Da Vinci robot versus thoracoscopic surgery for lymph node dissection in radical lung cancer: a propensity score matching study

doi:10.21203/rs.3.rs-2607667/v1

Objective: To compare the efficacy of robot-assisted thoracoscopic surgery (RATS) with video-assisted thoracoscopic surgery (VATS) in lymph node dissection for radical lung cancer.

Methods: Retrospective analysis of 262 minimally invasive surgically treated lung cancer patients who underwent radical lung cancer surgery via RATS (n=122) or VATS (n=140) completed by the same operator in the Department of Thoracic Surgery, Gansu Provincial People’s Hospital from August 2019 to August 2022. Propensity score matching (PSM) analysis was performed to compare the procedure-related information of the two groups of patients.

Results: All patients in both groups successfully completed radical lung cancer surgery with no perioperative deaths. There are 100 patients in each group after PSM. The RATS group had an advantage in terms of intraoperative bleeding, postoperative drainage time, postoperative hospital stay, number of lymph nodes cleared (6, 10, 11 stations), number of lymph nodes cleared, and escalation of lymph node pathological stage (cN0 to pN1). In terms of total postoperative chest drainage and hospital costs, the VATS group was more advantageous. There was no statistically significant difference between the two groups in terms of operative time, postoperative complications and intraoperative intermediate chest opening (P>0.05).

Conclusion: RATS has technical and short-term efficacy advantages, especially in lymph node dissection, but has the disadvantage of expensive.

Robot-assisted thoracic surgery

Video-assisted thoracoscopic surgery

Lung cancer

Lymph node dissection

Propensity score matching

Lung cancer is one of the most common malignancies worldwide and the leading cause of tumor-related deaths [1]. The gold standard of treatment for early-stage non-small cell lung cancer (NSCLC) is surgical resection [2]. VATS offers less pain, shorter hospital stays, and fewer perioperative complications than conventional open-chest surgery, and is not inferior to open-chest surgery in terms of long-term oncologic outcomes [3]. VATS has been widely used in NSCLC surgery, but VATS has some shortcomings. The application of RATS further solves the problems of long learning curve of VATS, counter-intuitive operation logic, lack of stereoscopic vision and poor instrument mobility [4,5]. At the same time, RATS can effectively reduce surgeon fatigue, and for procedures that require more delicate and complex operations with longer operating times, RATS helps the operator to focus and ensures a smoother procedure [6].

Lymph node dissection is an important component of NSCLC surgery that improves prognosis and increases the accuracy of staging. Several previous studies have evaluated RATS versus VATS for lymph node dissection in NSCLC surgery, but controversy remains. In addition, few studies have analyzed in detail the outcomes associated with lymph node dissection in patients with NSCLC treated with RATS versus VATS. Therefore, in this study, we applied PSM to compare the short-term efficacy and safety of RATS versus VATS radical lung cancer treatment in our single medical group with a focus on outcomes related to lymph node dissection.

Clinical information

A total of 262 patients with NSCLC treated by minimally invasive surgery completed by the same operator consecutively in the Department of Thoracic Surgery of Gansu Provincial People’s Hospital from August 2019 to August 2022 were selected. Inclusion criteria: (1) 18 to 80 years old, preoperative examination and assessment of cardiopulmonary function to tolerate surgery; (2) preoperative tracheoscopy, computed tomography (CT) guided puncture biopsy or intraoperative rapid cryopathological examination was performed to clarify the diagnosis of NSCLC. Exclusion criteria: (1) intraoperative finding of pleural dissemination; (2) patients who cannot tolerate surgery due to cardiopulmonary or hepatic or renal insufficiency; (3) to prevent the problem of bias due to different operators or assistants, we excluded some of the data of patients operated by different operators and analyzed them with data from the same operator and assistant.

This study has been reviewed by the Ethics Committee of Gansu Provincial People’s Hospital, approval number: 2022-394. All patients signed the informed consent form for surgery before surgery.

