvant chemotherapy4 (24)11 (13)0.35
 Postoperative chemotherapy6 (35)55 (64)0.028
 Postoperative radiotherapy6 (35)20 (23)0.301
Tumour characteristics
 Laterality, n (%)0.14
  Left9 (53)29 (34)
  Right8 (47)57 (66)
 Histological status, n (%)0.31
  Adenocarcinoma09 (11)
  Squamous cell carcinoma13 (76)62 (72)
  Small cell lung cancer1 (6)4 (5)
  Others3 (18)11 (13)
 Stump, n (%)0.56
  R016 (94)77 (90)
  R11 (6)9 (10)
 Stage, n (%)0.42
  Ia + Ib6 (35)36 (42)
  IIa + IIb5 (30)29 (34)
  IIIa6 (35)21 (24)
 T size, mean ± SD3.48 ± 1.273.58 ± 1.690.82
 T stage, n (%)0.11
  1a + 1b5 (29)33 (39)
  2a + 2b9 (53)51 (59)
  33 (18)2 (2)
 N stage, n (%)0.79
  N07 (42)36 (42)
  N15 (29)29 (34)
  N25 (29)21 (24)
 Grade, n (%)0.28
  Well differentiated11 (66)11 (13)
  Moderately differentiated1 (6)19 (22)
  Poorly differentiated3 (18)29 (34)
  Unknown2 (12)27 (31)

LN: lymph node; N: node; S: segment; SD: standard deviation; T: tumour.

Postoperative complications

The postoperative outcomes are listed in Table 3. Four (24%) patients in the robotic group and 22 (26%) patients in the thoracotomy group experienced postoperative complications (P = 0.86). No intraoperative deaths occurred in either group. There was no significant difference in postoperative stay (P = 0.42), intensive care unit (ICU) stay (P = 0.22) and drainage time (P = 0.26) between the 2 groups. The 30-day mortality in the robotic group and the thoracotomy group was 1 (6%) and 2 (2%) patients, respectively, with no significant difference (P = 0.43). Specifically, the patient in the robotic group experienced bronchial anastomosis bleeding, pneumonia, bronchial anastomosis leakage and pyothorax and finally died of multiple organ failure. In thoracotomy group, 1 patient died of the anastomosis bursting 7 days later, whereas the other patient experienced bronchopleural fistula and pyothorax and finally died of sudden massive haemoptysis 2 weeks after the operation. In addition, 1 patient in the robotic group, who experienced pyothorax 1 month after the operation, was treated with drainage and discharged 2 months later. One patient in the thoracotomy group was readmitted, along with dyspnoea, due to anastomotic obstruction that was finally alleviated after implantation of a bronchial stent.

Table 3:

