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ORIGINAL RESEARCH

Efficacy and Perioperative Safety of Robot-

Assisted Minimally Invasive Esophagectomy for
Esophageal Cancer
Mingquan Ma, MM; Peng Ren, MM; Haitong Wang, MM; Hongdian Zhang, MM; Lei Gong, MM;
Yufeng Qiao, MM; Xiangming Liu, MM; Peng Tang, MM

ABSTRACT
Background • Esophageal cancer (EC) remains a Results • The research group demonstrated longer
significant global health concern. Minimally invasive operative times, a higher number of dissected lymph
surgical techniques, including robot-assisted approaches, nodes, reduced intraoperative bleeding, and quicker
have emerged as promising options for improving postoperative recovery compared to the control group,
outcomes and patient recovery in EC management. with significantly fewer complications (P < .05).
Objective • This study aims to evaluate the clinical utility Furthermore, the research group exhibited lower levels of
of robot-assisted minimally invasive esophagectomy postoperative IFs and MDA, along with higher levels of
(RAMIE) in the treatment of EC. SOD and GSH-Px, compared to the control group (P <
Methods • A total of 160 EC patients undergoing treatment .05). There was no significant difference between the two
at our hospital were included in this study. Patients were groups in terms of prognostic survival and EC recurrence
randomly assigned to either the research group, receiving rates (P > .05).
RAMIE, or the control group, undergoing thoracoscopic Conclusion • RAMIE demonstrates superior efficacy in
minimally invasive esophagectomy (MIE). Surgical enhancing therapeutic outcomes and accelerating
outcomes, postoperative recovery, complication rates, and postoperative recovery in patients with EC, thus
changes in inflammatory factors (IFs) such as establishing its value in EC treatment protocols. RAMIE is
malondialdehyde (MDA), superoxide dismutase (SOD), suggested as a valuable therapeutic option and warrants
and glutathione peroxidase (GSH-Px) levels were compared clinical adoption for EC management. (Altern Ther Health
between the two groups. Additionally, prognostic survival Med. [E-pub ahead of print.])
and EC recurrence rates were assessed at a 1-year follow-up.

Mingquan Ma, MM; Peng Ren, MM; Haitong Wang, MM; the disease.2 Moreover, recent shifts in dietary habits have
Hongdian Zhang, MM; Lei Gong, MM; Yufeng Qiao, MM; contributed to a consistent rise in EC incidence, with the
Xiangming Liu, MM; Peng Tang, MM, Department of global rate in 2020 soaring to 4.3 times higher than that
Esophageal Cancer; Tianjin Medical University Cancer recorded in 2000.3
Institute and Hospital; Key Laboratory of Cancer Prevention EC often exhibits significant concealment during its
and Therapy of Tianjin; Tianjin’s Clinical Research Center for initial stages, characterized by nonspecific clinical features in
Cancer; National Clinical Research Center for Cancer; the majority of patients.2,3 Consequently, the emergence of
Tianjin; China. symptoms like dysphagia and sternal pain typically signals
disease advancement to the middle and late stages, thereby
Corresponding author: Peng Tang, MM heightening treatment complexity and substantially
E-mail: tang407863@163.com augmenting patient mortality risk.4 Clinically, malignant
neoplastic diseases are primarily managed through surgical
intervention, often supplemented with adjuvant therapies
INTRODUCTION such as radiotherapy and chemotherapy.3-5
Esophageal cancer (EC) stands as one of the most Traditional radical surgery for EC often induces
prevalent gastrointestinal malignancies, ranking sixth in considerable trauma, imposes significant stress on patients,
overall cancer incidence.1 Statistics reveal approximately 1.4 and is associated with numerous postoperative complications,
million new cases of EC diagnosed worldwide each year, with hindering their recovery.5 The advancements in science,
an estimated 300 thousand patients ultimately succumbing to technology, and medical techniques have led to the emergence