Surgical methods

RATS group: The patient was intubated with a double-lumen trachea and general anesthesia with intravenous inhalation complex. Take the healthy side lying position, healthy side single lung ventilation, padding the chest, both upper limbs flexion pillow folding knife position, lower the shoulder and hip to avoid mechanical compression. The da Vinci robot is loaded and punched using the three-arm, four-hole method. The anterolateral approach 3-4-6-8/9 perforation strategy was used, i.e. the mirror hole was placed at the 6th intercostal space in the posterior axillary line, the remaining two operating holes were placed at the 8th/9th intercostal space in the posterior axillary line and the 3rd intercostal space in the anterior axillary line, and the auxiliary operating port was placed at the 4th intercostal space in the midclavicular line. Surgery begins with freeing the inferior pulmonary ligament, depending on the development of the pulmonary fissures, either anatomically if the fissures are well developed or unidirectionally by lobectomy if the fissures are poorly developed. Clearing the hilum (groups 10 and 11) and mediastinal lymph nodes (left side: groups 5, 6, 7, 8 and 9 lymph nodes; right side: groups 2, 4, 7, 8 and 9 lymph nodes) after successful resection of the diseased lung lobes. Figure of the intraoperative lymph node dissection are shown in Figure 1. One or two drainage tubes were left in place postoperatively.

VATS group: The patient was intubated with a double-lumen trachea and general anesthesia with intravenous inhalation complex. One-lung ventilation on the healthy side, with the healthy side lying down and both upper limbs flexed and holding the pillow in the folding knife position. Generally, a 12-mm incision in the 7th or 8th intercostal space in the mid-axillary line is taken as the access hole, and a 30-mm incision in the 4th or 5th intercostal space in the anterior axillary line is taken as the operating hole.

Observed indicators

Gender, age, body mass index (BMI), smoking history, underlying disease, tumor size, surgical procedure, resection site, pathological type, T-stage, N-stage and TNM-stage. Perioperative indicators included operative time, intraoperative bleeding, total postoperative chest drainage, postoperative chest drainage time, postoperative hospital stay, transfer chest surgery, hospitalization cost, postoperative complications, complications associated with lymph node dissection, number of lymph nodes cleared stations, number of lymph nodes cleared, lymph node pathology staging upgrade.

Statistical analysis

A 1:1 PSM analysis was performed using SPSS 26.0 software(SPSS Inc., Chicago, IL, USA), and the caliper value was set at 0.02. Matching factors included gender, age, BMI, smoking history, underlying disease, tumor size, surgical procedure, energy devices, tumor site, pathological type, T-stage, N-stage, and TNM-stage. Continuous variables were expressed as mean ± standard deviation ( ±s), and two independent samples t-test was used for comparison between groups. Categorical variables were expressed as frequencies and percentages (%), and group comparisons were made using the chi-square test or Fisher test. Herein, P<0.05 was considered to be a statistically significant difference.

Propensity score matching

The differences in age and tumor site between the two groups of patients before PSM were statistically significant. Factors of gender, age, BMI, smoking history, underlying disease, tumor size, surgical procedure, energy devices, tumor site, pathological type and TNM stage were included in PSM, and 100 patients in the RATS group and 100 patients in the VATS group were successfully matched after 1:1 matching, and none of the differences in confounding variables were statistically significant; as listed in Table 1.

Table 1 Comparison of baseline information before and after propensity score matching between the two groups [cases (%)/ ±s]