Postoperative outcomes

EventRobotic (n = 17)Open (n = 86)P-value
Postoperative stay (days), mean ± SD11.24 ± 8.409.50 ± 4.140.42
ICU stay (days), mean ± SD4.47 ± 7.342.15 ± 3.270.22
Drainage time (days), mean ± SD9.24 ± 9.266.59 ± 2.820.26
30-Day mortality, n (%)1 (6)2 (2)0.43
Complications, n (%)4 (24)22 (26)0.86
 Subcutaneous emphysema2 (12)3 (4)
 Cardiac arrhythmia2 (12)4 (5)
 Pulmonary infection2 (12)8 (9)
 Pyothorax2 (12)2 (2)
 Bronchial anastomosis bleeding1 (6)0
 Bronchopleural fistula1 (6)6 (7)
 Anastomosis bursting01 (1)
 Multiple organ failure1 (6)0
 Transfusion2 (12)5 (6)
 Intraoperative massive bleeding (more than 800 ml)03 (4)
 Recurrent laryngeal nerve injury01 (1)
 Anastomotic stenosis/obstruction02 (2)
 Postoperative tracheotomy01 (1)
Progression, n (%)
 Recurrence6 (35)21 (24)0.36
  Local5 (29)10 (12)
  Distant1 (6)11 (13)
 No recurrence11 (65)65 (76)
EventRobotic (n = 17)Open (n = 86)P-value
Postoperative stay (days), mean ± SD11.24 ± 8.409.50 ± 4.140.42
ICU stay (days), mean ± SD4.47 ± 7.342.15 ± 3.270.22
Drainage time (days), mean ± SD9.24 ± 9.266.59 ± 2.820.26
30-Day mortality, n (%)1 (6)2 (2)0.43
Complications, n (%)4 (24)22 (26)0.86
 Subcutaneous emphysema2 (12)3 (4)
 Cardiac arrhythmia2 (12)4 (5)
 Pulmonary infection2 (12)8 (9)
 Pyothorax2 (12)2 (2)
 Bronchial anastomosis bleeding1 (6)0
 Bronchopleural fistula1 (6)6 (7)
 Anastomosis bursting01 (1)
 Multiple organ failure1 (6)0
 Transfusion2 (12)5 (6)
 Intraoperative massive bleeding (more than 800 ml)03 (4)
 Recurrent laryngeal nerve injury01 (1)
 Anastomotic stenosis/obstruction02 (2)
 Postoperative tracheotomy01 (1)
Progression, n (%)
 Recurrence6 (35)21 (24)0.36
  Local5 (29)10 (12)
  Distant1 (6)11 (13)
 No recurrence11 (65)65 (76)

ICU: intensive care unit; SD: standard deviation.

Table 3:

Postoperative outcomes

EventRobotic (n = 17)Open (n = 86)P-value
Postoperative stay (days), mean ± SD11.24 ± 8.409.50 ± 4.140.42
ICU stay (days), mean ± SD4.47 ± 7.342.15 ± 3.270.22
Drainage time (days), mean ± SD9.24 ± 9.266.59 ± 2.820.26
30-Day mortality, n (%)1 (6)2 (2)0.43
Complications, n (%)4 (24)22 (26)0.86
 Subcutaneous emphysema2 (12)3 (4)
 Cardiac arrhythmia2 (12)4 (5)
 Pulmonary infection2 (12)8 (9)
 Pyothorax2 (12)2 (2)
 Bronchial anastomosis bleeding1 (6)0
 Bronchopleural fistula1 (6)6 (7)
 Anastomosis bursting01 (1)
 Multiple organ failure1 (6)0
 Transfusion2 (12)5 (6)
 Intraoperative massive bleeding (more than 800 ml)03 (4)
 Recurrent laryngeal nerve injury01 (1)
 Anastomotic stenosis/obstruction02 (2)
 Postoperative tracheotomy01 (1)
Progression, n (%)
 Recurrence6 (35)21 (24)0.36
  Local5 (29)10 (12)
  Distant1 (6)11 (13)
 No recurrence11 (65)65 (76)
EventRobotic (n = 17)Open (n = 86)P-value
Postoperative stay (days), mean ± SD11.24 ± 8.409.50 ± 4.140.42
ICU stay (days), mean ± SD4.47 ± 7.342.15 ± 3.270.22
Drainage time (days), mean ± SD9.24 ± 9.266.59 ± 2.820.26
30-Day mortality, n (%)1 (6)2 (2)0.43
Complications, n (%)4 (24)22 (26)0.86
 Subcutaneous emphysema2 (12)3 (4)
 Cardiac arrhythmia2 (12)4 (5)
 Pulmonary infection2 (12)8 (9)
 Pyothorax2 (12)2 (2)
 Bronchial anastomosis bleeding1 (6)0
 Bronchopleural fistula1 (6)6 (7)
 Anastomosis bursting01 (1)
 Multiple organ failure1 (6)0
 Transfusion2 (12)5 (6)
 Intraoperative massive bleeding (more than 800 ml)03 (4)
 Recurrent laryngeal nerve injury01 (1)
 Anastomotic stenosis/obstruction02 (2)
 Postoperative tracheotomy01 (1)
Progression, n (%)
 Recurrence6 (35)21 (24)0.36
  Local5 (29)10 (12)
  Distant1 (6)11 (13)
 No recurrence11 (65)65 (76)

ICU: intensive care unit; SD: standard deviation.