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of robot-assisted minimally invasive esophagectomy Research Group. The bedside robotic manipulator
(RAMIE) as a pivotal aspect of modern EC treatment.6 system was positioned as follows: No.1 manipulator in the
In addition to sharing advantages similar to traditional third intercostal space of the axillary midline, No.2
thoracoscopic minimally invasive esophagography (MIE), manipulator in the ninth intercostal space of the axillary
RAMIE facilitates surgeons in obtaining a clear visualization of posterior line, lens aperture in the sixth intercostal space of
patients’ esophageal internal conditions through 3D imaging.7 the midaxillary line, and the assistant hole in the fourth
Furthermore, RAMIE offers the benefits of hand tremor intercostal space of the anterior axillary line. Sequential
filtration and robotic arm flexibility, aiding surgeons in separation of the venous arch and thoracic esophagus was
performing EC radical surgery with greater precision and performed, along with dissection of mediastinal lymph
efficiency.8 While recent studies have confirmed RAMIE’s nodes and bilateral para-recurrent laryngeal nerve lymph
significant positive impact and high safety in treating various nodes. Subsequently, the patient was repositioned supine for
chest tumors,9,10 its application in EC treatment remains abdominal surgery, during which the stomach was fashioned
relatively underreported. Meanwhile, there is a significant lack into a tubular shape approximately 4cm wide and anastomosed
of applied research on RAMIE for EC patients in China, largely at the neck using a stapler.
due to variations in medical standards across different regions. Control Group. In the control group, a 1.5cm
Since 2020, our hospital has actively adopted RAMIE and thoracoscopic incision was made in the sixth intercostal
accumulated a substantial case volume. Therefore, this study space of the axillary midline, and a 12mm torca was inserted
systematically assesses the application of RAMIE in EC as the observation hole. The rest of the surgical procedure
treatment, aiming to furnish updated reference materials and was the same as the research group.
guidance for future clinical approaches to managing EC. Our Postoperative Care and Monitoring in the ICU. After
findings offer valuable insights into its efficacy and safety. for the surgical procedure, patients were promptly transferred to
updated guidance in clinical practice by providing comprehensive the intensive care unit (ICU) for close postoperative
evaluation and informing future treatment strategies. monitoring and observation. This standard protocol ensures
vigilant surveillance of patients’ vital signs, surgical outcomes,
MATERIALS AND METHODS and overall recovery progress. Within the ICU, specialized
Study Design medical personnel administer tailored care and interventions
This study employed a comparative design involving 160 to optimize patient recovery and mitigate potential
EC patients admitted to our hospital between March 2020 postoperative complications.
and August 2021. Patients were randomly assigned to either
the research group, undergoing RAMIE, or the control Blood Sample Collection and Analysis
group, receiving thoracoscopic MIE. Approval for the study Fasting venous blood samples were obtained both before
was obtained from the Ethics Committee of Tianjin Medical and 3 days post-surgery. After centrifugation, serum was
University Cancer Institute and Hospital, and informed collected to assess levels of inflammatory factors (IFs)
consent was obtained from all participants prior to their interleukin-1β/6 (IL-1β/6) and tumor necrosis factor-α
inclusion in the study. (TNF-α), as well as oxidative stress markers malondialdehyde
(MDA), superoxide dismutase (SOD), and glutathione
Inclusion and Exclusion Criteria peroxidase (GSH-Px). Enzyme-linked immunosorbent assay
Inclusion criteria were as follows: (1) All patients (ELISA) kits, procured from Beijing TransGen Biotech, were
included in the study were pathologically confirmed to have utilized according to manufacturer recommendations for
EC;11 (2) patients meeting the surgical indications; (3) had accurate measurement.
complete clinicopathological data; and (4) underwent surgery
performed by the same surgical team. Prognostic Follow-Up
Exclusion criteria were as follows: (1) Patients with All patients underwent a one-year follow-up period,
preoperative clinical stage IV EC; (2) those requiring with regular reviews scheduled every two months. During
conversion to thoracotomy intraoperatively due to tumor these follow-up appointments, prognostic survival rates and
invasion of adjacent thoracic structures such as the aorta, incidences of EC recurrence were meticulously analyzed and
trachea or lung; (3) those with severe cardiopulmonary documented.
insufficiency incompatible with anesthesia and surgery; (4)
patients with epilepsy; (5) mental disorders; (6) or Outcome Measures
communication barriers were excluded from the study. Perioperative Inflammation and Oxidative Stress. The
levels of inflammatory factors IL-1β/6 and TNF-α, as well as
Surgical Procedure oxidative stress markers MDA, SOD, and GSH-Px, were
After general anesthesia (combined anesthesia), patients measured both pre-and post-operatively to evaluate
underwent intubation with a double-lumen endotracheal perioperative inflammation and oxidative stress.
tube. The research group received RAMIE, and the control Surgical and Postoperative Parameters. Various
group received thoracoscopic MIE surgical intervention. surgical and postoperative parameters were carefully