Characteristic	Before PSM			After PSM
Characteristic	RATS group (n=122)	VATS group (n=140)	P	RATS group (n=100)	VATS group (n=100)	P
Gender			0.666			0.671
Male	56 (45.9)	68 (48.6)		46 (46.0)	49 (49.0)
Female	66 (54.1)	72 (51.4)		54 (54.0)	51 (51.0)
Age (years)	59.95±4.29	61.43±4.65	0.008	60.40±4.15	61.06±4.79	0.299
BMI（kg/m²）	23.24±2.35	23.01±2.29	0.438	23.23±2.34	22.90±2.27	0.312
Smoking history			0.832			0.533
Yes	36 (29.5)	43 (30.7)		27 (27.0)	31 (31.0)
No	86 (70.5)	97 (69.3)		73 (73.0)	69 (69.0)
Basic Diseases			0.655			0.774
Yes	53 (43.4)	57 (40.7)		43 (43.0)	41 (41.0)
No	69 (56.6)	83 (59.3)		57 (57.0)	59 (59.0)
Tumor size (mm)	29.52±4.85	29.99±4.88	0.445	29.50±5.08	29.76±4.70	0.708
Surgical procedure			0.295			0.377
Sublobar resection	42 (34.4)	57 (40.7)		33 (33.0)	39 (39.0)
Lobectomy	80 (65.6)	83 (59.3)		67 (67.0)	61 (61.0)
Energy Devices			-			-
Electric hook	106	140		100	100
Maryland Pliers	14	0		0	0
Tumor site			0.039			0.143
LUL	21 (17.2)	35 (25.0)		17 (17.0)	23 (23.0)
LLL	15 (12.3)	24 (17.2)		12 (12.0)	18 (18.0)
RUL	43 (35.2)	31 (22.1)		37 (37.0)	23 (23.0)
RML	27 (22.1)	22 (15.7)		20 (20.0)	16 (16.0)
RLL	16 (13.2)	28 (20.0)		14 (14.0)	20 (20.0)
Pathological type			0.776			0.848
Adenocarcinoma	72 (59.0)	77 (55.0)		60 (60.0)	63 (63.0)
Squamous carcinoma	46 (37.7)	57 (40.7)		37 (37.0)	35 (35.0)
Other	4 (3.3)	6 (4.3)		3 (3.0)	2 (2.0)
TNM Stage			0.292			0.713
Ⅰ	102 (83.6)	108 (77.1)		84 (84.0)	88 (88.0)
Ⅱ	10 (8.2)	12 (8.6)		9 (9.0)	7 (7.0)
Ⅲ	10 (8.2)	20 (14.3)		7 (7.0)	5 (5.0)

Abbreviation: BMI Body mass index, LUL Left upper lobe, LLL left lower lobe, RUL right upper lobe, RML right middle lobe, RLL right lower lobe

Surgical results

The surgical data of the two groups of patients after PSM are specified in Table 2. In terms of intraoperative bleeding [(63.10±13.61) ml vs. (91.40±24.41) ml], postoperative drainage time [(4.05±0.91) days vs. (4.92±1.16) days], postoperative hospital stay [(5.43±0.95) days vs. (6.72±1.39) days], number of lymph node dissection stations [(5.67±1.22) stations vs. (1.22) stations vs. (4.49±1.17) stations], number of lymph nodes cleared [(14.75±2.56) vs. (11.22±2.03)], and lymph node pathology staging upgrade (cN0 to pN1), the RATS group was more advantageous, and the difference was statistically significant (P<0.05). In terms of total postoperative chest drainage [(700.00±151.42) ml vs. (828.00±168.97) ml] and hospital costs [(57,755.86±5483.90) yuan vs. (78,262.03±4323.68) yuan], the VATS group was more advantageous with statistically significant differences (P<0.05). There was no statistically significant difference between the two groups in terms of operative time [(132.40±14.10) min vs. (136.90±19.37) min], postoperative complications, postoperative complications related to lymph node dissection, and transfer to open chest (P>0.05).

The RATS group cleared more lymph nodes at stations 10 and 11, and cleared/sampled more frequently at stations 7, 8, 10, 11, and 12 (Table 3).