Survival analysis

Univariable analysis revealed that a stump, stage, tumour size, tumour stage, nodal stage, postoperative chemotherapy and postoperative radiotherapy were significant predictors of RFS, whereas complications, ICU stay, postoperative hospital stay, stage, tumour size, tumour stage, nodal stage and pleural invasion were significant predictors of OS (Table 4). Furthermore, tumour size and postoperative radiotherapy were still significant predictors of RFS, whereas only ICU stay was a significant predictor of OS in multivariable analysis (Table 5).

Table 4:

Univariable analyses for RFS and OS in sleeve resection patients

RFS
OS
VariablesOR95% CIP-valueOR95% CIP-value
Age (years)0.990.954–1.0420.891.050.991–1.1170.095
Gender0.040.000–23.3520.330.050.000–128.9110.45
Smoking history1.320.501–3.4960.572.480.575–10.7110.22
Surgical procedure1.910.768–4.7320.160.680.156–2.9100.59
Comorbidities0.480.166–1.3940.180.340.079–1.4750.15
BMI (kg/m2)0.990.877–1.1280.931.000.872–1.1560.96
ASA score0.900.437–1.8720.791.140.479–2.7080.77
Stump2.761.040–7.3290.0412.690.893–8.1300.079
Tumour location0.190.849–2.3101.4011.090.582–2.0380.79
Complications1.260.531–2.9750.6033.341.387–8.0350.007
ICU stay, d1.020.848–1.2150.871.211.106–1.323<0.001
Postoperative hospital stay, d1.020.924–1.1290.681.151.077–1.228<0.001
Histology0.810.472–1.3730.430.510.237–1.0890.082
Stage2.261.384–3.6910.0012.111.202–3.6860.009
T size (cm)1.721.345–2.187<0.0011.521.212–1.907<0.001
T stage3.191.460–6.9720.0044.631.831–11.7090.001
N stage2.351.430–3.8520.0012.161.231–3.7980.007
Pleural invasion2.390.958–5.9060.0623.181.208–8.3680.019
Grade1.170.851–1.5980.341.010.697–1.4570.97
Neoadjuvant chemotherapy1.540.580–4.0640.392.220.805–6.1370.12
Postoperative chemotherapy2.771.049–7.3190.0400.980.395–2.4400.97
Postoperative radiotherapy3.741.752–7.9770.0011.610.641–4.0620.31
RFS
OS
VariablesOR95% CIP-valueOR95% CIP-value
Age (years)0.990.954–1.0420.891.050.991–1.1170.095
Gender0.040.000–23.3520.330.050.000–128.9110.45
Smoking history1.320.501–3.4960.572.480.575–10.7110.22
Surgical procedure1.910.768–4.7320.160.680.156–2.9100.59
Comorbidities0.480.166–1.3940.180.340.079–1.4750.15
BMI (kg/m2)0.990.877–1.1280.931.000.872–1.1560.96
ASA score0.900.437–1.8720.791.140.479–2.7080.77
Stump2.761.040–7.3290.0412.690.893–8.1300.079
Tumour location0.190.849–2.3101.4011.090.582–2.0380.79
Complications1.260.531–2.9750.6033.341.387–8.0350.007
ICU stay, d1.020.848–1.2150.871.211.106–1.323<0.001
Postoperative hospital stay, d1.020.924–1.1290.681.151.077–1.228<0.001
Histology0.810.472–1.3730.430.510.237–1.0890.082
Stage2.261.384–3.6910.0012.111.202–3.6860.009
T size (cm)1.721.345–2.187<0.0011.521.212–1.907<0.001
T stage3.191.460–6.9720.0044.631.831–11.7090.001
N stage2.351.430–3.8520.0012.161.231–3.7980.007
Pleural invasion2.390.958–5.9060.0623.181.208–8.3680.019
Grade1.170.851–1.5980.341.010.697–1.4570.97
Neoadjuvant chemotherapy1.540.580–4.0640.392.220.805–6.1370.12
Postoperative chemotherapy2.771.049–7.3190.0400.980.395–2.4400.97
Postoperative radiotherapy3.741.752–7.9770.0011.610.641–4.0620.31

