ABSTRACT
Background
We compared short-term clinical outcomes between robotic-assisted minimally invasive esophagectomy (RAMIE) and video-assisted thoracic esophagectomy (VATS-E) using propensity score-matched analysis.
Methods
We enrolled 114 patients with esophageal cancer who underwent esophagectomy at our institution from January 2013 to January 2022. Propensity score matching was performed to minimize selection bias between the RAMIE and VATS-E groups.
Results
After propensity score matching, 72 patients (RAMIE group, n = 36; VATS-E group, n = 36) were selected for analysis. No significant differences in clinical variables were observed between the two groups. The RAMIE group had a significantly longer thoracic operation time (313 ± 40 vs. 295 ± 35 min, P = 0.048), a higher number of right recurrent laryngeal nerve lymph nodes (4.2 ± 2.7 vs. 2.9 ± 1.9, P = 0.039), and a shorter postoperative hospital stay (23.2 ± 12.8 vs. 30.4 ± 18.6 days, P = 0.018) than the VATS-E group. The RAMIE group tended to have a lower rate of anastomotic leakage (13.9% vs. 30.6%) than the VATS-E group, although the difference was not statistically significant (P = 0.089). No significant differences were found in recurrent laryngeal nerve paralysis (11.1% vs. 13.9%, P = 0.722) or pneumonia (13.9% vs. 13.9%, P = 1.000) between the RAMIE group and the VATS-E group.
Conclusion
Although RAMIE for esophageal cancer requires a longer thoracic surgery time, it might be a feasible and safe alternative to VATS-E for treating esophageal cancer. Further analysis is needed to clarify the advantages of RAMIE over VATS-E, especially in terms of long-term surgical outcomes.
Keywords: esophageal cancer, robotic esophagectomy
Esophageal cancer has a poor prognosis and is the sixth leading cause of cancer-related death worldwide.1, 2 The treatment strategy for esophageal cancer involves surgery, and both thoracic and abdominal operations are required. Esophagectomy is one of the most invasive gastrointestinal surgeries, with higher complication and mortality rates than surgery for other diseases.3, 4 Very important complications in esophagectomy include recurrent laryngeal nerve palsy, pneumonia, and anastomotic leakage.5, 6 Although lymph node dissection around the recurrent laryngeal nerve is important in esophageal cancer surgery, it is associated with unique complications such as recurrent laryngeal nerve palsy. Several studies have shown that complications worsen the prognosis of esophageal cancer,7, 8 and various attempts are being made to reduce complications. The performance of video-assisted thoracoscopic esophagectomy (VATS-E) has been increasing in recent years as a minimally invasive procedure to reduce complications, and the use of robot-assisted minimally invasive esophagectomy (RAMIE) is also increasing to achieve more accurate surgery.9,10,11,12 Robotic surgery has been shown to be useful in a variety of fields,13,14,15 and various reports have described its use in the treatment of esophageal cancer. However, the short-term results of RAMIE still remain insufficient.
This study examined the short-term results of VATS-E and RAMIE performed at our institution using propensity score matching (PSM).
SUBJECTS AND METHODS
Patients
This retrospective study involved 130 patients with esophageal cancer who underwent RAMIE or VATS-E at our institution from January 2013 to January 2022. Patients who underwent total pharyngo-laryngo-esophagectomy, patients who underwent two-stage esophagectomy, and patients with other cancer were excluded. Finally, 114 patients were included in this study (Fig. 1). We began performing RAMIE in February 2020; since then, we have treated all patients with esophageal cancer by RAMIE. In this study, there were three surgeons for VATS-E, one of them also being a surgeon for RAMIE. The clinicopathological findings were determined according to the Japanese Classification of Esophageal Cancer (11th edition).16, 17 PSM was performed to minimize selection bias between the two groups. The following variables were selected and matched because they were determined to have a significant survival impact: age, sex (male, female), tumor location (upper, middle, lower), neoadjuvant chemotherapy (present, absent), lymphadenectomy (two-field, three-field), clinical depth of tumor invasion (T1, T2, T3, T4), clinical lymph node metastasis (N0, N1, N2, N3), histologic type (squamous cell carcinoma, adenocarcinoma), and clinical stage (I, II, III).
Fig. 1.
CONSORT diagram.