Table 2 Surgical data of patients [cases (%)/ ±s]

Characteristic	RATS group (n=100)	VATS group (n=100)	P
Operative time (min)	132.40±14.10	136.90±19.37	0.062
Intraoperative bleeding (ml)	63.10±13.61	91.40±24.41	<0.001
Total postoperative chest drainage (ml)	828.00±168.97	700.00±151.42	0.003
Duration of postoperative drainage (d)	4.05±0.91	4.92±1.16	0.008
Postoperative hospital stay (d)	5.43±0.95	6.72±1.39	<0.001
Transfer to open chest	1 (1.0)	3 (3.0)	0.312
Total hospitalization expenses (yuan)	78262.03±4323.68	57755.86±5483.90	<0.001
Postoperative complications			0.066
Yes	13 (13.0)	23 (23.0)
No	87 (87.0)	76 (76.0)
Complications related to lymph node dissection	3 (3.0)	5 (5.0)	0.470
Chylothorax	2 (2.0)	1 (1.0)	0.561
Bronchopleural fistula	1 (1.0)	2 (2.0)	0.561
Phrenic nerve palsy	0	2 (2.0)	0.155
Number of lymph node dissection stations	5.67±1.22	4.49±1.17	<0.001
N2	2.95±1.00	2.67±0.91	0.039
N1	2.72±0.83	1.82±0.76	<0.001
Number of lymph nodes dissected	14.75±2.56	11.22±2.03	<0.001
Lymph node pathology staging upgrade	12 (12.0)	9 (9.0)	0.489
cN0 to pN1	7 (7.0)	3 (3.0)	0.036
cN0 to pN2	4 (4.0)	5 (5.0)	0.733
N1 to pN2	1 (1.0)	1 (1.0)	1.000

Table 3 Comparison of lymph node dissection [cases (%)/ ±s]

Number of lymph node stations	RATS group (n=100)	VATS group (n=100)	P
#2 Station
Number of lymph nodes	2.61±0.96	2.49±0.98	0.383
Cleaning/sampling	30 (30.0)	27 (27.0)	0.638
#3 Station
Number of lymph nodes	2.10±0.94	1.93±0.91	0.195
Cleaning/sampling	10 (10.0)	8 (8.0)	0.621
#4 Station
Number of lymph nodes	2.63±0.93	2.49±0.97	0.298
Cleaning/sampling	36 (36.0)	34 (34.0)	0.767
#5 Station
Number of lymph nodes	1.86±0.84	1.74±0.79	0.299
Cleaning/sampling	29 (29.0)	28 (28.0)	0.876
#6 Station
Number of lymph nodes	1.94±0.79	1.71±0.72	0.032
Cleaning/sampling	13 (13.0)	10 (10.0)	0.506
#7 Station
Number of lymph nodes	2.59±0.84	2.49±0.87	0.410
Cleaning/sampling	90 (90.0)	80 (80.0)	0.028
#8 Station
Number of lymph nodes	1.67±0.82	1.58±0.81	0.434
Cleaning/sampling	62 (62.0)	12 (12.0)	＜0.001
#9 Station
Number of lymph nodes	1.48±0.66	1.37±0.70	0.251
Cleaning/sampling	44 (44.0)	48 (48.0)	0.570
#10 Station
Number of lymph nodes	2.99±1.05	2.68±0.91	0.027
Cleaning/sampling	95 (95.0)	87 (87.0)	0.048
#11 Station
Number of lymph nodes	2.36±0.80	1.92±0.92	＜0.001
Cleaning/sampling	97 (97.0)	70 (70.0)	＜0.001
#12 Station
Number of lymph nodes	1.83±0.82	1.80±0.80	0.792
Cleaning/sampling	66 (66.0)	12 (12.0)	＜0.001

The installed base of da Vinci robots worldwide has grown rapidly in recent years. The overall efficacy of RATS versus VATS in the treatment of lung cancer is still being explored, and few studies have been conducted to analyze in detail the outcomes associated with lymph node dissection for both procedures. Therefore, in this study, we compared the short-term efficacy and safety of RATS with VATS for lung cancer and focused on the differences in outcomes related to lymph node dissection.