ASA: American Society of Anesthesiologists; BMI: body mass index; CI: confidence interval; ICU: intensive care unit; OR: odds ratio; OS: overall survival; RFS: relapse-free survival; T: tumour.

Table 4:

Univariable analyses for RFS and OS in sleeve resection patients

RFS
OS
VariablesOR95% CIP-valueOR95% CIP-value
Age (years)0.990.954–1.0420.891.050.991–1.1170.095
Gender0.040.000–23.3520.330.050.000–128.9110.45
Smoking history1.320.501–3.4960.572.480.575–10.7110.22
Surgical procedure1.910.768–4.7320.160.680.156–2.9100.59
Comorbidities0.480.166–1.3940.180.340.079–1.4750.15
BMI (kg/m2)0.990.877–1.1280.931.000.872–1.1560.96
ASA score0.900.437–1.8720.791.140.479–2.7080.77
Stump2.761.040–7.3290.0412.690.893–8.1300.079
Tumour location0.190.849–2.3101.4011.090.582–2.0380.79
Complications1.260.531–2.9750.6033.341.387–8.0350.007
ICU stay, d1.020.848–1.2150.871.211.106–1.323<0.001
Postoperative hospital stay, d1.020.924–1.1290.681.151.077–1.228<0.001
Histology0.810.472–1.3730.430.510.237–1.0890.082
Stage2.261.384–3.6910.0012.111.202–3.6860.009
T size (cm)1.721.345–2.187<0.0011.521.212–1.907<0.001
T stage3.191.460–6.9720.0044.631.831–11.7090.001
N stage2.351.430–3.8520.0012.161.231–3.7980.007
Pleural invasion2.390.958–5.9060.0623.181.208–8.3680.019
Grade1.170.851–1.5980.341.010.697–1.4570.97
Neoadjuvant chemotherapy1.540.580–4.0640.392.220.805–6.1370.12
Postoperative chemotherapy2.771.049–7.3190.0400.980.395–2.4400.97
Postoperative radiotherapy3.741.752–7.9770.0011.610.641–4.0620.31
RFS
OS
VariablesOR95% CIP-valueOR95% CIP-value
Age (years)0.990.954–1.0420.891.050.991–1.1170.095
Gender0.040.000–23.3520.330.050.000–128.9110.45
Smoking history1.320.501–3.4960.572.480.575–10.7110.22
Surgical procedure1.910.768–4.7320.160.680.156–2.9100.59
Comorbidities0.480.166–1.3940.180.340.079–1.4750.15
BMI (kg/m2)0.990.877–1.1280.931.000.872–1.1560.96
ASA score0.900.437–1.8720.791.140.479–2.7080.77
Stump2.761.040–7.3290.0412.690.893–8.1300.079
Tumour location0.190.849–2.3101.4011.090.582–2.0380.79
Complications1.260.531–2.9750.6033.341.387–8.0350.007
ICU stay, d1.020.848–1.2150.871.211.106–1.323<0.001
Postoperative hospital stay, d1.020.924–1.1290.681.151.077–1.228<0.001
Histology0.810.472–1.3730.430.510.237–1.0890.082
Stage2.261.384–3.6910.0012.111.202–3.6860.009
T size (cm)1.721.345–2.187<0.0011.521.212–1.907<0.001
T stage3.191.460–6.9720.0044.631.831–11.7090.001
N stage2.351.430–3.8520.0012.161.231–3.7980.007
Pleural invasion2.390.958–5.9060.0623.181.208–8.3680.019
Grade1.170.851–1.5980.341.010.697–1.4570.97
Neoadjuvant chemotherapy1.540.580–4.0640.392.220.805–6.1370.12
Postoperative chemotherapy2.771.049–7.3190.0400.980.395–2.4400.97
Postoperative radiotherapy3.741.752–7.9770.0011.610.641–4.0620.31