Treatment strategy
Our treatment strategy for esophageal cancer was as follows: patients with T1 tumors who did not have lymph node metastasis underwent surgery without preoperative treatment; patients with ≥ T2, non-T4b, or node-positive tumors (Stage ≥ 2) received neoadjuvant chemotherapy followed by esophagectomy; and patients with T4 tumors suspected to have invaded other organs (T4b) received chemoradiation therapy. The standard surgical approach was subtotal esophagectomy and reconstruction using a gastric tube. Either two- or three-field lymphadenectomy was performed. Cervical lymph node dissection was not performed in patients with lower thoracic or abdominal esophageal cancer without cervical or upper mediastinal lymph node metastasis.
Surgical procedures
We performed thoracoscopic subtotal esophagectomy with mediastinal lymph node dissection in the prone position under right pneumothorax in all patients in both the VATS-E and RAMIE groups. Lymphadenectomy was performed for the mediastinal lymph nodes, including the right and left recurrent laryngeal nerve nodes, tracheal bifurcation nodes, thoracic paraesophageal nodes, and diaphragmatic nodes. After completion of the thoracic procedure, the patients were repositioned in the supine position, and the cervical and abdominal procedures were started simultaneously. The abdominal procedure was basically performed by hand-assisted laparoscopic surgery except in patients with massive metastasis of abdominal lymph nodes or a history of major abdominal surgery such as laparotomy. In cases of hand-assisted laparoscopic surgery, an 8-cm small laparotomy was performed in the upper abdomen after completion of abdominal lymph node dissection, and the gastric tube was created under direct vision in all cases. From July 2018, we standardized the surgical anastomotic technique using indocyanine green fluorescence imaging as previously reported.18 The gastric tube was pulled up to the neck through the posterior mediastinal route, and esophagogastric anastomosis was performed on the left side of the neck.
Definitions of perioperative complications
Anastomotic leakage was defined as saliva leakage from the cervical wound, contrast leakage outside the gastrointestinal tract on gastrointestinal series, and abnormal air or fluid accumulation around the anastomosis on computed tomography. Pneumonia was defined as the appearance of consolidation on chest X-ray or computed tomography and the detection of bacteria on sputum culture. Recurrent laryngeal nerve paralysis was diagnosed in patients who complained of hoarseness and dysphagia and when insufficient movement of the vocal cords was observed by laryngofiberscopy.
Statistical analysis
Continuous variables were compared using the Mann–Whitney U test. Categorical variables were compared using Fisher’s exact test or the χ2 test. PSM was performed with a logistic regression model and 1:1 nearest neighbor matching (caliper width = 0.2). SPSS for Windows Version 24 (IBM Corp., Armonk, NY) was used for all statistical analyses.
RESULTS
The RAMIE group comprised 46 patients, and the VATS-E group comprised 68 patients (Table 1). The patients’ mean age was 65.4 ± 8.0 years, and the study population comprised 99 men and 15 women. Neoadjuvant chemotherapy was performed in 41 patients, and the histology was squamous cell carcinoma in almost all patients. The clinical disease stage was I, II, III, and IV in 39, 36, 38, and 1 patient, respectively.
Table 1. Patient characteristics.