According to a previous study [7], the procedure time for RATS is usually longer, which may be attributed to the fact that RATS has additional loading time and the effect of the learning curve. In this study, the operative time was shorter in the RATS group than in the VATS group, but the difference between the two groups was not statistically significant. As the operator gains experience and the robotic team becomes more skilled at working together, the operating time for RATS can be significantly reduced. In this study, the postoperative drainage time was shorter in the RATS group than in the VATS group, while the total postoperative chest drainage was more in the RATS group than in the VATS group, this is similar to the results of Li et al [8]. Few studies have analyzed the differences in chest drainage between RATS and VATS for pulmonary procedures. In our experience, RATS allows for the removal of more lymph nodes, which may result in damage to the bronchial arteries, veins and lymphatic vessels connected to the lymph nodes during resection and therefore increased postoperative chest drainage. Differences in the energy devices used in RATS versus VATS when performing lymph node dissection may also have an impact on postoperative drainage. Another possible explanation is increased thoracic drainage due to surgical trauma, with the RATS group routinely having four incisions, while the VATS group required only one or two incisions. Although the total postoperative chest drainage was greater in the RATS group, the postoperative drainage time was shorter in the RATS group. This may be due to the lower incidence of postoperative pulmonary air leak in the RATS group and less intraoperative trauma to the patient’s finishing. In this study, intraoperative bleeding was significantly lower in the RATS group than in the VATS group, and the postoperative hospital stay was shorter in the RATS group than in the VATS group. We attribute this to the fact that RATS provides a three-dimensional magnified view during surgery, greater dexterity and eliminates hand tremors, allowing accurate exposure of the complex anatomy surrounding the resection target. This helps the surgeon to perform precise maneuvers during the procedure and to better control bleeding from small vessels. Also, because RATS is more minimally invasive, it produces less postoperative pain and faster recovery. Patients recover faster after surgery and also shorten the postoperative hospital stay to some extent, which is in line with the concept of accelerated rehabilitation surgery [9]. In terms of total postoperative complications, there was no significant difference between the two groups; the rate of postoperative complications related to lymph node dissection was lower in the RATS group than in the VATS group, but the difference between the two groups was not statistically significant.

Lymph node dissection is critical in minimally invasive surgery for NSCLC. Several previous studies have evaluated RATS for lymph node dissection and have produced conflicting results. Nelson et al [10] showed that RATS can clear more number of lymph nodes and lymph node groups compared to VATS. This finding was also validated by several retrospective studies [11,12]. However, a multicenter retrospective study based on 64,676 cases [13] found that the mean number of lymph nodes cleared was higher in VATS than in RATS (11.3 vs. 10.9, P<0.01), but it did not further analyze the source of the difference. According to Kneuertz et al [14], the number of lymph nodes cleared and the number of lymph node groups were comparable between the two surgical approaches. They further compared the frequency of clearance between RATS and VATS at different lymph node stations and found that RATS was superior to VATS for paratracheal (group 4), inferior pulmonary ligament/paraesophageal (groups 8/9) and hilar (group 10) lymph node clearance, while the opposite was true for interlobular lymph node clearance [14]. Our study showed that the RATS group had more advantages in terms of the number of lymph nodes cleared, the number of lymph nodes cleared stations, the number of N2 lymph nodes cleared stations, and the number of N1 lymph nodes cleared stations. In addition, the RATS group cleared more lymph nodes at stations 10 and 11, and cleared/sampled more frequently at stations 7, 8, 10, 11, and 12.