ASA: American Society of Anesthesiologists; BMI: body mass index; CI: confidence interval; ICU: intensive care unit; OR: odds ratio; OS: overall survival; RFS: relapse-free survival; T: tumour.

Table 5:

Multivariable analyses of RFS and OS in patients who had sleeve resections

RFS
OS
VariablesOR95% CIP-valueOR95% CIP-value
Stump1.810.639–5.1480.26
Complications0.960.285–3.2040.94
ICU stay, d1.171.044–1.3080.007
Postoperative hospital stay, d1.050.940–1.1820.37
T size (cm)2.171.391–3.3780.0011.380.931–2.0340.11
T stage0.480.111–2.0430.322.080.592–7.3140.25
Pleural invasion1.040.328–3.3060.95
Postoperative chemotherapy0.120.374–3.3190.85
Postoperative radiotherapy3.981.542–10.2760.004
RFS
OS
VariablesOR95% CIP-valueOR95% CIP-value
Stump1.810.639–5.1480.26
Complications0.960.285–3.2040.94
ICU stay, d1.171.044–1.3080.007
Postoperative hospital stay, d1.050.940–1.1820.37
T size (cm)2.171.391–3.3780.0011.380.931–2.0340.11
T stage0.480.111–2.0430.322.080.592–7.3140.25
Pleural invasion1.040.328–3.3060.95
Postoperative chemotherapy0.120.374–3.3190.85
Postoperative radiotherapy3.981.542–10.2760.004

CI: confidence interval; ICU: intensive care unit; OR: odds ratio; OS: overall survival; RFS: relapse-free survival; T: tumour.

Table 5:

Multivariable analyses of RFS and OS in patients who had sleeve resections

RFS
OS
VariablesOR95% CIP-valueOR95% CIP-value
Stump1.810.639–5.1480.26
Complications0.960.285–3.2040.94
ICU stay, d1.171.044–1.3080.007
Postoperative hospital stay, d1.050.940–1.1820.37
T size (cm)2.171.391–3.3780.0011.380.931–2.0340.11
T stage0.480.111–2.0430.322.080.592–7.3140.25
Pleural invasion1.040.328–3.3060.95
Postoperative chemotherapy0.120.374–3.3190.85
Postoperative radiotherapy3.981.542–10.2760.004
RFS
OS
VariablesOR95% CIP-valueOR95% CIP-value
Stump1.810.639–5.1480.26
Complications0.960.285–3.2040.94
ICU stay, d1.171.044–1.3080.007
Postoperative hospital stay, d1.050.940–1.1820.37
T size (cm)2.171.391–3.3780.0011.380.931–2.0340.11
T stage0.480.111–2.0430.322.080.592–7.3140.25
Pleural invasion1.040.328–3.3060.95
Postoperative chemotherapy0.120.374–3.3190.85
Postoperative radiotherapy3.981.542–10.2760.004

CI: confidence interval; ICU: intensive care unit; OR: odds ratio; OS: overall survival; RFS: relapse-free survival; T: tumour.