| Before PSM | After PSM | ||||||
| All | RAMIE | VATS-E | RAMIE | VATS-E | |||
| (n = 114) | (n = 46) | (n = 68) | P value | (n = 36) | (n = 36) | P value | |
| Age (years) | 65.4 ± 8.0 | 65.8 ± 8.2 | 65.0 ± 7.8 | 0.575 | 65.8 ± 8.1 | 65.1 ± 8.0 | 0.591 |
| Sex | 0.552 | 0.527 | |||||
| Male | 99 (86.8) | 41 (89.1) | 58 (85.3) | 31 (86.1) | 29 (80.6) | ||
| Female | 15 (13.2) | 5 (10.9) | 10 (14.7) | 5 (13.9) | 7 (19.4) | ||
| ASA PS | 0.059 | 0.149 | |||||
| 1 | 10 (8.8) | 1 (2.2) | 9 (13.2) | 1 (2.8) | 5 (13.9) | ||
| 2 | 82 (71.9) | 33 (71.7) | 49 (72.1) | 26 (72.2) | 26 (72.2) | ||
| 3 | 22 (19.3) | 12 (26.1) | 10 (14.7) | 9 (25.0) | 5 (13.9) | ||
| BMI, kg/m2 | 21.5 ± 3.3 | 22.2 ± 3.5 | 21.1 ± 3.0 | 0.12 | 21.9 ± 3.1 | 21.0 ± 3.4 | 0.203 |
| Tumor location | 0.5 | 0.929 | |||||
| Upper | 26 (22.8) | 5 (10.9) | 21 (30.9) | 4 (11.1) | 5 (13.9) | ||
| Middle | 59 (51.8) | 22 (47.8) | 37 (54.4) | 18 (50.0) | 18 (50.0) | ||
| Lower | 29 (25.4) | 19 (41.3) | 10 (14.7) | 14 (38.9) | 13 (36.1) | ||
| Neoadjuvant therapy | 0.539 | 1.000 | |||||
| None | 73 (64.0) | 31 (67.4) | 42 (61.8) | 23 (63.9) | 23 (63.9) | ||
| Chemotherapy | 41 (36.0) | 15 (32.6) | 26 (38.2) | 13 (36.1) | 13 (36.1) | ||
| Histology | 0.085 | 1.000 | |||||
| SCC | 104 (91.2) | 39 (84.8) | 65 (95.6) | 33 (91.2) | 33 (91.2) | ||
| Adenocarcinoma | 8 (7.0) | 5 (10.9) | 3 (4.4) | 3 (8.8) | 3 (8.8) | ||
| Other | 2 (1.8) | 2 (4.3) | 0 (0.0) | 0 (0.0) | 0 (0.0) | ||
| cT | 0.555 | 0.667 | |||||
| T1 | 43 (37.7) | 14 (30.4) | 29 (42.6) | 11 (30.6) | 13 (36.1) | ||
| T2 | 27 (23.7) | 11 (23.9) | 16 (23.5) | 8 (22.2) | 11 (30.6) | ||
| T3 | 42 (36.8) | 20 (43.5) | 22 (32.4) | 16 (44.4) | 11 (30.6) | ||
| T4 | 2 (1.8) | 1 (2.2) | 1 (1.5) | 1 (2.8) | 1 (2.8) | ||
| cN | 0.22 | 0.767 | |||||
| N0 | 64 (56.1) | 21 (45.7) | 43 (63.2) | 17 (47.2) | 18 (50.0) | ||
| N1 | 19 (16.7) | 10 (21.7) | 9 (13.2) | 8 (22.2) | 7 (19.4) | ||
| N2 | 26 (22.8) | 14 (30.4) | 12 (17.6) | 11 (30.6) | 10 (27.8) | ||
| N3 | 5 (4.4) | 1 (2.2) | 4 (5.9) | 0 (0.0) | 1 (2.8) | ||
| cStage | 0.165 | 0.893 | |||||
| I | 39 (34.2) | 14 (30.4) | 25 (36.8) | 11 (30.6) | 12 (33.3) | ||
| II | 36 (31.6) | 11 (23.9) | 25 (36.8) | 8 (22.2) | 9 (25.0) | ||
| III | 38 (33.3) | 21 (45.7) | 17 (25.0) | 17 (47.2) | 15 (41.7) | ||
| IV | 1 (0.9) | 0 (0.0) | 1 (1.5) | 0 (0.0) | 0 (0.0) | ||
Data are presented as mean ± standard deviation or number (percentage) of patients. ASA PS, American Society of Anesthesiologists physical status; BMI, body mass index; cN, clinical lymph node metastasis; cStage, clinical stage; cT, clinical depth of tumor invasion; PSM, propensity score matching; RAMIE, robot-assisted minimally invasive esophagectomy; SCC, squamous cell carcinoma; VATS-E, video-assisted thoracoscopic esophagectomy.
The patients’ clinical variables are shown in Table 1. No significant differences were observed in age, sex, American Society of Anesthesiologists physical status, body mass index, tumor location, neoadjuvant chemotherapy, histology, clinical depth of tumor invasion, clinical lymph node metastasis, or clinical stage between the RAMIE group and the VATS-E group. The patients’ surgical variables are shown in Table 2. The RAMIE group had a significantly longer thoracic operation time, lower proportion of abdominal open procedures, higher number of right recurrent laryngeal nerve lymph nodes (lymph node station 106recR), and shorter postoperative hospital stay than the VATS-E group. The postoperative complications are shown in Table 3. No 30-day mortality was observed in either group, but 90-day mortality occurred in one patient in the VATS-E group. The RAMIE group had a significantly lower rate of anastomotic leakage than the VATS-E group. No significant differences in recurrent laryngeal nerve paralysis or pneumonia were observed between the RAMIE group and the VATS-E group.