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recorded and analyzed. Operation-related metrics, including Table 1. Comparison of Pathological Data
operation time, number of dissected lymph nodes,
Data Control Group (n=80) Research Group (n=80) t (or χ2) P value
intraoperative bleeding, and instances of intraoperative Age 62.83±6.10 61.45±6.30 1.403 .163
conversion to thoracotomy, were documented. Additionally, Sex 0.681 .409
Male 49 (61.25) 54 (67.50)
postoperative variables such as the duration of chest drainage, Female 31 (38.75) 26 (32.50)
Location of The Tumor 1.040 .594
feeding duration, length of hospital stay, and incidence of Upper 9 (11.25) 13 (16.25)
postoperative complications were comprehensively assessed. Middle 68 (85.00) 62 (77.50)
Lower 6 (7.50) 5 (6.25)
Prognosis Assessment. Prognostic outcomes, including Type of Tumor 1.006 .605
Adenocarcinoma 0 (0.0) 1 (1.25)
survival rates and the recurrence of EC, were carefully Squamous Carcinoma 79 (98.75) 78 (97.50)
assessed to estimate the overall prognosis of patients Other 1 (1.25) 1 (1.25)
Degree of Differentiation 0.975 .614
undergoing treatment. Hypo-Differentiated 10 (12.50) 8 (10.00)
Moderately-Differentiated 48 (60.00) 54 (67.50)
Highly-Differentiated 22 (27.50) 18 (22.50)
Statistical Analysis
Data analysis was performed using SPSS version 23.0 Note: Data presented as mean ± standard deviation or frequency [n (%)].
P values are calculated using independent samples t test or chi-square test,
software. Count data were expressed as percentages [n (%)] as appropriate. The statistical significance threshold was set at P < .05.
and compared between groups using the chi-square test (χ2).
Measurement data were presented as mean ± standard Figure 1. Comparison of Surgical Situations
deviation (x̄ ± s), and between-group and within-group
comparisons were conducted using the independent t-test and
paired t test, respectively. Survival rates were calculated using
the Kaplan-Meier method and compared using the Log-rank
test. A value of P < .05 was considered statistically significant.

RESULTS
Note: Figure 1A: Comparison of Operation Time; Figure 1B: Comparison of
Comparison of Pathological Data between Two Groups Intraoperative Bleeding; Figure 1C: Comparison of Number of Lymph Node
Comparison of patients’ age, sex, pathological stage, and Dissections between the research group and the control group. The research
EC site between the research group and control group revealed group exhibited a longer operative time and a greater number of lymph node
no statistically significant differences (P > .05), refer to Table 1. dissections while experiencing lower intraoperative bleeding compared to
the control group.
This result indicates the comparability of the two groups in
terms of baseline characteristics and pathological features. Figure 2. Comparison of Postoperative Conditions