Few studies have reported data on lymph node pathological staging escalation. lee et al [15], after analyzing data from 211 NSCLC surgeries, concluded that there was no statistically significant difference between RATS and VATS in terms of postoperative lymph node pathological staging escalation. Another study [14] showed that the proportion of overall lymph node pathological staging escalation was higher in RATS than in VATS (16.2% vs. 12.3%), however, multifactorial logistic regression analysis suggested that the difference was not statistically significant. The results of this study showed that the RATS group was more advantageous in the ascending of cN0 to pN1, and there was no significant difference between the two groups in the ascending of cN0 to pN2 and cN1 to pN2. We further analyzed that the upgraded pathologic staging of N1 lymph nodes in the RATS group may be due to the fact that RATS provides a three-dimensional high-resolution view, better maneuverability, and better flexibility, allowing the thoracic surgeon to better dissect the vascular and peribronchial lymph nodes, allowing for a higher number of N1 lymph nodes to be cleared, resulting in more accurate pathologic staging of the lymph nodes, which also facilitates postoperative treatment and follow-up.

Most of the lung cancer procedures in our center were done with electric hooks, and later we introduced Maryland forceps. We also have an appreciation of the differences between the two instruments in lymph node dissection. In the past, we found that some of the lymph nodes were difficult to be exposed and the lymph nodes were prone to fragmentation and bleeding due to the technique of electric hook. At the same time, for areas with greater sand and dust and a higher incidence of pulmonary infections such as tuberculosis, intraoperative lymph node calcification and enlargement are often seen, and the incidence of portal nail lymph nodes is also higher, placing higher demands on intraoperative lymph node dissection. Based on our experience, we found that Maryland forceps were more advantageous in lymph node dissection, especially in the freeing of group 4 and 7 lymph nodes, and the incidence of lymph node fragmentation and bleeding was significantly lower compared to electric hook. The Maryland clamp allows for precise spot coagulation to minimize bleeding while maintaining the integrity of the lymph nodes. Previously, for the management of hilar nail lymph nodes, the larger energy spread of the electric hook often leads to bleeding from pulmonary artery injury, whereas Maryland tip spot coagulation has significant advantages in hilar nail lymph node dissection.

There are some limitations and shortcomings of this study: (1) the results may be biased due to the single-center data source of the included studies; (2) no more specific analysis of the surgical data of the electric hook versus Maryland clamp in the RATS group; (3) despite the application of PSM to control for confounding factors between groups, potential selection bias was not completely eliminated; (4) this study lacks postoperative recurrence and long-term survival analysis, and it is proposed to further refine the data through follow-up.

In summary, an analysis of the short-term efficacy of RATS and VATS in lung cancer surgery showed that the overall short-term efficacy of RATS was better than VATS, especially in lymph node dissection.

RATS Robot assisted thoracoscopic surgery

VATS Video assisted thoracic surgery

PSM Propensity score matching

NSCLC non-small cell lung cancer

CT Computed tomography

BMI Body mass index

LUL: left upper lobe

LLL: left lower lobe

RUL: right upper lobe

RML: right middle lobe

RLL: right lower lobe.

Acknowledgements

Not applicable.

Authors’ contributions

Ziqiang Hong, Yunjiu Gou and Yannan Sheng: conception and design and administrative support; Xiangdou Baiand Baiqiang Cui: provision of study materials or patients; Tao Cheng, and Dacheng Jin: collection and assembly of the data; Kai Wang and Xusheng Wu: data analysis and interpretation; manuscript writing: all authors. The authors read and approved the final manuscript.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

This research was supported by Gansu Province Key R&D Project (22YF7FA095) and Gansu Provincial People’s Hospital Intramural Fund (22GSSYD-29).

Ethics approval and consent to participate

This study has been reviewed by the Ethics Committee of Gansu Provincial People’s Hospital, approval number: 2022-394. All patients signed the informed consent form for surgery before surgery.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Author details

¹The First Clinical Medical College of Gansu University of Chinese Medicine, Gansu Provincial Hospital, Lanzhou, China.

²Department of thoracic surgery, Gansu Provincial Hospital, Lanzhou, China.

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No competing interests reported.

Da Vinci robot versus thoracoscopic surgery for lymph node dissection in radical lung cancer: a propensity score matching study

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Abstract

Figures

Introduction

Materials And Methods

Results

Discussion

Conclusion

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1