Table 2. Perioperative outcomes of patients with esophageal cancer after thoracoscopic esophagectomy.
| Before PSM | After PSM | ||||||
| All | RAMIE | VATS-E | RAMIE | VATS-E | |||
| (n = 114) | (n = 46) | (n = 68) | P value | (n = 36) | (n = 36) | P value | |
| Total operation time, min | 617 ± 62 | 626 ± 58 | 610 ± 64 | 0.097 | 618 ± 57 | 600 ± 54 | 0.136 |
| Thoracic operation time, min | 306 ± 44 | 317 ± 40 | 299 ± 45 | 0.016 | 313 ± 40 | 295 ± 35 | 0.048 |
| Bleeding, mL | 114 ± 105 | 113 ± 86 | 115 ± 115 | 0.273 | 113 ± 79 | 111 ± 103 | 0.382 |
| Lymphadenectomy | 0.059 | 0.800 | |||||
| Two-field | 38 (33.3) | 20 (43.5) | 18 (26.5) | 12 (33.3) | 11 (30.6) | ||
| Three-field | 76 (66.7) | 26 (56.5) | 50 (73.5) | 24 (66.7) | 25 (69.4) | ||
| Abdominal procedure | < 0.001 | < 0.001 | |||||
| Open | 23 (20.2) | 1 (2.2) | 22 (32.4) | 1 (2.8) | 12 (33.3) | ||
| Laparoscopic | 91 (79.8) | 45 (97.8) | 46 (67.6) | 35 (97.2) | 24 (66.7) | ||
| Number of harvested lymph nodes | |||||||
| 106recR | 3.6 ± 2.5 | 4.2 ± 2.5 | 3.3 ± 2.4 | 0.037 | 4.2 ± 2.7 | 2.9 ± 1.9 | 0.039 |
| 106recL | 2.9 ± 2.6 | 3.0 ± 2.3 | 2.8 ± 2.8 | 0.491 | 3.3 ± 2.4 | 2.4 ± 2.1 | 0.122 |
| Radicality of surgery | 0.438 | 0.314 | |||||
| R0 | 108 (94.7) | 45 (97.8) | 64 (94.1) | 36 (100) | 35 (97.2) | ||
| R1/2 | 5 (5.3) | 1 (2.2) | 4 (5.9) | 0 (0.0) | 1 (2.8) | ||
| Postoperative hospital stay, days | 31.1 ± 28.3 | 22.4 ± 11.7 | 37.2 ± 34.3 | < 0.001 | 23.2 ± 12.8 | 30.4 ± 18.6 | 0.018 |
Data are presented as mean ± standard deviation or number (percentage) of patients. PSM, propensity score matching; RAMIE, robot-assisted minimally invasive esophagectomy; VATS-E, video-assisted thoracoscopic esophagectomy; 106recL, left recurrent laryngeal nerve lymph node station; 106recR, right recurrent laryngeal nerve lymph node station.
Table 3. Complications in patients with esophageal cancer after thoracoscopic esophagectomy.
| Before PSM | After PSM | ||||||
| All | RAMIE | VATS-E | RAMIE | VATS-E | |||
| (n = 114) | (n = 46) | (n = 68) | P value | (n = 36) | (n = 36) | P value | |
| Recurrent laryngeal nerve paralysis | 0.393 | 0.722 | |||||
| Present | 19 (16.7) | 6 (13.0) | 13 (19.1) | 4 (11.1) | 5 (13.9) | ||
| Absent | 95 (83.3) | 40 (87.0) | 55 (80.9) | 32 (88.9) | 31 (86.1) | ||
| Pneumonia | 0.154 | 1.000 | |||||
| Present | 25 (21.9) | 7 (15.2) | 18 (26.5) | 5 (13.9) | 5 (13.9) | ||
| Absent | 89 (78.1) | 39 (84.8) | 50 (73.5) | 31 (86.1) | 31 (86.1) | ||
| Anastomotic leakage | 0.005 | 0.089 | |||||
| Present | 28 (24.6) | 5 (10.9) | 23 (33.8) | 5 (13.9) | 11 (30.6) | ||
| Absent | 86 (75.4) | 41 (89.1) | 45 (66.2) | 31 (86.1) | 25 (69.4) | ||
| 30-day mortality | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1.000 | 0 (0.0) | 0 (0.0) | 1.000 |
| 90-day mortality | 1 (0.9) | 0 (0.0) | 1 (1.5) | 0.409 | 0 (0.0) | 0 (0.0) | 1.000 |
Data are presented as number (percentage) of patients. PSM, propensity score matching; RAMIE, robot-assisted minimally invasive esophagectomy; VATS-E, video-assisted thoracoscopic esophagectomy.