Surgical Outcome Analysis

The statistical analysis of surgical outcomes revealed that
only one patient in the control group required conversion to
thoracotomy. In the research group, the operation time,
intraoperative bleeding, and the number of dissected lymph
nodes were 341.74±50.46 minutes, 114.59±36.35 milliliters,
Note: Figure 2A: Duration of Postoperative Chest Drainage Time; Figure 2B:
and 23.81±6.90, respectively. Notably, the operation time and Feeding Time; Figure 2C: Hospitalization Time, between the research group
number of lymph nodes dissected were significantly higher and the control group. All values in the research group were lower than
in the research group compared to the control group, those in the control group.
whereas the intraoperative bleeding was significantly lower
(P < .05), see Figure 1. Table 2. Postoperative Adverse Reactions
Adverse Reactions Control Group (n=80) Research Group (n=80) χ2 P value
Comparison of Postoperative Parameters Hoarseness 3 (3.75) 2 (2.50)
In the research group, the duration of postoperative Pneumonia 4 (5.00) 3 (3.75)
Anastomotic fistula 3 (3.75) 0 (0.0)
chest drainage, feeding, and hospitalization were 7.76±1.84 Arrhythmia 2 (2.50) 1 (1.25)
Atrial Fibrillation 1 (1.25) 0 (0.0)
days, 6.44±1.23 days, and 17.33±2.16 days, respectively. Pleural effusion 2 (2.50) 1 (1.25)
These durations were significantly shorter compared to those Cutaneous infection 1 (1.25) 0 (0.0)
Pneumothorax 2 (2.50) 1 (1.25)
observed in the control group (P < .05), see Figure 2. Total incidence 22.50% 10.00% 4.592 .032
Furthermore, the incidence of postoperative complications
Note: Data presented as frequency [n (%)]. P values calculated using chi-
was 10.00% in the research group, which was also significantly square test (χ2). The statistical significance threshold was set at P < .05.
lower than that in the control group (P < .05), Table 2.
results (P > .05). However, postoperatively, levels of IL-1β,
Comparison of Postoperative Inflammatory Reaction IL-6, and TNF-α increased in both groups, with significantly
In comparing inflammatory factors (IFs), no significant lower levels observed in the research group compared to the
inter-group differences were observed in preoperative test control group (P < .05), see Figure 3.

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Figure 3. Comparison of Inflammatory Factors years of clinical practice, RAMIE has demonstrated comparable
surgical indications to traditional thoracoscopic MIE. However,
its distinct advantages are particularly evident in challenging
surgical scenarios and confined anatomical spaces. Therefore,
RAMIE has garnered increasing adoption by hospitals seeking
to tackle complex operations and enhance surgical precision.12
RAMIE offers several advantages, including high-
Note: Figure 3A: Interleukin-1β (IL-1β) Levels; Figure 3B: Interleukin-6 (IL- definition stereoscopic 3D vision magnified by more than 10
6) Levels; Figure 3C: Tumor Necrosis Factor-α (TNF-α) Levels between the times, flexible mechanical arms, and hand tremor filtration.
research group and the control group. Postoperative inflammatory factors
These features ensure the safety and feasibility of thoracic
were lower in the research group than in the control group.
surgery for various diseases. RAMIE enables clear exposure
Figure 4. Comparison of Oxidative Stress Responses of lymph nodes in different regions of the pulmonary hilum
and mediastinum, facilitating extensive lymph node
dissection. This enhances the accuracy of the operation,
reduces the risk of intraoperative bleeding and perioperative
complications, and ultimately shortens hospitalization time.13
In the era of high-tech and information technology,
RAMIE emerges as a modality that aligns well with the
Note: Figure 4A: Superoxide Dismutase (SOD) Levels; Figure 4B: Glutathione contemporary healthcare landscape. This is evident in light of
Peroxidase (GSH-Px) Levels; Figure 4C: Malondialdehyde (MDA) Levels
between the research group and the control group. Postoperative SOD and the escalating clinical demand and heightened health
GSH-Px levels were higher, and MDA levels were lower in the research awareness among patients.14 In the current medical landscape
group than in the control group. of China, RAMIE is still at a developmental stage, and there
is limited research available on the subject.15 Furthermore,
Figure 5. Comparison of Prognosis there is a notable absence of guidance regarding technical
challenges, such as coordinating multiple robotic arm
operations during surgery and the absence of tactile feedback
for surgeons during the procedure.
This study systematically evaluated the therapeutic effect of
RAMIE on EC. Initially, upon comparing the operative
conditions, it was observed that the operation time in the
research group was significantly prolonged, likely attributable to
the complexity of the RAMIE procedure. However, despite this
Note: Figure 5A: Prognostic Survival Curves; Figure 5B: Prognostic Recurrence prolonged duration, the research group exhibited an increased
Rates, respectively, between the research group and the control group. There number of dissected lymph nodes, reduced intraoperative
was no significant difference in prognosis between the two groups.
bleeding, and shortened postoperative rehabilitation time. These
Comparison of Oxidative Stress Reaction findings suggest a more substantial therapeutic efficacy and less
Upon comparison of oxidative stress responses, no trauma associated with RAMIE in EC management. This
significant differences were observed in preoperative stress finding aligns with the treatment outcomes observed in studies
levels between the research group and control group (P > investigating the effectiveness of RAMIE in treating lung cancer,
.05). However, postoperatively, levels of MDA increased in as demonstrated by Berzenji et al.16
both groups, with notably higher levels detected in patients We speculate that this outcome may be attributed to the
in the control group (P < .05). Conversely, levels of SOD and enlarged surgical field of view offered by RAMIE, which
GSH-Px decreased postoperatively, with lower levels observed proves particularly beneficial for intraoperative anatomy.
in the research group compared to the control group (P < This enhanced visualization allows for a more precise
.05), Figure 4. dissection of tissues around the esophagus along critical
structures such as the trachea, thoracic duct, aorta, and vagus
Follow-Up and Prognosis Assessment nerve.17 Meanwhile, RAMIE demonstrates more pronounced
All patients in the research group and 77 patients in the advantages in confined areas such as the mediastinum and
control group were successfully followed up. Upon bilateral recurrent laryngeal nerves. It allows for the execution
comparison, no significant difference was observed between of more intricate minimally invasive procedures18 while
the two groups in terms of overall survival rate and EC mitigating damage to surrounding normal tissues during
recurrence rate (P > .05), see Figure 5. surgery, thereby reducing blood loss.
Furthermore, the lower incidence of postoperative
DISCUSSION complications in the research group supports this perspective,
RAMIE represents a new frontier in thoracic surgery, suggesting that RAMIE offers enhanced safety in the treatment of
offering significant advancements in surgical techniques. After EC. In the comparison of inflammation and oxidative stress