The median follow-up time was 20 months. During the follow-up period, 6 (35%) patients in the robotic group and 21 (24%) patients in the thoracotomy group experienced a relapse. Two (12%) and 18 (21%) patients died, respectively. The 2-year survival rate was 88.2% in the robotic group, whereas the rate was 78.5% in the thoracotomy group. There was no significant difference in RFS (log-rank P = 0.16) and OS (log-rank P = 0.59) for patients in the robotic group compared with patients in the thoracotomy group (Fig. 3). Local and distant recurrence occurred in 5 (29%) and 1 (6%) patients, respectively, in the robotic group, whereas 10 (12%) and 11 (13%) cases occurred in the thoracotomy group, respectively (Table 3).

Figure 3:

Kaplan–Meier survival curves for relapse-free survival (A) and overall survival (B).

DISCUSSION

An increasing number of patients will have lung cancer, given the high incidence of the disease. A remarkable proportion of these individuals have centrally located neoplasms. Pan et al. [20] demonstrated that the sleeve resection yielded at least equivalent oncological results and a better 5-year survival rate, especially in elderly patients, than open procedures. Consequently, sleeve resection should be performed, provided a complete resection can be achieved, not only in patients with marginal lung function but whenever technically feasible [5, 21]. In this retrospective study of patients with centrally located tumours, robotic bronchial sleeve resection was not inferior to open sleeve resection in terms of comparable complication rates and mid-term survival rates.

Minimally invasive surgery has been widely adopted in thoracic surgery, especially for peripheral early-stage lung cancer. As operative experience with VATS lung resection has increased, VATS sleeve resection has been attempted by some experienced centres. Zhou et al. [10] reported on 10 patients who underwent VATS sleeve resection and showed that sleeve lobectomy can be performed safely with similar short-term and long-term outcomes compared with sleeve resections performed by thoracotomy. Unfortunately, the mean operative time was significantly longer in the VATS group than in the open group (226 min vs 166 min, P <0.001), which may be caused by the inherent deficiency of VATS—the lack of depth perception and manoeuvrability. Despite the controversy since the advent of robotic surgery, focused mainly on cost, operative time, postoperative outcomes and long-term survival, the 3D vision and EndWrist technology that accompany the robotic surgical system help the surgeons to gain proficiency performing procedures with the robotic equipment. A recent meta-analysis confirmed that robotic surgery is a feasible and safe alternative to VATS for radical resection of lung cancer [22, 23]. In our study, there was no difference in average operative time between the 2 groups (robotic versus thoracotomy 155.06 min vs 150.30 min, P = 0.71), although the 17 patients were our initial robotic cases. The mean console time was 113.59 min. In addition, intraoperative blood loss in the robotic group was somewhat less but was not statistically significant. There are several reasons for the preceding differences. First, a robotic surgical system, as a kind of minimally invasive technique, inherits the merits of VATS. Therefore, it is reasonable that robotic surgery would have less blood loss and less pain. Second, with the hands of experienced VATS surgeon, the learning curve of robotic surgery could be steep.

The first clinical application of robotic sleeve resection was reported by Schmid et al. [14] in 2011. They performed a hybrid right upper sleeve lobectomy on a 30-year-old woman; she had an uneventful postoperative course and was discharged on postoperative Day 15. In 2013, Nakamura et al. [15] also successfully performed a robotic bronchoplastic lobectomy for lung squamous cell carcinoma. The patient did not experience a relapse 14 months after the surgery; they therefore concluded that the operability of robotic bronchoplasty surpasses that of VATS. Lately, Cerfolio [18] reported operative details and short-term outcomes of 8 cases of robotic sleeve resection. There were no perioperative deaths and no major complications in his report.

Conducting a bronchial anastomosis is the key step in bronchoplastic lobectomy. We prefer to use continuous running sutures to perform the bronchial anastomosis, which is basically in line with the procedure of Schmid et al. [14], whereas Nakamura et al. [15] and Cerfolio [18] used multiple interrupted sutures. However, despite broad acceptance of sleeve lobectomy, there is currently no standard for the anastomotic technique. Palade et al. [24] compared the impact on the postoperative complication rate between the 2 suture techniques and reported that both of the suture techniques performed well. Moreover, the interrupted suture has the advantage of compensating for size mismatch, whereas the continuous running suture saves time and is valuable in patients with large-calibre bronchi and relevant size mismatch.