After PSM, 72 patients (RAMIE group, n = 36; VATS group, n = 36) were selected for analysis. No significant differences in the clinical variables were observed between the two groups (Table 1). The RAMIE group had a significantly longer thoracic operation time, higher number of 106recR lymph nodes, and shorter postoperative hospital stay than the VATS-E group (Table 2). The RAMIE group tended to have a lower rate of anastomotic leakage than the VATS-E group, although the difference was not statistically significant (P = 0.089) (Table 3). No significant differences in recurrent laryngeal nerve paralysis or pneumonia were observed between the RAMIE group and the VATS-E group.
DISCUSSION
This study examined the short-term results of RAMIE and VATS-E and showed that the RAMIE group had a significantly longer thoracic operation time, higher number of 106recR lymph nodes, and shorter postoperative hospital stay than the VATS-E group. In terms of postoperative complications, the RAMIE group tended to have a lower rate of pneumonia and recurrent laryngeal nerve palsy than the VATS-E group; however, there was no significant difference between the two groups after PSM. The RAMIE group had a significantly lower rate of anastomotic leakage than the VATS group before PSM, and the RAMIE group tended to have a lower rate of anastomotic leakage than the VATS-E group after PSM.
Recurrent laryngeal nerve palsy is an important complication in esophagectomy. It is caused by intraoperative damage to the recurrent laryngeal nerve secondary to heat injury or nerve traction. RAMIE has the potential to reduce the incidence of recurrent laryngeal nerve palsy through precise surgical techniques. In the present study, the frequency of recurrent laryngeal nerve palsy was lower in the RAMIE than VATS-E group, although there was no statistically significant reduction in recurrent laryngeal nerve palsy before and after PSM. The importance of lymph node dissection around the bilateral recurrent laryngeal nerve in esophagectomy has also been noted, and the present study examined the number of right and left recurrent laryngeal nerve lymph nodes dissected. The number of lymph nodes dissected around the right recurrent laryngeal nerve was significantly higher in the RAMIE group than in the VATS-E group both before and after PSM. The number of nodes dissected around the left recurrent laryngeal nerve tended to be higher in the RAMIE group than in the VATS-E group, although the difference was not significant. These results suggest that RAMIE may be useful in increasing the number of lymph nodes dissected while preserving the function of the recurrent laryngeal nerve through precise surgical techniques. A trend toward an increased frequency of pneumonia has been noted in patients with recurrent laryngeal nerve palsy; in the present study, however, the frequency of pneumonia in the RAMIE group was lower than that in the VATS-E group (although this difference was not statistically significant).
A disadvantage of RAMIE is the long operation time. Our result of a long thoracic operation time in the RAMIE group is the same as in a previous report by Tsunoda et al.19 They performed PSM of 165 patients with esophageal cancer who underwent RAMIE or minimally invasive surgery and found significantly longer thoracic operative times in the RAMIE group than in the minimally invasive surgery group both before and after PSM.19 Morimoto et al.20 retrospectively analyzed 87 patients who underwent minimally invasive esophagectomy and found that the median operative time of the thoracic approach was significantly longer in the RAMIE group than in the minimally invasive surgery group. Factors that may have contributed to this longer operation time may have been the roll-in/roll-out and docking process unique to robotic surgery as well as the learning curve to operate the robot itself.21, 22 By contrast, some high-volume centers have reported that RAMIE has rather shorter operative times.12 Future proficiency with the RAMIE technique may lead to shorter operation times and further reduce complications.