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reactions, it was observed that both groups of patients experienced CONCLUSION

significantly heightened postoperative inflammation and oxidative In conclusion, this study demonstrates that RAMIE
stress responses. It is a typical physiological response following significantly enhances the therapeutic efficacy of EC patients,
invasive mechanical procedures and partial tissue resection. leading to faster postoperative rehabilitation and improved
However, the postoperative inflammatory and oxidative stress surgical safety. Despite the longer operation time associated with
reactions were found to be less severe in the research group. RAMIE, the procedure results in increased lymph node dissections
This result indicates that patients undergoing RAMIE and decreased intraoperative bleeding, indicating its efficacy and
experience less internal tissue damage and maintain a more reduced trauma compared to traditional methods. RAMIE also
stable internal environment. This advantage not only exhibits advantages in managing complications such as hoarseness,
facilitates quicker functional recovery post-surgery but also pneumonia, and anastomotic fistula. While further research with
diminishes the likelihood of postoperative infection and longer follow-up periods is warranted to confirm its prognostic
other complications, thereby reinforcing our findings. Wang effects, the findings underscore the clinical value of RAMIE in
et al.19 also found that RAMIE helps alleviate postoperative treating EC. Additionally, ongoing efforts to refine surgical skills
stress responses in patients with gastric cancer and supports and broaden operator experience are essential for the wider
their rehabilitation, which is consistent with our findings. adoption of RAMIE in clinical practice.
In addition, clinical emphasis has been placed on the
importance of including bilateral para-recurrent laryngeal COMPETING INTERESTS
The authors report no conflict of interest.
nerve lymph nodes in the mediastinal lymph node dissection
for EC treatment.20 However, during MIE surgery, probing FUNDING
None.
bilateral para-recurrent laryngeal nerve lymph nodes presents
significant challenges,21 whereas the utilization of RAMIE ACKNOWLEDGEMENTS
None.
aids physicians in accurately visualizing these lymph nodes.22
However, this study did not observe any significant difference AVAILABILITY OF DATA AND MATERIALS
The data that support the findings of this study are available from the corresponding author upon
in patient prognosis, which could be attributed to the short reasonable request.
follow-up period and limited number of subjects in the study.
In a previous study, researchers observed that RAMIE led REFERENCES
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