Four (24%) patients in the robotic group and 22 (26%) patients in the open group experienced perioperative complications. Given the 3D vision for magnification of the operative field and precise dissection with improved ergonomics for the surgeon, the robotic surgical system provided more delicate manipulation to perform bronchoplastic procedures and resulted in fewer anastomotic complications or intraoperative injuries. In our study, anastomotic complications occurred in only 1 (6%) robotic case and in 9 (11%) open procedures, respectively (P = 0.002). In addition, there was no intraoperative haemorrhage or nerve injury in the robotic group. Furthermore, sleeve resection leads to hypersecretion of mucus and lessened mucociliary clearance due to the destruction of parasympathetic nerves and lymphatic vessels [25]. Thus, perioperative airway management is vitally important. In our series, with careful perioperative airway nursing, only 2 (2%) patients had anastomotic stenosis/obstruction, and all of them received targeted remedies and recovered before discharge from the hospital. There were no intraoperative deaths, either in the robotic group or in the thoracotomy group. One (6%) patient in the robotic group was converted to thoracotomy because of severe calcification of the lymph node, which was comparable to the results (1 of 8, 13%) of Cerfolio [18]. The 30-day mortality rate of robotic surgery was 6%, which was no different than that with open procedures. The mean hospital stay was 11.24 days. It seemed a little longer for sleeve resection because they were the initial cases, 2 of whom experienced severe postoperative complications that required long stays in the ICU, long drainage times and long hospital stays.

Five (29%) robotic cases and 21 (24%) open cases were identified as N2 positive in the final pathology reports. Several reasons contributed to the relatively high rate of final mediastinal N2-positive lymph nodes: (i) The existence of nodal upstaging—some patients who were thought to have N2-negative disease following a preoperative examination (even positron emission tomography-CT was performed [26]) were found to have N2-positive disease. (ii) For patients with a positive single N2 station, we still considered surgery after neoadjuvant chemotherapy.

The 2-year survival rate was 88.2% in the robotic group, whereas the rate was 78.5% in the thoracotomy group. The results were comparable to those of previous studies [2, 3, 21]. Furthermore, multivariable analysis revealed that tumour size and postoperative radiotherapy were significant predictors of RFS, whereas only ICU stay was a significant predictor of OS. Postoperative radiotherapy was commonly adopted in patients with an R1 stump and consequently resulted in a higher relapse rate. A longer stay in the ICU was associated with postoperative complications and therefore could easily affect prognosis.

Limitations

Our study has several limitations. First, this study represents a retrospective analysis from a single centre, which would have selection bias. Second, although this study currently contains the largest number of robotic bronchial sleeve resections published thus far, the sample size is still relatively small, and some of these operations were affected by our learning curve. In addition to the initial cases and the relatively small sample size in the robotic group, we had limited degrees of freedom to uncover all the significant factors, and the study may be underpowered. Third, with the short follow-up time, the long-term outcomes are still uncertain and need further study. These facts must be taken into consideration when interpreting the results of this study. A randomized controlled trial is still needed to clarify the advantages and disadvantages between robotic and open procedures in the near future and to obtain meaningful results that can be used to better guide clinical practice.

CONCLUSION

In conclusion, robotic surgery for bronchial sleeve resection is safe and feasible and has oncological outcomes similar to those obtained with open procedures. Nevertheless, long-term survival rates still need further investigation.

Funding

This work was supported by the National Natural Science Foundation of China [81572245]; and Shanghai Municipal Commission of Health and Family Planning [20144Y0169].

Conflict of interest: none declared.

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Author notes

Chang Gu and Xufeng Pan contributed equally to this work.