In the present study, we found a significantly lower incidence of anastomotic leakage in the RAMIE group than in the VATS-E group. This result may not be due to the influence of robotic surgery but rather to standardization of the anastomotic technique. As we previously reported, the incidence of anastomotic leakage was historically high in our institution because the anastomotic technique was not standardized and indocyanine green was not used.18 Therefore, we standardized the anastomotic technique in July 2018, and the frequency of anastomotic leakage improved thereafter. Since RAMIE was started in 2020, the low frequency of anastomotic leakage was due to the standardization of the anastomotic technique, and the significant reduction in the postoperative hospital stay in the RAMIE group may have been due to the lower incidence of anastomotic leakage.
This study had two main limitations. First, this was a retrospective study from a single institution and involved a small number of patients. PSM was used to balance the two groups, but the results must be interpreted carefully because unknown confounding factors might have still affected the results. Second, because of the small number of patients with esophageal cancer at our institution, relatively old cases from 2013 were included in this study.
In conclusion, although RAMIE for esophageal cancer requires a longer thoracic surgery time, it might be a feasible and safe alternative to VATS-E for treating esophageal cancer. Further analysis is needed to clarify the advantages of RAMIE over VATS-E, especially in terms of long-term surgical outcomes.
Acknowledgments
Acknowledgment: We thank Angela Morben, DVM, ELS, from Edanz (https://jp.edanz.com/ac), for editing a draft of this manuscript.
Footnotes
The authors declare no conflict of interest.
REFERENCES
- 1.Herskovic A,Russell W,Liptay M,Fidler MJ,Al-Sarraf M. Esophageal carcinoma advances in treatment results for locally advanced disease: review. [review]. Ann Oncol. 2012;23:1095-103. 10.1093/annonc/mdr433 [DOI] [PubMed] [Google Scholar]
- 2.Bray F,Ferlay J,Soerjomataram I,Siegel RL,Torre LA,Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394-424. 10.3322/caac.21492 [DOI] [PubMed] [Google Scholar]
- 3.Merritt RE,Whyte RI,D’Arcy NT,Hoang CD,Shrager JB. Morbidity and mortality after esophagectomy following neoadjuvant chemoradiation. Ann Thorac Surg. 2011;92:2034-40. 10.1016/j.athoracsur.2011.05.121 [DOI] [PubMed] [Google Scholar]
- 4.Schlottmann F,Strassle PD,Nayyar A,Herbella FAM,Cairns BA,Patti MG. Postoperative outcomes of esophagectomy for cancer in elderly patients. J Surg Res. 2018;229:9-14. 10.1016/j.jss.2018.03.050 [DOI] [PubMed] [Google Scholar]
- 5.Low DE,Alderson D,Cecconello I,Chang AC,Darling GE,D’Journo XB,et al. International Consensus on Standardization of Data Collection for Complications Associated With Esophagectomy. Ann Surg. 2015;262:286-94. 10.1097/SLA.0000000000001098 [DOI] [PubMed] [Google Scholar]
- 6.Reynolds JV,Donlon N,Elliott JA,Donohoe C,Ravi N,Kuppusamy MK,et al. Comparison of Esophagectomy outcomes between a National Center, a National Audit Collaborative, and an International database using the Esophageal Complications Consensus Group (ECCG) standardized definitions. Dis Esophagus. 2021;34:34. 10.1093/dote/doab052.548 [DOI] [PubMed] [Google Scholar]
- 7.Lerut T,Moons J,Coosemans W,Van Raemdonck D,De Leyn P,Decaluwé H,et al. Postoperative complications after transthoracic esophagectomy for cancer of the esophagus and gastroesophageal junction are correlated with early cancer recurrence: role of systematic grading of complications using the modified Clavien classification. Ann Surg. 2009;250:798-807. 10.1097/SLA.0b013e3181bdd5a8 [DOI] [PubMed] [Google Scholar]
- 8.Tamagawa A,Aoyama T,Tamagawa H,Ju M,Komori K,Maezawa Y,et al. Influence of Postoperative Pneumonia on Esophageal Cancer Survival and Recurrence. Anticancer Res. 2019;39:2671-8. 10.21873/anticanres.13392 [DOI] [PubMed] [Google Scholar]
- 9.Glatz T,Marjanovic G,Kulemann B,Sick O,Hopt UT,Hoeppner J. Hybrid minimally invasive esophagectomy vs. open esophagectomy: a matched case analysis in 120 patients. Langenbecks Arch Surg. 2017;402:323-31. 10.1007/s00423-017-1550-4 [DOI] [PubMed] [Google Scholar]
- 10.Mariette C,Markar SR,Dabakuyo-Yonli TS,Meunier B,Pezet D,Collet D,et al. ; Fédération de Recherche en Chirurgie (FRENCH) and French Eso-Gastric Tumors (FREGAT) Working Group. Hybrid Minimally Invasive Esophagectomy for Esophageal Cancer. N Engl J Med. 2019;380:152-62. 10.1056/NEJMoa1805101 [DOI] [PubMed] [Google Scholar]
- 11.Yang Y,Zhang X,Li B,Li Z,Sun Y,Mao T,et al. Robot-assisted esophagectomy (RAE) versus conventional minimally invasive esophagectomy (MIE) for resectable esophageal squamous cell carcinoma: protocol for a multicenter prospective randomized controlled trial (RAMIE trial, robot-assisted minimally invasive Esophagectomy). BMC Cancer. 2019;19:608. 10.1186/s12885-019-5799-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Yang Y,Li B,Yi J,Hua R,Chen H,Tan L,et al. Robot-assisted Versus Conventional Minimally Invasive Esophagectomy for Resectable Esophageal Squamous Cell Carcinoma. Ann Surg. 2022;275:646-53. 10.1097/SLA.0000000000005023 [DOI] [PubMed] [Google Scholar]
- 13.Guo F,Ma D,Li S. Compare the prognosis of Da Vinci robot-assisted thoracic surgery (RATS) with video-assisted thoracic surgery (VATS) for non-small cell lung cancer. Medicine (Baltimore). 2019;98:e17089. 10.1097/MD.0000000000017089 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Sheng S,Zhao T,Wang X. Comparison of robot-assisted surgery, laparoscopic-assisted surgery, and open surgery for the treatment of colorectal cancer. Medicine (Baltimore). 2018;97:e11817. 10.1097/MD.0000000000011817 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Ojima T,Nakamura M,Hayata K,Kitadani J,Katsuda M,Takeuchi A,et al. Short-term Outcomes of Robotic Gastrectomy vs Laparoscopic Gastrectomy for Patients With Gastric Cancer. JAMA Surg. 2021;156:954-63. 10.1001/jamasurg.2021.3182 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Japanese Classification of Esophageal Cancer. 11th Edition: part I. Esophagus. 2017;14:1-36. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Japanese Classification of Esophageal Cancer. 11th Edition: part II and III. Esophagus. 2017;14:37-65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Shishido Y,Matsunaga T,Makinoya M,Miyauchi W,Shimizu S,Miyatani K,et al. Circular stapling anastomosis with indocyanine green fluorescence imaging for cervical esophagogastric anastomosis after thoracoscopic esophagectomy: a propensity score-matched analysis. BMC Surg. 2022;22:152. 10.1186/s12893-022-01602-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Tsunoda S,Obama K,Hisamori S,Nishigori T,Okamura R,Maekawa H,et al. Lower Incidence of Postoperative Pulmonary Complications Following Robot-Assisted Minimally Invasive Esophagectomy for Esophageal Cancer: Propensity Score-Matched Comparison to Conventional Minimally Invasive Esophagectomy. Ann Surg Oncol. 2021;28:639-47. 10.1245/s10434-020-09081-6 [DOI] [PubMed] [Google Scholar]
- 20.Morimoto Y,Kawakubo H,Ishikawa A,Matsuda S,Hijikata N,Ando M,et al. Short‐term outcomes of robot‐assisted minimally invasive esophagectomy with extended lymphadenectomy for esophageal cancer compared with video‐assisted minimally invasive esophagectomy: A single‐center retrospective study. Asian J Endosc Surg. 2022;15:270-8. 10.1111/ases.12992 [DOI] [PubMed] [Google Scholar]
- 21.Kosumi K,Baba Y,Yamashita K,Ishimoto T,Nakamura K,Ohuchi M,et al. Monitoring sputum culture in resected esophageal cancer patients with preoperative treatment. Dis Esophagus. 2017;30:1-9. 10.1093/dote/dox092 [DOI] [PubMed] [Google Scholar]
- 22.Park S,Hyun K,Lee HJ,Park IK,Kim YT,Kang CH. A study of the learning curve for robotic oesophagectomy for oesophageal cancer. Eur J Cardiothorac Surg. 2018;53:862-70. 10.1093/ejcts/ezx440 [DOI] [PubMed] [Google Scholar]